Luis M. P. Ceríaco · Ricardo F. de Lima
Martim Melo · Rayna C. Bell
Editors
Biodiversity of
the Gulf of Guinea
Oceanic Islands
Science and Conservation
Biodiversity of the Gulf of Guinea Oceanic Islands
Luis M. P. Ceríaco • Ricardo F. de Lima •
Martim Melo • Rayna C. Bell
Editors
Biodiversity of the Gulf
of Guinea Oceanic Islands
Science and Conservation
Editors
Luis M. P. Ceríaco
Museu de História Natural e da Ciência da
Universidade do Porto
Porto, Portugal
Martim Melo
CIBIO, Centro de Investigação em
Biodiversidade e Recursos Genéticos
InBIO Laboratório Associado
Universidade do Porto
Vairão, Portugal
Ricardo F. de Lima
Centre for Ecology, Evolution and
Environmental Changes (cE3c)
Faculdade de Ciêncas, Universidade de Lisboa
Lisbon, Portugal
Rayna C. Bell
Herpetology Department
California Academy of Sciences
San Francisco, CA, USA
ISBN 978-3-031-06152-3
ISBN 978-3-031-06153-0
https://doi.org/10.1007/978-3-031-06153-0
(eBook)
Associação BIOPOLIS
Sponsoring Party
Research Centre in Biodiversity and Genetic Resources - Research Network in Biodiversity and
Evolutionary Biology (CIBIO), University of Porto, Campus de Vairão, Vila do Conde, Portugal
Represented by Nuno Miguel dos Santos Ferrand de Almeida (Director of CIBIO)
© The Editor(s) (if applicable) and The Author(s) 2022. This book is an open access publication.
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Foreword 1
The islands of São Tomé and Príncipe emerged from relatively ancient volcanic
activity, dating back 30 million years. Due to their isolation from the African
continent, the fauna and flora are quite unique. The refuges that resulted from
these volcanic phenomena gave rise to a high degree of endemic species, including
bats, birds, reptiles, amphibians, butterflies, molluscs, as well as a great variety of
flora. The richness of the islands’ biodiversity is recognized by the scientific world,
which considers the tropical forest of São Tomé and Príncipe as the second most
important for the conservation of avifauna, among 75 African forests.
Biological diversity in São Tomé and Príncipe is manifested not only in terms of
species richness and endemism. Despite the country’s relatively small area, the
diversity of its ecosystems is equally impressive, particularly in the forestry domain.
The shade forests are particularly noteworthy as they house cocoa crops that support
the national economy. Cocoa production requires the maintenance of forest cover to
shade the plants, a practice that also helps to maintain high levels of forest biodiversity in producing countries.
With a total land area of around 1000 km2, the islands of São Tomé and Príncipe
are home to a great diversity of habitats ranging from savannas and mangroves in the
coastal areas, to shade forests, low and medium altitude forests, and fog forests at
altitudes of more than 2000 m. The forests are characterized by several endemic
species, including the Giant Lobelia, Lobelia barnsii and many species of mammals,
amphibians, reptiles, and insects. The birds are truly exceptional with more than
28 species of endemic birds including Maroon Pigeons, Columba thomensis, the São
Tomé Green-Pigeon, Treron sanctithomae, the Sao Tome Ibis, Bostrychia bocagei,
and the famous Sao Tome Prinia, Prinia molleri. The Prinia is also present in urban
areas of the country and greets the islands’ human inhabitants with its rhythmic wing
flaps in the morning.
The Tinhosas islets, located 22 km from the island of Principe, are home to one of
the largest colonies of seabirds in our African sub-region, which makes them the
main nursery of seabirds in the Gulf of Guinea. This status, according to Birdlife
International, makes them an area of worldwide importance for bird conservation.
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Foreword 1
The extraordinary biodiversity of the islands contributed to the island of Príncipe
becoming part of the UNESCO World Network of Biosphere Reserves in 2012.
Throughout its existence, the population of São Tomé and Príncipe has been
closely linked to the country’s biological resources, through agriculture, fishing,
harvesting, medicine, recreation, tourism, and also through cultural events. In
recognition of the importance of biodiversity for the lives of the population, and
that the issue of biodiversity conservation is a common concern for all of Humanity,
the Democratic Republic of São Tomé and Príncipe became a signatory to the
Convention on Biological Diversity in June 1992, in Rio de Janeiro. States must
assume the main responsibility in the search for feasible and effective conservation.
After its ratification, several steps were taken at the international level to obtain
the necessary means to implement the recommendations contained in Article 6 of the
Convention, namely in terms of the elaboration and implementation of national
strategies, plans and programmes aiming at conservation and sustainable use of
biological diversity, as well as the integration of these same objectives in the specific
framework of the different sectoral and intersectoral plans and programmes. The
Biodiversity Action Plan of São Tomé and Príncipe aims for the local population to
use natural resources in a way that contributes to poverty reduction and allows for
sustainable socio-economic development.
The present work “The Biodiversity of the Oceanic Islands of the Gulf of Guinea”
represents without a doubt, an important contribution to the knowledge of the rich
biodiversity of São Tomé and Príncipe. Biodiversity is central to the current and
future socio-economic development of the county, and there is a clear need to
expand research that furthers knowledge of our biodiversity and identifies solutions
that lead to its sustainable use.
I proudly provide a foreword to the present work, certain of its potential to
encourage our national academia and inspire a new generation of researchers.
President of the Democratic Republic of São
Tomé and Príncipe, Neves, São Tomé and Príncipe
December 2021
Carlos Vila Nova
Foreword 2
For more than 30 years, the EU and its partners have been supporting the preservation of biodiversity and fragile ecosystems in Central Africa, notably through the
ECOFAC programme. ECOFAC was launched in 1993 with the objective to
promote the conservation and rational use of Central Africa’s forest heritage, taking
into account the socio-economic and environmental particularities of its landscapes.
This programme follows the intentions expressed in the “Lomé III” Convention
(8 December 1984), between the European Economic Community and the African,
Caribbean, and Pacific Group of States, aiming to strengthen cooperation for the
economic, cultural, and social development of these States. In the Brazzaville
Declaration of 31 May 1990, on the conservation and rational use of forest ecosystems in Central Africa, the representatives of seven countries submitted a request to
the Commission, which was agreed on 26 October 1990. São Tomé and Príncipe has
been benefitting directly from the Programme since its inception.
A great deal of knowledge has been gained over the last 30 years that has helped
to shape the conservation sector in Central African countries. This knowledge has
led to a better understanding of species diversity and ecosystems, the development of
a sub-regional network of protected areas, and to valuable information for their
effective management. The ECOFAC Programme has also played a pivotal role to
build capacity and human capital in conservation in Central Africa. Over the course
of these three decades, paradigms around protected areas have evolved. These areas
were mainly oriented towards strict conservation in the beginning, but the approach
is increasingly integrating the needs of human populations and the notion of
landscape, establishing a new paradigm around “conservation for development”.
Fundamental and applied conservation research continues to be an essential component of the management of protected areas and their surroundings. This work
encompasses a wide range of themes, and increasingly integrates socio-economic
and biological research. Understanding how ecosystems and species respond to
human pressures is essential as human population growth accelerates.
With continuous support from the European Union, the ECOFAC Programme is
now in its sixth phase. This makes ECOFAC the oldest European programme in
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Foreword 2
Central Africa, a sign of the European Union’s lasting political commitment to the
region, specifically regarding conservation. The general objective of the ECOFAC
6 Programme is to improve the governance of natural resources and the management
of protected areas, to contribute to a green economy characterized by endogenous,
sustainable, and inclusive economic development. As the implementing partner of
the ECOFAC 6 component for the Democratic Republic of São Tomé and Príncipe,
BirdLife International has been working closely with park management authorities,
government ministries, and communities to promote research, empowerment, and
the conservation of threatened and unique birds and their habitats.
This book is an important step towards meeting these objectives, synthesizing
centuries of research into a single volume that is freely accessible to researchers,
educators, policy makers, and the public.
The oceanic islands of the Gulf of Guinea—Príncipe, São Tomé, and Annobón—
are three small volcanic islands off the west coast of Central Africa. They are home
to a remarkable number of unique species across the tree of life, including plants,
mushrooms, spiders, butterflies, molluscs, amphibians, reptiles, birds, and mammals, inhabiting the forests that envelop the islands’ inactive volcanic slopes. The
surrounding marine ecosystems are also teeming with life, hosting diverse communities that include sea turtles, sharks, cetaceans, reef fishes, and marine invertebrates.
The human populations on the islands are mostly concentrated along the coasts
where they rely heavily on the balance of both terrestrial and marine environments.
On a global scale, biological diversity is declining and the rate of species
extinction is accelerating, threatening the ecological processes that sustain life on
Earth. Unfortunately, the ecosystems of the oceanic islands in the Gulf of Guinea
have not been spared from the negative impacts of human activity. Centuries of
intensive monoculture have left a lasting imprint on the island landscapes, and the
human population has grown quickly over the last 50 years, which has increased the
pressure on already vulnerable ecosystems. It is now widely recognized that biodiversity conservation is a fundamental element of sustainable development, increasing resilience and reducing environmental vulnerability.
The new European Green Deal adopted on 14 July 2021, identifies environmental
degradation as an existential threat to the world. To overcome these challenges, the
European Green Deal is committed to intensify the integration of environmental and
climate change objectives, in particular the biodiversity, forests, oceans, and soils,
across all sectors of cooperation. It is in this context that the EU has been fomenting
the NaturAfrica initiative, aiming to support biodiversity conservation in Africa
through an innovative, people-centred approach. NaturAfrica is the successor of
ECOFAC and it consists of identifying key landscapes for conservation and development where the EU will focus its support for job creation, improved security, and
sustainable livelihoods, while preserving ecosystems and wildlife that are vital to all.
This initiative will directly benefit the island landscapes of Príncipe, São Tomé, and
Annobón.
Moreover, the Global Gateway Strategy launched on 1 December 2021, stands
for sustainable and trusted connections that work for people and the planet. It will
help to tackle the most pressing global challenges, including fighting climate change.
Foreword 2
ix
Global Gateway is a great start to lead on climate action with developing countries,
tackling climate change with a closing window of opportunity against global
warming, taking into account the needs of partner countries and ensuring lasting
benefits for local communities.
This book is the first synthesizing knowledge on the biodiversity of these islands.
It is being published at a time when humanity is facing a serious ecological crisis due
to the unprecedented collective impacts of human activities on nature, and the timely
publication of this book will serve as an important resource to guide the next phase
of biodiversity conservation of this unique archipelago.
Thus, the information in this book is fundamental to guide development strategies
for the islands.
EU Ambassador in Gabon to São Tomé
and Príncipe and ECCAS, Gabon,
São Tomé and Príncipe
H. E. Rosario Bento Pais
Foreword 3
Ex Africa Semper Aliquid Novi
Some two decades ago, I found myself on a small aircraft en route to the island of
São Tomé. I had just attended a meeting of the World Wildlife Fund in Libreville,
Gabon and was now headed to meet an old San Francisco family friend. Ned
Seligman, a former Peace Corps volunteer (later Country Director) and fellow
lover of Africa had moved to the island and founded a non-profit organization called
STeP UP that focused on education and health initiatives. He had been urging me to
visit for some years. As a scientist with the California Academy of Sciences in San
Francisco, I had by this time already travelled and worked in much of continental
Africa, but I was unaware that one of the most meaningful and satisfying phases of
my scientific career was about to begin; it would also be the last.
It has been said that nothing compares with the thrill of discovery. In the
academic and scientific world, this might be a single novel idea or a series of related
discoveries leading to a new understanding of a more complex whole. The Gulf of
Guinea Islands are teeming with unique species of plants, animals, and fungi whose
diversity and biology have inspired centuries of research, but the islands also present
a unique geological setting in which to understand broader questions about how
biodiversity evolves and accumulates on oceanic islands. Very early discoveries of
the unique species inhabiting Gulf of Guinea Islands collected by early explorers
such as Greef, Newton, and Fea, mostly during the nineteenth century, were
tantalizing to biologists of the time. However, after a fruitful initial period of
biological discoveries, the islands remained overlooked by the large majority of
the scientific community. More recently, the spectacular Gulf of Guinea Islands
opened again to collaborative biological exploration. The early results of this long
overdue exploration and analysis include numerous intriguing, fascinating discoveries, many of which are presented in this volume.
While many of these results represent work by groups and individuals from
scientific institutions in North America, Europe, and Brazil, they are most importantly the result of cooperation and efforts with the citizens and civic leaders of the
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Foreword 3
islands. The islands’ residents are the ultimate custodians of the biological wealth
partially described herein. To that end, it must be mentioned that many of the results
presented in this volume have already been and are still being transmitted directly to
national and regional governmental entities. Past and ongoing efforts to spread
environmental awareness to island residents of all ages and to inspire stewardship
of the islands’ biological heritage are also described in this volume.
The islands’ residents are the custodians of something unique and special to the
rest of the world. It has been the honour of my career to play a small role in
advancing this new phase of discovery and collaboration.
SOMENTE AQUI! (ONLY HERE!)
Curator Emeritus of the California
Academy of Sciences, San Francisco,
CA, USA
Robert C. Drewes, PhD
Acknowledgements
This book is born of the shared dream of a group of researchers, conservationists,
and educators dedicated to the study and preservation of the biodiversity of the Gulf
of Guinea Oceanic Islands. A total of 87 contributors based in institutions in Portugal
(32), São Tomé and Príncipe (20), the United States of America (14), France (10),
United Kingdom (9), South Africa (3), Belgium (2), Gabon (2), Spain (2), Germany
(1), and the Netherlands (1) gave their time and dedication to put together the
26 chapters that comprise this book. The editors are deeply grateful for their
contributions, which were critical for the success, quality, and comprehensiveness
of this synthesis.
This synthesis is a direct result of sustained efforts in biodiversity research,
conservation, and outreach that have taken place in the oceanic islands of the Gulf
of Guinea over the last two decades. This new wave of work was only possible
thanks to the interest and full institutional and logistic support of the authorities of
São Tomé and Príncipe and of Equatorial Guinea. In São Tomé and Príncipe, this
includes foremost the Direcção Geral do Ambiente (Dept. of the Environment), the
Direcção de Florestas e Biodiversidade (Forestry and Biodiversity Dept.), the Ôbo
Natural Park (São Tomé, Príncipe), and the University of São Tomé e Príncipe. The
Regional Government of Príncipe has also been an important partner. In Equatorial
Guinea this work is consistently supported by UNGE (National University of
Equatorial Guinea) and INDEFOR-AP (National Institute of Forests and Protected
Areas). Non-governmental organizations and other partners have also provided key
support, including Associação Monte Pico (São Tomé), Fundação Príncipe
(Príncipe), the Portuguese School of São Tomé and Príncipe (São Tomé), and the
Bioko Biodiversity Protection Program (Equatorial Guinea). Most advances in the
knowledge of the biodiversity of this region were only made possible with vast
amounts of fieldwork, often in very challenging conditions. The success of this
endeavour relied on the expertise, enthusiasm, and hard work of many field assistants throughout the years. Many others have provided crucial help along the way for
different projects. These are specifically acknowledged in the respective chapters.
The quality of all chapters greatly improved with the input of numerous reviewers
who provided important comments, corrections, and suggestions. The editors are
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Acknowledgements
greatly indebted to Jason Ali, Aaron M. Bauer, Manuel Biscoito, David Blackburn,
Bernard Bourles, Robert Cameron, Mariana Carvalho, Jacob Cooper, Sónia Ferreira,
Betânia Ferreira-Airaud, José Manuel Grosso-Silva, Václav Gvoždík, Charles
Haddad, Roy Halling, Brian Huntley, Peter J. Jones, David H. Kavanaugh, Pete
Lowry, Gabriel Nève, Kevin Njabo, Francisco Roque de Oliveira, Michel Papazian,
Alison Peel, Graham Pierce, Peter Ryan, Brígida Rocha Pinto, Diego SantiagoAlarcon, Andreas Schmitz, Artur Serrano, Dinarte Teixeira, Manjula Tiwari, JeanFrançois Trape, Cristiana Vieira, Sara Vieira, Caroline Weir, and Peter Wirtz.
The editors are also indebted to the photographers who provided their spectacular
photos to illustrate the different chapters of this book, and many other scientific and
outreach projects over the last two decades. All of the photographs are credited and
acknowledged in the respective chapters.
Financial and logistic support was provided by CIBIO (Research Centre in
Biodiversity and Genetic Resources, University of Porto)—through the UNESCO
Chair “Life on Land” and the BIOPOLIS Association through the European Union’s
Horizon 2020 Research and Innovation Programme under the Grant Agreement
Number 857251, as well as by the Museu de História Natural e da Ciência (University of Porto). The Gulf of Guinea Research Program is a long-term partnership
between SUPERNOVA Technologies and CIBIO through the programme
BIOPOLIS. These acknowledgements are especially extended to the director of
CIBIO and BIOPOLIS Nuno Ferrand de Almeida for his strong support to this
project. We are especially grateful to the EU, the ECOFAC 6 Programme, and to
Birdlife International for funding the production of the Portuguese version of this
book. Fundação para a Ciência e a Tecnologia (FCT, Portugal) provided structural
funding to CIBIO (UIDB/50027/2021) and to cE3c (UID/BIA/00329/2021).
Finally, we thank Harini Devi, Lars Koerner, and Parthiban Gujilan Kannan of
Springer Nature (English Edition) and Jorge Reis-Sá of Arte e Ciência (Portuguese
Edition), for their consistent and professional support throughout the project.
Contents
1
Biodiversity in the Gulf of Guinea Oceanic Islands: A Synthesis . . .
Luis M. P. Ceríaco, Ricardo F. de Lima, Rayna C. Bell,
and Martim Melo
1
2
Physical Geography of the Gulf of Guinea Oceanic Islands . . . . . . .
Luis M. P. Ceríaco, Bruna S. Santos, Ricardo F. de Lima,
Rayna C. Bell, Sietze J. Norder, and Martim Melo
13
3
Classification, Distribution, and Biodiversity of Terrestrial
Ecosystems in the Gulf of Guinea Oceanic Islands . . . . . . . . . . . . .
Gilles Dauby, Tariq Stévart, Patricia Barberá, Laura Benitez,
Maria do Céu Madureira, Filipa C. Soares, Gaëlle Viennois,
and Ricardo F. de Lima
4
5
Territory, Economy, and Demographic Growth in São Tomé
and Príncipe: Anthropogenic Changes in Environment . . . . . . . . . .
Xavier Muñoz-Torrent, Ngouabi Tiny da Trindade,
and Signe Mikulane
The History of Biological Research in the Gulf of Guinea Oceanic
Islands . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Luis M. P. Ceríaco, Bruna S. Santos, Sofia B. Viegas, Jorge Paiva,
and Estrela Figueiredo
37
71
87
6
Biogeography and Evolution in the Oceanic Islands of the Gulf of
Guinea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 141
Martim Melo, Luis M. P. Ceríaco, and Rayna C. Bell
7
Species Ecology in the Gulf of Guinea Oceanic Islands: Distribution,
Habitat Preferences, Assemblages, and Interactions . . . . . . . . . . . . 171
Filipa C. Soares, Joana M. Hancock, Jorge M. Palmeirim,
Hugulay Albuquerque Maia, Tariq Stévart, and Ricardo F. de Lima
xv
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Contents
8
Fungi of São Tomé and Príncipe Islands: Basidiomycete
Mushrooms and Allies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 189
Dennis E. Desjardin and Brian A. Perry
9
The Bryophyte Flora of São Tomé and Príncipe
(Gulf of Guinea): Past, Present and Future . . . . . . . . . . . . . . . . . . . 217
César Garcia, Cecília Sérgio, and James R. Shevock
10
Diversity of the Vascular Plants of the Gulf of Guinea
Oceanic Islands . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 249
Tariq Stévart, Gilles Dauby, Davy U. Ikabanga, Olivier Lachenaud,
Patricia Barberá, Faustino de Oliveira, Laura Benitez,
and Maria do Céu Madureira
11
A Checklist of the Arachnids from the Gulf of Guinea Islands
(Excluding Ticks and Mites) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 273
Sarah C. Crews and Lauren A. Esposito
12
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón . . . . 295
Gabriel Nève, Patrick Bonneau, Alain Coache, Artur Serrano,
and Gérard Filippi
13
Butterflies and Skippers (Lepidoptera: Papilionoidea)
of the Gulf of Guinea Oceanic Islands . . . . . . . . . . . . . . . . . . . . . . . 349
Luís F. Mendes and António Bivar-de-Sousa
14
Dragonflies and Damselflies (Odonata) of Príncipe,
São Tomé, and Annobón . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 371
Klaas-Douwe B. Dijkstra, Russell B. Tate, and Michel Papazian
15
Diversity and Distribution of the Arthropod Vectors
of the Gulf of Guinea Oceanic Islands . . . . . . . . . . . . . . . . . . . . . . . 383
Claire Loiseau, Rafael Gutiérrez-López, Bruno Mathieu,
Boris K. Makanga, Christophe Paupy, Nil Rahola,
and Anthony J. Cornel
16
Terrestrial Mollusca of the Gulf of Guinea Oceanic Islands . . . . . . 407
Martina Panisi, Ricardo F. de Lima, Jezreel do C. Lima,
Yodiney dos Santos, Frazer Sinclair, Leonor Tavares,
and David T. Holyoak
17
The Fishes of the Gulf of Guinea Oceanic Islands . . . . . . . . . . . . . . 431
Luis M. da Costa, Hugulay Albuquerque Maia,
and Armando J. Almeida
18
The Amphibians of the Gulf of Guinea Oceanic Islands . . . . . . . . . 479
Rayna C. Bell, Luis M. P. Ceríaco, Lauren A. Scheinberg,
and Robert C. Drewes
Contents
xvii
19
The Terrestrial Reptiles of the Gulf of Guinea Oceanic Islands . . . . 505
Luis M. P. Ceríaco, Mariana P. Marques, Rayna C. Bell,
and Aaron M. Bauer
20
The Sea Turtles of São Tomé and Príncipe: Diversity, Distribution,
and Conservation Status . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 535
Betania Ferreira-Airaud, Vanessa Schmitt, Sara Vieira,
Manuel Jorge de Carvalho do Rio, Elisio Neto, and Jaconias Pereira
21
The Avifauna of the Gulf of Guinea Oceanic Islands . . . . . . . . . . . . 555
Martim Melo, Peter J. Jones, and Ricardo F. de Lima
22
Current Knowledge and Conservation of the Wild Mammals of the
Gulf of Guinea Oceanic Islands . . . . . . . . . . . . . . . . . . . . . . . . . . . . 593
Ana Rainho, Christoph F. J. Meyer, Sólveig Thorsteinsdóttir,
Javier Juste, and Jorge M. Palmeirim
23
Cetaceans of São Tomé and Príncipe . . . . . . . . . . . . . . . . . . . . . . . . 621
Inês Carvalho, Andreia Pereira, Francisco Martinho, Nina Vieira,
Cristina Brito, Márcio Guedes, and Bastien Loloum
24
Biodiversity Conservation in the Gulf of Guinea Oceanic Islands:
Recent Progress, Ongoing Challenges, and Future Directions . . . . . 643
Ricardo F. de Lima, Jean-Baptiste Deffontaines, Luísa Madruga,
Estrela Matilde, Ana Nuno, and Sara Vieira
25
Environmental Education in São Tomé and Príncipe: The Challenges
of Owning a Unique Biodiversity . . . . . . . . . . . . . . . . . . . . . . . . . . . 671
Roberta Ayres, José Carlos Aragão, Mariana Carvalho,
Francisco Gouveia, Estrela Matilde, Martina Panisi,
Jormicilesa Sacramento, and Vanessa Schmitt
26
A Thriving Future for the Gulf of Guinea Oceanic Islands . . . . . . . 691
Rayna C. Bell, Luis M. P. Ceríaco, Ricardo F. de Lima,
and Martim Melo
Contributors
Armando J. Almeida Centro de Ciências do Mar e do Ambiente (MARE),
Laboratório Marítimo da Guia, Faculdade de Ciências, Universidade de Lisboa,
Cascais, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa,
Lisbon, Portugal
José Carlos Aragão Projeto Escola +, São Tomé, São Tomé and Príncipe
Roberta Ayres Gulf of Guinea Project, Department of Herpetology, Institute for
Biodiversity Science and Sustainability, California Academy of Sciences, San
Francisco, CA, USA
Patricia Barberá Missouri Botanical Garden, Africa & Madagascar Department,
St. Louis, MI, USA
Aaron M. Bauer Department of Biology and Center for Biodiversity and Ecosystem Stewardship, Villanova University, Villanova, PA, USA
Rayna C. Bell Department of Herpetology, Institute for Biodiversity Science and
Sustainability, California Academy of Sciences, San Francisco, CA, USA
Laura Benitez Fauna & Flora International, Cambridge, UK
Fundação Príncipe, Santo António, Príncipe, São Tomé and Príncipe
António Bívar-de-Sousa Departamento de Zoologia e Antropologia (Museu
Bocage), Museu Nacional de História Natural e da Ciência, Universidade de Lisboa,
Lisbon, Portugal
Sociedade Portuguesa de Entomologia, Lisbon, Portugal
Patrick Bonneau OPIE-Provence-Alpes-du-Sud, Muséum d’Histoire Naturelle de
Marseille, Marseille, France
Cristina Brito CHAM – Centro de Humanidades, FCSH, Universidade NOVA de
Lisboa, Lisbon, Portugal
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Contributors
Inês Carvalho IGC, Instituto Gulbenkian de Ciência, Population and Conservation
Genetics Group, Oeiras, Portugal
APCM, Associação para as Ciências do Mar, Lisbon, Portugal
Mariana Carvalho Tropical Biology Association, Cambridge, UK
Luis M. P. Ceríaco Museu de História Natural e da Ciência da Universidade do
Porto, Porto, Portugal
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO
Laboratório Associado, Universidade do Porto, Vairão, Portugal
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, Vairão, Portugal
Departamento de Zoologia e Antropologia (Museu Bocage), Museu Nacional de
História Natural e da Ciência, Universidade de Lisboa, Lisbon, Portugal
Alain Coache Impasse de l’Artémise, La Brillanne, France
Anthony J. Cornel Mosquito Control and Research Laboratory, Department of
Entomology and Nematology, and Vector Genetics Laboratory, Department of
Pathology, Microbiology and Immunology, University of California, Davis, Parlier,
CA, USA
Sarah C. Crews Department of Entomology, Institute for Biodiversity Science and
Sustainability, California Academy of Sciences, San Francisco, CA, USA
Luis M. da Costa Centro de Ciências do Mar e do Ambiente (MARE), Faculdade
de Ciências, Universidade de Lisboa, Lisbon, Portugal
Departamento de Zoologia e Antropologia (Museu Bocage), Museu Nacional de
História Natural e da Ciência, Universidade de Lisboa, Lisbon, Portugal
Royal Museum for Central Africa (RMCA), Vertebrates Section, Ichthyology,
Tervuren, Belgium
Ngouabi Tiny da Trindade Instituto Nacional de Estatística de São Tomé e
Príncipe, São Tomé, São Tomé and Príncipe
Gilles Dauby AMAP, botAnique et Modélisation de l’Architecture des Plantes et
des végétations, Université Montpellier, CIRAD, CNRS, INRAE, IRD, Montpellier,
France
Ricardo F. de Lima Centre for Ecology, Evolution and Environmental Changes
(cE3c), Faculdade de Ciêncas, Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa,
Lisbon, Portugal
Gulf of Guinea Biodiversity Centre, São Tomé, São Tomé and Príncipe
Faustino de Oliveira Projeto TRI, Direção das Florestas e da Biodiversidade, São
Tomé, São Tomé and Príncipe
Herbário Nacional de São Tomé e Príncipe (STPH), Centro de Investigação
Agronómica e Tecnológica, Alto Potó, São Tomé and Príncipe
Jean-Baptiste Deffontaines BirdLife International, Cambridge, UK
Contributors
xxi
Dennis E. Desjardin Department of Biology, San Francisco State University, San
Francisco, CA, USA
Klaas-Douwe B. Dijkstra Naturalis Biodiversity Center, Leiden, The Netherlands
Manuel Jorge de Carvalho do Rio ONG MARAPA, São Tomé, São Tomé and
Príncipe
Yodiney dos Santos Fundação Príncipe, Santo António, Príncipe, São Tomé and
Príncipe
Robert C. Drewes Department of Herpetology, Institute for Biodiversity Science
and Sustainability, California Academy of Sciences, San Francisco, CA, USA
Lauren A. Esposito Department of Entomology, Institute for Biodiversity Science
and Sustainability, California Academy of Sciences, San Francisco, CA, USA
Betania Ferreira-Airaud Associação Programa Tatô, Barão de São João, Portugal
Estrela Figueiredo Department of Botany, Nelson Mandela University, Gqeberha
[Port Elizabeth], South Africa
Gérard Filippi MICROLAND, Maison de la vie associative, Le Ligoures, Aix-enProvence, France
César Garcia Museu Nacional de História Natural e da Ciência, Universidade de
Lisboa, Lisbon, Portugal
Centre for Ecology, Evolution and Environmental Changes (cE3c), CHANGE
Associated Laboratory - Global Change and Sustainability Institute, Faculdade de
Ciências, Universidade de Lisboa, Lisbon, Portugal
Francisco Gouveia Arribada Initiative, Cheshire, UK
Márcio Guedes ONG MARAPA, São Tomé, São Tomé and Príncipe
Rafael Gutiérrez-López CIBIO, Centro de Investigação em Biodiversidade e
Recursos Genéticos, InBIO Laboratório Associado, Universidade do Porto, Vairão,
Portugal
Joana Madeira Hancock Centre for Ecology, Evolution and Environmental
Changes (cE3c), Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal
Centro de Ciências do Mar e do Ambiente (MARE), ISPA, Instituto Universitário de
Ciências Psicológicas, Sociais e da Vida, Lisbon, Portugal
David T. Holyoak Quinta da Cachopa, Cabeçudo, Portugal
Davy U. Ikabanga Missouri Botanical Garden, Africa & Madagascar Department,
St. Louis, MI, USA
Laboratoire d’Ecologie Végétale et de Biosystématique, Département de Biologie,
Faculté des Sciences, Université des Sciences et Techniques de Masuku, Franceville,
Gabon
Peter J. Jones Chirnside, Scotland
xxii
Contributors
Javier Juste Department of Evolutionary Biology, Estación Biológica de Doñana
(CSIC), Seville, Spain
CIBER de Epidemiología y Salud Pública. Instituto de Salud Carlos III, Madrid,
Spain
Olivier Lachenaud Meise Botanic Garden, Domein van Bouchout, Meise,
Belgium
Jezreel do C. Lima Associação Monte Pico, Monte Café, São Tomé and Príncipe
Claire Loiseau CIBIO, Centro de Investigação em Biodiversidade e Recursos
Genéticos, InBIO Laboratório Associado, Universidade do Porto, Vairão, Portugal
CEFE, Université de Montpellier, Centre National de la Recherche Scientifique
(CNRS), Montpellier, France
Bastien Loloum ONG MARAPA, São Tomé, São Tomé and Príncipe
Luisa Madruga Fauna & Flora International, The David Attenborough Building,
Pembroke Street, Cambridge, UK
Fundação Príncipe, Santo António, Príncipe, São Tomé and Príncipe
Maria do Céu Madureira Centre for Functional Ecology, Departamento de
Ciências da Vida, Universidade de Coimbra, Coimbra, Portugal
Hugulay Albuquerque Maia Department of Natural Sciences, Life and Environment, Universidade de São Tomé e Príncipe, São Tomé, São Tomé and Príncipe
Boris K. Makanga Institut de Recherche en Écologie Tropicale/CENAREST,
Libreville, Gabon
Mariana P. Marques Departamento de Zoologia e Antropologia (Museu Bocage),
Museu Nacional de História Natural e da Ciência, Universidade de Lisboa, Lisbon,
Portugal
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO
Laboratório Associado, Universidade do Porto, Vairão, Portugal
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO, Vairão,
Portugal
Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Porto,
Portugal
Francisco Martinho APCM, Associação para as Ciências do Mar, Lisbon,
Portugal
Ecco Ocean, Lisbon, Portugal
Bruno Mathieu Université de Strasbourg, DIHP, Strasbourg, France
Estrela Matilde Fundação Príncipe, Santo António, Príncipe, São Tomé and
Príncipe
Martim Melo Museu de História Natural e da Ciência da Universidade do Porto,
Porto, Portugal
Contributors
xxiii
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO
Laboratório Associado, Universidade do Porto, Vairão, Portugal
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO, Vairão,
Portugal
FitzPatrick Institute of African Ornithology, University of Cape Town, Rondebosch,
South Africa
Luis F. Mendes Departamento de Zoologia e Antropologia (Museu Bocage),
Museu Nacional de História Natural e da Ciência, Universidade de Lisboa, Lisbon,
Portugal
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO
Laboratório Associado, Universidade do Porto, Vairão, Portugal
Christoph F. J. Meyer Environmental Research and Innovation Centre, School of
Science, Engineering and Environment, University of Salford, Salford, UK
Signe Mikulane Institute for Building Information Modeling, Interdisciplinary
Institute of Architecture, Civil and Environmental Engineering and Geodesy,
Bochum University of Applied Sciences, Bochum, Germany
Xavier Muñoz-Torrent Servei d’Estudis i Observatori de la Ciutat de Terrassa,
Terrassa, Catalonia, Spain
Associação Caué—Amigos de São Tomé e Príncipe, Barcelona, Catalonia, Spain
Elísio Neto ONG MARAPA, São Tomé, São Tomé and Príncipe
Gabriel Nève Institut Méditerranéen de Biodiversité et d’Ecologie (IMBE), Aix
Marseille University, Centre National de la Recherche Scientifique (CNRS), Institut
de Recherche pour le Développement (IRD), Avignon University, Marseille, France
Sietze J. Norder Copernicus Institute of Sustainable Development, Environmental
Science Group, Utrecht University, Utrecht, The Netherlands
Ana Nuno Interdisciplinary Centre of Social Sciences (CICS.NOVA), School of
Social Sciences and Humanities, NOVA University Lisboa, Lisbon, Portugal
Centre for Ecology and Conservation, College of Life and Environmental Sciences,
University of Exeter, Cornwall, UK
Jorge Paiva Centre for Functional Ecology, Departamento de Ciências da Vida,
Universidade de Coimbra, Coimbra, Portugal
Jorge Manuel Palmeirim Centre for Ecology, Evolution and Environmental
Changes (cE3c), Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa,
Lisbon, Portugal
Martina Panisi Centre for Ecology, Evolution and Environmental Changes (cE3c),
Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa,
Lisbon, Portugal
Alisei Onlus NGO, São Tomé, São Tomé and Príncipe
xxiv
Contributors
Christophe Paupy MiVEGEC, Université de Montpellier, Institut de Recherche
pour le Développement, Centre National de la Recherche Scientifique (CNRS),
Montpellier, France
Andreia Pereira APCM, Associação para as Ciências do Mar, Lisbon, Portugal
Instituto Dom Luiz, Faculdade de Ciências da Universidade de Lisboa, Lisbon,
Portugal
Jaconias Pereira Fundação Príncipe, Santo António, Príncipe, São Tomé and
Príncipe
Brian A. Perry Department of Biological Sciences, California State University
East Bay, Hayward, CA, USA
Nil Rahola MiVEGEC, Université de Montpellier, Institut de Recherche pour le
Développement, Centre National de la Recherche Scientifique (CNRS), Montpellier,
France
Ana Rainho Centre for Ecology, Evolution and Environmental Changes (cE3c),
Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa,
Lisbon, Portugal
Jormicilesa Sacramento Fundação Príncipe, Santo António, Príncipe, São Tomé
and Príncipe
Bruna S. Santos CIBIO, Centro de Investigação em Biodiversidade e Recursos
Genéticos, InBIO Laboratório Associado, Universidade do Porto, Vairão, Portugal
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO, Vairão,
Portugal
Departamento de Biologia, Faculdade de Ciências da Universidade do Porto, Porto,
Portugal
Museu de História Natural e da Ciência da Universidade do Porto, Porto, Portugal
Lauren A. Scheinberg Department of Herpetology, Institute for Biodiversity Science and Sustainability, California Academy of Sciences, San Francisco, CA, USA
Vanessa Schmitt Fundação Príncipe, Santo António, Príncipe, São Tomé and
Príncipe
Cecília Sérgio Museu Nacional de História Natural e da Ciência, Universidade de
Lisboa, Lisbon, Portugal
Centre for Ecology, Evolution and Environmental Changes (cE3c), CHANGE
Associated Laboratory - Global Change and Sustainability Institute, Faculdade de
Ciências, Universidade de Lisboa, Lisbon, Portugal
Artur Serrano Centre for Ecology, Evolution and Environmental Changes (cE3c),
Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa,
Lisbon, Portugal
Contributors
xxv
James R. Shevock Department of Botany, Institute for Biodiversity Science and
Sustainability, California Academy of Sciences, San Francisco, CA, USA
Frazer Sinclair Fundação Príncipe, Santo António, Príncipe, São Tomé and
Príncipe
Fauna & Flora International, Cambridge, UK
Filipa Coutinho Soares Centre for Ecology, Evolution and Environmental
Changes (cE3c), Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa,
Lisbon, Portugal
Tariq Stévart Missouri Botanical Garden, Africa & Madagascar Department, St.
Louis, MI, USA
Herbarium et Bibliothèque de Botanique africaine, Université Libre de Bruxelles,
Brussels, Belgium
Meise Botanic Garden, Domein van Bouchout, Belgium
Russell B. Tate HCV Africa, Johannesburg, South Africa
Leonor Tavares Departamento de Biologia Animal, Faculdade de Ciências,
Universidade de Lisboa, Lisbon, Portugal
Sólveig Thorsteinsdóttir Centre for Ecology, Evolution and Environmental
Changes (cE3c), Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa,
Lisbon, Portugal
Sofia B. Viegas Centro Interuniversitário de História das Ciências e da Tecnologia,
Faculdade de Ciência, Universidade de Lisboa, Lisbon, Portugal
Museu de História Natural e da Ciência da Universidade do Porto, Porto, Portugal
Nina Vieira APCM, Associação para as Ciências do Mar, Lisbon, Portugal
CHAM, Centro de Humanidades, FCSH, Universidade NOVA de Lisboa, Lisbon,
Portugal
Sara Vieira Associação Programa Tatô, São Tomé, São Tomé and Príncipe
Gaëlle Viennois AMAP, botAnique et Modélisation de l’Architecture des Plantes
et des végétations, Université Montpellier, CIRAD, CNRS, INRAE, IRD, Montpellier, France
Chapter 1
Biodiversity in the Gulf of Guinea Oceanic
Islands: A Synthesis
Luis M. P. Ceríaco, Ricardo F. de Lima, Rayna C. Bell, and Martim Melo
Abstract The Gulf of Guinea oceanic islands (Príncipe, São Tomé, and Annobón)
are among the most endemic-rich regions of the planet. Historical scientific studies
of the islands’ unique biodiversity are scattered in a variety of publications, many of
which are difficult to access. More recently, there has been a growing interest in the
islands, which is reflected in a burst of new studies, reports, and ongoing projects.
L. M. P. Ceríaco (*)
Museu de História Natural e da Ciência da Universidade do Porto, Porto, Portugal
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório
Associado, Universidade do Porto, Vairão, Portugal
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, Vairão, Portugal
Departamento de Zoologia e Antropologia (Museu Bocage), Museu Nacional de História
Natural e da Ciência, Universidade de Lisboa, Lisbon, Portugal
e-mail: lmceriaco@mhnc.up.pt
R. F. de Lima
Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências,
Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon,
Portugal
Gulf of Guinea Biodiversity Centre, São Tomé, Sao Tome and Principe
R. C. Bell
Department of Herpetology, Institute for Biodiversity Science and Sustainability, California
Academy of Sciences, San Francisco, CA, USA
M. Melo
Museu de História Natural e da Ciência da Universidade do Porto, Porto, Portugal
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório
Associado, Universidade do Porto, Vairão, Portugal
FitzPatrick Institute of African Ornithology, University of Cape Town, Rondebosch,
South Africa
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, Vairão, Portugal
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_1
1
2
L. M. P. Ceríaco et al.
Here we aim to provide an updated and comprehensive synthesis, covering all the
key information and references on the biodiversity of these islands. The goal of the
book is to be a comprehensive reference for students, researchers, and conservationists dedicated to the study and preservation of this unique biodiversity. It also intends
to serve as a basis for local stakeholders to make informed decisions, namely
regarding conservation actions. The book is divided into three main sections: (1) a
general overview of the islands and their biodiversity, including aspects of natural
and human history (six chapters); (2) detailed accounts on different taxonomic
groups (16 chapters); and (3) the conservation, environmental education, and
research challenges that lie ahead (three chapters).
Keywords Biogeography · Conservation · Ecology · Endemics · History of science ·
Taxonomy
Introduction
É realmente notável a fauna da ilha de S. Tomé
e mais notável é ainda a diferença que faz da
sua irmã o Príncipe. No Príncipe os animais
que se encontram são em grande parte do
continente, enquanto que em S. Tome há uma
forma especial com bastantes espécies que
julgo serem privativas da ilha. A distancia que
há entre as duas ilhas é apenas de 90 milhas
mas o cabo submarino lançado tem 120 milhas
devido às ondulações de terreno no fundo do
mar. Com relação à Atlântida, não serão as
ilhas do Golpho da Guiné e mesmo as
Canarias, Cabo verde, Stª Helena, Assumpção
etc, restos d’esse grande continente?
The fauna of S. Tome Island is truly
remarkable, and it is even more remarkable
the difference to its sister island of Príncipe.
The animals that are found in Príncipe are
mostly from the continent, while in S. Tomé
there is a special form with several species that
I believe are private to the island. The distance
between the two islands is only 90 miles but the
submarine cable has 120 miles due to the
ruggedness of the sea floor. Regarding Atlantis, aren’t the islands of the Gulf of Guinea,
and even the Canaries, Cabo Verde,
St. Helena, Ascension, etc., the remains of that
large continent?
Francisco Newton, letter from São Tomé Island
23 January 1887
The Portuguese explorer Francisco Newton was one of the first naturalists to
dedicate almost one decade to the study of the outstanding diversity of the Gulf of
Guinea oceanic islands. The collections he made, in what was largely unexplored
territory for science, allowed the description of dozens of new species and began to
reveal intriguing biogeographic patterns. Gazing at the species he was collecting,
many of which would turn out to be endemic, the naturalist found them so spectacular that he dared to suggest the islands could be the remains of the mythical
continent of Atlantis. While this suggestion lacks any scientific basis, it is a perfect
example of the sense of awe that the biodiversity of the Gulf of Guinea oceanic
islands imparts to any naturalist who visits them. Although Newton’s “Atlantis
hypothesis” did not gain traction, other comparisons between these islands and
other iconic places around the world have since been proposed. A quick search
about these islands on the Internet, newspapers, popular magazines, or tourism
advertisements will likely find them labeled as “a paradise on Earth” or “the
Galapagos of Africa.” The Galapagos archipelago in the Pacific Ocean is one of
1
Biodiversity in the Gulf of Guinea Oceanic Islands: A Synthesis
3
the most famous group of islands for naturalists and wildlife enthusiasts, especially
due to their role in British naturalist Charles Darwin’s (1809–1882) genesis of the
theory of evolution through natural selection. The observation of the diverse environments, unique species, and incredible adaptations of the Galapagos fauna and
flora were fundamental to Darwin’s growing body of evidence, forever linking the
Galapagos to the theory of evolution. Darwin never set foot in the Gulf of Guinea but
the type of evidence he found in the Galapagos is also abundantly available in these
oceanic islands. Thus, the label “the Galapagos of Africa” is certainly fitting.
Since their emergence millions of years ago, due to the activity of the Cameroon
Volcanic Line, the islands of Príncipe, São Tomé, and Annobón have been isolated
from the African continent. Their prolonged isolation and complex geological
history led to the evolution of unique species that sustain distinctive ecosystems.
Humans arrived approximately 500 years ago, when Portuguese navigators found
these uninhabited islands teeming with biodiversity. Since then, human impact on
the islands has increased considerably, with lasting impacts to both the landscape
and biodiversity. The human impact on the biota has been considerable, and a
number of species and ecosystems are now threatened.
The islands’ unique biodiversity has attracted several generations of researchers
working in a wide diversity of taxonomic groups and biological topics. Biodiversity
research in the region received a renewed focus when in June 1993 the Jersey
Wildlife Preservation in Jersey (UK) organized a workshop on the biodiversity of
the Gulf of Guinea islands. The aim of this meeting was to synthesize the data
available at the time, and led to the establishment of a network of experts: the Gulf of
Guinea Conservation Group. Managed by Angus Gascoigne (1962–2012), a passionate British amateur naturalist who was living in São Tomé, it supported many
scientific endeavors. The results of the meeting were published in a special edition of
the journal Biodiversity and Conservation (Juste and Fa 1994). This issue became
the major reference for the biodiversity of the islands for more than two decades,
serving as the main source of data and theoretical support for the new generation of
island biologists and conservationists, many of whom are contributors to this
volume.
On October 16, 2020, a virtual meeting brought together several dozen scientists,
conservationists, educators, and local stakeholders, all with shared interests in
the biodiversity of the Gulf of Guinea oceanic islands. This meeting aimed to set
the foundation for the Gulf of Guinea Biodiversity Center, a collaboration to satisfy
the urgent needs of an ever-growing community to have an institution fully dedicated to the biodiversity of the islands. This new generation is dedicated to surveying
the islands to document biodiversity, to understand and mitigate the current threats,
and to raise local and global awareness for this unique natural heritage. This book
aims to represent this new wave of research and to set the stage for the next phase of
biodiversity research and conservation.
4
L. M. P. Ceríaco et al.
Historical Biodiversity Syntheses
Prior to the 1994 special issue of Biodiversity and Conservation (Jones 1994), efforts
to synthesize knowledge on the biodiversity of the Gulf of Guinea islands were few
and far between. Many tended to be taxonomically and geographically focused. In
the early twentieth century, the Portuguese zoologist José Vicente Barbosa du
Bocage (1823–1907) was the first to produce a synthesis on the land vertebrates of
the Gulf of Guinea islands, based on the knowledge that had been amassed during
the second half of the nineteenth century (Bocage 1903, 1905). According to him,
the list of species for Príncipe included four mammals, 43 birds, ten reptiles, and two
frogs, whereas that of São Tomé hosted 12 mammals, 64 birds, 11 reptiles, and five
amphibians. For Annobón, the species list of Bocage (1903) recorded only two
mammals, 14 birds, five reptiles, and no amphibians. Similar to Bocage’s checklists
of vertebrate fauna, the British botanist Arthur Wallis Exell (1901–1993) was the
first to publish a checklist of the vascular flora of the Gulf of Guinea oceanic islands
(Exell 1944). He benefited from the work of previous researchers, such as Júlio
Henriques (1838–1928), former director of the herbarium of the University of
Coimbra, providing an extensive series of publications (Exell 1956, 1958, 1959,
1963, 1973). By 1973 he had recorded 810 angiosperms for the islands (539 dicotyledons and 271 monocotyledons), of which 601 occurred on São Tomé, 314 on
Príncipe, and 208 on Annobón (Exell 1973). Some taxonomic groups have received
special attention in comparison to others. Birds, in particular, received regular
syntheses through the years (Bocage 1889; Amadon 1953; Naurois 1994; Jones
and Tye 2006; Lima and Melo 2021).
While many syntheses have been taxonomically oriented (vertebrates, angiosperms), others have focused on single islands. The work of Júlio Henriques on
the natural history and agriculture of São Tomé (Henriques 1917) is a perfect
example: across almost 300 pages, this monographic work aimed to cover all the
aspects of the natural history of the island, listing its fauna, flora, geology, topography, agriculture, and even the organization of the local society. Other attempts to
compile information on the biodiversity of the islands took place later on, including
the bibliographic compilation of “pure and applied botany” of São Tomé and
Príncipe by Fernandes (1982), and that on the fauna of the three oceanic islands
by Gascoigne (1993, 1996).
Continuously updating species lists is vital for refining taxonomy, identifying
knowledge gaps, recording changes in species composition, studying community
ecology and biogeography, understanding ecosystem function, and supporting conservation decisions. Jones (1994) presented an updated overview of the number of
vertebrate species and endemics on each island (Table 1.1). According to this
compilation, the Príncipe species list of terrestrial vertebrates included four mammals, 35 birds, eight reptiles, and three frogs, that of São Tomé nine mammals,
49 birds, 14 reptiles, and six amphibians, and that of Annobón two mammals, nine
birds, seven reptiles, and no amphibians (Table 1.1). Regarding plants, numbers
would not be updated until the much more recent publication of bryophyte (Sérgio
1
Amphibia
Reptilia
Aves
Mammalia
All
Island
Príncipe
São Tomé
Annobón
Total
Príncipe
São Tomé
Annobón
Total
Príncipe
São Tomé
Annobón
Total
Príncipe
São Tomé
Annobón
Total
Príncipe
São Tomé
Annobón
Total
Previous
Total
3
6
0
7
8
14
7
35
49
9
9
16
55
85
Current
3
6
0
9
14
12
8
28
32
50
11
66
12
17
4
19
61
85
23
122
Previous
Current
Single-island endemics
1 (33)
3 (100)
4 (67)
6 (100)
0
0
5 (71)
9 (100)
2 (25)
8 (57)
1 (7)
7 (58)
2 (29)
6 (75)
5
21 (75)
6 (17)
8 (25)
15 (31)
17 (34)
2 (22)
1 (9)
23
26 (39)
1 (11)
2 (17)
3 (19)
5 (29)
0
0 (0)
4
7 (37)
10 (18)
21 (34)
23 (27)
35 (41)
4
7 (30)
37
63 (52)
Previous
All endemics
3 (100)
6 (100)
0
7 (100)
7 (88)
6 (43)
3 (43)
10
11 (31)
20 (41)
3 (33)
28
1 (11)
3 (19)
0
4
22 (40)
35 (41)
6
49
Current
3 (100)
6 (100)
0
9 (100)
10 (71)
9 (75)
6 (75)
23 (82)
11 (34)
20 (40)
2 (18)
29 (44)
2 (17)
5 (29)
0 (0)
7 (37)
26 (43)
40 (47)
8 (35)
68 (56)
Current
Introduced
0
0
0
0
2 (14)
2 (17)
2 (25)
3 (11)
5 (16)
17 (34)
3 (27)
17 (26)
5 (42)
6 (35)
2 (50)
6 (32)
12 (20)
25 (29)
7 (30)
26 (21)
Biodiversity in the Gulf of Guinea Oceanic Islands: A Synthesis
Table 1.1 Comparison between confirmed extant resident terrestrial vertebrates since the previous synthesis (Jones 1994), considering all species, single-island
endemics, and all endemics. The percentage of endemic species is shown in parenthesis. The number of species currently thought to be introduced is shown in
the last column. A few cells are blank because those figures were not available in the previous synthesis
5
6
L. M. P. Ceríaco et al.
and Gargia 2011), fern and lycophyte (Figueiredo 2002; Klopper and Figueiredo
2013), and angiosperm checklists (Figueiredo et al. 2011). There are noticeable
differences in the number of species and endemics for taxa that have multiple
checklists, reflecting the development of knowledge of the islands’ biodiversity
over the last century. New species continue to be added every year, even among
the best studied groups, representing both species that are new to science and just
newly recorded on the islands. Nevertheless, systematic and well-curated species
checklists are still the exception for most taxa in the Gulf of Guinea oceanic islands.
For many groups, notably terrestrial and marine invertebrates, there are still no
comprehensive species checklists, or they were first published recently, highlighting
how little is still known about the biodiversity of the islands (Lima 2016).
A New Synthesis
The outputs of the long history of research in the oceanic islands of the Gulf of
Guinea are scattered in hundreds of publications—scientific papers, reports, and
books. Most works published since the late eighteenth century to the present day are
very specific, focusing on few taxa and on a single island, or even a single species
and particular regions of an island. Publications are available in several different
languages—Portuguese, Spanish, English, French, German, Italian, Latin,
Russian—and formats—from books to peer-review scientific journals, theses,
unpublished reports, and more recently also in non-printed media, such as online
images, audio, and video. Access to many historical works has greatly improved in
recent years, especially due to important online platforms, such as the Biodiversity
Heritage Library (Gwinn and Constance 2009). However, this immense diversity of
sources also makes it challenging to gain a complete and updated view on the
biodiversity of these islands. Similarly, thousands of scientific specimens are held
in natural history collections around the world, providing the baseline to our present
knowledge and enabling exciting new findings and research. Many of these collections have not been included in recent studies and some have only recently been
rehabilitated and once more made accessible to the scientific community (e.g.,
Monteiro et al. 2016; Ceríaco et al. 2021). For such a small area, the Gulf of Guinea
oceanic islands may be one of the most intensively studied parts of Africa (e.g.,
Droissart et al. 2018). However, most of the scientific output and associated data are
not synthesized or readily available.
This book attempts to compile the key information and references regarding the
past and current knowledge on the biodiversity of the Gulf of Guinea oceanic
islands. The goal is to be a comprehensive reference for students, researchers, and
conservationists dedicated to the study and preservation of this unique biodiversity.
It also intends to serve as a basis for local stakeholders to make informed decisions,
namely regarding conservation actions. Above all, it is an act of celebration of the
scientific achievements of several generations of biologists and conservationists, a
1
Biodiversity in the Gulf of Guinea Oceanic Islands: A Synthesis
7
manifest in support of the astonishing biodiversity of these islands, and a plea for its
conservation.
Book Structure
The book is divided into three main sections: (1) a general overview of the islands
and their biodiversity, including aspects of natural and human history (six chapters);
(2) detailed accounts on different taxonomic groups (16 chapters); and (3) the
conservation, environmental education, and research challenges that lie ahead
(three chapters).
Section one starts with an outline of the physical geography, geological history,
climate, and sea level evolution of the study area, providing also its political
boundaries and administrative divisions (Chap. 2; Ceríaco et al. 2022a). This is
followed by a revision of the classification and cartography of the terrestrial ecosystems (Chap. 3; Dauby et al. 2022). Chapter 4 (Muñoz-Torrent et al. 2022) analyzes
the five centuries of human presence on the better-known island of São Tomé,
presenting demographic trends, cultural heritage, and how the history of the main
economic activities has impacted biodiversity. Chapter 5 (Ceríaco et al. 2022b)
reviews the history of scientific research, from mid-eighteenth century to the
twenty-first century. The fascinating evolutionary patterns that shaped the biodiversity of the “Galapagos of Africa” are presented in Chap. 6 (Melo et al. 2022a). In
Chap. 7 (Soares et al. 2022), our current understanding of island species ecology is
synthesized, including information about species distributions, habitat preferences,
species assemblages, and the interactions that maintain functioning ecosystems.
The second section constitutes the bulk of the book and corresponds to the
taxonomic chapters. The level of detail varies between chapters, mostly reflecting
disparities in knowledge across taxonomic groups. However, all chapters have a
similar structure, including an introduction to the group, a brief review of the history
of research on the islands, an account of the group’s diversity and endemism, an
updated checklist, and a section on conservation. Most of these chapters also
highlight important areas for future research.
Chapter 8 (Desjardin and Perry 2022) reports 260 species of mushrooms and
allies of the Agaricomycetes lineages of the Basidiomycota in São Tomé and
Príncipe. These correspond to 109 genera, 51 families, and 13 orders, and given
how little scientific attention this group has received, species richness will likely
increase with future work. Chapter 9 (Garcia et al. 2022) provides a review of the
bryophytes of São Tomé and Príncipe, based on historical herbarium data
complemented by the results of recent fieldwork. A preliminary list of 299 taxa
(128 mosses, 171 liverworts and hornworts) is provided, and the authors note that
several species likely remain undescribed or at least undocumented. Chapter 10
(Stévart et al. 2022) presents an updated checklist of vascular plants, combining data
from historical material and bibliographic references with extensive new field
surveys conducted since 2017. The current number of vascular plants includes
8
L. M. P. Ceríaco et al.
1285 taxa, with 164 endemics, of which at least 18 are new to science. A report on
medicinal plants is also provided.
Six chapters focus on invertebrate groups. Chapter 11 (Crews and Esposito 2022)
explores the diverse and little-known arachnid fauna of São Tomé and Príncipe,
which includes 266 recorded species of six different orders. Chapter 12 (Nève et al.
2022) provides a first checklist for the beetles of the three oceanic islands, listing
403 species, of which 190 are endemic. The butterflies and skippers (Lepidoptera:
Papilionoidea) are reviewed in Chap. 13 (Mendes and Bivar-de-Sousa 2022), with
91 confirmed taxa, and extensive discussion resolving previous doubtful records.
Chapter 14 (Dijkstra and Tate 2022) notes the impoverished dragonfly and damselfly
fauna of the islands, which includes only 22 confirmed records and one endemic
species, from Príncipe. Chapter 15 (Loiseau et al. 2022) reviews the arthropod
species that can act as vectors of diseases. Given the particularity of this group,
the structure of this chapter is slightly different but its scientific relevance is
undisputable due to the public health implications. The chapter also provides
important insights into species interactions, and underscores the possibility of new
vector-borne diseases arriving on the islands. Chapter 16 (Panisi et al. 2022) deals
with the 96 species of land gastropods, of which 62 are endemic, providing new
insights on the ecology, biogeography, and conservation of these species, including
the famous endemic giant land snail Archachatina bicarinata Bruguière, 1792.
Regarding vertebrates, there are four taxonomic chapters for terrestrial groups
and three for aquatic taxa. Chapter 17 (Costa et al. 2022) lists and discusses the more
than 1000 species of fishes that potentially occur in the fresh and marine waters of
the islands. Chapter 18 (Bell et al. 2022) deals with amphibians, which include three
species on Príncipe and six on São Tomé, all of which are endemic (Annobón has no
amphibians). The chapter provides a detailed overview of species biology, ecology,
and biogeography. Chapter 19 (Ceríaco et al. 2022c) presents the 29 species of
established terrestrial reptiles, reporting also historical and recent records of vagrant,
doubtful, or introduced species. The five species of sea turtles that occur on the
islands are reviewed in Chap. 20 (Ferreira-Airaud et al. 2022). All sea turtles are
threatened, and this chapter includes extensive discussion of conservation successes
and challenges. Chapter 21 (Melo et al. 2022b) revises information on birds, one of
the best-known and most charismatic taxa from the islands that includes at least
29 endemic species. It summarizes historical data and provides updated insights into
a group that has been at the forefront of research and conservation. Chapter 22
(Rainho et al. 2022) revises information on the 19 species of non-domesticated
resident land mammals, including 11 bats, seven endemic species, and six introduced species. Finally, Chap. 23 (Carvalho et al. 2022) draws on new data collected
since 2002 to present the updated list of the 12 cetaceans confirmed in the waters of
the region, five of which are recent records. This chapter also provides a synthesis of
the whaling history in the region.
The final section of the book focuses on the conservation, education, and future of
research in the oceanic islands of the Gulf of Guinea. Chapter 24 (Lima et al. 2022)
summarizes the state of conservation: from the cultural links to nature to the history
of conservation initiatives. This chapter also lists priority species, sites, and actions.
1
Biodiversity in the Gulf of Guinea Oceanic Islands: A Synthesis
9
Chapter 25 (Ayres et al. 2022) assesses recent strategies of formal and non-formal
environmental education on São Tomé and Príncipe, which are vital to augment
local capacity for conservation and scientific research. Chapter 26 (Bell et al. 2022)
proposes a path toward biodiversity resilience for future naturalists, biologists,
conservationists, and educators.
Current Numbers, Current Biases
Comparing the number of species presented in previous compilations, such as
Bocage (1903, 1905) or Jones (1994), with those recorded in this book is not a
straightforward task. The coverage of previous syntheses was taxonomically more
limited than the present work, and methods for counting endemic and non-endemic
species varied. In comparing the number of vertebrate species and endemics provided by Jones (1994) with those in the current synthesis, however, one major trend
stands out—our improved understanding led to an increase in endemism across most
taxa (Table 1.1). In many cases, this was due to recognizing that each island had a
distinct endemic species, and that shared endemics are rare. While it is likely that
these numbers change little for vertebrate groups, they will certainly keep changing
for less studied taxa, such as fungi, plants, invertebrates, and marine vertebrates.
There are several other biases in our knowledge of the biodiversity of these
islands. Annobón is by far the least studied island. Most of the chapters focus on
terrestrial habitats and species, and while several teams and projects are currently
focusing on marine biodiversity and conservation, knowledge is still very limited.
The study of marine biomes in the Gulf of Guinea oceanic islands is of critical
importance, not only because the region is likely an important hotspot for marine
biodiversity, but also because human residents depend heavily on marine resources.
Another major gap is the limited number of ecological and natural history studies.
While there is now a considerable amount of traditional and modern taxonomic
research—describing, naming, and listing the several thousands of species known
from the islands—there are very few studies on the ecology and natural history of
these taxa. For most species, almost nothing is known besides the diagnosis and a
few anecdotal pieces of information about its ecology. This lack of information
hinders the development of effective conservation measures, which are increasingly
necessary to ensure a thriving future for this unique archipelago.
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Chapter 2
Physical Geography of the Gulf of Guinea
Oceanic Islands
Luis M. P. Ceríaco, Bruna S. Santos, Ricardo F. de Lima, Rayna C. Bell,
Sietze J. Norder, and Martim Melo
Abstract The Gulf of Guinea, in the Atlantic coast of Central Africa, has three
oceanic islands that arose as part of the Cameroon Volcanic Line. From northeast to
southwest these are Príncipe (139 km2), São Tomé (857 km2), and Annobón
(17 km2). Although relatively close to the adjacent mainland, the islands have
distinct climactic and geomorphologic characteristics, and have remained isolated
throughout their geological history. Consequently, they have developed a unique
biodiversity, rich in endemic species. We provide an integrated overview of the
L. M. P. Ceríaco (*)
Museu de História Natural e da Ciência da Universidade do Porto, Porto, Portugal
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório
Associado, Universidade do Porto, Vairão, Portugal
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, Vairão, Portugal
Departamento de Zoologia e Antropologia (Museu Bocage), Museu Nacional de História
Natural e da Ciência, Universidade de Lisboa, Lisbon, Portugal
e-mail: lmceriaco@mhnc.up.pt
B. S. Santos
Museu de História Natural e da Ciência da Universidade do Porto, Porto, Portugal
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório
Associado, Universidade do Porto, Vairão, Portugal
Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Porto, Portugal
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, Vairão, Portugal
R. F. de Lima
Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências,
Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon,
Portugal
Gulf of Guinea Biodiversity Centre, São Tomé, Sao Tome and Principe
R. C. Bell
Department of Herpetology, Institute for Biodiversity Science and Sustainability, California
Academy of Sciences, San Francisco, CA, USA
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_2
13
14
L. M. P. Ceríaco et al.
physical setting of the islands, including their geographic location, geological origin,
topography, geology and soils, climate zones, and prevailing wind and ocean
currents—key features that underlie the evolution of their biodiversity.
Keywords Annobón · Geology · Ocean currents · São Tomé · Príncipe · Soils ·
Volcanism
Introduction
The Gulf of Guinea is a major topographical feature of western equatorial Africa that
marks the distinctive shape of the continent on its Atlantic coast (Fig. 2.1). The Gulf
of Guinea has three oceanic islands (Príncipe, São Tomé, and Annobón), one landbridge island (Bioko), and two seamounts, which together comprise the offshore part
of the Cameroon Volcanic Line. The biodiversity of the oceanic islands is characterized by a small number of species but exceptional endemism (Jones 1994;
Gascoigne 2004; Ceríaco et al. 2022). This chapter provides an introduction to the
physical setting of the islands that created the conditions for the evolution of their
unique biodiversity, including their geography and topography, geological history,
geological substrates and soils, climate, and prevailing patterns of ocean sea
currents.
Some of the most complete sources of data for these topics are found in works
published under the seal of the Portuguese scientific colonial institute—the Junta de
Investigações do Ultramar—during the 1950s, 1960s, and 1970s. Of these sources,
Lains e Silva (1958) provides key information on climate, soils, vegetation, and
agricultural potential of São Tomé and Príncipe islands (see also Lains e Silva and
Cardoso 1958). Building on earlier work, Tenreiro (1961) further addressed some of
these topics for São Tomé Island. Cardoso and Garcia (1962) is a key reference for
the soils of São Tomé and Príncipe—providing detailed maps of the soils of each
island. Rodrigues (1974) synthesized the information on climate and soils presented
by Lains e Silva (1958) and Cardoso and Garcia (1962). Jones et al. (1991) provide a
S. J. Norder
Copernicus Institute of Sustainable Development, Environmental Science Group, Utrecht
University, Utrecht, The Netherlands
M. Melo
Museu de História Natural e da Ciência da Universidade do Porto, Porto, Portugal
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório
Associado, Universidade do Porto, Vairão, Portugal
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, Vairão, Portugal
FitzPatrick Institute of African Ornithology, University of Cape Town, Rondebosch,
South Africa
2
Physical Geography of the Gulf of Guinea Oceanic Islands
15
Fig. 2.1 Map of the Gulf of Guinea islands, western Central Africa. This system includes an
ecological island (Mount Cameroon), a land-bridge island (Bioko), and the three oceanic islands,
which are the focus of this book. Adapted from Jones and Tye (2006)
16
L. M. P. Ceríaco et al.
useful synthesis of background information available at the time. More recently,
Diniz and Matos (2002) added to our understanding of the climate and soils of São
Tomé and Príncipe islands, providing an updated and detailed map of the ecosystems
and land-use types of the islands. A series of geological studies conducted by Munhá
et al. (2002), Caldeira et al. (2003), Caldeira (2006), Munhá et al. (2006a, b, c, d,
2007), and Barfod and Fitton (2014) have provided important updates to our
knowledge of the geology of São Tomé. Chou et al. (2020) provided the first modern
analysis of the climate of São Tomé and Príncipe, downscaling global projections of
climate change to these islands. For Annobón, the information is scarcer with initial
geological works by Schultze (1913), petrological studies by Fuster Casas (1954)
and Cornen and Maury (1980), work on volcanic geochemistry by Liotard et al.
(1982), and a review by De Castro and De la Calle (1985), with subsequent additions
by Fa (1991) and Velayos et al. (2014). Besides these island specific studies, several
reviews summarize the main geophysical characteristics of the Gulf of Guinea
islands (e.g., Lee et al. 1994; Jones 1994; Jones and Tye 2006; Juste and Fa 1994;
Schlüter 2008).
Location, Extent, and Political Boundaries
The Gulf of Guinea island system (sensu lato) includes the ecological or “sky” island
of Mount Cameroon, the land-bridge island of Bioko, and the three oceanic islands
of Príncipe, São Tomé, and Annobón (Fig. 2.1). They are, from northeast to
southwest:
Mount Cameroon, with an approximate area of 1750 km2 (50 35 km), is an
ecological island in the southwest province of the Republic of Cameroon. Mount
Cameroon is the highest mountain in West Africa, with a peak elevation of 4095 m
above sea level.
Bioko Island is a land-bridge island with an area of 2027 km2 (roughly
35 km 72 km). Bioko sits upon the continental shelf 32 km from the coast of
Cameroon from which it is presently separated by a sea 60 m deep. During recent
glacial periods, however, Bioko experienced recurring cycles of isolation and
connectivity (Ali 2018), and was most recently connected c. 11,000 years ago
(Einsentraut 1965; Lambert and Chappel 2001). Rising to an impressive 3011 m
above sea level, Pico Basilé is the highest point of the island and one of its main
landmarks.
The three oceanic islands that are the focus of this book have never been
connected to the continent, and they are:
Príncipe Island (Fig. 2.2(1)) with a total area of 139 km2 (c. 17 km 8 km) is
located 210 km SSW of Bioko and 220 km west of continental Africa. The island has
six main satellite islets: Pedra da Galé, Mosteiros, and Bom-Bom in the north,
Caroço (also known as the Jockey’s Cap; Fig. 2.2(3)) in the southeast, and Tinhosa
Grande and Tinhosa Pequena (Fig. 2.2(2)), which are about 20 km to the south. The
highest point, Pico do Príncipe, is 942 m above sea level.
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Physical Geography of the Gulf of Guinea Oceanic Islands
17
Fig. 2.2 (1) Pico Agulhas, Príncipe Island; (2) Tinhosa islets; (3) Jockey Bonet; (4) Pico São
Tomé, São Tomé Island; (5) Pico Cão Grande, São Tomé Island; (6) Rolas islet; (7) Lagoa Amélia,
São Tomé Island; (8) Lake A Pot, Annobón Island. Photo credits: (1 and 8) Martim Melo, (2, 3, 5–7)
Luis M. P. Ceríaco; (4) Ricardo Lima
São Tomé Island with a total area of 857 km2 (47 km 28 km) lies 150 km SSW
of Príncipe and 255 km west of Gabon. The island has several islets, of which Cabras
to the north, Santana in the east, and Sete Pedras and Rolas (Fig. 2.2(6)) in the south
18
L. M. P. Ceríaco et al.
Fig. 2.3 Administrative divisions of Príncipe (a), São Tomé (b), and Annobón (c)
are the largest. The Equator passes through the center of Rolas Islet. The highest
point, Pico de São Tomé (Fig. 2.2(4)), is 2024 m above sea level.
Annobón Island has an area of 17 km2 (6 km 3 km) and is the smallest and
remotest of the Gulf of Guinea islands. It sits 180 km to the SSW of São Tomé and is
about 340 km from the continent. The highest peak is Santa Mina, which rises 610 m
above sea level.
Politically, the Gulf of Guinea oceanic islands belong to two countries: the
Democratic Republic of São Tomé e Príncipe and the Republic of Equatorial Guinea.
São Tomé e Príncipe is a nation state made up of Príncipe and São Tomé islands and
the surrounding islets. It was once a colonial province of Portugal, from which it
gained independence in 1975. It is one of the smallest countries in the world, with an
approximate area of 1001 km2. The country is internally organized into different
levels of political and administrative divisions. São Tomé Island hosts the capital, the
city of São Tomé, and is divided into six districts (Água Grande, Cantagalo, Caué,
Lembá, Lobata, and Mé-Zóchi); Príncipe Island is an Autonomous Region, and is
comprised of a single district, Pagué (Fig. 2.3).
Annobón (formerly known as Pagalu; Fig. 2.3), the smallest and most southwestern of the Gulf of Guinea oceanic islands, is one of eight provinces of Equatorial
Guinea. This geographically disjunct country was a Spanish colony from 1778 to
1968. Equatorial Guinea is composed of a territory in continental Africa, Rio Muni,
bordered by Cameroon to the north and Gabon in the east and south, the surroundings islets of Corisco, Elobey Chico, and Elobey Grande, the land-bridge island of
Bioko (formerly known as Fernando Pó), where the country’s capital is (Malabo),
and finally the small oceanic island of Annobón. Whereas the mainland territory and
Bioko have a long history of human occupation, Annobón was not peopled at the
time of its discovery by the Portuguese, in 1473.
Geological History
The Gulf of Guinea islands form the southern part of the Cameroon Volcanic Line, a
1000-km line of volcanoes that has been active since the Cenozoic, and that extends
from the Mandara Mountains on the Nigeria-Cameroon border to Annobón Island
2
Physical Geography of the Gulf of Guinea Oceanic Islands
19
Fig. 2.4 Topographic representation of the offshore section of the Cameroon Volcanic Line.
Figure created with the rayshader R package (Morgan-Wall 2021) using GEBCO data (GEBCO
Compilation Group 2021)
(Burke 2001). This line runs in a NE-SW direction and includes four islands and two
seamounts (Fig. 2.4). Onshore, there are four continental massifs (Mount Cameroon,
Mount Manengouba, Mount Bambouto, and Mount Oku), all of which are in the
Republic of Cameroon. Often, the Ngaoundéré and Biu swells, also in Cameroon,
are considered part of the line, in which case the line becomes Y-shaped and
1600 km long (Fitton 1987; Lee et al. 1994; Fig. 2.5). Volcanic activity in the
continental and oceanic sector has been more or less continuous since the Cretaceous
(Fitton 1987; Lee et al. 1994; Burke 2001). There is no age progression in the line,
except in the offshore section—with the oldest sub-aerial origins estimated at about
31 Ma for Príncipe, 15 Ma for São Tomé, and 6 Ma for Annobón (Lopes 2020).
The age of the oldest lava flows only provides estimates of the minimum age
when each island was sub-aerial because older rocks may be buried under the most
recent ones. For example, all the exposed lavas on Mount Cameroon are less than
one million years old, but the mountain is built upon much older lava flows (Fitton
1987). Furthermore, volcanic activity persisted until recently on all the islands, and
is still ongoing in Mount Cameroon and to a lesser extent in Bioko. This dynamic
aspect of the islands is well illustrated in São Tomé, where the oldest rocks, at about
15.7 Ma, are from the small Cabras Islet, while the surface rocks of more than half of
the island, including its highest peak, date between 1.5 and 0.4 Ma (Caldeira et al.
2003; Barfod and Fitton 2014). Although still poorly understood, the volcanic
history of the Gulf of Guinea islands has no doubt played a major role in the
assembly of their current biological communities. For instance, landslides or lava
flows can split species ranges or cause extinctions, and distinct islands and islets may
fuse and split over time (Milá et al. 2010; Gillespie and Roderick 2014; Ramalho
et al. 2015).
20
L. M. P. Ceríaco et al.
Fig. 2.5 The Cameroon line of volcanoes. Note the similarity in shape between the volcanic line
(black) and the Benue Rift (grey). This was likely due to the rotation of the African plate
c. 30–35 Ma that displaced the asthenospheric hot zone underlying the Benue Rift to its current
position—resulting in a volcanic line without a rift and a rift without volcanoes, a unique feature on
Earth. After decades of debate, the alignment of the volcanic centers is now thought to be controlled
by the geometry of the northwest edge of the Congo Craton. Adapted from Lee et al. (1994)
2
Physical Geography of the Gulf of Guinea Oceanic Islands
21
Quaternary Sea-Level Fluctuations
Across the globe, glacial-interglacial sea-level fluctuations have shaped insular
biodiversity and diversification by repeatedly connecting and isolating populations
on coastal landmasses (e.g., Ali and Aitchison 2014; Rijsdijk et al. 2014; FernándezPalacios 2016; Weigelt et al. 2016; Norder et al. 2018, 2019). Ceríaco et al. (2020)
modeled the area of the islands throughout the last glacial period to the present day
and demonstrated that the Gulf of Guinea islands show marked changes in area in
response to eustatic sea-level fluctuations. During the exceptionally low sea level of
the Last Glacial Maximum, as much as 134 m lower than present day (Lambeck et al.
2014), Bioko was connected to continental Africa, Annobón was five times its
present size, Príncipe was about six times its present size, and São Tomé was
approximately 50% larger than present day (Ceríaco et al. 2020; Fig. 2.6).
Topography and Hydrography
Due to recent volcanic activity, Príncipe, São Tomé, and Annobón are old islands
that have the topography of young islands, including rugged mountains with steep
slopes, deep valleys, volcanic chimneys, table mountains, and huge waterfalls
(Figs. 2.7). The topography varies between islands. São Tomé is dominated by
steep slopes and mountains across the majority of the island, with the exception of
the flatter areas in the northeast (Figs. 2.7e, f). The maximum elevation reaches
2024 m at Pico de São Tomé, and several other mountain and peaks areas in the
center of the island are well above 1000 m (Figs. 2.2(5), 2.7e). Príncipe has a plateau
in the north but is mountainous in the south, where several peaks rise above 500 m,
including Pico do Príncipe at 942 m (Figs. 2.7b). Annobón is small and steep, except
for a small portion in the north, where most of the human population resides. The
elevation rises considerably in the center and south, reaching 613 m at Santa Mina
(Fig. 2.7h).
The available data on the terrestrial hydrography of the islands are limited. Both
São Tomé and Príncipe are mostly covered by the hydrographic basin of a few large
rivers in a dense network and also include several small coastal rivers (Fig. 2.7a, d).
São Tomé Island has many small lagoons, estuaries, and mangroves, including the
Malanza river estuary in the south, which forms the most extensive mangrove in the
country. São Tomé also has a unique freshwater palustrine system in the crater of
Lagoa Amélia (Fig. 2.2(7)), which is the source of the largest rivers in the north of
the island (Fig. 2.7d). Annobón only has a few small streams, but Lago A Pot crater
lake (Fig. 2.7g, shown in red; Fig. 2.2(8)) is a dominant feature of the island with a
diameter of approximately 700 m at 150 m above sea level.
22
L. M. P. Ceríaco et al.
(a)
(b)
Fig. 2.6 Paleogeographic reconstructions of the Gulf of Guinea: (a) Area change curves of
Príncipe, São Tomé, and Annobón islands; (b) area of islands today (dark green), and extreme
area at the last glacial maximum (LGM, approximately 21 ka; light green). Adapted from Ceríaco
et al. (2020)
2
Physical Geography of the Gulf of Guinea Oceanic Islands
23
Fig. 2.7 Overview of the hydrography and topography of (a, b, c) Príncipe, (d, e, f) São Tomé, and
(g, h, i) Annobón. For each island, elevation is presented in meters above sea level and steepness in
degrees. Main rivers and waterbodies: São Tomé Rivers (d): 1—Provaz; 2—Lembá; 3—Xufexufe;
4—Quija; 5—Mussacavú; 6—Pedras; 7—Gumbela; 8—Malanza; 9—Gogô; 10—Caué; 11—
Martim Mendes; 12—Miranda Guedes; 13—João Nunes; 14—Ana Chaves; 15—Ió Grande;
16—Angobó; 17—Angra Toldo; 18—Pedra Furada; 19—Ribeira Afonso; 20—Abade; 22—
Ouro. São Tomé Crater Lake: 21—Lagoa Amélia. Príncipe Rivers (a): 1—Ribeira Banzú; 2—
Ribeira São Tomé; 3—Ribeira Porco; 4—Chibala; 6—Papagaio. Annobón (g) has no significant
rivers; the crater lake Lago A Pot is shown in red
24
L. M. P. Ceríaco et al.
Geology and Soils
The geology of São Tomé and Príncipe has been well studied since the early
twentieth century. This is partly due to the importance of geology and soils for
agriculture, which has been the major driver of the local economy for centuries
(Lains e Silva 1958; Lains e Silva and Cardoso 1958; Rodrigues 1974). The first
overview of the geology of São Tomé Island was provided by Carvalho in Henriques
(1917), followed by a more detailed study on the microscopic characteristics of its
rocks (Carvalho 1921). Teixeira (1948–1949, 1949) provided a more complete
overview of the geology of the islands, followed by a petrological work by Pereira
(1943). The most extensive and complete contributions to the geology of the islands
were provided by the Portuguese geologist João Manuel Cotelo Neiva (1917–2015),
whose work was fundamental to understanding the geochemistry and geomorphology (Neiva 1946, 1954, 1955a, b, 1956a, b, c; Neiva and Pureza 1956; Neiva and
Neves 1956). Assunção (1956, 1957) and Barros (1960) also contributed to our
understanding of the geochemistry. In the twenty-first century, new research on the
geology of São Tomé (Munhá et al. 2002; Caldeira et al. 2003; Caldeira 2006) has
resulted in updated geological maps (Munhá et al. 2006a, b, c, d, 2007). By contrast,
the geology of Annobón has received far less attention. The first information on its
geological history and composition was provided by Schultze (1913), followed by
studies by Tyrrell (1934), Fuster Casas (1954), Cornen and Maury (1980), and
Liotard et al. (1982). More recently, De Castro and De la Calle (1985) and Fa
(1991) provided an overview of the geology of Annobón. On Príncipe, basaltic rocks
predominate in the north and phonolites and tephrites in the south, whereas São
Tomé and Annobón are mostly built by basaltic lavas (Fig. 2.8). A more detailed
description of the geology of the islands is provided by Schlüter (2008).
Regarding the soils of Príncipe and São Tomé, Lains e Silva (1958) and Cardoso
(1958) drafted the first maps, with a more comprehensive map and revision by
Cardoso and Garcia (1962). Other works were done by Pissarra and Rocha (1963)
and Pissarra et al. (1965). The dominant soil types of Príncipe and São Tomé are
highly weathered, such as Ferralsols and Lixisols (Lains e Silva 1958; Cardoso and
Garcia 1962; Diniz and Matos 2002), which are typical of tropical climates. Vertisols
are restricted to the dry north and northeast of São Tomé, while Lithosols can be
found everywhere on the island, often associated with ridges, steep slopes, and cliffs
near the coast (Diniz and Matos 2002). Fluvisols, as expected, are mostly associated
with riparian areas. Very little is known about the soils of Annobón, other than that
they are ultrabasic with low silica and high proportions of ferromagnesian elements
(De Castro and De la Calle 1985; Fa 1991).
The only reported fossils are from Príncipe and date to the Miocene (Teixeira
1949; Silva 1956a, b, 1958a, b; Serralheiro 1957). These include marine organisms
such as gastropods, bivalve mollusks, coelenterates, echinoderms, and fishes’ teeth,
but also calcareous algae, radiolarians, and foraminifera. Modern foraminifera are
known from both Príncipe and São Tomé beaches (Moura 1961). A palaeoecological
study is currently taking place on Príncipe and São Tomé collecting data from
2
Physical Geography of the Gulf of Guinea Oceanic Islands
25
Fig. 2.8 Geological overview of the islands of Príncipe, São Tomé, and Annobón. Adapted with
permission from Springer Nature Geological Atlas of Africa by Schlüter © Springer-Verlag Berlin
Heidelberg 2006 (2008)
pollen, spores, charcoal, and sedimentology to reconstruct ecosystem changes associated with glacial cycles and the impacts of human activities (unpublished data by
Alvaro Castilla-Beltrán).
26
L. M. P. Ceríaco et al.
Fig. 2.9 Annual average temperature (in Celsius) for the islands of Príncipe, São Tomé, and
Annobón. Data obtained from the Global Solar Atlas 2.0, provided by the World Bank Group
Climate
The Gulf of Guinea oceanic islands have an oceanic equatorial climate. Mean
temperatures are above 25 C at sea level but decrease with altitude (Fig. 2.9). The
year is divided into rainy and dry seasons, which are determined by the Intertropical
Convergence Zone, and by the interaction between the southern monsoon winds
from the Atlantic Ocean and the northern dry harmattan winds from the Sahara.
Seasons differ between the continental and the oceanic sectors. On Mount Cameroon
and Bioko, the main dry season is from December to March, and a shorter dry season
occurs from July to August (Juste and Fa 1994). In Príncipe and São Tomé, the long
dry season, locally known as gravana, extends from June to mid-September, while a
shorter dry season, the gravanito, lasts for a few weeks that may fall anywhere
between mid-December and mid-March (Lains e Silva 1958). Annobón, south of the
Equator, has a single extended dry season from mid-May to the end of October
(Jones and Tye 2006).
Due to their small area and heterogeneity, modern rainfall and climate measurements based on remote sensing likely do not accurately describe the climate of
Príncipe, São Tomé, and Annobón. To the best of our knowledge, until recently
Annobón had no functional meteorological station, while there was only one on
Príncipe and five on São Tomé, of which only one had been collecting long-term
data systematically (Chou et al. 2020). This network was greatly improved over the
last decade (https://www.thegef.org/project/strengthening-climate-information-andearly-warning-systems-sao-tome-and-Príncipe-climate), but detailed long-term
information on the climate of the islands is still lacking.
The topography of Príncipe and São Tomé islands is similar, resulting in a similar
distribution of climatic zones (Diniz and Matos 2002). The high relief areas of the
south and center intercept the predominant warm and moist south-westerly winds,
creating a striking north–south divide in precipitation (the Foehn effect). The
southern-facing regions are “Super Humid,” with annual precipitation above
2
Physical Geography of the Gulf of Guinea Oceanic Islands
27
Fig. 2.10 Climatic zones for the islands of São Tomé (left) and Príncipe (right). Adapted from
Diniz and Matos (2002)
3000 mm, and often much higher (c. 5000 mm on Príncipe, above 7000 mm on São
Tomé—Diniz and Matos 2002), enhanced by extremely high humidity levels and
low sun exposure (Fig. 2.10). The north, under the rain-shadow effect, has climatic
belts associated with the decreasing levels of humidity with decreasing altitude. The
higher slopes benefit from the monsoon winds that pass over the peaks, and have
precipitation levels between 1500 and 3000 mm, making the “Humid” belt
(Fig. 2.10). Lower down, from the coast to about 400 to 550 m, moderate slopes
(below 15%) receive between 1000 and 1500 mm of rain per year, making up the
“Sub-Humid” belt, which has a well-defined rainy season (Fig. 2.10). Finally, only
on São Tomé, the littoral area in the flatter N-NE platform, below 1000 m, has a
“Semi-Arid” belt that has annual precipitation levels between 600 and 1000 mm
(Fig. 2.10). This general zonation, with more humid climates in the south and drier
climates in the north, also seems to apply to Annobón and to the continental islands.
Annual precipitation on the southwestern slopes of Mount Cameroon may be over
10,000 mm, and between 1500 and 2000 mm in the northern slopes. In the south of
Bioko Island, annual precipitation can be over 11,000 mm (Juste and Fa 1994) while
the capital Malabo, in the north, receives <2000 mm/year.
28
L. M. P. Ceríaco et al.
Wind and Ocean Currents
Understanding the wind and ocean currents is fundamental to infer potential colonization pathways for island fauna and flora. The prevailing winds in the Gulf of
Guinea are the southwestern monsoon winds and the northern dry harmattan winds.
The southwestern monsoon winds are unlikely to have dispersed colonizers from
continental Africa but may have played a role in southwest-to-northeast dispersal
between islands. During glacial cycles, the northern dry harmattan winds extended
their influence southward, displacing the meteorological equator further south
(Lézine et al. 1994), likely having a more important role in bringing colonizers to
the island during those periods.
Data on sea surface currents originate from a combination of historical ship drifts,
hydrographical data, surface-drifting buoy trajectories, and Argo floats surface drifts
(Richardson and Walsh 1986; Arnault 1987; Stramma and Schott 1999; Renner
2004; Lumpkin and Garzoli 2005; Ollitrault and Rannou 2013). The Gulf of Guinea
is dominated by two currents (northward and eastward) that follow the shoreline. In
the north, the eastward current, also known as Guinea Current (GC), moves west to
east along the southern coast of West Africa, and, when reaching the Biafra Bay,
converges with the northward current and becomes more diffuse, turning back
westward around the Equator (Feiler 1988; Haft 1993; Dupont et al. 2000;
Fig. 2.11). In the southeast, the northward current, known as the Benguela Current
(BC), moves along the northern coast of South Africa, the coast of Namibia, and is
diverted west to the Atlantic around the mouth of the Cunene River, the natural and
political border between Namibia and Angola. It also feeds the South Equatorial
Current (SEC), which represents the northern limb of the South Atlantic Ocean
subtropical gyre (Philander 2001; Rodrigues et al. 2007). Moving north, the coast of
Angola is dominated by two different currents, the Benguela Coastal Current (BCC),
a cold and less-saline northward flow, and the Angola Current (AC), a fast and
narrow southward geostrophic flow of warm and saline water found between the
equatorial band and about 15 S. The intersection of these two currents, around 15 S,
is known as the Angola Benguela Front (Hopkins et al. 2013; Lass and Mohrholz
2008, their Fig. 1; Houndegnotono et al. 2021, their Fig. 1b). The discharge of the
Congo River, which extends offshore as the Congo River plume, is a thin layer (3 m
thick at the river mouth) of fresher/lower salinity water. This freshwater plume is
entrained mostly westward, through Ekman-driven circulation in which the wind
deflects surface water to the left of its direction in the southern hemisphere.
Ocean currents are important for understanding the biogeographic history of
aquatic organisms and terrestrial organisms that disperse in water—such as some
seed plants—but, in the Gulf of Guinea, they may also hold the key to understanding
how many non-volant, non-swimming, or salt-intolerant species made their way to
the islands (Melo et al. 2022). The prevailing hypothesis to explain the origin of such
unlikely oceanic island taxa proposes that they came as passengers of natural rafts
that drifted to the islands along “freshwater pathways” on the ocean surface (Measey
et al. 2007). Such rafts would reach the islands along “freshwater pathways” created
2
Physical Geography of the Gulf of Guinea Oceanic Islands
29
Fig. 2.11 Main ocean currents in the Gulf of Guinea. Angolan Current (AC), Benguela Current
(AC), Benguela Coastal Current (BCC), Guinea Current (GC), and South Equatorial Current (SEC).
Warm currents in red; cold currents in dark blue
by the large input of freshwater plumes and precipitation into the Gulf of Guinea
(Fig. 2.11; Dessier and Donguy 1994; Large and Yeager 2009; Hopkins et al. 2013;
Berger et al. 2014). Because saltwater is denser than freshwater, during the rainy
season the ocean surface in the Gulf of Guinea exhibits reduced salinity—a wellknown phenomenon by local fishermen (Measey et al. 2007; Hopkins et al. 2013).
These “freshwater pathways” would give the rafts some protection against saltwater
as they cross the sea.
The Gulf of Guinea receives the freshwater discharge of three major rivers that
originate from different regions: the Niger in West Africa, the Congo in East-Central
Africa, and the Ogooué in West-Central Africa (Fig. 2.12). The Congo River is only
second to the Amazon in terms of discharge, having an average discharge of
40103 m3s 1 (Mahé and Olivry 1999), while the Niger River has about
7103 m3s 1 (Dai and Trenberth 2002). When reaching the ocean, these waters
are directed toward the islands by the surface currents of the Atlantic Ocean.
30
L. M. P. Ceríaco et al.
Fig. 2.12 Monthly average sea surface salinity for the months of February (left) and July (right)
2021. Values displayed with a range of 20 and 37 using the Practical Salinity Scale (PSS), roughly
equivalent to parts per thousand of salt. Data from the Remote Sensing Systems SMAP Ocean
Surface Salinities [Level 3 Monthly] Dataset, Version 4.0 validated release (Meissner et al. 2019)
Although the mouth of the Ogooué River is the closest to the islands (approximately
250 km), the currents in the Gulf of Guinea direct the freshwater plumes from the
Niger and Congo rivers toward the islands (Richardson and Walsh 1986), such that
vegetation rafts originating in the more distant West and East African drainages may
also reach the islands.
Conclusions
Despite their small area, the oceanic islands of the Gulf of Guinea include a wealth of
geological substrates and topographical features that underlie the development of
diverse soils and micro-climates (Fig. 2.2). This diversity of geological features has
been recognized by ten formations being proposed as geosites on São Tomé Island,
which have a wide range of cultural, scientific, and scenic values (Henriques and
Neto 2015). These landscapes have also promoted the appearance of distinct ecosystems (Dauby et al. 2022) and species (Melo et al. 2022). The location of the
islands, at moderate distances from the mainland and at the crossroads of freshwater
plumes from three large rivers, has likely further contributed toward the assembly of
their rich biological communities. These rivers are thought to have been the source
of natural rafts bringing species that would otherwise be unable to cross saltwater
barriers.
Acknowledgments The authors thank Jason Ali and Bernard Bourles for suggestions on the
original draft of this manuscript, and Branca Moriés, from the library of the Museu de História
Natural e da Ciência, Universidade de Lisboa, for her support with historical bibliography. Data for
2
Physical Geography of the Gulf of Guinea Oceanic Islands
31
map of Fig. 2.9 were obtained from the “Global Solar Atlas 2.0,” a free, web-based application,
developed and operated by the company Solargis s.r.o. on behalf of the World Bank Group,
utilizing Solargis data, with funding provided by the Energy Sector Management Assistance
Program (ESMAP). For additional information: https://globalsolaratlas.info. SMAP salinity data
are produced by Remote Sensing Systems and sponsored by the NASA Ocean Salinity Science
Team. They are available at www.remss.com. MM was supported via the European Union’s
Horizon 2020 Research and Innovation program under grant agreement 854248. “Fundação para
a Ciência e a Tecnologia” (Portugal) funded BSS (2021.06659.BD), cE3c (UID/BIA/00329/2021;
to RFL), and (UIDB/50027/2021; to MM). SJN was supported by the European Research Council
under the EU H2020 and Research and Innovation program (SAPPHIRE grant 818854).
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Chapter 3
Classification, Distribution,
and Biodiversity of Terrestrial Ecosystems
in the Gulf of Guinea Oceanic Islands
Gilles Dauby, Tariq Stévart, Patricia Barberá, Laura Benitez,
Maria do Céu Madureira, Filipa C. Soares, Gaëlle Viennois,
and Ricardo F. de Lima
Supplementary Information The online version contains supplementary material available at
[https://doi.org/10.1007/978-3-031-06153-0_3].
G. Dauby (*) · G. Viennois
AMAP, Univ Montpellier, CIRAD, CNRS, INRAE, IRD, Montpellier, France
e-mail: gilles.dauby@ird.fr
T. Stévart
Africa & Madagascar Department, Missouri Botanical Garden, St. Louis, MO, USA
Herbarium et Bibliothèque de Botanique africaine, Université Libre de Bruxelles, Brussels,
Belgium
Meise Botanic Garden, Meise, Belgium
P. Barberá
Africa & Madagascar Department, Missouri Botanical Garden, St. Louis, MO, USA
L. Benitez
Fauna & Flora International, Cambridge, UK
Fundação Príncipe, Santo António, Sao Tome and Principe
M. do Céu Madureira
Centre for Functional Ecology, Departamento de Ciências da Vida, Universidade de Coimbra,
Coimbra, Portugal
F. C. Soares
Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências,
Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon,
Portugal
R. F. de Lima
Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências,
Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon,
Portugal
Gulf of Guinea Biodiversity Centre, São Tomé, Sao Tome and Principe
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_3
37
38
G. Dauby et al.
Abstract The oceanic islands of the Gulf of Guinea display a large diversity of
environmental conditions and biological communities, whose interactions have
contributed to the development of a great variety of ecosystems, from mangroves
to montane grasslands. Human activities have extensively and profoundly altered
many of these natural ecosystems over the past five centuries. We review key studies
to propose an updated classification map of terrestrial ecosystems, taking advantage
of up-to-date spatial information on abiotic gradients and biological distributions. To
guide future research and conservation programs, we highlight challenges and
pending questions regarding our understanding of the structure, integrity, and
dynamics of terrestrial ecosystems in these islands.
Keywords Abiotic gradients · Biological communities · Introduced species · Novel
ecosystems · Topography · Vegetation types
Introduction
The oceanic islands of the Gulf of Guinea (GGOI) comprise three islands: Príncipe,
São Tomé (together forming the Democratic Republic of São Tomé and Príncipe),
and Annobón (part of the Republic of Equatorial Guinea). Despite their small size
(c. 1000 km2), their combined human population is ca. 225,000 inhabitants (INEGE
2017; INESTP 2020), and they are also host to a rich endemic fauna and flora (Jones
1994).
The tropical humid climate, complex topography, altitudinal gradients, and
isolation (distance to mainland from 220 to 350 km) are often invoked to explain
the endemic-rich biodiversity of these islands (Jones 1994). The abiotic gradients
generate a diversity of habitats with distinct biological communities, whose interactions contribute to the development of a great variety of natural ecosystems, from
mangroves to montane grasslands (Monod 1960). Over the past five centuries,
human activities have profoundly altered most of these natural ecosystems across
large areas (Eyzaguirre 1986). Impacts have varied in intensity across time and space
among the three islands, but agricultural land use in particular has intensified (Jones
et al. 1991), which has likely facilitated the expansion of introduced species (e.g.,
Soares et al. 2020).
The first attempts to delineate the ecosystems of the GGOI date back to the first
half of the twentieth century, and aimed at documenting vegetation types (Henriques
1917; Chevalier 1938–1939; Exell 1944). These studies relied almost entirely on
variations in vegetation physiognomy and on the degree of human interference.
These authors paid particular attention to defining altitudinal vegetation belts. Other
studies tried to identify phytogeographical units based mostly on the co-distribution
of plant species, but ended up having to rely heavily on abiotic proxies (Stévart
1998; Ogonovszky 2003). Phytogeographical units can be misleading for identifying
ecosystems because biogeographical processes can lead to different species
3
Classification, Distribution, and Biodiversity of Terrestrial. . .
39
assemblages in similar ecosystems. However, given the relatively small size of these
islands, we can assume that the co-distributions of species within each island reflect
environmental conditions and anthropogenic disturbances, while biogeographical
processes, such as limited dispersal and speciation rates, are negligible.
Recently, many large-scale studies have inferred the integrity, distribution, and
dynamics of ecosystems, taking advantage of the increasing availability of remote
sensing data (e.g., Hansen et al. 2013; Gosling et al. 2020; Vancutsem et al. 2021).
Unfortunately, these products are of little relevance for the GGOI, due to their coarse
resolution and unavailability of high-quality aerial images without atmospheric
obstructions, such as haze and aerosols.
In this chapter, we review the key studies that attempted to document the
terrestrial ecosystems of the islands, and then propose an updated classification,
taking advantage of up-to-date spatial information on abiotic gradients and biological communities to map proposed vegetation types. Finally, to guide future research
and conservation efforts, we identify several challenges and pending questions
regarding our understanding of the structure, integrity, and dynamics of the terrestrial ecosystems in the GGOI.
Ecological Setting and Previous Classifications
São Tomé Island
Abiotic Gradients
Rainfall measurements using remote sensing lack the accuracy required for a small
and heterogeneous area like São Tomé (Chou et al. 2020). Thus, our understanding
of rainfall patterns must still rely on the rough isohyets drawn from 50-year-old
observations (Bredero et al. 1977). These isohyets show that annual rainfall varies
strongly across the island, ranging from <1000 mm in the northeast to more than
7000 mm in the southwest (Fig. 3.1). Four seasons are recognized: a humid season
from mid-September to mid-December, a mild dry season from mid-December to
mid-march (“gravanito”), a humid season from mid-March to June, and a prolonged
dry season from July to mid-September (“gravana”).
The rainfall pattern can be explained by the rugged topography and the resulting
rain shadow (“foehn effect”; Ceríaco et al. 2022). Elevation reaches a maximum of
2024 m at Pico de São Tomé, to the northwest of the center of the island, which is
surrounded by a multitude of smaller peaks, ridges, and steep slopes. Overall, the
island is divided by a north–south ridge, extending from Pico de São Tomé to
Cabumbé, which separates the island into a wetter west flank and a drier east
flank. Apart from the northeast and a few flat areas and gentle slopes in the south
and southeast, the topography of most of the island is complex and dominated by
steep ridges and mountains (Fig. 3.1).
40
G. Dauby et al.
Fig. 3.1 Main physico-climatic gradients on São Tomé Island. Sources of data can be found on
https://github.com/gdauby/stpa_ecosystems_review
3
Classification, Distribution, and Biodiversity of Terrestrial. . .
41
Cloud cover influences biological processes and species distribution (Wilson and
Jetz 2016). On São Tomé, according to remotely sensed data, the mean monthly
cloud cover ranges from 70% in the extreme north to nearly permanent in the
western highlands (Fig. 3.1). Rainfall and cloud cover do not fully coincide,
although together they typify the constant high moisture on the west side of the
island. Persistent cloud cover coincides with altitudes between 500 and 1500 m on
the west flank, and above 1000 m on the south and east flanks as a result of the foehn
effect. Intra-annual cloud cover varies little, but reflects the stronger seasonality in
the north (Fig. 3.1).
São Tomé soils have been studied and mapped, and their properties are conditioned by topography and climate that often vary at fine scales (Cardoso and Garcia
1962). The most frequent soil types are highly weathered, such as Ferralsols and
Lixisols, characteristic of tropical climates. Vertisols, Lithosols, and Fluvisols are
noteworthy because they interact with vegetation. Vertisols are heavy clay soils
frequently associated with grasslands and forests that develop deep wide cracks
when dry, making them difficult to use for agriculture (Kovda 2020). This soil type is
restricted to the dry north and northeast (Fig. 3.1). Lithosols are thin soils that have
very little organic matter, and can be found everywhere on the island, often associated with ridges, steep slopes, and cliffs near the coast (Diniz and Matos 2002).
Fluvisols, derived from alluvial deposits, are nutrient-rich, often associated with
large riverbanks, and can be flooded or have weak drainage (IUSS Working Group
WRB 2015).
Human Disturbance
Around three-quarters of the native vegetation of São Tomé has been lost, most of
which was converted into large plantations (Fig. 3.2a; Soares et al. 2020). This
transformation started in the late fifteenth century when humans began colonizing
the island, clearing large extents of forest mostly in the dry northern coastal areas to
establish sugarcane plantations (Eyzaguirre 1986). In the early sixteenth century, the
island became a top producer of sugar globally, developing a cash crop economy that
collapsed later that century (Garfield 1979), slowing down the deforestation rate.
Throughout the seventeenth and eighteenth centuries, the island became an important slave trading post and the traditional “gleba” agroforestry system (based on tree
and root crops grown in dense mixed stands with minimal tillage) expanded
(Eyzaguirre 1986). In the nineteenth century, the deforestation rate increased and
expanded further inland and upland, giving way to intensive plantations dedicated
mostly to coffee and cacao, but also to oil palm, coconut, quinine, and cinnamon.
This period saw the spread of shade plantations that can be defined as plantations
where a canopy is maintained above crops (typically cacao or coffee). The canopy is
often composed of introduced tree species (typically of the Erythrina genus).
Deforestation in São Tomé reached its peak early in the twentieth century, when
the island became the world’s largest producer of cacao. For various reasons, this
system became economically unsustainable and during the late 1930s many
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G. Dauby et al.
Fig. 3.2 (a) Degraded or transformed land cover on São Tomé. Note that the “open vegetation”
category includes both agricultural lands and savanna-like vegetation (Adapted from Soares et al.
2020). (b) Annual fire frequency (data for the last 10 years). The inset barplot shows the distribution
of fires along the year
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Classification, Distribution, and Biodiversity of Terrestrial. . .
43
Table 3.1 Total area and relative importance of transformed or degraded land cover in each island
(Calculated from Norder et al. 2020; Soares et al. 2020; Frazer Sinclair and Yodiney dos Santos,
unpublished data). Note that the open vegetation category also includes naturally open
vegetation type
Land cover
Open vegetation
Urban areas
Industrial palm plantations
Roads/paths network
Secondary forest
Shade forest
Annobón
2.8 km2 (13.4%)
1.8 km2 (8.5%)
–
–
–
–
São Tomé
92.5 km2 (10.9%)
23.3 km2 (2.7%)
23.4 km2 (2.7%)
17.8 km2 (2.1%)
240.6 km2 (28.2%)
218.6 km2 (25.6%)
Príncipe
6.6 km2 (4.8%)
1.9 km2 (1.4%)
–
2.9 km2 (2.1%)
37.4 km2 (26.8%)
41.3 km2 (29.6%)
plantations were abandoned, creating large extents of secondary forests in the higher
altitudes, while the flatter lowland remained as plantations. Following independence
in 1975, and especially after land privatization in the early 1990s, logging and
residential areas expanded significantly, especially in the shade plantations. Meanwhile, swidden agriculture emerged to satisfy local food needs, producing horticultural crops such as potatoes, maize, cabbage, beans, and carrots (Eyzaguirre 1986).
Strong demographic growth led to an increase in timber consumption (the main
building material in the country), resulting in increasing pressure on forest resources
(Salgueiro and Carvalho 2001). More recently, agro-industrial concessions to foreign companies have reconverted large areas of secondary forest to export crop
plantations, such as oil palm, cacao, and coffee (Oyono et al. 2014).
This complex history led to the patchwork of land uses that characterizes the
landscape on São Tomé (Fig. 3.2a, Table 3.1; Soares et al. 2020). Native forests
(ca. 26.4% of the island) are mostly found in the rugged wetter areas at the center and
southwest. Around these are mostly secondary forests (ca. 30.5%), resulting from
agricultural abandonment, notably more widespread in the south. Agroforests
(ca. 28.5%), comprising the traditional “glebas” but also more intensive shade
plantations of cacao and coffee, are dominant in the northeast and in the south
along the coast. The remainder of the island is characterized by non-forested land
uses (ca. 14.5%), including urban areas and anthropogenic savannas in the northern
coast and horticultural areas at higher altitudes. Terrain ruggedness predominantly
shapes the extent of remaining native vegetation cover, suggesting that topography
constrains human occupation across the island (Norder et al. 2020). Anthropogenic
impacts have been felt mostly in the flat lowlands of the drier north, where fire
maintains large extents of open vegetation, even though other areas are not spared.
At higher altitudes, for instance, the distinct climate and fertile soil has promoted
agricultural expansion of crops like quina, arabica coffee, cinnamon, and annuals,
especially in the flatter areas around Monte Café.
Besides land-use change, human disturbance is also felt through more subtle
modifications, namely through the exploitation of forest resources and the facilitation of introduced species. Logging (Espírito et al. 2020), hunting (Carvalho 2015),
silviculture, and the gathering of other forest products such medicinal plants
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G. Dauby et al.
(Madureira et al. 2008) are known to have impacts on the vegetation and overall
functioning of forest ecosystems. Being at the crossroads of the Atlantic slave trade,
having fertile soils and diverse ecological conditions, São Tomé was often used as an
agricultural experimental ground, receiving crops from all over the world (Ferrão
2005), as well as many other species of flora (Figueiredo et al. 2011) and fauna
(Dutton 1994). Agriculture greatly changed the ecology of the island, creating the
conditions for many introduced species to expand across the island (Soares et al.
2020) that sometimes also became invasive in native undisturbed forests (Lima et al.
2014; Panisi 2017; De Menezes and Pagad 2020).
Previous Vegetation and Phytogeographical Classification
Previous works aimed to document vegetation types focused mostly on its physiognomy, the intensity and nature of anthropic impacts, and the use of abiotic gradients
as proxies, such as altitude and precipitation (Table 3.2).
Chevalier (1938–1939) was the first to mention different vegetation types. However, it was Exell (1944) who proposed a delimitation and detailed description of
several vegetation types. Exell recognized mangroves and coastal dunes as distinct
and narrowly distributed vegetation types, and used three altitudinal belts to distinguish the remaining vegetation: low-altitude (mostly degraded) forests (up to 700 or
900 m), montane rainforests (between 800 and 1400 m), and mist forests (above
1400 m; Fig. 3.3).
Silva (1958) distinguished “primary” from “secondary” vegetation, and “climatedriven” from “edaphic-driven” vegetation, including summit shrubland and dry
northern savannas in the latter (Fig. 3.3c). This approach also acknowledged the
crucial role of human activities in transforming the landscapes of São Tomé.
Table 3.2 Key references proposing spatial delimitations of the islands in ecological, ecosystems,
or phytogeographical units
References
Mildbraed
(1922)
Exell (1944)
Silva (1958)
Monod
(1960)
Peris (1962)
Stévart (1998)
Diniz and
Matos (2002)
Island(s)
Annobón
São Tomé
and Príncipe
São Tomé
and Príncipe
São Tomé
and Príncipe
Annobón
São Tomé
and Príncipe
São Tomé
and Príncipe
Content
Five vegetation
types
Elevational belt
Criteria
Flora and vegetation physiognomy,
elevation
Abiotic gradients
Map of vegetation
units
Documentation of
vegetation type
Six vegetation types
Elevation and land use
Map of vegetation
units
Map of agroecological entities
Elevation, presence of endemic plant
species
Flora and vegetation physiognomy, elevation, agricultural activities
Elevation, annual rainfall, presence of
orchids species
Field observations, topography, edaphic
properties, elevation
3
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45
Fig. 3.3 Previous delimitations of vegetation types or phytogeographical territories on São Tomé
Island. (a) According to Monod (1960) and Exell (1944); (b) According to Stévart (1998);
(c) According to Silva (1958); (d) According to Diniz and Matos (2002). For the Diniz and
Matos (2002) map, only the main regions are shown
Monod (1960) was especially interested in the altitudinal variation of vegetation.
He extended previous classifications (Fig. 3.3a), highlighting the uniqueness of the
high-altitude shrublands distributed in several small patches above 1900 m, which
hosts some emblematic endemic plant species, such as Erica thomensis (Henriq)
Dorr & E.G.H. Oliv. 1999 and Lobelia barnsii Exell 1944.
Stévart (1998) proposed a phytogeographical classification based on the distribution of orchid species and their auto-ecology (Fig. 3.3b). He was the first author to
explicitly consider the rainfall pattern distinguishing the dry north and the wet south
of the island, following the 3000 mm annual rainfall isohyet. He suggested that the
area around Lagoa Amélia could be a distinct vegetation type. Stévart (1998) also
pointed out that several ridges at lower elevation (below 800 m) in the southeast had
a unique assemblage of orchid species. The floristic distinction of those ridges could
46
G. Dauby et al.
be driven by the combination of topographic position and high precipitation,
although data were very limited at the time.
Diniz and Matos (2002) provided a detailed map of 109 agro-ecological units
distributed in two main regions (Fig. 3.3d). Although their primary goal was to
assess the potential of each unit for agricultural production, they also provide
detailed descriptions of vegetation and flora in each unit. The northern region
broadly corresponds to the area with <2000 mm of annual rainfall, and is divided
into three sub-regions; the littoral plain with a semi-arid climate, the transition area
with a sub-humid climate, elevations between 300 and 550 m with slopes that do not
exceed 15%, and the mountainous more humid area. The southern region is
described as more homogenous, being characterized by the steep transition between
the central mountainous highland and the littoral band, composed of ridges and deep
valleys.
Príncipe Island
Abiotic Gradients
The mainland of Príncipe Island has a maximum length of 18.5 km (north to south)
and 11 km in its maximum width (east to west), with an area of approximately
139 km2. It is located 220 km off the West African coast and 146 km north of São
Tomé (Diniz and Matos 2002; Dallimer and Melo 2010). The north of the island is
relatively flat, whereas the south-center has the largest elevated area (>500 m),
including Pico do Príncipe that reaches 942 m, and multiple peaks surrounded by
steep slopes and ridges (Fig. 3.4).
Just like São Tomé, our knowledge of rainfall patterns still relies on rough
isohyets drawn several decades ago. Annual rainfall ranges from more than
4000 mm in the southeast to <2000 mm in the northeast, which is a remarkable
contrast in such a small area. Cloud cover follows broadly the same pattern as annual
rainfall, highlighting the elevated and rugged area around the Pico Príncipe (Diniz
and Matos 2002). Four seasons are also recognized for Príncipe, following the same
patterns found in São Tomé.
Soils have been studied and mapped (Diniz and Matos 2002). Bedrocks are
predominantly volcanic, mostly in the north, while Phonolite rocks are more common in the south. As on São Tomé, the most frequent soils are highly weathered such
as Ferralsols and Lixisols (Cardoso and Garcia 1962).
Human Disturbance
The history of land occupation on Príncipe is broadly similar to that of São Tomé.
However, contrary to São Tomé, no large areas are regularly burned. A peculiarity in
the history of Príncipe is the intense deforestation campaign that took place between
3
Classification, Distribution, and Biodiversity of Terrestrial. . .
Fig. 3.4 Main physico-climatic gradients in Príncipe Island
47
48
G. Dauby et al.
1911 and 1916 to eradicate the tsetse fly vector of sleeping sickness (da Costa et al.
1916):
The steps taken (. . .) consisted principally in the clearing away of herbaceous and bushy
vegetation, in the opening out to the sun’s rays of the margins of watercourses and swamps,
straightening out and leveling the banks and the beds of these, draining and filling swamps,
and forest fellings on a large scale.
More than 15 km2 of native forests in the northern part of the island were deforested
(11% of the island), while many plantations were also being abandoned (da Costa
et al. 1916; da Silva 2019).
Nearly all lowland forests in Príncipe have been disturbed by human activity
(Fig. 3.5), creating a mosaic of native and secondary forest, as well as active and
abandoned agricultural lands (Dallimer et al. 2012). Most of the remaining native
vegetation occurs at mid and high elevation and is included in the Príncipe Natural
Park, a protected area created in 2006 that covers around 21% of Príncipe, mostly in
the south (Ministry of Infrastructure, Natural Resources and Environment 2016).
Fig. 3.5 Degraded or transformed land cover in Príncipe (Adapted from Frazer Sinclair and
Yodiney dos Santos, unpublished data). Note that the “open vegetation” category includes both
agricultural lands and savanna-like vegetation but also potentially natural edaphic open vegetation
3
Classification, Distribution, and Biodiversity of Terrestrial. . .
49
The whole island was declared a UNESCO Man and Biosphere Reserve by 2012
(UNESCO 2021).
Previous Vegetation and Phytogeographical Classification
The distribution of forests on Príncipe was first depicted in a land cover map (IGC
1964) based on aerial photos and ground surveys. This map delimited the island
according to land use in several categories, as natural forests or abandoned plantations, cacao plantations, coffee plantations, oil palm plantations, coconut plantations,
agriculture, gardens, vegetable gardens or orchards, bush, undergrowth, or
grasslands.
The native vegetation of Príncipe is similar to that of São Tomé, with plant
families Rubiaceae, Euphorbiaceae, and Orchidaceae dominant (Figueiredo et al.
2011). It includes mangroves, but not savannas. Submontane forest is recorded only
on the summit, at Pico do Príncipe, though Exell (1944) claimed that the composition of the vegetation at higher altitudes on Príncipe (namely Pico Papagaio; 680 m
and Pico do Príncipe; 948 m) resembled that of lowland rainforest on São Tomé.
Diniz and Matos (2002) relied on climate, topography, and soil types to identify
28 agro-ecological units, which they described and delimited in detail. The vegetation is characterized by forests, ranging from primary (“obô”) to secondary formations (“capoeira”) and to strongly anthropized environments, including diverse types
of plantations such as shaded cacao or coconut monocultures.
Forest tree communities were recently studied across the island, documenting
floristic differentiation across north-south and altitudinal gradients (Fauna and Flora
International 2018). These patterns were driven, at least partly, by a decrease in the
relative abundance and diversity of tree species in secondary forests, highlighting the
influence of past disturbances on forest tree composition.
Annobón Island
Abiotic Gradients
Of the three Gulf of Guinea Islands, Annobón is the smallest (17 km2) and farthest
from the mainland, located 360 km west of Gabon and 190 km southwest of São
Tomé. Despite the small size, its geography is diverse. There is a 700 m wide crater
at 150 m elevation, occupied by Lake A Pot, which has several adventitious cones,
including the 400 m wide crater of Punta Manjob in the SE, the Quioveo and Santa
Mina mountains, and northeast-southwest corridor that links the bays of San Pedro
and Santa Cruz to the Anganchi river (Fig. 3.6). Santa Mina is the highest elevation
at 613 m.
Annobón has an average temperature of 26 C with little annual variation.
Rainfall is primarily affected by the oceanic winds that cause a pronounced dry
50
G. Dauby et al.
season from May to October, while the rest of the year is wet (Juste and Fa 1994). No
accurate rainfall data is available, but maximum precipitation is around 3000 mm
(Juste and Fa 1994; Velayos et al. 2014). Remotely sensed data suggests that intraannual variability in cloud cover is less pronounced than on Príncipe or São Tomé,
even though there is still a north-south humidity gradient, ranging from <70% in the
north to almost 90% in the south (Fig. 3.6).
The soils of Annobón have not been thoroughly studied and mapped. However,
they are ultrabasic and have the same volcanic origin as those of Bioko with lower
silica and higher proportions of ferromagnesian elements (De Castro and De la Calle
1985).
Human Disturbance
Humans have modified most of the vegetation on Annobón (Fig. 3.7), except for the
high peaks of Santa Mina and Quioveo. San Antonio de Palé or “Ambo,” located in
the extreme north of the island, is the only permanent town. Most subsistence farms
are on the fertile plains around the town, producing yuca (Manihot esculenta Crantz
1766), banana, and malanga (Xanthosoma violaceum Schott 1853). However, these
small-scale plantations (“fincas”) can now be found everywhere on the island, even
in steep slopes (Velayos et al. 2014), and their encroachment in the montane forests
of Quioveo and Santa Mina is set to cause irreversible damage. Other villages are
temporarily occupied during the dry season or holiday months. More recently, the
expansion of the airport and seaport must have had considerable environmental
impacts.
Previous Vegetation and Phytogeographical Classification
Only two studies attempted to delineate and document vegetation on Annobón. The
first (Mildbraed 1922) proposed five vegetation types: (1) coastal “Sandstrand,”
(2) “Vorland,” a savanna-like forest mixed with plantations, (3) “Buschwald,” oil
palm artisanal plantations mixed with others tree species, (4) lowland dry forest,
“Trockener Wald,” and (5) “Nebelwald,” a cloud forest found mostly above 500 m
that is rich in orchid and fern species, including tree ferns Alsophila spp.
The second study (Peris 1962) proposed six vegetation types: (1) coastal,
subdivided into rocky and sandy shores, (2) open vegetation strongly transformed
by human activities, which was divided into herbaceous savanna-like vegetation,
large-leaved savanna-like vegetation, cassava plantation, and shrubland, (3) dry
forest, equivalent mostly to “trockener Wald,” (4) wet forest, also included in
“trockener Wald” but distinguished by the presence of Olea welwitschii Gilg &
G. Schellenb. 1913, (5) Hymenophyllum spp. cloud forest in the peaks of Santa Mina
and Quioveo (see Fig. 3.8), and (6) tree fern areas in the summit of Santa Mina.
3
Classification, Distribution, and Biodiversity of Terrestrial. . .
51
Fig. 3.6 Main physico-climatic gradients in Annobón island. The dark gray polygon represents the
crater lake A Pot
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G. Dauby et al.
Fig. 3.7 (a) Degraded or transformed land cover on Annobón (Adapted from Norder et al. 2020).
Note that the “open vegetation” category includes both agricultural lands and savanna-like vegetation but also naturally open vegetation type. (b) Annual fire frequency (data for the last 20 years).
Inset barplot shows the distribution of these fires during the year
3
Classification, Distribution, and Biodiversity of Terrestrial. . .
53
Fig. 3.8 Examples of terrestrial ecosystem types from the oceanic islands of the Gulf of Guinea.
From top left to bottom right: (1) Mesic old-growth lowland rainforest in southwest São Tomé,
where upper strata is dominated by Uapaca vanhouttei Pax 1908; (2) Vegetation on the Pico
Pequeno characterized by small trees and shrub and the largest known population of Erica
thomensis (Henriq.) Dorr & E.G.H. Oliv. 1999, endemic to this area; (3) typical mangrove with
Rhizophora L. 1753 stilt roots in São Tomé; (4) the mosaic of lowland deciduous forest and savanna
in the north of São Tomé; (5) lowland semi-deciduous forest in the background and savanna in the
forefront, in Annobón; (6) rainforest in Annobón on the Quioveo peak above 500 m. According to
the new classification, it is lowland rainforest, but the abundance of ferns and epiphyte suggests it is
instead submontane rainforest similar to what can be found above 800 m in São Tomé; (7) Lowland
54
G. Dauby et al.
Classification Synthesis
Ecosystems are by definition open, dynamic, and scale-dependent, emerging from
the interactions between organisms and the physical environment. Assuming that
classifications are necessarily a simplification of reality, it makes sense to use
variations in environmental conditions and biological communities to classify terrestrial ecosystems. Our goal here is to provide an updated classification, based on
previous attempts and current knowledge, offering baselines for management and
future scientific research on the dynamics of biodiversity.
Methodology
Spatial Information
We compiled previous classifications (Table 3.2) and mapped key ones, using QGIS
(QGIS Development Team 2021) and R (R Core Team 2021) for georeferencing and
analyzing spatial data. We retrieved several spatial features from Open Street Map
(OSM) database using “osmdata” R package (Padgham et al. 2017) and other freely
available shapefiles (see https://github.com/gdauby/stpa_ecosystems_review for further details on codes and data sources).
Synthetic Classification Mapping
We first considered abiotic gradients that drive potential natural ecosystems (e.g.,
temperature, rainfall, topography), and then vegetation types or proxies of anthropogenic impacts (e.g., secondary vegetation, shade tree plantation, fire frequency,
urban area). This approach requires defining thresholds for characterizing ecosystems for continuous abiotic gradients, and acquiring spatial information on the
distribution, nature, and intensity of human impacts. Thus, one map presents “potential natural ecosystems,” which can be discussed in terms of potential vegetation
types. A second map presents the developmental stages, resulting from natural or
anthropogenic land-use changes. To analyze the relative importance of developmental stages in each ecosystem, we estimated the total area and proportion of each stage
in each potential natural ecosystem. Spatial analyses were conducted in R using the
packages “sf” (Pebesma 2018), “cleangeo” (Blondel 2019), and “sp” (Bivand et al.
2013) (see R codes here: https://github.com/gdauby/stpa_ecosystems_review).
Fig. 3.8 (continued) moist forest from the north of Príncipe, partly secondarized as indicated by the
presence of Elaeis guineensis Jacq. 1763; (8) Lowland wet forest from the south of Príncipe. Photo
credits: (1) G. Dauby, (2) D. U. Ikabanga, (3) Paula Chainho, (4) R. F. de Lima, (5,6) P. Barbéra,
(7) L. Benitez, (8) T. Stévart
3
Classification, Distribution, and Biodiversity of Terrestrial. . .
55
Annobón was excluded from this analysis because rainfall data was missing, but we
still discuss similarities with the other islands.
Mapping Non-Forested Areas
To evaluate developmental stages of terrestrial ecosystems on Príncipe and São
Tomé, an important first step was to identify forested and non-forested areas. To do
so, we uploaded very high-resolution satellite images (sentinel-2) (https://peps.cnes.
fr/rocket/) from the long dry season to minimize cloud cover. Then, we used
eCognition software (Trimble Inc.) to segment spectrally homogeneous non-forest
polygons based on thresholding normalized difference vegetation index. The
resulting polygons were manually checked using Google Earth and added to a vector
layer, which was combined with the land cover types retrieved from OSM, namely
polygons identified as “scrub” and various built categories (residential, commercial).
We also selected the “roads” tag polylines to be converted into polygons by adding a
10 m buffer. The final shapefiles distinguished non-forested “urban areas,” “roads
and path network,” and “any other non-forested areas,” which included agricultural
land, deforested wastelands, but also naturally open vegetation types that could not
be distinguished at fine scale.
High-quality satellite images were not available for Annobón, so we used the
OSM shapefile to extract buildings and forest polygons. The “buildings” shapefile
was edited based on Google Earth, and a 100 m buffer was added to identify areas
impacted by urban activities.
Ecosystem Delimitations
The methodology is based on principles from the Ecosystemology approach recently
proposed by Senterre et al. (2021). We defined regional-scale ecosystems based on
relevant available abiotic gradients, namely altitude, precipitation, distance to coast,
and cloud frequency. Within each of these units, we identified the distribution and
extent of stand-scale units using abiotic gradients at a finer scale, such as topography,
and soil features including humidity and salinity (Table 3.3). Thresholds were set
based on the literature and on personal experiences and observations of the authors.
Regional- and stand-scale ecosystems were listed, and their features discussed.
In parallel, we gathered spatial information on the distribution of human impacts
on São Tomé and Príncipe (Fig. 3.2; Table 3.2), which were not included in the
classification process, but were overlaid over the regional-scale units (Supp. Mat.).
We estimated that secondary forests and shade plantations together cover over half
of São Tomé and of Príncipe (28 and 27%, and 26 and 30%, respectively), while
native vegetation covers around one-third or less (27 and 35%, respectively). Similar
information was not available for Annobón, but recent observations suggest that
native vegetation is mostly restricted to the highest peaks.
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G. Dauby et al.
Table 3.3 Total area and relative importance of each stand-scale ecosystem defined for São Tomé
and Príncipe
Ecosystem type
Montane forests
Mesic
On steep slope
On ridge
Montane low forest, grasslands, and shrublands
Submontane rainforest
Mesic
In valley
On ridge
On steep slope
Lowland deciduous forests and woodlands
Mesic
On Vertisols
In valleys
On steep slope
On Fluvisols
Lowland moist and wet rainforests
Mesic
On ridge
On steep slope
In valleys
On Fluvisols
Coastal ecosystems
Undifferentiated shores
Mangroves
Sandy shores
Palustrine areas
São Tomé
7.9 km2 (0.9%)
3.3 km2 (0.4%)
3.1 km2 (0.4%)
1.5 km2 (0.2%)
0.7 km2 (0.1%)
80.1 km2 (9.4%)
39.9 km2 (4.7%)
4.5 km2 (0.5%)
7.8 km2 (0.9%)
28 km2 (3.3%)
344.2 km2 (40.4%)
248.6 km2 (29.2%)
51.4 km2 (6%)
10.4 km2 (1.2%)
21.6 km2 (2.5%)
12.1 km2 (1.4%)
459.7 km2 (54%)
329.6 km2 (38.7%)
30.7 km2 (3.6%)
63.6 km2 (7.5%)
24.2 km2 (2.8%)
11.6 km2 (1.4%)
10.4 km2 (1.2%)
9.2 km2 (1.1%)
0.9 km2 (0.1%)
0.3 km2 (< 0.1%)
0.1 km2 (< 0.1%)
Príncipe
–
–
–
–
–
0.8 km2 (0.6%)
0.2 km2 (0.1%)
0.04 km2 (0%)
0.1 km2 (0.1%)
0.5 km2 (0.3%)
43.4 km2 (31.1%)
43.1 km2 (30.9%)
–
0.1 km2 (0.1%)
0.2 km2 (0.1%)
–
92.2 km2 (66.2%)
74.3 km2 (53.3%)
4.8 km2 (3.4%)
9.3 km2 (6.7%)
3.8 km2 (2.8%)
–
2.6 km2 (1.9%)
2.1 km2 (1.5%)
0.02 km2 (< 0.1%)
0.4 km2 (0.3%)
0.1 km2 (< 0.1%)
All classifications produced in this chapter and associated resources are accessible
online (https://github.com/gdauby/stpa_ecosystems_review).
Coastal Ecosystems
The coasts of São Tomé, Príncipe, and Annobón are approximately 204, 100, and
35 km long respectively, and include mangroves, other palustrine areas, sandy
coasts, and cliffs.
At the interface between terrestrial, freshwater, and marine realms, mangroves are
the most distinctive coastal ecosystems on the islands (Herrero-Barrencua et al.
2017; Afonso 2019). On São Tomé, at least 14 mangroves areas persist (Fig. 3.8).
Malanza and São João dos Angolares are the largest, and Malanza and Praia das
3
Classification, Distribution, and Biodiversity of Terrestrial. . .
57
Conchas are the only ones within a protected area. In Príncipe, mangroves persist at
Praia Caixão, Praia Grande, and Praia Salgada. Even though there is no estimate of
the lost mangrove area, past distribution was certainly wider, especially in the north
of São Tomé (Herrero-Barrencua et al. 2017). Mangroves are absent on Annobón
(Juste and Fa 1994).
Other estuarine ecosystems often occupy similar conditions surrounding mangroves, some of which might have resulted from mangrove degradation on São
Tomé. Sandy coasts are sparsely distributed across the three islands and host distinct
psammophile communities.
Cliffs are frequent but their distribution and associated biota are poorly characterized. In the south of São Tomé, dense populations of Pandanus thomensis Henriq.
1887 frequently colonize them. Given its distinct edaphic properties, this ecosystem
might be less impacted by human activities than others, but its vulnerability to
invasive species remains unknown.
At least 15% of the coast of São Tomé and 12% of that of Príncipe have been
strongly impacted and transformed into urban areas or roads. More than 50% of
coastal ecosystems on São Tomé and 13% in Príncipe are covered by, or are next to
secondary forests or shade plantations (Supp. Mat.).
Non-coastal Wetlands
Non-coastal wetlands include all habitats that are seasonally or permanently inundated by freshwater. We distinguished riverine forests, waterfalls, lowland swamp,
and montane swamps.
Riverine forests can be defined as areas that are influenced by river soaking and
flooding. Their distribution, extent, and associated biological communities are
poorly characterized in the GGOI. Their width is expected to be small, considering
most valleys are narrow, but this influence can be larger, particularly in flatter areas.
Waterfalls display specific geomorphic and micro-habitats features with strong
but very localized, environmental heterogeneity and originality (Clayton and Pearson 2016). They also act as natural barriers, dividing streams and their associated
biotas into distinct populations. Their biota characteristics and ecosystem functions
have rarely been investigated in tropical regions, but some studies have highlighted
their ecological and conservation significance (Baker et al. 2017). The distribution
and ecological characteristics of waterfalls in the GGOI are not well known and
deserve further attention, especially since they may be threatened by dams in the near
future.
Lowland swamps are infrequent and small on São Tomé but seem to be somewhat
more widespread in the northern plateau of Príncipe. This situation contrasts with
continental central Africa, where swamp forests are frequent and harbor specific
biological communities (e.g., Boupoya et al. 2017), but almost nothing is known
about swamp forests in the GGOI. We do know, however, that large areas of
Príncipe’s swamps were drained during the tsetse eradication campaign in the
early twentieth century (da Costa et al. 1916).
58
G. Dauby et al.
The only significant example of a montane swamp is the Lagoa Amélia, at
c. 1400 m on São Tomé. Floristically, there is no evidence that this area has a
distinct assemblage, but it represents a unique combination of environmental conditions in the GGOI, being a super humid, high-altitude swamp.
Inland Uplands
Inland uplands represent almost the entirety of the GGOI. In São Tomé and Príncipe,
we divided them first by elevation, by thresholds at 800 m, 1400 m, and 1800 m, and
then by the 2000 mm annual rainfall threshold. This allowed us to distinguish
(1) lowland deciduous forests, (2) lowland moist and wet forests, (3) submontane
rainforests, (4) montane forests, and (5) montane shrublands and grasslands. For
each of these, we identified abiotic factors that may exacerbate or mitigate the local
influence of temperature or water availability relative to the mesic environment.
Namely, we considered specific soil types, slopes with steep gradients, and specific
topographic categories, such as valleys and ridges. Steep slopes (> 30 ) are likely to
have superficial soils (Lithosols), increased susceptibility to erosion (landslides), and
distinct micro-climate due to stronger (or weaker) insolation, depending on the
aspect (Chapin III et al. 2011). They are also less directly threatened by anthropogenic activities.
Lowland Deciduous Forests
Occurring up to 800 m of elevation and registering <2000 mm of rainfall annually,
these ecosystems are mostly found on the flat or gentle slopes of northern São Tomé.
Given the limited rainfall, lower cloud frequency, and higher temperatures, water
availability is probably the main limiting factor for vegetation growth. Vegetation
composition and physiognomy also support the local influence of edaphic or topographical features. As such, we distinguished (1) forests on flat terrain and Fluvisols,
(2) forests on flat terrain and Vertisols, (3) forests in valleys, and (4) forests on steep
slopes. Almost none of this native forest vegetation remains, but we can assume the
vegetation type in mesic conditions should have been a (semi)-deciduous or dry
forest.
Fluvisols occur along large rivers on flat terrain, and are usually susceptible to
occasional flooding. Native vegetation must have been moist semi-deciduous forest
with higher frequency of species tolerant to poorly drained soils. This is the most
disturbed ecosystem on São Tomé; ca. 23% are covered by roads and urban areas,
and more than 30% by open agricultural land (Supp. Mat.). Fluvisols are infrequent
on Príncipe (Diniz and Matos 2002).
Forest on flat terrain and Vertisols is only found on São Tomé, where it corresponds mostly to savanna-like vegetation. Soil moisture on Vertisols is highly
variable, leaving plants vulnerable to drought. However, it is noteworthy that there
are no indications that these savannas existed when human colonization started on
3
Classification, Distribution, and Biodiversity of Terrestrial. . .
59
São Tomé, 500 years ago. It has been proposed that any such areas originally
covered by the dry forest were lost to fires and sugarcane plantations (Diniz and
Matos 2002). Later on, sugarcane production was mostly abandoned, but forests
could not reestablish due to changes in soil properties and to regular fires during the
dry season (Fig. 3.2). Nowadays, more than half of this area has open vegetation,
mainly savanna-like but also agricultural lands, and around 15% has been converted
to urban areas or to roads. Several plant communities occur in this mosaic of forest
and savannas, where the landscape is locally dominated by the African baobab
Adansonia digitata L. 1759. This complex mosaic might present some similarities
with the north of Annobón, nowadays mostly occupied by urban areas.
In large and narrow valleys, particularly in the extreme north of São Tomé, water
is less limited thanks to run-off from the central highlands. Floristic composition
(Diniz and Matos 2002, personal observations) suggests that this specific topography
holds distinct plant communities. This stand-scale ecosystem may also be significant
for conservation as it might host the last remnant of lowland moist forests in the
north of São Tomé, as almost all of these have been converted to shade cacao
plantations, urban areas, and roads.
The forests surrounding the large valleys of São Tomé occur on the steep slopes,
occupying a significant area (Table 3.3) that is less directly impacted by human
activities, although most of these are nevertheless secondary forests.
Lowland Moist and Wet Rainforests
This regional-scale ecosystem includes all areas up to 800 m of elevation and above
2000 mm of annual rainfall, which are less limited by water availability due to lower
seasonality. We considered topographic and soil features to distinguish forests (1) in
valleys, (2) on ridges, (3) on steep slopes, and (4) on Fluvisols. Natural vegetation in
mesic conditions is undoubtedly rainforest that still occupies most of São Tomé and
Príncipe, even if most is secondary. On São Tomé, industrial palm plantations
occupy more than 5% of this ecosystem. Overall, we estimate that native forests
persist in <40% of its original area.
Forests in valleys occupy 4% of this region-scale ecosystem in Príncipe and 5% in
São Tomé.
Forests on ridges have limited extent both on Príncipe and São Tomé but also
seem to have been less impacted, due to their lower accessibility and reduced
potential for agriculture. The biological communities here are poorly known. It has
been suggested that lowland peaks, such as the Pico Maria Fernandes on São Tomé
and Morro Fundão on Príncipe, host distinct plant assemblages that are more closely
related to submontane vegetation than to surrounding lowland forests (Stévart 1998;
Ogonovszky 2003). Biota and physico-climatic similarities of lowland ridges
between the GGOI are likely and should be assessed. Indeed, these specific habitats
are covered by low and open vegetation, close to those occurring on mainland
inselbergs. However, the proximity to the ocean should increase moisture even
60
G. Dauby et al.
during dry seasons, allowing for the development of a distinct vegetation type in
these rocky places.
Forests on steep slopes occupy a significant extent and also seem to have been
less impacted than other forest types due to their lower accessibility and potential for
agriculture.
Forests on Fluvisols have only been identified in the large watersheds of Iô
Grande and Xufe-Xufe on São Tomé. These correspond to flat lowland areas near
the coast and that have thus been strongly impacted by human activities, namely by
agricultural development.
Submontane Rainforest
Submontane rainforests include areas between 800 and 1400 m, and apart from
mesic conditions, we distinguished forests (1) on ridges, (2) on steep slopes, and
(3) in valleys. On São Tomé, we estimated that 9% of the potential area for
submontane rainforest is currently non-forested, most of which is agricultural,
while 15% is secondary forest and 2.5% shade forest. The extent on Príncipe is
very limited (Table 3.3) but has been spared from human activities. A small portion
of this territory (>5%) appears to be non-forested, probably due to natural treeless
Lithosols. Annobón has no area above 800 m and thus submontane rainforests may
not occur there (but see discussion).
Forests on ridges are often characterized by the endemic gymnosperm Afrocarpus
mannii (Hook.) C.N. Page 1989. They represent nearly 10% of submontane forests
on São Tomé, while forests on steep slopes represent almost 35%. Both these forest
types are likely to be spared from direct human disturbances, even though natural
disturbances, such as landslides, are probably frequent.
Montane Forests
The area between 1400 and 1800 m is restricted to São Tomé and includes mainly
montane rainforests. This ecosystem is almost intact, although introduced plant
species can be locally abundant (e.g., tree species Cinchona spp. L. 1753). We
distinguished (1) forests on ridges, (2) forests on slopes and plateau, and (3) montane
grasslands.
Montane forests on ridges occupy nearly 20% of this region and are similar to
submontane ridge forests, as indicated by the sun-loving tree Afrocarpus mannii, but
also by herbs such as Begonia thomeana C. DC. 1892 and Mapania ferruginea Ridl.
1887. Forests on slopes and plateaus remain poorly documented because of their
limited accessibility, even though they represent nearly half of this region. Both
submontane and montane forests are characterized by forest species like Palisota
pedicellata K. Schum. 1897, Homalium henriquesii Gilg ex Engl. 1921
Tabernaemontana stenosiphon Stapf 1895, and Craterispermum cerinanthum
Hiern 1877 (formerly C. montanum Hiern 1877 but considered as synonym by
3
Classification, Distribution, and Biodiversity of Terrestrial. . .
61
Taedoumg (2020)). However, certain montane forest species, such as Symphonia
globulifera L. f. 1782, can also be found on ridges at lower elevations, indicating that
the transition between submontane and montane forest depends on the local topography, a topic that surely deserves attention in future studies. The physiognomy and
the floristic composition of the montane grassland have been relatively well
described, but its precise extent is unknown.
Montane Low Forest, Grasslands, and Shrublands
We consider this ecosystem above 1800 m as distinct from the Montane Forests
because of its specific physiognomy characterized by the frequency of shrubby
vegetation and smaller trees on ridges. Grass mat is also abundant along the ridges,
but these grasslands can also be observed at lower altitude along ridges. The
presence of plant taxa such as Erica, Lobelia, and the tree Balthasaria mannii
(Oliv.) Verdc. 1969 makes this ecosystem as the most distinct in the GGOI, showing
affinities to biological assemblages observed in other mountains ranges, such as on
Bioko and in East Africa (Monod 1960). In addition to its unique species assemblage, the upper montane area of São Tomé also seems to display distinct abiotic
properties. The “prevalent mist” of the “mist rainforests” is impressive but might be
less important for the development of this specific community than the superficial
soils (Exell 1944). Indeed, as Monod (1960) described, the area above 1800 m is
often above the clouds and therefore tends to be relatively dry (especially during the
dry season), while the montane and submontane forests at lower altitude remain
wetter thanks to the nearly permanent mist (Fig. 3.1). Monod (1960) even noticed
(in August, hence at the end of the dry season) that the vegetation was dry enough to
be vulnerable to fires.
Besides ecotourism activity (which may bring seeds of invasive species, foster
clearings along ridges, and provoke accidental fires during the dry season), this
ecosystem has been mostly spared from direct human degradation. However, it may
very well be one of the most threatened, considering its narrow distribution
(ca. 0.66 km2), the impact of climate change, and the spread of invasive species,
in particular Cinchona spp. trees. This genus has been considered among the most
invasive in many tropical islands (Jäger 2015), and especially in naturally treeless
environments (Jäger et al. 2007). We do not know if these taxa are replacing native
plant populations, but it is the dominant species (mono-dominant locally) along
several ridges. This may be the consequence of vegetation clearings in the past and
Cinchona plantings (Monod 1960).
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Discussion
Defining ecosystems as discrete units is a simplification (Boitani et al. 2015) but can
be useful to facilitate our understanding of a complex reality (Senterre et al. 2021).
While the delineation of some ecosystems is straightforward, it is often not the case
because transitions are usually not abrupt (Exell 1944; Monod 1960). The classification we propose tries to improve on existing classifications based on the best
available data, to provide better baselines for management, and for testing hypotheses regarding biodiversity dynamics. This synthetic classification is thus likely to
evolve as more data become available, namely regarding the distribution of ecosystems, and specifically of vegetation types on different islands. For future reference,
all maps and spatial information are available on an open-access portal (https://
github.com/gdauby/stpa_ecosystems_review).
Below, we point out several pending questions and challenges that became
apparent during this exercise and that could help guide future research on the
terrestrial ecosystems of the GGOI.
Is It Still Valid to Define Ecosystems Based on Altitude?
Most changes in large units of natural vegetation in the GGOI, and in the distribution
of species, appear to be associated with altitude, explaining why the first naturalists
(Exell 1944; Monod 1960) focused on the influence of this environmental gradient
on biological communities. Altitude (i.e., a proxy for temperature pattern) interacts
with topography and rainfall, creating micro-environmental conditions that can
affect vegetation at a fine scale, and that remain poorly understood due to their
subtle variations and complex effects on the distribution and abundance of species.
Moreover, the intensity of anthropogenic disturbances interacts with this natural
complexity, further complicating our understanding of ecosystem dynamics. As an
example, these disturbances (and deforestation in particular) are typically more
intense in the lowlands, where several populations of native species might have
already been extirpated. In this scenario, their current distributions are artificially
correlated with altitude, misguiding our understanding of the ecology of those
species.
Even if altitude is still the best available proxy for delimiting large natural
vegetation types, it may be hard to understand, or even misleading when trying to
infer drivers of species distribution. For example, if those drivers are linked to
precipitation or moisture, (sub)montane species may persist as satellite populations
at lower altitudes where micro-habitats are sufficiently humid, such as deep valleys
or riverine areas. Setting a threshold of 800 m for submontane forest, as we did,
means this forest type does not occur on Annobón where the maximal altitude is
600 m. However, the description of the floristic and physiognomic features of the
forest above 500 m (Peris 1962) does suggest some similarities with submontane
3
Classification, Distribution, and Biodiversity of Terrestrial. . .
63
forests found on São Tomé. If confirmed, this would suggest that humidity matters
more than altitude for defining submontane forest. Comprehensive surveys of biota
and physical features are still required across the islands to improve our understanding of the distribution of vegetation types and underlying environmental drivers.
What Is the Extent of Novel Ecosystems?
All three islands have high proportions of introduced species, whose frequency and
abundance vary between ecosystems. Increasing proportions of introduced species
can lead to changes in ecosystem functioning (Wardle et al. 2011). These taxonomic
and functional turnovers can lead to the development of “novel” ecosystems
resulting from human intervention; i.e., the ecosystem becomes self-sustaining in
an alternative stable state (Hobbs et al. 2009; Morse et al. 2014). Applying these
concepts for characterizing altered ecosystems is key for conservation and management, especially in oceanic islands where ecosystems are more prone to the threats
posed by introduced species (Sax and Gaines 2008; Morse et al. 2014). Novel
ecosystems, such as secondary vegetation and plantations, cover most of the
GGOI and are far from homogenous, presenting a wide variety of species assemblages. The functioning of these new assemblages, whether they differ from that of
native ecosystems and affect ecosystem services, remains to be investigated.
Which Factors Drive the Establishment of Novel Ecosystems?
The development of novel ecosystems results from the expansion of introduced
species, which often but not always results from anthropogenic land-use changes
(Morse et al. 2014). Novel ecosystems in the GGOI, and their accompanying
introduced species, are probably more widespread in active and abandoned lowland
agricultural areas, where historical land-use changes have been more significant
(Muñoz-Torrent et al. 2022). This has already been shown for GGOI birds (Soares
et al. 2020), and mollusk species assemblages (Panisi et al. 2022), for which invasion
success is highest in the lowland areas. Nevertheless, although less abundant and
diverse than in the lowlands, introduced species also occur in highland ecosystems
where native vegetation largely dominates. Similar patterns are expected for other
groups, such as plants. For example, species of Cinchona can be locally dominant in
lower strata of montane and submontane forests, where it was planted for bark
production (Chevalier 1938–1939). Populations of this species persist in
old-growth forests, but it is unknown if they are spreading and replacing native
species. In Estação Sousa on São Tomé, few individuals persist (unpublished results)
in an area that was a plantation over 100 years ago (Chevalier 1938–1939). It is
crucial to assess the vulnerability of highland ecosystems to introduced species,
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G. Dauby et al.
since these endemic-rich and diverse ecosystems have so far been the least impacted
by human activities (Muñoz-Torrent et al. 2022).
How to Prioritize Conservation Efforts?
An understanding of the distribution of endemic and threatened species across
ecosystems is necessary for allocating conservation efforts. Unfortunately, this
information remains insufficient for several areas and clades (Stévart et al. 2022;
Nève et al. 2022). Available data suggest that endemism tends to be higher in
submontane and montane ecosystems (Stévart et al. 2022). On the other hand,
lowland ecosystems are the most impacted and are often undersampled. For example, the extreme north of São Tomé hosts a complex mosaic of forest and savannas
that is probably the best example of a novel ecosystem in the GGOI. Most scientists
have focused on endemic-rich ecosystems, which at least partly explains why flora
and fauna in the extreme north remain undersampled (Stévart et al. 2022). However,
recent fieldwork (unpublished results) has led to the identification of some endemic
plants, including two putative new species, suggesting that native biodiversity
persists in these ecosystems. These discoveries highlight the importance of these
areas for conservation, emphasizing the urgent need for further studies in novel
ecosystems, particularly since native populations persisting in these areas may be
some of the most vulnerable to extinction.
How to Improve Ecosystem Monitoring Through Space
and Time?
Efficient ecosystem monitoring cannot rely solely on field observations, as these
demand too many resources. The use of remote sensing data can help extend current
assessments, in particular to document vegetation features and dynamics, but so far,
these have been limited by their coarse resolution, which are not appropriate to study
the complex landscapes of the GGOI. The availability of spectroscopic data and
analytical tools is constantly improving and, in combination with in situ observations, might enable meaningful ecosystem monitoring in the near future (CavenderBares et al. 2020). For example, hyperspectral images could help characterize the
dynamics of introduced plant species and thus infer the distribution of novel
ecosystems.
3
Classification, Distribution, and Biodiversity of Terrestrial. . .
65
The Need for a Unified Classification of Ecosystems for Central
Africa
Island ecosystems are ideal natural experiments to test hypotheses regarding the
links between biodiversity and ecosystem properties (Pimm 1984). To investigate
these hypotheses, it is useful to define ecosystem units that are transferable across
regions. In practice, such classification is challenging because there is no clear
definition on how ecosystems should be identified (but see Senterre et al. 2021),
despite international initiatives such as the Red List of Ecosystems (Keith et al.
2013). We support the development of an ecosystem classification that can be shared
between the GGOI and continental Africa, as it would allow comparative studies that
could greatly improve our understanding of regional biogeography and patterns of
species diversity.
Conclusions
The three GGOI present similar humidity gradients, increasing from the northeast to
the southwest due to the rugged topography and resulting foehn effect. These
gradients, along with altitude and anthropogenic disturbance, can be used to identify
distinct ecosystems and their distributions, and help to explain differences between
islands. The high concentration of biotic and abiotic complexity in these small island
territories creates unique combinations of features that shape ecosystem properties,
making them ideal for studying the dynamics of tropical ecosystems. However,
much of what is known about the GGOI is based mostly on São Tomé: by far the best
known but also the most diverse island. Overcoming existing knowledge gaps will
require multidisciplinary, collaborative frameworks and research agendas, which in
turn rely on long-term observatories and capacity building. We hope that the
synthetic ecosystem classification we have presented in this chapter, together with
all the underlying resources that we have made available, will foster the future
research needed for a better understanding and conservation of the tropical ecosystems of the GGOI.
Acknowledgments This work has been supported by the Critical Ecosystem Partnership Funding,
joint initiative of l’Agence Française de Développement, Conservation International, the European
Union, the Global Environment Facility, the Government of Japan, and the World Bank, through
the project CEPF-104130. RFL and FCS were funded by the Portuguese Government through
“Fundação para a Ciência e a Tecnologia” (FCT/MCTES – UID/BIA/00329/2021 and PD/BD/
140832/2018). Data collection in Príncipe was supported by the Global Trees Campaign through
multiple grants. Some map contains data © OpenStreetMap contributors, www.openstreetmap.org/
copyright. GD thanks Robin Pouteau for fruitful discussion on several ideas presented in this
chapter. We thank Tania Bird for revising the language. GD, TS, MCM and LB thank local teams
for their support on field work and data collection (ST: Angela Lima, António Camuenha, Dilson
M. Deus, Estevão Soares, Lewis Eduardo, Pascoal Sousa; P: Davide Dias, Jeremias Prazeres,
Osvaldo Lima).
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Chapter 4
Territory, Economy, and Demographic
Growth in São Tomé and Príncipe:
Anthropogenic Changes in Environment
Xavier Muñoz-Torrent, Ngouabi Tiny da Trindade, and Signe Mikulane
Abstract Nearly five centuries of human presence on the islands of the Gulf of
Guinea have considerably marked the landscape with the replacement of natural
habitats by roças (plantations) and other settlements, the introduction of numerous
exotic plant and animal species, and the exploitation of resources needed for urban
construction and daily life of the growing human population. Exponential population
growth and, consequently, the urban sprawl are resulting in deforestation, illegal
beach sand mining, exhaustion of natural resources, expansion of non-endemic
species, and extermination of the endemic ones, thus causing immense resource
exploitation and rapid environmental deterioration. The absence of an effective
territorial planning amplifies the island’s vulnerability and increases the fragility of
the ecosystems, posing clear threats to the islands’ unique biodiversity.
Keywords São Tomé and Príncipe · Biodiversity · Demographic growth ·
Economy · Environmental impact · Insularity · Environment-society interactions
Gulf of Guinea Oceanic Islands: A Biological Laboratory
of Landscape Alteration
In the context of the European expansion, African islands in the Atlantic were prime
spaces for experimentation of new agricultural species (Ferrão 2005). Since the early
period of the European Age of Expansion, and especially for the Portuguese
X. Muñoz-Torrent (*)
Servei d’Estudis i Observatori de la Ciutat de Terrassa, Terrassa, Catalonia, Spain
Associação Caué—Amigos de São Tomé e Príncipe, Barcelona, Catalonia, Spain
e-mail: xavier.munoz@saotomeprincipe.eu
N. T. da Trindade
Instituto Nacional de Estatística de São Tomé e Príncipe, São Tomé, Sao Tome and Principe
S. Mikulane
BIM Institut (Interdisziplinäres Institut der Fachbereiche Architektur, Bau- und
Umweltingenieurwesen und Geodäsie), Hochschule Bochum, Bochum, Germany
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_4
71
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Colonial Empire, these islands became biological laboratories for the acclimatization
of different economically interesting plants and animals from Europe and Africa, and
even later from South and Central America and Asia. Initially, the most basic need
for maritime expansions was the creation of safe ports for transoceanic trips, where
horticultural commodities could restock the ships. The Gulf of Guinea Oceanic
Islands served as a strategic base for the European colonial enterprise, especially
because the islands of Príncipe, São Tomé, and Annobón were uninhabited (e.g.,
Seibert 2004). Here, we describe the history of the relationships between the human
societies that inhabited these islands and their surrounding environment, with a focus
on the island of São Tomé from which the most information is available.
According to the existing historiography, Portuguese navigators were the first
humans to reach and colonize the oceanic islands of the Gulf of Guinea. São Tomé
and Príncipe islands were discovered by the Portuguese navigators João de Santarém
and Pêro Escobar on December 21, 1470, and January 17, 1471, respectively. The
island of Annobón was discovered on January 1, 1473, by the Portuguese navigator
Fernão do Pó who was attempting to find the maritime route to India. After a
previous failed colonization attempt, in 1486 the Portuguese military leader Álvaro
de Caminha became the third “donatário” (governor) of São Tomé and promoted the
first successful colonization of São Tomé, establishing a small village in the area
around Ana Chaves Bay, in the north-eastern part of the island (Seibert 2015). The
original settlers included Europeans consisting of volunteers, exiles, and a group of
Jewish children, as well as Africans, most of whom were enslaved (Seibert 2015).
The island of Príncipe would only start to become populated in the early sixteenth
century (Seibert 2015), and Annobón decades later, in 1592.
From these initial settlements until the mid-nineteenth century, the main economic activities of the islands were linked to the slave trade, in which the islands
functioned as an important entrepôt for the transatlantic trade (especially until the
mid-seventeenth century). The islands were also transformed by extensive sugarcane
monoculture plantations (mainly throughout the sixteenth century), especially in the
northeast of São Tomé (Seibert 2015). By the mid-sixteenth century, the island of
São Tomé was the world’s main producer of sugar, but the development of sugarcane cultivation in Brazil led to the collapse of São Tomé’s plantations by the
beginning of the seventeenth century (Seibert 2015). Revolts by enslaved Africans
also contributed to this decline, such as those led by the iconic King Amador in 1595
that devastated a considerable number of sugar mills (Seibert 2015). With the end of
the large sugarcane plantations, the islands’ economy was reduced to the production
of supplies to be sold to the ships that docked there. Many of these were linked to the
slave trade, which was limited in 1836 and completely banned with the abolition of
slavery in São Tomé and Príncipe in 1875, when enslaved plantation workers
transitioned to a subsistence wage labor model (Seibert 2015).
Despite the impact of sugar mills on the local landscape, the human population
during this early period was considerably low, with a total of 12,672 people on the
islands of São Tomé and Príncipe in 1758, of which only 53 were white Europeans
(Seibert 2015). From the second half of the nineteenth century onward, the islands
would witness the rapid expansion of coffee and cocoa crops, which came to
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Territory, Economy, and Demographic Growth in São Tomé and Príncipe:. . .
73
Fig. 4.1 Evolution of land occupation in São Tomé Island from the late sixteenth century (left:
1 Obô—forests, 2 sugarcane plantations and fields, 3 coconut palm and banana, 4 factories and
sugar mills, 5 wetlands) to 1957 (right: 1 cocoa, 2 coffee, 3 oleaginous trees, 4 quinines, 5 quintal
cultures, family horticulture, 6 Obô—forests). The diminishing cover of the Obô (dark gray area) is
evident. Tenreiro (1961)
dominate the economy and landscape through the establishment of dozens of roças
(plantations and their dependencies; Seibert 2015). According to available historical
data, cocoa plantations in 1913 occupied about three-fourths of the surface of São
Tomé and Príncipe islands, a proportion that would gradually start to decline after
the First World War, due to the infestation of cocoa trees by pests, soil erosion, and
expansion of cocoa cultivation in other regions (Seibert 2015). This decrease in
cocoa cultivation was such that by the time São Tomé and Príncipe became independent in 1975, the total planted area was only one-fourth of the country’s territory
(Seibert 2015). Nearly five centuries of human presence on the islands have considerably marked the landscape with the replacement of natural habitats by roças, the
introduction of numerous exotic plant and animal species, and the exploitation of
resources needed for urban construction and daily life of the growing human
population.
Similar to other Atlantic islands off the coast of Africa, the recent ecological and
landscape history of Sao Tomé and Príncipe is strongly linked to the growth of
human activity, including the degradation of native ecosystems and the establishment of alien species. This process was strongly associated with cycles of agricultural development, initially the production of sugarcane, and then coffee and cocoa
(Eyzaguirre 1986—Fig. 4.1). Cocoa in particular was decisive for the economic
development of the islands, with regressive stages leading to the generation of
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X. Muñoz-Torrent et al.
secondary forest, or scrub, which emerged mainly as a result of agricultural abandonment. More recently, ecosystems continue to be altered, namely by the installation of extensive areas of oil palm monoculture (Oyono et al. 2014).
By the end of the 1950s, the geographer Francisco Tenreiro noted that the original
forests of São Tomé were no longer found below 1400 m altitude and thus that only
1/140 of the total land on the island was covered by the original vegetation. He
denounced that “by clearing the woods, degrading spontaneous formations, even
replacing them entirely with new formations, men almost completely transformed
the primitive physiognomy of the island” (Tenreiro, 1961; Fig. 4.2). These dramatic
changes had pronounced impacts on the islands’ biological diversity, adding several
alien species (Muñoz-Torrent 2013) and likely eradicating many natives ones.
Landscape transformations were associated with the process of developing human
settlements, such as the drainage of swamps, the creation of dams and canalization of
river courses, the construction of buildings and roads (especially on the coastal
fringes), and overexploitation of natural resources, both on land and at sea. Some
species were directly targeted for extirpation, such as attempts to eradicate species
that transmit diseases like the tsetse fly (Costa 1913) and more modern attempts to
eliminate malaria. These eradication campaigns employed methods including deforestation, draining swamps, and harsh chemicals that likely contributed to significant
ecological loss. Thus, the presence of humans on the islands from the early colonization to the present day has dramatically shaped the landscape and ecosystem
ecology.
In São Tome, Tenreiro compared landscape units to reconstruct the changes that
occurred throughout the island’s colonization history: from the closed forest of the
Obô (Creole term referring to the original forest, called Obô jiji when it is dense and
impenetrable) to the sugarcane fields (which emerged in the sixteenth to seventeenth
centuries), passing through secondary forests and plantations of cocoa, coffee,
oilseeds, and bananas (which emerged from the nineteenth century onward). The
intensive agricultural use resulted in the gradual impoverishment of soils, giving rise
to a savanna area in the north of São Tomé that is dotted with palm groves, riparian
forests, and micondos (local name given to baobab trees) (Fig. 4.2—Diniz and Matos
2002; Figueiredo et al. 2011).
Despite these landscape alterations, the first impression of those arriving to the
Gulf of Guinea islands is lush rainforest, which in some places reaches the coastline
giving the landscape an appearance of dense and untouched forest, almost limitless
(Fig. 4.2a). That first impression gives contemporary visitors the idea that they are in
front of the original landscape of the Obô, never altered. The reality, however, is that
plant diversity across the landscape varies not only as a function of climate, relief,
and soils, but also as a function of the history of human occupation and, in particular,
of the different plantation regimes that existed on the islands. These islands clearly
illustrate the consequences of an incessant landscape modification: how demographic expansion and economies based on intensive cash crop monocultures and
forest cultures impact the climate, environment, and biodiversity. Thus, addressing
contemporary environmental challenges must account for the reality that the landscape is fundamentally different than it was 500 years ago and the biological
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Territory, Economy, and Demographic Growth in São Tomé and Príncipe:. . .
75
Fig. 4.2 The different
processes that modified the
São Tomé landscape, from
the original humid jungles to
drier savannahs with
micondós (baobabs) and
palm groves. Top: the
mountainous and more
humid regions that preserve
dense forests (photo
© Rogério Nave—2003).
Middle: the most intense
deforestation in the coastal
and drier areas of the island,
which reached its first peak
between the late nineteenth
century and early twentieth
century. In the photo, corn
plantation fields among
coconut palm groves (photo
© Orlando Ribeiro—1955).
Bottom: drier area of the
northern parts of the island,
which currently presents a
very modified vegetation, as
is the case of the humanmade savannahs (photo
© Thomas Schenk—2007)
communities now include many introduced species that have since become
acclimated.
Furthermore, even for those with a deep understanding of landscape richness and
biological diversity, the impression of leafiness, of dense forest which is stubbornly
resisting to humanization, induces a misleading perception about the islands’ dimensions, making them bigger than they really are. Therefore, when addressing
76
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environmental issues, both the original vegetal landscape, that most Santomean
people never stepped on, and also the current landscape constituted mainly of
non-native species must be taken into account. In other words, when we are talking
about ecosystems and biodiversity of the Gulf of Guinea Ocean Islands, biological
and landscape evolution has to be regarded in a wider sense, considering also the
adaptation of introduced species and not only the endemic ones, although, in any
case, the latter are those which distinguish the islands’ ecologic richness.
Despite the intense landscape transformation experienced since the first human
settlements, the diversity of both plant and animal species that can only be found on
these islands is extraordinary. The latest report on the biodiversity of São Tomé and
Príncipe states that 15% of the vascular plant species catalogued on the islands are
endemic, while 57% of birds in São Tomé and 54% in Príncipe, 44% of reptiles, and
100% of amphibians are also endemic (MIRNASTP 2016). However, many of the
species presently found on the islands were introduced, constituting an important
source of products that make up the traditional basic diet of the population, as well as
their housing (wood) and energy source (firewood and charcoal). Likewise, agricultural crops are non-native and are a key driver of the national economy, both in terms
of the domestic and export markets (Oliveira 1993).
This is especially important considering the exponential growth of the population
in recent decades and also the projected growth for the decades to come, which,
following the improvement in living standards, will certainly continue to intensify
territorial uses and result in further landscape changes. Future risks include further
deforestation due to increased demand for building materials and agricultural production, and depletion of fisheries and other natural resources. Accelerated growth,
which is often poorly planned and rarely monitored, constitutes a real—and in some
cases already imminent—threat to the islands’ extraordinary biological richness and
the people who rely on the ecosystem services they provide.
Demographic Growth, Territory, and Urban Sprawl
Until the 1960s, 32% of the up to 65,000 inhabitants of São Tomé and Príncipe lived
in the Mé-Zóchi district (in the center of the island), where many of the most
populated agricultural fields were concentrated (INESTP 2012a). From 1970
onward, the distribution of the population began to change, with the district of
Água Grande becoming the most populous. This is where the capital city, São
Tomé, is located, and this change in distribution clearly reflects the decline in the
plantation economy and the trend toward urbanization. There was also an inversion
in the structure of the resident population, which became female-biased. This
phenomenon was due to the reduction of men brought to work in the fields and
emigration of men searching for better working and living conditions abroad.
Meanwhile, with the proclamation of independence in 1975, thousands of people
left the country, including many of the most educated and prominent members of
society. At the same time, many of those who had left in search of better
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Territory, Economy, and Demographic Growth in São Tomé and Príncipe:. . .
77
Fig. 4.3 Human population growth in São Tomé and Príncipe (source: INESTP 2012a)
opportunities abroad began to return to São Tomé and Príncipe due to the war in
Angola. Comparing immigration and emigration around the time of independence, it
appears the population grew, and became more concentrated around the capital city
and other urban centers. Data from the last Portuguese census, in 1970, and from the
first censuses of independent São Tomé and Príncipe illustrate these changes
(Fig. 4.3).
Between 1976 and 1991, the colonial infrastructure was largely intact and in full
operation, and the majority of the population remained in the rural areas, where the
roças constituted authentic autonomous villages. Drops in production from former
plantations, associated with the depletion of trees and production resources, together
with increased competition and lower prices on the international cacao market,
resulted in a collapse of the economic structure. Many of the agricultural companies
that had become nationalized after the independence were privatized again, but most
of them failed and became abandoned, intensifying the regression of intensive crops
and the expansion of capoeira areas (scrubs, shrubby habitat). In 1981, the general
population and housing census reported 96,566 inhabitants in the country,
representing an increase of 30.8% compared to 1970. In the following decade, this
rate of growth dropped to 20.6%, to reach a resident population of 116,504 inhabitants in 1991. It was during this period that the rural exodus toward the urban centers
of the country further intensified, in particular to the outskirts of the city of São
Tomé, resulting from the agrarian reform financed by the World Bank (INESTP
2012a). Between 1992 and 2020, there were two censuses, one in 2001 and the other
in 2012 (INESTP 2012a). Between 1991 and 2012, the population increased by
53.41%, to 178,739 people, an increase of 62,235 inhabitants in just 21 years and
almost double the population at independence. The average annual growth rate
between 2001 and 2012 was 2.45%. At the district level, this index reveals that
Lembá had the highest growth rate (2.96%), followed by Água Grande (2.74%),
while the lowest was Caué (0.86%). These values illustrate the trend toward
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X. Muñoz-Torrent et al.
Fig. 4.4 Distribution of São Tomé and Príncipe population in each district (2012 and projections
for 2035) (Source: INESTP 2012a)
population concentration around urban areas, especially around the São Tomé-Trindade axis, as seen in recent studies.
Average growth rates make it possible to carry out population projections to
better understand demographic dynamics and design a more realistic territorial
planning. Between 2012 and 2015, the annual population growth was 2.03%, and
between 2012 and 2025, annual population growth is projected to be 2.08%, and
2.01% from 2025 to 2035. Consequently, population growth is projected to be
approximately 26% between 2012 and 2035, which would place the total population
at 284,293 inhabitants by 2035 (INESTP 2012c).
The demographic increases have taken place mainly in the suburbs of urban areas.
In the 1990s, the number of agricultural workers, most of them residing in farmland
and other rural areas, decreased from 14,500 to 8860 (INESTP 2012b). This trend
was likely in response to the agrarian reform promoted and financed by the World
Bank, which encouraged the government to dismantle large plots of land. These
were divided into small parcels and distributed among 8735 former agricultural
workers, under a usufruct regime (Oliveira 1993). The implementation of this policy
had perverse effects on urban centers, namely in conditioning the capacity and
sustainability of the country’s current structures and basic services, increasing its
population density, and clearly unbalancing the distribution of the population across
the national territory (Seibert 2015). However, this trend is expected to be attenuated
in the near future: if in 2012 67% of the population lived in urban areas, in 2035 it is
estimated that it will reach only 70% (INESTP 2012c). The rural exodus reached its
greatest extent in 1991 with the land reform, but it did not stop and has only
decreased in intensity. The extreme poverty of rural areas was the main reason for
this exodus, forcing populations to move in search of better living conditions, which
resulted in the saturation of urban areas. It is estimated that 38.9% of the population
will reside in the district of Água Grande by 2035, where the capital is located, and
that by then its population will exceed 100,000 inhabitants (INESTP 2012a—
Fig. 4.4). The rapid emergence of high population densities concentrated around a
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79
few urban areas has created several environmental problems, with clear implications
for human well-being, such as intense road traffic and high concentrations of noise,
light, and chemical pollution, as well as a deregulation of urban expansion and
exploitation of resources, with far broader environmental implications.
Several indicators already point to a “demographic transition” (see Thompson
1929) in São Tomé and Príncipe. The large difference between high birth rates and
low mortality rates provides a marked growth, which explains the observed rapid
demographic expansion. On the other hand, the exacerbated increase in urban
development, the widespread use of contraceptive methods, the evident appearance
of women in the formal employment market, the costs associated with educating
children, the improvement in the level of education, and the increase in family
planning point to a reduction in the birth rate, which will soon approach the death
rate and lead to the stabilization of the population. Other demographic indicators
reveal these same trends: the average age of the population will go from 19 years old
in 2012 to 26 years old in 2035 and the time needed for the population to double will
go from 35 to 38 years. In any case, despite the trend of the main demographic
indicators, the population of São Tomé will maintain a high population growth rate,
and it is estimated that it will reach a synthetic fertility rate of 2.01 in 2030.
The districts of Água Grande, Mé-Zóchi, and Lobata, in the north of the island of
São Tomé, have three-fourths of the national population, despite corresponding to
less than one-fourth of the country’s area (INESTP 2012a). The highest density in
2012 was in the district of Água Grande, with 4209 inhab./km2 in 16.5 km2. At the
opposite extreme, was the district of Caué, with 23 inhab./km2 in 267 km2, illustrating the great territorial imbalance in terms of population distribution, which also
affects the available services and the type of economic activity in each region. Since
2001, the entire district of Água Grande has been considered urban, which homogenizes the analyses referring to the capital, although it is clear that some regions
within this district maintain elements of rurality. In the 2012 census, population
distribution was georeferenced for the first time, which will constitute an important
tool for understanding its evolution (Fig. 4.5). The urban expansion is very evident,
using as main axes the national roads that leave the capital, connecting it with
residential neighborhoods in Trindade to the west, in Santana to the south, and
several villages in the north, toward Guadalupe. This trend is particularly evident
along national road 3, from the neighborhood of Madredeus and industrial areas in
Água Grande to the village of Trindade and beyond in the district of Mé-Zóchi,
which effectively constitute an urban continuum. This expansion entails an increasing urban sprawl, the impacts of which are especially significant because the
Santomean residential tradition is not compact, consisting mainly of detached
single-family houses built of wood on family plots, known as quintais.
Between 2012 and 2035, the rural population is expected to continue to decline,
in contrast to urban population growth. Underlying these trends is an increase in the
territory’s vulnerability, especially given the scarcity of effective regulatory instruments that control urban expansion and the use of natural resources. In other words,
the population is becoming even more urban, reaching 70% of the total population in
2020, which will especially affect the forecast of needs for basic services and
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(a)
X. Muñoz-Torrent et al.
(b)
(c)
Fig. 4.5 (a) Population density derived from the 2012 census, (b) road density, and (c) landscape
vulnerability based on a multifactorial analysis of São Tomé Island in Mikulane (2019). The
coloration for all three graphs represents linear standardization
mobility, which will be greater. At the same time, this presupposes, following the
traditional settlement and housing model, a clear tendency to occupy more territory:
the city of São Tomé, which had an orthogonal plan of origin, will tend to grow
sharply, irregularly, and haphazardly rather than a compact model in line with
sustainable urbanism. However, the National Plan for Spatial Planning PNOT,
currently under preparation (MIRNASTP 2020a), may be an important guide to
improve territorial management, as long as they are able to support regulated and
enforceable public policies in planning and controlling growth in urban and suburban areas, which take into account the demographic and occupation dynamics of the
territory that we have just described.
Culture and the Concepts of Obô and Omali: When
Conservation Collides with Development
Anthropogenic pressure on the environment should not only be measured in terms of
demographic expansion and the occupation of space, but also in terms of income
levels, traditional uses, and the population’s perception of the ecological wealth of
the islands (Boya-Busquet 2008a, b, Mikulane 2019). Furthermore, the same
anthropic pressure must be contextualized in the awareness of the pernicious impact
of uncontrolled growth in demographic terms, and in terms of an economy that does
not respect the environment and instead follows the trends of a globalized capitalist
system. This is increasingly the reality on these islands, where the extreme poverty
of most families, an unstable economy, low wages, low saving capacity, etc., are all
at play. These constraints mean that even in the most urban environments, traditional
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81
cultures persist with basic livelihoods that are largely supported by agriculture and
the extraction of resources from the natural environment. The Obô still provides
wood for construction and to make canoes, furniture and other utensils, firewood and
charcoal for cooking, fruits, condiments, medicinal herbs, and sources of animal
protein. Omali (sea) provides fish and shellfish, vital protein sources on the islands,
as well as sand for construction. The highly informal and poorly quantified domestic
market largely depends on these predominantly extractive activities. For example, it
was estimated that in 2014 alone, São Tomé and Príncipe bakeries consumed around
5000 tons of firewood, mostly obtained from illegal harvesting in national forests
(MOPIRNASTP 2019).
As an illustrative example of a prevailing mentality among islanders, the following testimony of a resident from Porto-Real, Príncipe, states: “Here [in Príncipe]
there are no jobs, but there is moandim (a local tree) in the woods to make charcoal.
Coal is easy money. If you take it to the market, it is sold straight away. If you cut a
bunch of bananas, where do you sell them? With a sack of charcoal, I haven’t even
arrived in the city yet and I’m already doing business” (Temudo 2008). In other
words, the forest is a sure source of income for families, frequently used by many of
the island’s inhabitants. Consequently, Obô and the Omali are seen by most
islanders as an inexhaustible source of easily accessible resources, unlike plantations
that are largely operated by the state or large agricultural companies, or existing jobs
in the city, often with uncertain profit or low pay. It is the combination of a deficient
family economy with abundant natural resources that reinforces the inhabitants’
direct dependence on natural resource extraction. This relationship was once more
respectful and balanced, forming part of the animist beliefs themselves. For example,
it was customary for fishermen to ask Mother Nature’s permission in advance and
the tree’s forgiveness, before cutting it to make a canoe (Torres 2005). Currently,
strong social changes, largely due to increased contact with the outside world, but
also due to population growth itself, put at risk not only nature but also cultural
identity. This interdependence between society and nature creates a certain perception of citizenship, which plays a crucial role in the conservation of ecosystems
(Boya-Busquet 2008a).
The dense forests, in addition to being a source of resources, are also an unknown,
dark, hidden, changing space for many islanders. This is where witches and sorcerers
live, where outlaws hide, where the fearsome cobra-preta dwells (endemic to São
Tomé), and where there is danger of illness or death. It is also in the depths of the
forest that the spirits of the deceased live and are invoked, where uncertainty and fear
are generated. It is wild place that at the same time imposes and deserves respect and
challenges men to dominate it, as it is the antithesis of the civilized, the known, the
controlled, which all originated from the devastation of this dark place. This feeling
is also experienced in other cultures, at other times and under different circumstances
(e.g., Urteaga González 1987). For instance, in school surveys (Boya-Busquet
2008a), drawings express the prejudice about the unknown space of forests, streams,
and seas, and in which there is a clear ladder of values—evolving from the forest to
the roça and to the city, as an evolution from a wild place to a civilized one. In any
case, the same representations demonstrate the perception of the existence within the
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X. Muñoz-Torrent et al.
Obô jiji, of an indomitable, still virgin place, where it is possible to find spirits, from
which new knowledge, certain remedies, occult magic or the power of healers can be
found.
There is, therefore, a great contradiction that can be explained by the generational
shift (or disinterest) in relation to ancient beliefs and by the relativization of the
importance of animism for the conservation of Nature. In essence, the impenetrable
Obô is a place to respect, so perhaps it is not strange to think that the majority of the
modest population considers the Obô (and the Omali as well) as a kind of “open
bar,” “an immense and inexhaustible cornucopia” (Valverde 2000), a place to
civilize and explore. As such, it is difficult to think of valuing biodiversity if it is
not recognized as a shared and finite heritage, which if it disappears as a result of
economic development will take with it a large part of the unique identity of the
peoples of the oceanic islands of the Gulf of Guinea.
The strongly impregnated idea that natural resources are infinite and for the
enjoyment and benefit of the immediate needs of its inhabitants, associated with
rapid demographic growth, the exchange of habits and social references, and the
liberalization of access to land, have caused the destruction of natural resources to
accelerate in recent decades, making it urgent to apply a strict policy of conservation
and modification of territorial planning standards. A multifactorial analysis of the
elements that are affecting the ecosystems of the island of São Tomé revealed that
more than two-thirds of the island have a high degree of landscape vulnerability
(Fig. 4.5—Mikulane 2019). This approach reveals the long-evident trend of degradation (Tenreiro 1961), even in areas protected by law.
The awareness of the unique value of the forests, rivers, beaches, and seas of these
islands by its inhabitants is relatively new, and becoming more widespread since the
beginning of the twenty-first century. This transition was largely externally inspired,
stemming from international programs such as ECOFAC (Albuquerque and
Carvalho 2015), but is currently reflected in several national strategic documents
(e.g., MIRNASTP 2016, MIRNASTP 2020a, b), which identify the values to be
protected in coastal and marine ecosystems, inland waters, forestry, and agrarian
ecosystems, and from which the establishment of the Obô Natural Park was derived
(DGA 2006a, b). Despite clearly pointing out threats and challenges, awareness
programs on these values have not been satisfactorily established or implemented,
starting with the low presence of this topic in school curricula (Carvalho et al. 2010).
Despite legal regulations and strategies created to promote responsible environmental management, poor enforcement results in widespread transgressions in
illegal activities such as systematic cutting of trees in protected areas without
authorization (Espírito et al. 2020), indiscriminate extraction of sand from beaches,
poaching of protected species, or fishing with prohibited gear. Awareness of the
value of biodiversity as a shared heritage remains poorly rooted, or is outweighed by
necessity, and the debate about its importance continues to have little practical effect.
Agricultural and urban land use are also often at odds with environmental protections. In addition to the expansion and intensification of small-scale agriculture
carried out mainly by small owners, there are strong pressures inflicted by large
concessions (Oyono et al. 2014). This is true both on the part of agricultural
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83
corporations, which work to recover and intensify plantations, and on the part of
urban interests, sometimes linked to tourism, which have even intruded into
protected areas. As already denounced long ago (Tenreiro 1961), the development
of intensive agriculture, concerned with above all profit and export, has been at the
expense of natural ecosystems. In addition to the direct impacts of agriculture, the
impact of improving the network of roads and other infrastructures has also resulted
in further land use intensification. All these elements of modernization will continue
to require more land; for example, continued horizontal expansion of single-family
homes at the current urban growth rate is unsustainable.
Deforestation means not only an abrupt landscape change in the context of the
islands, but also a change in climate regimes, with implications for the islands’
ecology (Henriques 1917). These changes can be especially notable in terms of
rainfall and, therefore, water supply. In this context, it is evident that it is difficult to
strike a balance between conservation and development. As such, in the medium and
long term, the prospect of retaining functional ecosystems on the islands is sobering.
With the continued decline of local biological diversity, and, in particular, of
endemic species, the islands’ ecosystems will likely become increasingly fragile.
On the island of Príncipe, low demographic pressure and lower accessibility,
associated with a more pro-conservationist policy, provide some hope for the
preservation of its biodiversity and landscape integrity. The island was declared a
UNESCO Biosphere Reserve in 2012 (UNESCO 2013), which is paired with a
tourism model that leverages the unique landscape and cultural heritage. These
circumstances have also attracted the interest of scientists and conservationists,
leading to the description of new endemic species and the implementation of several
successful conservation programs (e.g., Fundação Príncipe 2021). This approach
seems to have influenced a more positive perception of biodiversity and stronger
enforcement of environmental regulations, halting the trend of environmental degradation. These changes end up benefiting an economic model that centers nature
conservation, although perhaps the benefits for the local population are less clear: so
far, this theory has not been associated with changes in population demography or
urban planning. One important consequence, however, is growing social inequalities
created by strong foreign investment that has led to an increase in prices on the
island. In addition, the small size of Príncipe means the species on this island are
much more vulnerable to anthropogenic pressure, as they have much smaller
distributions.
As a consequence of all of this, the first draft of the PNOT (MIRNASTP 2020a)
outlines a more solid basis for the delimitation of uses in the territory and the urban
expansion model. These include strict safeguarding of natural habitats and ensuring
the balance of biophysical systems, and the sustainability of hydrological cycles,
both those that constitute a forest or fish reserve and their buffer zones and agricultural regime zones. This document highlights a chapter on establishing the planning
model that adopts the culture of territorial management, and a second chapter on
measures to protect the environmental and cultural system. Proposed measures
include the promotion of institutional and population awareness to preserve and
enhance the notable natural and cultural elements, and the establishment of a
84
X. Muñoz-Torrent et al.
national policy for the environment, nature conservation, and protection of biodiversity, very much in line with correcting the effects of uncontrolled growth
described above. It is therefore an encouraging instrument, or at the very least a
basic statement of good intentions.
The Limits of Environmental Change: A Dystopian
Panorama?
Given the current moment of social and economic development, the outlook for
biodiversity conservation in the islands of the Gulf of Guinea is not very optimistic.
In particular, the exponential growth of the population and, consequently, the
increasing pressure exerted on natural resources suggest the future scenario will be
one of rapid environmental degradation, with the ultimate outcome being the general
depletion of the territory, deforestation, disappearance of beaches, the gradual
erosion of ecosystems, and disappearance of endemic species, but also threats to
the persistence of the allochthonous richness already adapted to the territory.
Is it possible to put limits on this Malthusian drama in these jewels of the
Atlantic? Is it really impossible to think of an economic development that is not
based on the exhaustion of territory? Will the islands’ unique biological diversity
persist? There is still time to promote effective territorial planning, to which must be
added demographic containment, and the implementation of a rigorous environmental policy, based on good management of uses, but also on awareness and, primarily,
on basic education. There is great difficulty in reconciling the management of
resources recommended by specialists with local practices, needs, and interests,
and even private or corporate ones. In this sense, there is still a lot of work to be
done, and it will be a great challenge to overthrow many of the vested interests.
Keeping up with the current pace, the current landscape of the islands may become
unrecognizable in a short time. To curb the prospects created by the current development path and avoid the most devastating environmental scenarios, it is necessary
to increase social and economic equity, allowing access to sufficient income to help
change the population model and demographic and social growth. The ultimate goal
is a shift in mentality that positively influences the valorization of the islands’ unique
biodiversity as a common heritage, which is in fact the clearest pillar for a differentiated and long-term sustainable economic and social development model.
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Open Access This chapter is licensed under the terms of the Creative Commons Attribution 4.0
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the copyright holder.
Chapter 5
The History of Biological Research
in the Gulf of Guinea Oceanic Islands
Luis M. P. Ceríaco, Bruna S. Santos, Sofia B. Viegas, Jorge Paiva,
and Estrela Figueiredo
Abstract The oceanic islands of the Gulf of Guinea (Príncipe, São Tomé, and
Annobón) have been the focus of biological research for over two hundred years.
Following small surveys that generated modest collections in the eighteenth and
early mid-nineteenth century, European institutions commissioned several exploratory missions to the region that resulted in the first major catalogues of its biodiversity. The following century brought a new wave of research investment, mostly
driven by the colonial interests. After the independence of both Equatorial Guinea
L. M. P. Ceríaco (*)
Museu de História Natural e da Ciência da Universidade do Porto, Porto, Portugal
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório
Associado, Universidade do Porto, Vairão, Portugal
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO, Vairão, Portugal
Departamento de Zoologia e Antropologia (Museu Bocage), Museu Nacional de História
Natural e da Ciência, Universidade de Lisboa, Lisbon, Portugal
e-mail: lmceriaco@mhnc.up.pt
B. S. Santos
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório
Associado, Universidade do Porto, Vairão, Portugal
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO, Vairão, Portugal
Departamento de Biologia, Faculdade de Ciências da Universidade do Porto, Porto, Portugal
Museu de História Natural e da Ciência da Universidade do Porto, Porto, Portugal
S. B. Viegas
Centro Interuniversitário de História das Ciências e da Tecnologia, Faculdade de Ciências,
Universidade de Lisboa, Lisbon, Portugal
Museu de História Natural e da Ciência da Universidade do Porto, Porto, Portugal
J. Paiva
Centre for Functional Ecology, Departamento de Ciências da Vida, Universidade de Coimbra,
Coimbra, Portugal
E. Figueiredo
Department of Botany, Nelson Mandela University, Gqeberha [Port Elizabeth], South Africa
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_5
87
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L. M. P. Ceríaco et al.
and São Tomé and Príncipe, novel research trends focusing on conservation aspects
of biodiversity research emerged. Here we present a chronological review of the
zoological and botanical expeditions to the region, commenting on their major
results, collectors, and the naturalists who studied them.
Keywords Expeditions · Herbaria · History of science · Natural history collections ·
Taxonomy
Introduction
From the beginning, humans have tried to understand, classify, and master the
biodiversity that surrounds them. Through time, and across different civilizations
and cultural groups, different approaches and classification schemes have been
proposed to try to classify the natural world. Despite many attempts, the creation
of a natural, objective, and replicable system to classify nature was only achieved in
the mid-eighteenth century, with the seminal works of the Swedish naturalist Carl
Linnaeus (1707–1778). The works of Linnaeus are universally recognized as marking the birth of modern natural history and all its resulting subdisciplines (biology,
ecology, etc.). As supporting evidence for its foundational importance in the current
international zoological and botanical codes of nomenclature, valid scientific names
are those starting in the 1750s, following the works of Linnaeus. For zoological
nomenclature, the fixed starting point is 1758 (ICZN 1999), which corresponds to
the publication of the tenth edition of Linnaeus’ Systema Naturae (Linnaeus 1758).
For botanical nomenclature, this point is only five years before, in 1753 (Turland
et al. 2018), corresponding to the publication of the first edition of Linnaeus’ Species
Plantarum (Linnaeus 1753). Although this renders all the previous works invalid,
from the narrow point of view of biological nomenclature, this does not mean that
earlier work does not provide important information and insights regarding the natural
world. In addition, many important contributions to scientific knowledge throughout
history (and today) are made outside of the formal scientific literature. For the oceanic
islands of the Gulf of Guinea, the reports made by some of the earliest Portuguese
navigators in the late fifteenth and early sixteenth centuries are teeming with information about the nature of these islands and the surrounding sea. This is the case of
the report produced by the Portuguese navigator Gonçalo Pires (dates of birth and
death unknown), transcribed by Valentim Fernandes (ca. 1450–1519) and subsequently published by Baião (1940), in which the author describes the geography,
fauna, and flora of the three oceanic islands in considerable detail.
This chapter aims to provide a general overview of more than two centuries of
scientific research on the biodiversity of the oceanic islands of the Gulf of Guinea.
Due to the impossibility of providing a fully detailed account on the life and work of
every naturalist or explorer that worked on the biodiversity of these islands, some of
which would be sufficiently rich and detailed to write an entire chapter or book
about, this text intends to be mostly a commented guide to the available publications.
In a way, it is an updated and commented version of the important bibliographic
compilations provided by Exell et al. (1952), Fernandes (1982) and Figueiredo
5
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(1994a) for plants and by Gascoigne (1993, 1996) for animals, but it also aims to
present the major research trends regarding biodiversity of the oceanic islands of the
Gulf of Guinea across time. Despite the historical importance of older records, such
as those of Gonçalo Pires, we do not include them here and focus solely on works
published after the Linnean revolution, as the latter ones are those more readily
accessible to the present-day researcher and student.
Eighteenth Century to Mid-Nineteenth Century
Formal zoological research in the Gulf of Guinea did not begin until the latter half of
the nineteenth century, although in the late eighteenth century and earlier decades of
the nineteenth century small collections made their way into Europe. Naturalists like
the Danish zoologist Otto Friedrich Müller (1730–1784), the Dutch merchant and
entomologist Pieter Cramer (1721–1776), and the French zoologist Jean Guillaume
Bruguiére (1749–1798) studied them and described the first known species of insects
and molluscs from the islands (Müller 1774; Cramer 1775/76; Bruguière 1792).
Most notably, the French Naval officer Sander Rang (1793–1844) docked the naval
brig La Champenoise in Príncipe for a month, where he collected terrestrial molluscs, which he later described (Rang 1831). During these early days of the modern
era, much of the collecting and research was conducted in a framework of private
collections and a dilettante approach to science, but these first records can be seen as
the beginning of taxonomic research in the region.
The oldest record of plants collected from the Gulf of Guinea Islands dates from
1787 and was collected by the French naturalist Ambroise Marie François Joseph
Palisot de Beauvois (1752–1820), during his stay in Príncipe Island while he was ill
(Exell 1944). Out of the four species he collected, Asplenium emarginatum,
Aeschynomene indica, Tristemma hirtum, and Agrostis tropica, the last has never
been collected again on Príncipe and no other specimen is known (Figueiredo et al.
2011). After Beauvois’ initial study, botanical specimens were only collected again
in the Gulf of Guinea during the nineteenth century. The Scotsman George Don
(1798–1856) spent three weeks collecting plants in São Tomé (15 May to 11 June
1822). All the sailors who accompanied him ashore died from a tropical disease after
leaving the island (Exell 1944). It was a good collection for the time, with about
twenty species new to science, some of which have not been found again in São
Tomé (Figueiredo et al. 2011). These “missing” species may in part be because some
of them, such as Cichorium intybus and Pluchea sagittalis (Epaltes brasiliensis),
were alien weeds (from Europe and South America, respectively) that did not
become established (Exell 1944) or were, perhaps, misidentified.
Later, Andrew Beveridge Curror (1811–1844), a British naval surgeon and
naturalist, visited Annobón between 1839 and 1843, where he reportedly collected
two species of plants, Begonia annobonensis and Vernonia amygdalina (Exell
1944). Figueiredo and Smith (2020a) cite the holotype of Begonia annobonensis
[Curror 9 (K000242508), Annobón 1841]. At Herb. K there is also a herbarium
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sheet with several specimens of Vernonia amygdalina from Annobón, two of which
were collected by Burton (Oct. 1863) and one by Curror (Curror 8, 1841). It is likely
that Curror made more collections in Annobón. Curror died of “remittent fever”,
during his last expedition (in 1844), off the coast of Gabon (Figueiredo and Smith
2020a). Curror also travelled to the island of Príncipe on four different occasions
during 1839 (Figueiredo and Smith 2020a). Even though none of Curror’s collections at Herb. K are labelled as originating from Príncipe, one of his collections is,
without a doubt, from that island, consisting of the fern Alsophila camerooniana var.
currorii, which is endemic to Príncipe (Figueiredo and Smith 2020a).
Near the end of this period, Désiré Edélestan Stanislas Aimé Jardin (1822–1896),
a clerk in the service to the French Navy, collected plants in Tropical West Africa
between 1845 and 1848 and visited Príncipe. Amongst the plants (about 50 species)
he mentioned from this island (Jardin 1850/51), he refers one Combretum without
the specific name. Exell (1944), who did not see the collection, referred to it as
Combretum platypterum, which has not been found again in Príncipe. This information was given to him by Georges Le Testu (Exell 1944), who, at Exell’s request,
had searched the Jardin collection, then held at Herb. CN and later transferred to the
Herb. P. The only species of Combretum recorded in Príncipe is Combretum
paniculatum (Figueiredo et al. 2011).
Mid-Nineteenth Century to Early Twentieth Century
From the mid-nineteenth century forward, a wave of interest in African territories
prompted several European institutions into commissioning naturalist expeditions to
the continent. The need to catalogue the colonial possessions, together with the
broader interest to uncover the planet’s biodiversity, led to the flourishing of
taxonomy. Most of the publications and research outputs of this time came in the
form of species descriptions, checklists, and catalogues.
The first publication was that of the Swedish mycologist Elias M. Fries
(1794–1878), who was the first naturalist to report fungi from São Tomé (Fries
1851), namely six Agaricomycetes species collected by Krebs (no additional collector information). This publication is of special relevance not only as the first
published account of fungi of the oceanic islands of the Gulf of Guinea, but also
as the first major bibliographical record to feature a report on the biodiversity of the
region following the investment boom in the continent.
In 1853, while en route to a botanical expedition to Angola, the Austrian botanist
Friedrich Welwitsch (1806–1872) collected specimens on the islands of São Tomé
and Príncipe, doing the same seven years later upon returning from the trip (Figueiredo and Smith 2020b). He visited Príncipe between 15 and 22 September 1853.
Almost all the species he collected were new records for the island, except the fern
Alsophila camerooniana var. currorii found years before by Curror in 1839 and
those species collected by Jardin. On 23 September of the same year, he paid a short
visit to São Tomé. In December 1860, on the return trip from Angola to Lisbon,
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Welwitsch stayed in São Tomé for some days and amassed a very good collection of
plants, with interesting new records and new species, some of which he described
(Exell 1944). The mollusc specimens collected by Welwitsch on the islands were
studied and published by Morelet (1868), and later mentioned in Crosse’s (1868)
compilation of known land molluscs from São Tomé. Pierre Marie Arthur Morelet
(1809–1892) was a renowned French naturalist specializing in molluscs, whereas
Joseph Charles Hippolyte Crosse was a French conchologist, co-editor of the
publication Journal de Conchyliologie. Additional malacological fauna collections
resulting from expeditions into the area undertaken by various naturalists were
studied by Morelet (1848, 1858, 1860, 1873).
During the seven years between Welwitsch’s two visits to these islands
(i.e. between 1853 and 1860) only the Scottish gardener Charles Barter
(1821–1859), collector on William Baikie’s second Niger Expedition
(1857–1863), visited Príncipe. In 1858, he made a small but important botanical
collection, primarily comprised of orchids (Exell 1944; Figueiredo and Smith
2020b). He caught dysentery and died on 15 July 1859 at Rabba, Nigeria. Barter
was replaced on this expedition by Gustav Mann (1835–1916), a German botanist,
who collected a great number of plants during the three years he participated in the
expedition (1859–1862). In August 1861, Mann collected across a large area of São
Tomé and reached Pico de São Tomé, discovering several new species and various
interesting plants that would be studied by Hooker (1863, 1864). Later, Mann
collected on Príncipe (22 September–26 October 1861), again uncovering new
species and novelties for the flora of the island (Exell 1944). A few years later,
Richard Francis Burton (1821–1890), who served as the British Consul in Bioko
from 1861 to 1864, visited Annobón (October 1863) on his way back to Bioko from
the Niger–Congo rivers expedition (August–October 1863) and made a small
collection, currently held at Herb. K (Burton 1876).
In 1865, the German explorer Heinrich Wolfgang Ludwig Dohrn (1838–1913)
spent six months in Príncipe, where he collected birds, reptiles, and snails. The
results were later published by him and by other specialists (Dohrn 1866a, b, c;
Keulemans 1866; Heynemann 1868; Peters 1868). Subsequently, the German zoologist Richard Greeff visited São Tomé and Rolas Islet between 1879 and 1880,
where he collected extensively and obtained important specimens that contributed to
the description of a considerable number of new species by him and others (Peters
1881; Greeff 1882a, b, c, d, 1884, 1886; Bocage 1886a; Koch 1886; Krauss 1890).
In 1871, the Portuguese naturalist Félix António Brito Capello (1828–1879)
published the first list of fishes from the Portuguese islands of Madeira and Azores,
with the inclusion of fishes from its overseas possessions Angola, Cabo Verde,
Mozambique, and São Tomé and Príncipe (Brito Capello 1871). After his death,
António Roberto Pereira Guimarães continued Capello’s analysis of the material
extant in the Lisbon Museum and published two additional papers on the topic
(Guimarães 1882, 1884).
In 1885, Adolfo Frederico Moller (1842–1920; Fig. 5.1), chief gardener of the
Botanical Garden of the University of Coimbra, was sent by the institution to collect
natural history specimens in São Tomé. Despite it being a short four-month
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Fig. 5.1 Portraits of Adolfo Moller (left) and Júlio Henriques (right). Moller’s portrait from
Henrique Eusébio Moller private family álbum, adapted from Gouveia (2014). Henriques’ portrait
reproduced with the permission of the Botanical Archive—Department of Life Sciences, University
of Coimbra, Portugal (PT-UC-FCT-DCV-ABUC-S2.13)
exploratory stint (23 May–25 September), Moller found time to teach Francisco
Quintas (dates of birth and death unknown), the son of a Portuguese owner of coffee
and cocoa plantations, how to continue his botanical collection (Gouveia 2014;
Figueiredo and Smith 2019). Quintas travelled and made remarkable collections in
the west and south of São Tomé between 1885 and 1889 and also in Príncipe
between January and March 1889 (Figueiredo and Smith 2019). Bedriaga (amphibians and reptiles: Bedriaga 1892, 1893a, b), Bocage (amphibians and reptiles:
Bocage 1893b), Moller (sponges: Moller 1894, studied by Weltner in Berlin),
Nobre (land molluscs: Nobre 1886b, 1894), Osório (fish: Osório 1891a), Verhoeff
(Chilopoda and Diplopoda: 1892, 1893), and Vieira (insects, spiders, and birds:
Vieira 1886, 1887a, b, 1894) published the majority of the zoological results from
the expedition. The botanical material was deposited at the Herb. COI and studied by
the botanist Júlio Augusto Henriques (1838–1928; Fig. 5.1) for his publications on
the flora of São Tomé and Príncipe.
Francisco Newton (1864–1909; Fig. 5.2), working for the Natural History
Museum of Lisbon, fruitfully explored the Gulf of Guinea for a decade between
1885 and 1895 (Santos and Ceríaco 2021). The collections amassed by Newton
during that period proved crucial in the first extensive faunal catalogues and the
description of new species from the region, resulting in numerous works. Of special
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Fig. 5.2 Portrait of Francisco Newton and a watercolour he painted of a Leptopelis palmatus from
Príncipe Island. Source: Arquivo Histórico do Museu Bocage
importance were those published by José Vicente Barbosa du Bocage (1823–1907),
director of the zoological section of the Natural History Museum of Lisbon. Bocage
provided the first comprehensive checklists of the islands’ vertebrate fauna, as well
as the description of several species new to science, including amphibians, reptiles,
birds, and mammals (Bocage 1886a, b, c, 1887a, b, c, 1888a, b, c, d, 1889a, b, c,
1891a, b, c, 1893a, b, c, 1895a, b, c, d, e, 1896, 1903, 1905). The butterflies collected
by Newton were studied and published by Emily Mary Sharpe (1893), while the land
molluscs were studied by Arruda Furtado (Furtado 1888), Girard (1893a, b, 1894,
1895), and Augusto Nobre (Nobre 1886a, 1887, 1909). Balthazar Osório studied
both crustaceans and fishes (Osório 1887, 1888, 1889 1890, 1891a, b, 1892a, b,
1893, 1895a, b, c, d, e), Júlio Bettencourt Ferreira was responsible for the reptiles
(Ferreira 1897, 1902), and the birds were studied by David Armitage Bannerman
(1931), José Augusto de Sousa (1887, 1888) and Richard Bowdler Sharpe (1892).
While Newton’s zoological collections were sent to Lisbon, his botanical specimens
were sent to the University of Coimbra where they were studied by Júlio Henriques.
An extensive collection of letters from Newton to Bocage and Osório is still extant in
the collections of the Museu Nacional de História Natural e da Ciência, Lisbon, and
are being processed for a future publication (Ceríaco and Santos, in prep.).
Despite the few publications on the islands’ botany published in the previous
decades, the research programme established by Henriques can be considered the
birth of systematic botanical studies in the islands. The first contact Henriques had
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with the flora of São Tomé was through a few specimens collected by Newton in
1881 (Henriques 1884a; Figueiredo et al. 2019a). After the return of Moller from São
Tomé, Henriques highlighted future plans for the study of the collections from the
island (Henriques 1895). For the first instalment of what Henriques would call “Flora
de S. Thomé” (Henriques 1886), he invited other specialists to identify and describe
the collections in his possession (i.e. those from Newton, Moller, and Quintas).
Henriques (1886) had the contributions of Charles Fuller Baker (ferns: in Henriques
1886, pp. 149–158 + 2 plates), Carl Muller (mosses: in Henriques 1886,
pp. 159–169), Franz Stephani (liverworts: in Henriques 1886, pp. 170–184 + 3
plates), Heinrich Georg Winter (fungi: in Henriques 1886, pp. 185–204 + 3 plates),
William Nylander (lichens: in Henriques 1886, pp. 205–217), and C. Agardh,
O. Nordstedt, F. Hauck, and Charles Flahault (algae: in Henriques 1886,
pp. 217–221).
This series of publications continued in the following years. In 1887, Henriques
coordinated two additional papers, one based on Newton’s collections (among other
collectors that were active in the African mainland; Henriques 1887a), and another
based on the collections of Welwitsch, Moller, and Quintas (Henriques 1887b). For
the latter, Henriques collaborated with foreign botanists such as Ernst Haeckel
(grasses), Henry N. Ridley (sedges and orchids), the Count Solms-Laubach (Pandanus), and Cornelis A. Backer who made general reviews and corrections to the
manuscript. For the paper on Newton’s collections, Henriques (1887a) had once
again contributions of Franz Stephani (liverworts: in Henriques 1887a, pp. 224–225)
and William Nylander (lichens: in Henriques 1887a, pp. 221–222).
Other contributions were published in 1889 by Henriques (1889a, b). Following
the strategy used in the 1886 instalment, besides his own contributions and identifications, Henriques sent material to other European botanists, who subsequently
provided the results of their observations. Henriques (1889b) had the collaboration
of Karl August Otto Hoffmann (Capparidaceae: in Henriques 1889b, p. 224;
Lithrarieae in Henriques 1889b, p. 229), Célestin A. Cogniaux (Melastomataceae:
in Henriques 1889a, p. 226; Cucurbitaceae: in Henriques 1889b, p. 227), and Robert
Allen Rolfe (Orchideae: in Henriques 1889b, pp. 236–238). In the same year,
Augusto Nobre was able to study some fresh material of Afrocarpus mannii collected by Moller in Lagoa Amélia and sent to him by Henriques (Nobre 1889). This
was the second study on this endemic and enigmatic conifer. Roumeguère (1889),
Saccardo and Berlese (1889), Bresadola and Roumeguère (1889), and Bresadola
(1890, 1891) studied and described several species of fungi from the collections sent
to them by Henriques. The bryophytes collected by Quintas were studied, described,
and published by Brotherus (1890).
Based on new material sent to Henriques by Quintas, Henriques (1891) published
a further article with the contributions of Hoffmann (Crassulaceae: in Henriques
1891, p. 135) and Rolfe (Orchideae: in Henriques 1891, pp. 137–143). Henriques’
last contribution to the flora of São Tomé in the nineteenth century (Henriques 1892)
stretched for about 160 pages and covered several families of plants. It included
several contributions: Cogniaux (Melastomataceae: in Henriques 1892,
pp. 118–119; Cucurbitaceae: in Henriques 1892, pp. 119–122), Casimir de Candolle
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(Begoniaceae: in Henriques 1892, pp. 122–124); Piperaceae: in Henriques 1892,
pp. 152–155), Adolf Engler (Anacardiaceae: in Henriques 1892, p. 110), Gustav
Lindau (Acanthaceae: in Henriques 1892, pp. 145–148), Ferdinand A. Pax
(Euphorbiaceae: in Henriques 1892, pp. 156–161), Jules E. Planchon (Ampelideae:
in Henriques 1892, pp. 108–109), and Karl M. Schumann (Rubiaceae: in Henriques
1892, pp. 126–134).
Sobrinho (1953a) refers some plants from Príncipe Island collected by Jacinto
Augusto de Souza Junior in February 1880. These collections were not included in
the revisions of Henriques. Efforts to identify this collector have yielded no results
besides his name and herbaria where his collections are deposited: Herb. COI and
LISU (Exell 1962, Liberato 1994). One of the most enigmatic results of Souza Junior
works in São Tomé and Principe is the description of the species Justicia thomensis
by Landau (Holotype at COI: COI00005706), a species of Acanthaceae that has
never been collected again since its original description, raising questions if the
specimens were in fact collected in the islands, or if the species may have become
extinct (Figueiredo et al. 2011). Portuguese museums also received several small
collections of zoological specimens from the Gulf of Guinea, mostly collected and
offered by Portuguese military personnel deployed in the area, studied by various
specialists (Bocage 1880a, b, 1887d; Nobre 1891, 1894, 1901; Osório 1887; Santos
1882).
The English diatomist John Rattray (1858–1900) participated in the Buccaneer
steamship 1885–1888 expedition that combined plans to conduct sound operations
and lay a telegraph line along the West African coast (Bencker 1930; Figueiredo
et al. 2019b) with the collection of biological specimens. A brief stop during early
1886 in the Gulf of Guinea resulted in a small zoological collection, the results of
which were later published by Hoyle (1887), Scott (1893), and Stebbing (1895), and
botanical collections.
Leonardo Fea (1852–1903), an experienced Italian naturalist, explored the Gulf
of Guinea from 1901 to 1902 under the sponsorship of the Museo Civico di Storia
Naturale of Genoa (Fea 1902). This was his last expedition before passing away in
1903. His results were studied in the following years by Boulenger (reptiles: 1905,
1906), Breuning (insects: 1955, 1956), Germain (molluscs: 1912a, b, 1915, 1916),
Griffini (Orthoptera: 1905), Kerremans (Buprestidae: 1905), Lewis (Histeridae:
1905), Lesne (1905), Martin (Odonata: 1908), Salvadori (birds: 1903a, b, c),
Silvestri (Thysanura: 1908), and Simon (Arachnids: 1907).
During the second half of the nineteenth century, besides the taxonomically
oriented works, several authors focused on the agricultural capacities and potential
of São Tomé (Castro 1867; Henriques 1884, 1898; Nogueira 1885; Moller 1899).
This resulted in the publication of several works related to coffee (Almeida 1858;
Carvalho 1858; Castro 1857–1858), cinchona (Henriques 1876, 1878, 1880a, b,
1882), fruits (Almeida 1865), and timbers (Castro 1894). These topics, especially
those related to coffee, would be explored in much more detail in the following
decades. Plant uses and vernacular names were addressed by Almada Negreiros
(1895, 1901) in publications that are arguably the first on ethnography of São Tomé.
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Early Twentieth Century to the Independence of Equatorial
Guinea (1968) and São Tomé and Príncipe (1975)
The taxonomic cataloguing efforts of the nineteenth century carried on into the first
decades of the twentieth century. Some new research trends started to emerge,
becoming quite prevalent in the mid-twentieth century and until the independence
of the two colonies. These trends were mostly dedicated to what was known as
“colonial sciences”—research dedicated to the improvement of the colonial enterprise in its different activities (but especially agriculture), as well the well-being of
the colonists and native populations. Therefore, studies dedicated to economic
entomology, fisheries, and parasites became the dominant focus. Traditional taxonomic work also continued on several groups.
The botanical collections amassed during the mid-nineteenth century contributed
to increased botanical interest in the islands of the Gulf of Guinea. To continue his
studies of the flora of São Tomé, Júlio Henriques in 1903 at the age of 65, fulfilled
his dream of travelling to São Tomé. Henriques travelled through a large part of the
island, but the weather conditions prevented him from ascending to the Pico. From
his trip to São Tomé and the consolidation of his already vast knowledge of the
island he published one of his most iconic monographs entitled “A ilha de S. Tomé
sob o ponto de vista histórico-natural e agrícola” [The Island of S. Tomé from the
historical-natural and agricultural point of view] (Henriques 1900, 1917). The study
of the material collected in the previous century continued (e.g. Hariot 1908, with a
revision of the algae collected by Moller and Quintas).
Exell (1944) gave a comprehensive account of botanical collecting in São Tomé,
Príncipe, and Annobón, naming all collectors recorded up to that date. In the account
he mentioned a “valuable collection” made by the Portuguese engineer “I. Campos”
in 1907 on São Tomé, mostly deposited at Herb. COI. It included specimens of
Adinandra manni re-collected on Pico de São Tomé, and three specimens which
were described in Exell (1944) as three species new to science: Urophyllum
camposii, Lachnopylis thomensis, and Peddiea thomensis. According to the data
on the label of the specimens the collector is E. Campos. This is likely Ezequiel de
Campos (1874–1965), an engineer who worked in São Tomé and Príncipe from
1899 (Campos 1920). He was later a professor and a member of Parliament in
Lisbon. Much later, in 1954, Campos became the chief of Missão Científica de São
Tomé (see below).
Among the most relevant collections referred by Exell (1962) is the one made by
Auguste Chevalier (1873–1956), a French explorer and botanist who visited São
Tomé and made collections from August to October 1905. Chevalier made over
700 collections (Chevalier 1914) in São Tomé that are deposited in the Herb. P,
COI, K, and LY (Exell 1962, Liberato 1994). In 1909, the agronomist José Joaquim
de Almeida (1862–1933), the first director of the Colonial Garden in Lisbon, made a
study visit to São Tomé, collecting some plants that he later deposited in Herb. COI
and LISJC (meanwhile integrated into LISC) (Exell et al. 1952, Liberato 1994).
An extensive botanical collection from Annobón was made by the German
botanist Johannes Gottfried Wilhelm Mildbraed (1879–1954) under the auspices
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of the Deutsche Zentral Afrika-Expedition (1910–1911) in 1911, including 32 pteridophyte species. Mildbraed spent over a month on the island of Annobón from
5 September to 13 October 1911 collecting almost everything that was in flower or in
fruit at the time. His collection was mainly kept at Berlin (Herb. B) but unfortunately, it was almost completely destroyed during the allied bombings of Berlin in
World War II. Nevertheless, there are duplicates of Mildbraed’s collections at Herb.
HBG, K, and BM. Mildbraed published his results (Mildbraed 1922) which were
later reviewed by Exell (1944, 1963).
A new array of zoologists visited the islands in the following years. French
zoologist Charles Gravier (1865–1938) was entrusted to lead a scientific mission
to São Tomé (C.C.A.M. 1938), with several papers resulting from his collections
(Polychaeta: Billard 1907; molluscs: Germain 1908; corals: Gravier 1906, 1907a, b,
1909, 1910; bivalves: Lamy 1907). The British Lieutenant of the Rifle Brigade,
Boyd Alexander (1873–1910), was a renowned explorer and ornithologist who
journeyed through the Gulf of Guinea in 1909 accompanied by his faithful Portuguese colleague José Lopes (Bannerman 1914). Alexander’s bird collections were
subsequently studied and published by Bannerman (1914, 1915a, b). Additionally,
mollusc specimens were sent to the British Museum around the same time, collected
by amateurs working in the Gulf of Guinea and later studied by Tomlin and
Shackleford (1912, 1913a, b, 1914/15, 1915), and Tomlin (1923). Seabra (1922)
studied the insects collected by Sousa da Câmara (1871–1955) in São Tomé, on
behalf of the Instituto Superior de Agronomia in Lisbon, and sent some material to
be studied in the Imperial Bureau of Entomology. This material was reviewed a year
later by Herbert Campion (1923). While on leave in Europe, the Trinidadian
entomologist Frederick William Urich (1870–1937) carried out a short expedition
to São Tomé in 1920, in which he rediscovered a parasitic dipteran species in its
original bat host (Urich et al. 1922). The English explorer Thomas Alexander Barns
(1881–1930) collected on behalf of the amateur entomologist James John Joicey
(1870–1932) in the region of the Gulf of Guinea during the end of 1925 and 1926, on
what was his third and last expedition (Talbot 1932). The results of this expedition
were published by Joicey and Talbot (1926, 1927), Prout (1927a, b) and Riley
(1928). José Correia (1881–1954; Fig. 5.3) and Virginia Correia (1900–1987), a
husband-and-wife team of collectors, explored the Gulf of Guinea during 1928 and
1929 on a trip funded by S. Brinckerhoff Thorne, trustee of the American Museum
of Natural History. Amadon (1953) published the ornithological results of their
expedition.
From October 1932 to March 1933, the entomologist Willie Horace Thomas
Tams (1891–1980) and the acclaimed botanist Arthur Wallis Exell (1901–1993)
conducted a scientific mission to the Gulf of Guinea on behalf of the British
Museum, sponsored by the Percy Sladen Memorial Fund and Godman Trusts
Fund (Tams 1934). The zoological specimens collected in this expedition were
examined and published by several authors (Diptera: Edwards 1934; Collembola:
Maldwyn-Davis 1935; Microlepidoptera: Meyrick 1934; Odonata: Longfield 1936).
During the four-month long British Museum expedition, Exell made extensive
botanical collections in São Tomé (mostly in the mountains), Príncipe, Bioko
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Fig. 5.3 The Portuguese
naturalist José Correia,
during his bird-collecting
mission to the Gulf of
Guinea (1928–1929).
Courtesy of the
Ornithological Archives of
the American Museum of
Natural History
(Moka region), and Annobón. Exell deposited his specimens at Herb. BM and sent
duplicates to Herb. COI and BR (Exell 1962); his collections include bryophytes,
algae, lichenes, and fungi (Exell 1944). Resulting from this collecting trip, Exell
published a catalogue of the vascular plants of the three islands (Exell 1944), in
which 75 new names were published (36 being for new species) and several new
records noted (Figueiredo et al. 2011). In the following years, Exell published a
supplement to the catalogue (Exell 1956), and a checklist of the angiosperms for the
four islands in the Gulf of Guinea (Exell 1973a). Although he visited and collected
on the four islands, Exell made use of earlier collections when compiling the plant
catalogues of these islands, namely from Herb. COI where he spent some time in
1934 (Figueiredo et al. 2018; Fig. 5.4). In addition to having intensively and
extensively collected and studied the botany of the islands of the Gulf of Guinea,
while using the existing collections in comparative studies with his own specimens,
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Fig. 5.4 From left to the
right (including
background), the botanists
Luis Grandvaux Barbosa,
Maria Leonor Gonçalves,
Arthur Exell, Mildred Exell,
Abílio Fernandes, Rosette
Fernandes, and A. V.
Bogdan in the Botanical
Garden of Coimbra,
September 1960
Exell was responsible for reviewing and re-organizing many of the pre-existing
collections, such as that of Herb. COI (Exell 1944, 1962; Figueiredo and Smith
2019). For the supplement of the catalogue, Exell (1956) studied some old collections that had not been examined previously or that he reassessed, and some recent
ones. A substantial collection made by Newton in 1893 in Annobón is included in
this supplement. The recent material consists mostly of the collections made by
Espírito Santo (see below) in São Tomé. A few specimens collected by the agronomist Branquinho de Oliveira (1904–1983) and E. Noronha in 1951 in São Tomé
(listed by Sobrinho 1953b), likely en route, were also included, consisting mostly of
weeds and aliens.
Exell was one of the most prolific figures when it came to the cataloguing of the
flora of the islands of the Gulf of Guinea. From 1944 to 1973, he produced a dozen
publications, some of which became classic references (Exell 1944, 1952, 1956,
1958, 1959, 1962, 1963, 1968, 1973a, b; Exell et al. 1952; Exell and Rozeira 1958).
Like Henriques, Exell also received the contributions of numerous botanists who
identified the collections: 16 botanists were acknowledged in Exell (1944) and
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21 botanists in Exell (1973b). Arthur Hugh Garfit Alston (1902–1958) who authored
the treatment of the pteridophytes (Alston 1944) in Exell’s Catalogue (1944) also
contributed with the pteridophytes for the Supplement (Alston 1956) and for two
additional articles (Alston 1958, 1959).
The algae of São Tomé and Príncipe, that had not been revised since 1908, were
finally treated by Rodrigues (1960).
Other plant collectors in the first half of the twentieth century were the Swiss
botanist John Gossweiler (1873–1952), who collected in Príncipe during stopovers
of his numerous trips between Angola and Portugal, in 1913, 1914, and 1938
(Liberato 1994), and the American botanist David H. Linder (1899–1846) on an
expedition by Harvard University from 1926 to 1927, the specimens of which are
deposited in Herb. GH (Exell 1944, Liberato 1994). On the zoological side, an
ornithological team from Oxford University went on a short visit to São Tomé and
Príncipe between September and October of 1949, providing additional notes about
several species, in the first major contribution on the subject since the works of José
Correia (Snow 1950).
In the second half of the twentieth century, the 1959 Peris-Álvarez Expedition to
Annobón (Alvarado and Álvarez 1964), headed by entomologist Salvador V. Peris
(1922–2007) and Julio Álvarez Sanchez, although short in duration, was fruitful in
advancing knowledge regarding the fauna of the area (Anthribidae: Hoffman 1959;
Nematoda: Gadea 1960a, b; Gastropoda: Ortiz de Zárate and Álvarez 1960;
Collembola: Selga 1960, 1962; fishes: Lozano Cabo 1961; Rodentia: Peris SJ
1991; Muscidae: Peris SV 1961, 1963; Odonata: Sart 1962; Orthoptera: Llorente
1968; Oribatida: Pérez-Iñigo 1969, 1982, 1983, 1984). Commissioned by the Institute of Marine Science at the University of Miami, a team of scientists lead by
Gilbert L. Voss (1918–1989), Frederick M. Bayer (1921–2007), and C. Richard
Robins (1928–2020) conducted a deep-sea biological investigation to the Gulf of
Guinea aboard the R/V Pillsbury between 1964 and 1965 (Voss 1966). In subsequent years, despite difficulties caused by the loss of manuscripts to a fire in
December 1967, the results were eventually published (Echinoidea: Chesher 1966;
shrimp: Holthuis 1966; Opisthobranchia: Marcus and Marcus 1966; birds: Robins
1966b, 1970; fishes: Courtenay 1970, Gibbs and Staiger 1970, Robins 1966a, 1970,
Robins and Nielsen 1970, Emery 1970, Fraser and Robins 1970, Iwamoto 1970;
Decapoda: Holthuis and Manning 1970; Foraminifera: Adegoke et al. 1971;
Brachiopoda: Cooper 1975; Stomatopoda: Manning 1970).
The French research vessel “Calypso” undertook a short exploratory stint to the
Gulf of Guinea in 1956, with a multitude of new publications resulting from the
material collected (Pycnogonida: Fage 1959; Polychaeta: Fauvel and Rullier 1959;
molluscs: Franc 1959; Chaetognatha: Furnestin 1959; Porifera: Levi 1959;
Annelida: Wesenburg-Lund 1959; Foraminifera: Mangin 1959; Crustacea: Forest
1959, 1966, Stubbings 1961, Crosnier and Forest 1966, Forest and Guinot 1966,
Manning 1973, de Saint Laurent and Le Loeuff 1979; Octocorallia: Tixier-Durivault
1961; fishes: Arnoult 1966; Amphipoda: Mateus and Mateus 1986). As part of a
Calypso expedition, Rose and Denizot made several botanical collections in São
Tomé and Príncipe, including living material; herbarium specimens were deposited
at Herb. P (Figueiredo 1998; Figueiredo et al. 2009).
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The French National Museum of Natural History in Paris commissioned several
excursions throughout the twentieth century to the Gulf of Guinea region, also
resulting in many new studies (Diptera: Alexander 1957; amphibians and reptiles:
Angel 1920; Tenebrionidae: Ardoin 1958; Coleoptera: Basilewsky 1957, 1958;
Orthoptera: Chopard 1958; Osoriinae: Fagel 1958; Lepidoptera: Herbulot 1958;
Dermaptera: Hincks 1958; Orthoptera: Kraus 1960; Trichoptera: Marlier 1959;
insects: Viette 1956, 1957, 1958; Coleoptera: Villiers 1957). After the creation of
the Institut fondamental d’Afrique noire [Fundamental Institute of Black Africa]
(IFAN) by the French naturalist Théodore Monod (1902–2000), its academic journal
published several papers regarding the Gulf of Guinea (Anthocleista: Monod 1957;
bryophytes: Potier de la Varde 1959; Annelida: Rullier 1965; fish: Blanc et al. 1968;
Lepidoptera: Darge 1970; insects: Kumar 1975; Decapoda: Monod 1975).
In 1936, in an effort to better understand the biological richness of its overseas
colonies, Portugal launched a scientific project for their study, Junta das Missões
Geográficas e de Investigações Coloniais (later renamed Junta de Investigação do
Ultramar and later still Junta de Investigações Científicas do Ultramar) (Marques
et al. 2018). The zoologist Fernando Frade [Viegas da Costa] (1898–1983; Fig. 5.5)
was in charge of the Centro de Zoologia de Lisboa, the zoological division under the
Fig. 5.5 A party of the participants of Missão Científica de São Tomé e Principe, in 1954 in São
Tomé, including the zoologist Fernando Frade (1), Isolina Campos (2) accompanying the husband
Ezequiel de Campos (3), and “Jaime” (4). Courtesy of the Herb. PO, Museu de História Natural e da
Ciência, Universidade do Porto
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Junta. During the 1950s and 1960s, several zoological expeditions were commissioned by the institution and from these expeditions important publications were
produced by an extended network of researchers up to present day (insects: Bacelar
1948, 1950, 1956a, b, Castel-Branco 1955a, b, 1956a, b, c, 1958a, b, c, 1963a, b, c,
1964, 1965, 1969, 1970a, 1972, Alves 1956a, b, 1965, Castel-Branco and Alves
1957, 1958, Tendeiro 1956a, b, c, d, 1957, Tordo 1956, 1969, 1974, Schmidt
1967a, b, Fernandes 1974; Diptera: Dias 1955, Azevedo et al. 1956, 1961, 1962,
Gandara 1956, Pinhão and Mourão 1961; birds, insects, and mammals: Frade 1955a,
1956; fishes: Frade and Correia da Costa 1956, Correia da Costa 1959, Alves and
Castel-Branco 1962, Almeida and Alves 2019; Copepoda: Marques 1956, 1960,
1965, 1975; diseases: Mourão 1964; Miocene fauna: Silva GH 1956a, b, 1958a, b,
Serralheiro 1957; amphibians and reptiles: Manaças 1958, 1973; Foraminifera: Reis
Moura 1961; Hymenoptera: Diniz 1964; Arachnida: Cabral and Carmona 1968/69,
Dias 1958, 1988; Aphidoidea: Ilharco and Van Harten 1975, Van Harten 1976;
birds: Frade 1959, Frade and Santos 1977; Gastropoda: Simões 1989; Chiroptera:
Lopes and Crawford-Cabral 1992).
From 1954 to 1955, Frade and Armando Castel-Branco (1909–1977) conducted
an expedition to the archipelago of São Tomé and Príncipe (Frade 1955b). This
expedition was part of the so-called Missão Científica de São Tomé e Principe. The
mission was conceived in 1954, comprising multiple scientific subjects and had the
specific aim of providing data to the International West African Conference
(Conferência Internacional dos Africanistas Ocidentais—C.I.A.O.) held in 1956 in
São Tomé. It was created by the Junta, with the objective of studying various aspects
of natural history, ethno-sociology, and economics of São Tomé and Príncipe (Vieira
and Viegas 2019). In 1956, C.I.A.O. started to work under the aegis of C.C.T.A./
C.S.A. (Commission for Technical Co-operation in Africa South of the Sahara/
Scientific Council for Africa South of the Sahara), international organizations aiming
to promote the application of science to the resolution of African problems and that
included several African and European countries (Anonymous 1956). This mission
was led by the previously mentioned Ezequiel de Campos. Campos, already in his
80s, returned to São Tomé and Príncipe (Fig. 5.5), where he had begun his professional activities. He collected new data, which together with his previous knowledge
of the islands resulted in important works about changes in the environment,
ecological disturbances, and landscape changes that he had observed over the
preceding decades (Campos 1956a, b, 1958).
The botanist Arnaldo Rozeira (1912–1984)—born in São Tomé and raised in
Portugal (Porto)—professor at the University of Porto, joined the Missão Científica
de São Tomé e Principe, as Mission Assistant and Chief of the Brigada de
Sociologia Botânica [Botanical Sociology Brigade]. During his participation in
this mission Rozeira visited São Tomé and Príncipe at least three times, in 1954,
1957, and 1958. In 1957, the Portuguese botanist Jorge Martins d’Alte (1912–death
unknown) accompanied the botanical expedition, making botanical collections
(Costa 2020). As a result of this mission a great diversity of material was collected
and deposited in Herb. PO. It comprised vascular plants (including pteridophytes),
bryophytes, lichens, algae, and a wood collection (Vieira and Viegas 2019). The
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singularity of these collections lies in the fact that Rozeira carried out the first
botanical collections on Pico do Príncipe, the highest mountain on the island
which had scarcely been accessed in earlier times. Furthermore, it was during
these expeditions that species collected by Barter were re-collected for the first time.
The African botanical collections at Herb. PO were only recently subject to an
inventory (Costa 2020), but some of these have been cited in previous works, namely
by Exell and Rozeira (1958; which included one species new to science and new
records for the islands, with pteridophytes identified by Alston), Rozeira (1958),
Barros-Ferreira (1963, 1965,1968a, b, Begoniaceae, Malvaceae, Melastomataceae;
including a new species of Tristemma), and Sampaio (1958, 1962, cyanophytes).
The Portuguese collector and naturalist Joaquim Sampaio (1899–1981) again
published about cyanophytes (Sampaio 1963), but this time on specimens collected
by Joaquim R. dos Santos Júnior (1901–1990) from Príncipe (specimens at
Herb. PO).
During the C.I.A.O. in 1956, several authors who had been working on the
islands of the Gulf of Guinea presented communications dedicated to botanical
topics (Campos 1956b; Almeida and Morais 1958a, b, c; Boughey 1958). Both the
French naturalist Théodore Monod (1902–2000) and the English botanist Charles
Aubrey Thorold (1906–1998) visited São Tomé and Príncipe during C.I.A.O. and
made botanical collections (specimens at Herb. BM and COI; Exell 1962, Liberato
1994). The pteridophytes were studied by Alston (1959), with several new records
being added to the flora of the islands (Figueiredo 1998). Exell (1959) published the
novelties for the Flora, referring to Monod’s material as “excellent collections”.
Exell (1959) referred to collections from Espírito Santo (see below). The majority of
the bryophytes collected by Monod and Thorold constituted the basis for the
publication by Robert André Léopold Potier de la Varde (1878–1961) (1959). It
was Monod (1960) who established and proposed the most commonly used classification of São Tomé vegetation, based on species composition (Figueiredo et al.
2011).
Between 1956 and 1973, the Santomean Joaquim Viegas da Graça Espírito Santo
(1901–unknown) made numerous botanical collections in São Tomé and Príncipe
(Espírito Santo 1970, 1974), with duplicates at Herb. COI, LISC, BM, and K,
including endemic plants (Figueiredo 1994c). In 1968, he was appointed by the
Brigada de Fomento Agro-Pecuária de S. Tomé to undertake botanical prospecting,
a task he executed for six months (Exell et al. 1952, Figueiredo 1994c, d, Liberato
1994).
In 1956, Helder Lains e Silva (1921–1984) and José Carvalho (dates of birth and
death unknown) also made a considerable collection in São Tomé and Príncipe. The
list of their collections was published by Silva HL (1958b). These collections were
made under the auspices of the Junta de Exportação do Café and are housed at Herb.
LISC (Exell, 1962, Silva HL 1958b, Sobrinho 1959, Liberato 1994).
Thomas Christopher Wrigley (1935–) and Fenella Ann Melville (later Mrs.
Wrigley) (1936–), both English botanists, participated in a joint Spanish-British
expedition to Bioko and Annobón in July and August 1959, together with Julio
Álvarez (dates of birth and death unknown), a Spanish zoologist. It was the most
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significant biological expedition to Annobón since that of Mildbraed in 1911. They
collected 316 specimens which are at Herb. K, with duplicates at Herb. BM, BR,
MPU, and MA. This collection was identified and published by Exell (1963).
Although Exell identified the majority of the collection, the pteridophytes had not
been studied until recently (Figueiredo et al. 2009). These collections were kept at
Herb. BM but had not been incorporated into the main collection (Figueiredo et al.
2009).
The French botanist Bernard Marie Descoings (1931–2018) collected in
Annobón from 24 February to 3 March 1964, as part of an expedition with several
researchers. There are 233 specimens of his collections deposited at Herb. MPU,
including 56 pteridophytes (Figueiredo et al. 2009; Velayos et al. 2014).
In cooperation with the Junta, the Brigada de Fomento Agro-Pecuário de São
Tomé e Príncipe (established in 1964) carried out studies regarding the fauna of the
islands, with special relevance to the Entomologists’ meeting in São Tomé and
Príncipe in August of 1967 (Quinta 1967; Carvalho 1968). The results of those
missions were published in the journal with the same name as the initiative (e.g.,
Castel-Branco 1967a, b, c, d, e, f, 1970b, 1971; Ferreira 1967a, b, c, d, 1968, 1969,
1971; Quinta 1967).
René de Naurois (1906–2006), a World War II veteran and catholic priest turned
ornithologist, authored dozens of papers and books regarding the birds of the coast
of West Africa and its offshore islands. From the early 1970s to the late 1990s,
Naurois thoroughly studied the ornithological fauna of the Gulf of Guinea and
published the results of his research (Naurois 1972a, b, 1973a, b, 1975a, b, 1979,
1980, 1981, 1982, 1983a, b, 1984a, b, c, d, 1985a, b, 1987a, b, c, 1988a, b, 1994;
Naurois and Antunes 1973; Naurois and Wolters 1975; Fry and Naurois 1984),
which culminated with the “Les oiseaux des îles du Golfe de Guinée: São Tomé,
Prince et Annobon” published in 1994. On behalf of the zoologist Henri Heim de
Balsac (1889–1979), Naurois also collected shrew specimens, in addition to his
work with birds (Heim de Balsac and Hutterer 1982).
Up until 1974, several more incursions to the Gulf of Guinea were commissioned,
with the extent of their collections resulting in important publications from various
taxonomic groups. Aurélio Basilio conducted an expedition to Annobón in 1957
(Basilio 1957) and some years later, in 1961, C.H. Fry did the same (Fry 1961). The
entomologist Jacques O. Derron, with the Brigada, spent three years (1972–1975)
studying the insects associated with cacao plantations in São Tomé, from which
stemmed several publications (Fursch 1974; Badonnel 1976; Wirth and Derron
1976).
On the years leading up to the independence of the country, many of the
collections in herbaria were revisited and studied by other researchers, or compared
to new material, resulting in new publications often focusing on a particular group,
family, genus, or even a species (e.g. Calvoa robusta: Cogniaux 1908/09; Fungi:
Henriques 1922; Câmara and Luz 1938; botanic collections: Romariz 1952; vascular
plants: Sobrinho 1952; Hepaticae: Arnell 1956; Algae: Rodrigues 1960; marine
algae: Steentoft 1967; Achyranthes: Cavaco 1968; Loranthaceae: Balle 1964;
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Nicandra, Physalis, and Withania: Fernandes 1969; Erythrina: Bocquet and Derron
1976; Uvaria: Paiva 1978/79).
In 1972, Maria Cândida Liberato (1944–) and Espírito Santo began taxonomic
revisions of families of the flora of the islands with the objective of producing a Flora
of São Tomé and Príncipe (Liberato and Espírito Santo 1972–1982). The project
was never completed, and only a few families were published (Papilionaceae,
Mimosaceae, Caesalpiniaceae, Connaraceae, Rosaceae: Liberato 1972, 1973,
1976, 1980a, b, 1982; Aquifoliaceae, Alangiaceae: Espírito Santo 1973a, b).
The common names of the plants of this archipelago were not neglected, being
the subject of multiple publications (Rozeira 1958; Silva HL 1959a; Espírito Santo
1969a). These approaches were often included in studies dedicated to the use of
plants for medicinal purposes. Several works and research were dedicated to pharmacology/pharmacognosy and uses of medicinal plants across this period (Alves and
Prista 1958, 1959, 1960; Prista and Alves 1958, 1959; Prista et al. 1960; Alves et al.
1961, 1962; Alves et al. 1960; Espírito Santo 1969b).
In geographical and economic studies undertaken on these islands, it was common to include an analysis of vegetation, ecology, landscape change, and productive
aptitude, providing data on vegetation cover and habitats (Chevalier 1906, 1910,
1938/39; Campos 1920, 1956a, 1958; Tenreiro 1961; Rodrigues 1971; White 1983/
84). Throughout the twentieth century, there were several studies and reviews of
applied botany, namely with an agronomic perspective, addressing topics such as
agricultural suitability, crops and associated problems (e.g. Câmara and Coutinho
1923; Cortesão 1956/57; Silva HL 1958a, 1959b; Ascenso 1964; Mariano 1966;
Espírito Santo 1973c; Rodrigues 1974), with a special focus on cocoa, coffee, and
quinine crops (e.g. cocoa: Cortesão 1921; Thorold 1955, 1959; Silva HL 1960;
Ascenso 1963, 1965; quinine: Costa 1941, 1944; coffee: Silva HL 1958b; coffee and
cocoa: Vieira da Silva 1960).
The First Decades of Independence
Following independence from Portuguese rule in 1975, São Tomé and Príncipe was
engulfed in a wave of political unrest that hindered the possibility of new biological
missions in the area (Jones 1994). Although the taxonomic enterprise continued, the
1970s saw the birth of the modern nature conservation movement and the raise of
public and scientific concerns regarding human impacts on the natural world. This
has led to an almost radical change of interests in the research community, who
became much more dedicated to the conservation aspects of biodiversity research,
which in the Gulf of Guinea archipelago translated to the study of the ecology and
conservation status of vertebrates.
In 1984, a team of zoologists from the Zoology and Anthropology Sections of the
Faculty of Sciences of the University of Lisbon led by entomologist Luis Mendes
(1946–) conducted a one-month zoological expedition to São Tomé (Mendes et al.
1988). The resulting publications were published by himself and other authors
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(Diptera: Grácio 1988, 1999; insects: Mendes 1988a, b, c; Mendes et al. 1988;
Drosophilidae: Rocha Pité 1993; Culicidae: Ramos and Capela 1988, Ramos et al.
1989, 1994; Ribeiro 1993, Ramos et al. 1994; Serrano et al. 1995; Ribeiro et al.
1998). Most of the vertebrates collected were not studied until very recently (see
Ceríaco et al. 2022).
From 1987 onwards, the International Council for Bird Preservation (ICPB)
sponsored several projects for the study of endemic birds of São Tomé and Príncipe
(Jones and Tye 1987, 1988; Burlinson and Jones 1988), one of them in cooperation
with the University of East Anglia (UEA) (Atkinson et al. 1991, 1994), as well as the
creation of a conservation educational programme with the support of the European
Economic Community (Harrison and Steel 1989). With the information Atkinson
and colleagues were able to gather in the UEA expedition, Dave E. Sargent travelled
with other birders in 1989 and 1991, publishing the results of their observations
(Sargent et al. 1992; Sargent 1994), which included the rediscovery of the São Tome
Grosbeak Crithagra concolor, 101 years after the previous record.
After a one-week trip to São Tomé, Eccles (1988) published the results of his
ornithological observations, highlighting the rediscovery of São Tome Short-tail
Motacilla bocagii. A short research stint to Annobón was conducted by Michael J. S.
Harrison in March 1989, as a part of a larger mission to São Tomé and Príncipe
sponsored by ICPB. The visit resulted in an updated bird checklist of some parts of
the island (Harrison 1990). The Polish entomologist Tomasz W. Pyrcz conducted
two small expeditions in 1989 (January–March) and 1990 (July–September) to São
Tomé and Príncipe aiming to create the first checklist for the butterfly species in the
archipelago, which resulted in three publications (Pyrcz 1991, 1992a, b). In cooperation with the Natural History Museum (NHM), the entomologist Janusz
Wojtusiak (1942–2012) was entrusted to lead a project to identify and catalogue
the macrolepidoptera species of São Tomé extant at the NHM as well as those
collected in September of 1990 in a small trip to the island (Honey and Wojtusiak
1994; Wojtusiak and Pyrcz 1995; Wojtusiak 1996a, b, c). Other entomological
expeditions to the region resulted in the description of new species and contributed
to the growth of knowledge regarding the entomofauna of the Gulf of Guinea
(Pinhey 1974; Villiers 1976; Darge 1991; Allard 1990; Herbulot 1991a, b; Antoine
1992; Basquin 1992; Bomans 1992; Canu 1994).
In the late 80s and early 90s, teams of Spanish researchers began working in the
Gulf of Guinea, some of them under the Spanish programme “Research and Nature
Conservation Programme in Equatorial Guinea” (Castroviejo et al. 1994b). Those
expeditions led to several publications on insects (Viejo 1984, 1990), mammals
(Juste and Ibañez 1993a, b, c, 1994), molluscs (Fernandes and Rolan 1989, 1992;
Kosuge and Fernandes 1989; Gofas and Fernandes 1991; Rolan and Fernandes
1990, 1991, 1992, 1995; Rubio and Rolan 1990; Rolan and Templado 1993;
Rolan 1996), and sea turtles (Castroviejo et al. 1994a).
Funded by Cooperación Española and led by the Associación Amigos de
Doñana, a Spanish expedition including the botanist Manuel Fidalgo de Carvalho
(dates of birth and death unknown) visited the island of Annobón. Between
September and October of 1987, Carvalho collected 113 specimens, now deposited
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at Herb. MA (Figueiredo et al. 2009; Velayos et al. 2014). In August 1986, in an
expedition to São Tomé organized by the Secció de Petits Països del CIDOB, Neus
Gabaldá Casado (dates of birth and date unknown) and Núria García Jacas (1961–)
collected specimens of 114 taxa, including pteridophytes; the specimens are deposited at Herb. COI and BC (Gabaldá and Jacas 1988).
Herpetological expeditions to São Tomé and Príncipe from 1989 and 1991 led by
Catherine Loumont (1942–) resulted in reviews of the amphibians and reptiles of
these islands (Loumont 1992; Schätti and Loumont 1992). Previously, Ronald
Nussbaum (1942–) and Michael Pfrender (1960–) had collected herpetological
specimens during June and July of 1988, with a particular special focus on caecilians. Those collections are currently extant in the University of Michigan’s Museum
of Zoology.
In the spring of 1991, a team of researchers from the University of Dresden
(Germany) conducted an exploratory mission to the Gulf of Guinea, with numerous
publications resulting (amphibians, reptiles and arachnids: Haft 1992, 1993a, b;
amphibians and reptiles: Schatti and Loumont 1992; amphibians and arachnids:
Fahr 1993a, b; Feiler 1993; mammals: Feiler et al. 1993, Dutton and Haft 1996;
Cnidaria: Kock 1993; Phthiraptera: Mey 1993; birds: Feiler and Nadler 1992, Nadler
1993; Nadler and Feiler 1993; reptiles: Nill 1993; Gastropoda: Schniebs 1993;
Lepidoptera: Schutz 1993; Myriapoda: Spelda 1993; Teleostei: Zarske 1993;
amphibians: Haft and Franzen 1996). Previously, Feiler and Günther had travelled
to the region and published several papers regarding the mammals of the Gulf of
Guinea (Feiler 1984, 1988; Günther and Feiler 1985).
Although the ichthyofauna of the islands is quite diverse, after the pioneering
work of Balthazar Osório there was a lack of further studies. Russian expeditions in
1983 and 1986 (Domanevskaya 1987, 1988) provided additional information on
the biodiversity and were followed by Project d’Évaluation des Ressources
Halieutiques, which resulted in important publications for improved baseline knowledge (Worms 1996a, b; D’Almeida 1996; Afonso et al. 1999).
The work of the English zoologist Angus Robin Gascoigne (1962–2012), who
lived in São Tomé for many years (Melo 2012), greatly contributed to the knowledge
of the molluscan fauna and other aspects of the biodiversity of the Gulf of Guinea
(Gascoigne 1993, 1994a, b, c 1995a, b). He also collected plants that were deposited
at Herb. LISC and co-authored some papers on flora (Figueiredo and Gascoigne
2001; Figueiredo et al. 2009).
A collaboration between the European Community conservation programme for
the forest ecosystems of central Africa (ECOFAC) and the U.S. Peace Corps
originated the first major survey on the sea turtles of the Gulf of Guinea
(1994–1996), which resulted in baseline information to move towards conservation
programmes (Graff 1996; Rosseel 1997). The ECOFAC programme is associated
with generating interest in the flora of these islands among the Belgium academic
community, which resulted in numerous collections made and the description of new
species (e.g. La Croix and Brune 1997; Cribb et al. 1999; Stévart and Geerinck 2000;
Joffroy 2001).
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Continuing the dynamics implemented by the ECOFAC programme on São
Tomé, further botanical inventories took place in the 1990s, notably those carried
out by the botanist Jean Lejoly (1945–) and his students between 1994 and 1998, and
by the Angolan agronomist Gilberto Cardoso de Matos (1935–) from 1994 to 1999.
These collections are deposited at Herb. BRLU and LISC. Some duplicates are also
deposited at Herb. STPH (Figueiredo et al. 2011). Matos was one of the main
collectors active in São Tomé and Príncipe in the 1990s, amassing ca. 3000 specimens during several expeditions. He often collected with Kathleen Van Essche
(fl. 1991–2001). Matos also produced agro-ecological and vegetation maps for São
Tomé and Príncipe with the agronomist Alberto Castanheira Diniz (1923–2008)
(Diniz and Matos 2002a, b).
Some collecting initiatives focused on orchids were developed by Belgian botanist Tariq Stévart (1974–). With the collaboration of Faustino de Oliveira (1963–) he
carried out a systematic survey of the island throughout 1998, after two preliminary
missions. On the island of Príncipe, three surveys were organized with the aim of
carrying out botanical inventories in the southwestern parts of the island. The results
were published in several papers and a guide to orchids of São Tomé and Príncipe
(Stévart et al. 2000; Stévart and Oliveira 2000).
The botanist Jorge Paiva (1933–) who undertook over 20 collecting expeditions
to São Tomé and Príncipe deposited his collections at Herb. COI. Many of his
botanical surveys and collections took place within the scope of diverse projects. For
instance, between 1989 and 1993, he collaborated on a project funded by the
European Communities Commission regarding the impact of coffee nematodes in
the different cultivars (Abrantes 1993).
Additionally, there are collections made in the 1990s by many others, such as the
Santomeans Sabino Pires Carvalho (1959–) and Oliveira, at Herb. BRLU and LISC,
Estrela Figueiredo (1963–; collected from 1993 to 2002) at Herb. K and LISC,
Gascoigne (collected in 1999) at Herb LISC, Maria Fernanda Pinto Basto (1938–;
collected in 1990) at Herb. LISC, and Maria do Céu Madureira (1961–) and Ana
Paula Martins (1962–) at Herb. COI. Most collections made in the 1990s were
deposited at Herb. BRLU, COI, and LISC.
By the end of the twentieth century, a series of taxonomic revisions of the flora of
the islands was initiated with the publication of a catalogue of pteridophytes
(Figueiredo 1998) and several revisions produced for Equatorial Guinea
(e.g. Fernández Casas 1992, Hepper 1992, Morales 1992, Leeuwenberg 1992).
These revisions would later give rise to the Flora de Guinea Ecuatorial.
In 1993, an ethnopharmacological study was initiated in São Tomé and Príncipe
in collaboration with the Ministry of Health of the country (Madureira 2006, 2012;
Madureira et al. 2008; Martins 2002). This study involved a survey of species and
had the collaboration of Paiva for the identification of the plant collections. Further
projects of applied botany ensued, including the doctoral project of Cristina Galhano
(1969–) (Galhano 2006) during which collections were made by Paiva in 1996. In
Bom Sucesso Botanical Garden (São Tomé), a tribute is paid to many of the
botanists mentioned here, who developed work on the flora of the arquipelago
(Fig. 5.6).
5
The History of Biological Research in the Gulf of Guinea Oceanic Islands
109
Fig. 5.6 Commemorative plate on the botanists who studied São Tomé and Príncipe flora, funded
by ECOFAC and placed in the Bom Sucesso Botanical Garden. Photo credits: Luis Ceríaco
In December 1994, the journal Biodiversity and Conservation published a special
issue dedicated exclusively to the review of old and new data regarding the Gulf of
Guinea’s species richness and endemism (Juste and Fa 1994). This publication was
based on works presented at the workshop “Biodiversity and Conservation of the
Gulf of Guinea Islands”, held in June 1993 at the Jersey Wildlife Preservation Trust
(Butnyski and Koster 1994; Castelo 1994; Castroviejo et al. 1994a, b; Colell et al.
1994; Del Val Pérez et al. 1994; Dutton 1994; Gascoigne 1994c; Jones 1994; Juste
and Fa 1994; Juste and Ibañez 1994; Peet and Atkinson 1994; Schaaf 1994;
Figueiredo 1994b; Sequeira 1994).
In the 1990s, environmental awareness initiatives stimulated the emergence of
publications dedicated to biodiversity conservation, such as the book Conservação
dos ecossistemas florestais na República Democrática de São Tomé e Príncipe
(Jones et al. 1991). Figueiredo (1997) produced a preliminary assessment of the
conservation status of 38 trees of São Tomé and Príncipe in a report for the World
Conservation Monitoring Centre (Oldfield et al. 1998).
Following the work of Espírito Santo (1969a, b) and Silva HL (1959a), the
medicinal uses and the common names of plants continued to be studied and
compiled (Sequeira 1994). Studies of agronomic content were also continued,
110
L. M. P. Ceríaco et al.
some directed to particular products (seeds: Ferrão 1979, Ferrão and Ferrão 1984;
plant uses: Roseira 1984; woods: Freitas 1987).
Twenty-First Century: A New Generation of Researchers
Taxonomic research initiated in the previous century continued well into the twentyfirst century, with several revisions and checklists being published. The flora of
Annobón was treated in a series of checklists of the flora of Equatorial Guinea
(e.g. Fero et al. 2003; Parmentier and Geerinck 2003; Cabezas et al. 2004) and in the
volumes of Flora de Guinea Ecuatorial, an on-going project with the first volume
being issued in 2008 (Velayos et al. 2008). Regarding São Tomé and Príncipe,
several papers on pteridophytes (Figueiredo 2001, 2002; Figueiredo and Gascoigne
2001; Figueiredo and Roux 2008; Figueiredo et al. 2009) and a checklist of the
pteridophytes and lycophytes (Klopper and Figueiredo 2013) were published. A new
catalogue of the flora of São Tomé and Príncipe that updated the over 35-years-old
checklist produced by Exell (1973b) was finally published (Figueiredo et al. 2011).
In the same year a catalogue of the bryophytes was also published (Sérgio and Garcia
2011). The Rubiaceae, one of the dominant families of the flora, was treated in a
series of revisions (Alves et al. 2005; Figueiredo 2005; Davies and Figueiredo 2007).
Applied botany studies integrated into environmental protection strategies also
continued (e.g. Martins 2002; Madureira 2006; Madureira et al. 2008).
At the dawn of the new century, a new wave of biodiversity researchers hit the
islands. Furthering knowledge gathered by the previous generations, this new
generation has not only continued to contribute to cataloguing the still undocumented and undescribed fauna and flora of the oceanic islands of the Gulf of Guinea,
but also implemented new techniques, methodologies, and approaches. Other topics,
such as biodiversity conservation, ethnobiology, ecosystem health, and ecology
have experienced a considerable growth. This research has been conducted by an
increasingly diverse group of international and national researchers and is mostly
covered in the subsequent chapters of the volume. Nevertheless, some aspects of this
new wave of research need to be highlighted here—both because they represent an
important turning point on the study and preservation of the local biodiversity, but
also due to the dimension and intensity of some of these activities.
One fundamental difference in the research carried out in the twenty-first century
is the use of molecular methods to study the taxonomy, phylogenety, and biogeography of the biodiversity of the islands. While this has not yet been applied to all
taxonomic groups, the use of molecular methods has been widely applied to the
study of the island’s herpetofauna (Bell et al. 2022; Ceríaco et al. 2022), birds (Melo
et al. 2022) and, to a lesser extent, plants (Plana et al. 2004; Soares et al. 2010). The
growing importance of ecological and conservation studies has also marked the
research landscape in the oceanic islands of the Gulf of Guinea, with dozens of
works and theses produced on the topic, especially at the University of Lisbon (see
Lima et al. 2022, Soares et al. 2022), but also the seminal works on marine turtles
5
The History of Biological Research in the Gulf of Guinea Oceanic Islands
111
(see Ferreira-Airaud et al. 2022), plants (see Stevart et al. 2022), and even land
molluscs (see Panisi et al. 2022). Finally, a revival of field expeditions to further
catalogue the diversity and distribution of islands’ species has resulted in important
modern collections, many of which have not yet been fully studied. Of critical
importance is the programme led by the California Academy of Sciences (CAS),
whose activities started in 2001. This programme, led by Robert “Bob” Drewes, has
conducted over a dozen expeditions to the islands and involved researchers from
across the world with expertise in a wide array of taxonomic groups. A considerable
part of the recently produced knowledge on the archipelago’s biodiversity stems
from this programme.
Acknowledgements The authors would like to thank Branca Moriés, librarian of the Museu de
História Natural e da Ciência, Universidade de Lisboa, for her support with historical bibliography,
Cristiana Vieira, Curator of the Herbarium of the Museu de História Natural e da Ciência,
Universidade do Porto, for her support in accessing documentation and data, and Ana Rita Simões,
Martin Xanthos, and Nicholas Hind, from Kew Gardens, for providing information. The authors are
also indebted to Aaron M. Bauer for a revision that greatly improved the original manuscript.
Fundação para a Ciência e a Tecnologia (Portugal) funded BSS (2021.06659.BD) and SBV
(2017.128574.BD).
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Chapter 6
Biogeography and Evolution in the Oceanic
Islands of the Gulf of Guinea
Martim Melo, Luis M. P. Ceríaco, and Rayna C. Bell
Abstract As with most archipelagos, geography played a central role in the assembly and evolution of the endemic-rich biological communities of the Gulf of Guinea
oceanic islands. The islands are located at moderate distances from the species-rich
African continent that surrounds them to the east and north. This proximity facilitated colonization by many branches of the tree of life, but gene flow between the
islands and continent was low enough that many lineages evolved in isolation once
they reached the archipelago, resulting in many endemic species. Furthermore,
several of the island taxa belong to groups typically considered to be “poor dispersers” across sea barriers, which strongly supports a role for natural rafts in
seeding the islands. Oceanic currents, including the freshwater pathways that extend
from large river drainages into the Gulf of Guinea during the rainy season, also
support this hypothesis. The distances between the islands are equivalent to those
between the islands and the continent such that inter-island dispersal events appear
M. Melo (*)
Museu de História Natural e da Ciência da Universidade do Porto, Porto, Portugal
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório
Associado, Universidade do Porto, Vairão, Portugal
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO, Vairão, Portugal
FitzPatrick Institute of African Ornithology, University of Cape Town, Cape Town,
South Africa
L. M. P. Ceríaco
Museu de História Natural e da Ciência da Universidade do Porto, Porto, Portugal
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório
Associado, Universidade do Porto, Vairão, Portugal
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO, Vairão, Portugal
Departamento de Zoologia e Antropologia (Museu Bocage), Museu Nacional de História
Natural e da Ciência, Universidade de Lisboa, Lisbon, Portugal
R. C. Bell
Department of Herpetology,, Institute for Biodiversity Science and Sustainability, California
Academy of Sciences, San Francisco, CA, USA
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_6
141
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M. Melo et al.
to be relatively rare and thus few taxa are shared between them. Still, the islands
present multiple cases of secondary contact leading to hybridization and genetic
introgression between closely related lineages—providing several models to study
the role and consequences of gene flow in evolution. Most taxa for which molecular
estimates of divergence time have been derived are much younger than the ages of
the islands. This pattern is consistent with high species turnover, likely resulting
from a combination of small island sizes, proximity to the African continent and a
long history of intense volcanic activity. The Gulf of Guinea oceanic islands provide
multiple examples of classical adaptations to island life (the “island syndrome”),
including giants and dwarves, ornament and color loss, among others. In addition,
emerging studies of birds are highlighting the importance of competition regimes in
driving phenotypic change—with examples of both character release (low interspecific competition) and character displacement (inter-specific competition upon
secondary contact). Collectively, the Gulf of Guinea oceanic islands offer unique
opportunities to study adaptation and speciation in a range of taxa and contexts.
Keywords Adaptation · Biogeography · Endemism · Gene flow · Island syndrome ·
Speciation
Introduction
Islands, and oceanic islands in particular, have always occupied a special place in
human imagination (cf. Schalansky 2010). Their isolation and well-defined borders
make them worlds apart, microcosms often populated by unique and peculiar
creatures. For the naturalist, oceanic islands are one of the most fruitful settings
for the study of evolutionary and ecological processes, including adaptation, speciation, and community assembly (Losos and Ricklefs 2009; Whittaker et al. 2017).
Charles Darwin hinted at islands serving as “natural laboratories” in his account of
the Beagle expedition, after having visited the Galapagos in September 1835
(Darwin 1845: 377–378). It was Alfred Russel Wallace, however, who put it clearly
in his fundamental work aptly named Island Life under the section Importance of
Islands in the Study of the Distribution of Organisms (Wallace 1880: 234):
In islands we have the facts of distribution often presented to us in their simplest forms,
along with others which become gradually more and more complex; and we are therefore
able to proceed step by step in the solution of the problems they present. (. . .) [W]hen we
have mastered the difficulties presented by the peculiarities of island life we shall find it
comparatively easy to deal with the more complex and less clearly defined problems of
continental distribution.
The depiction of islands as natural laboratories arises from their inherent simplicity (systems with well-defined boundaries, generally small, and with a depauperate biota), together with being striking centers of evolutionary change and
diversification by virtue of their isolation and specific environmental constraints
(Wallace 1880; Carlquist 1965; Grant 1998a; Emerson 2002; Losos and Ricklefs
2009; Whittaker et al. 2017). Both these characteristics are particularly evident in the
spectacular radiations of the most isolated island systems, as illustrated by the
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Biogeography and Evolution in the Oceanic Islands of the Gulf of Guinea
143
Hawaiian Drosophila in which up to 1000 species may have evolved from just one
or two species (Carson and Kaneshiro 1976; Kaneshiro et al. 1995). Correspondingly, much progress on the study of evolution on islands has stemmed from remote
islands such as the Hawaiian archipelago (Wagner and Funk 1995; Craddock 2000)
and the Galápagos (Grant and Grant 2008). More recently, it has become clear that
island systems closer to continents have the potential to significantly advance our
understanding of the processes driving diversification.
As one approaches the mainland, the complexity of island systems increases as
dispersal and gene flow between the mainland and the island populations become
more frequent (cf. Fig. 1.1 in Whittaker 1998). “Intermediate island systems” are
those archipelagos that lie between remote islands systems, virtually independent
from the mainland, and systems so close to the mainland that speciation in situ is not
possible (Melo 2007; Ricklefs and Bermingham 2007). Intermediate island systems
are promising natural laboratories as they may provide a simple setting to investigate
the role of gene flow in evolution, which remains a question of fundamental
importance in evolutionary biology (Dowling and Secor 1997; Seehausen 2004;
Pinho and Hey 2010; Feder et al. 2012; Abbott et al. 2013; Buerkle 2014; Arnold
2015; Taylor and Larson 2019; Matute and Cooper 2021). In addition, the faunas of
intermediate island systems are typically derived from several distinct families
(independent replicates for evolutionary studies), rather than being dominated by a
few species-rich genera that have adaptively radiated. Consequently, patterns of
community assembly in such archipelagos are likely more similar to those of
continents than are those of more isolated archipelagos where most of the diversity
is derived from a few extensive radiations (Melo 2007; Ricklefs and Bermingham
2007).
Here we provide an overview of the biogeography and evolution of the biota of
the oceanic islands of the Gulf of Guinea (Príncipe, São Tomé, and Annobón),
highlighting their potential to advance our understanding of the processes generating
diversity: from population divergence to speciation to community assembly. In
addition, this setting provides several excellent models to study the role of gene
flow with respect to the evolution of divergent phenotypes and patterns of genomewide differentiation. Readers will likely notice that this overview is limited and
biased towards terrestrial vertebrates. For other taxonomic groups, the diversity of
the islands is still incompletely documented and described (Ceríaco et al. 2022a),
and thus building the essential foundation for future hypothesis-driven studies is still
a work in progress for these other taxa. A brief overview of marine biogeography in
the Gulf of Guinea is described in Costa et al. (2022).
Biogeography
The Importance of Geography
The updated checklists for terrestrial groups in the oceanic islands of the Gulf of
Guinea (reference list in Ceríaco et al. 2022a) reveal a few principal patterns:
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M. Melo et al.
(1) high levels of endemism; (2) wide representation across the tree of life; (3) in situ
radiations are rare and result in few species; and (4) the biological communities of
each island are largely unique, with few endemics shared between them. With the
exception of the Odonata (dragonflies and damselflies), which have relatively low
species diversity in the Gulf of Guinea and just one endemic species (Dijkstra and
Tate 2022), the three islands have some of the highest concentrations of endemic
species in the world for several groups, including mosquitoes (Loiseau et al. 2019),
amphibians (Bell et al. 2022), terrestrial reptiles (Ceríaco et al. 2022b), and birds
(Melo et al. 2022). These patterns are particularly remarkable in relation to the small
size of these islands (just over 1000 km2 combined) and are likely a consequence of
their favorable geographic setting.
Just in the Right Place: Close, But Not Too Close, to a Large
and Species-Rich Continent
The diversity of unique genera and families in the archipelago across taxonomic
groups from fungi to frogs is indicative of a large number of colonizations from the
mainland. High levels of endemism, once again across many taxonomic groups,
indicate that many of these island colonizers have subsequently diverged from their
mainland counterparts. The islands are therefore close enough to the continent to
receive a diverse array of mainland dispersers but far enough away for these to
diverge once they arrive to the islands. These are two defining traits of intermediate
island systems: the likelihood of colonizations is higher than on remote systems and
the conditions for population divergence are preserved (Melo 2007; Ricklefs and
Bermingham 2007). For groups such as birds, where the concentration of island
endemics is the highest in the world (Melo et al. 2022), it is as if the oceanic islands
of the Gulf of Guinea are located at the perfect distance from the mainland to
optimize the balance between colonization (as a source of new lineages) and
isolation (reduced gene flow to allow for genetic differentiation). Such an optimal
distance will likely vary among taxonomic groups according to their dispersal
potential.
The adjacent African continent also hosts the species-rich Congolian rainforests
and the Guinean Forests of the West Africa biodiversity hotspot (IUCN 2015),
which surround the islands to the east and north, respectively. Thus, the islands
are proximal to extensive coastlines of a large and biodiverse landmass. Being
situated adjacent to a large landmass is the most important predictor of global
plant species diversity on islands (Weigelt and Kreft 2013). In addition, the islands
and much of the adjacent mainland share similar habitats (notably rainforest), which
increases the chance of successful establishment following sweepstakes dispersal
events (Weigelt and Kreft 2013).
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Biogeography and Evolution in the Oceanic Islands of the Gulf of Guinea
145
Colonization Outweighs In Situ Diversification as a Source
of New Species Diversity
Independent colonizations from the mainland, rather than in situ diversification, is
the dominant process by which species diversity accumulated in the archipelago
(Box 6.1). For example, the 29 endemic bird species present on the three oceanic
islands derive from 20 to 22 separate colonizations from the mainland, and only
three are shared between islands (Melo et al. 2022). Of the 164 endemic vascular
plant taxa of the Gulf of Guinea islands only a small subset is shared between more
than one island, and an even more diminutive number is shared with Bioko (Figueiredo 1994; Stévart et al. 2022). Likewise, all nine amphibian species are endemic to a
single island, and five are the sole representative of their family on their respective
island (Bell et al. 2022). Dispersal between islands, and subsequent isolation, has
also been a source of further endemic species in some vertebrate groups including
Hyperolius reed frogs (Bell et al. 2015a, b), Hemidactylus geckos (Miller et al.
2012), Trachylepis skinks (Ceríaco et al. 2016), Boaedon house snakes (Ceríaco
et al. 2021) and birds, of which the five-species radiation of Zosterops white-eyes is
the best example (Melo et al. 2011, 2022). However, for most organisms, each island
is closer to an independent unit rather than part of a tight-knit archipelago.
The extensive evolutionary radiations described from remote archipelagos are
facilitated by inter-island dispersal events within the archipelago followed by divergent adaptation to fill open ecological niches (Schluter 2000; Gillespie et al. 2020).
In the case of the oceanic islands of the Gulf of Guinea, the dearth of adaptive
radiation may be a consequence of low inter-island colonization (due to the large
distances that separate them), limited opportunities to adapt to novel ecological
space (due to the high phylogenetic and ecological diversity of colonizers from the
mainland; Schluter 2000; Ricklefs and Bermingham 2007; Rundell and Price 2009;
Gillespie et al. 2020), and reduced dispersal ability of island species (Box 6.2).
Box 6.1 Speciation on Oceanic Islands
The most detailed model of how populations diversify on oceanic islands was
proposed more than 100 years ago by the British naturalist Robert C. L.
Perkins (Grant 2000, 2001). His “archipelago radiation model” (Perkins
1913) was derived from his work on the radiation of Hawaiian honeycreepers
(Aves: Fringillidae; Perkins 1901), and subsequently strengthened with his
studies of other Hawaiian vertebrates (Perkins 1903) and insects (Perkins
1913). In Perkin’s archipelago radiation model (Panel 3 of figure below),
speciation is initiated by population subdivision (isolation: allopatry), which
leads to selection-driven divergence, potentially aided by random factors (the
concept of drift had not yet been formulated). In a second stage, populations
diverging in isolation may meet on the same island (secondary contact:
sympatry). They may either interbreed, obscuring the divergence and merging
(continued)
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M. Melo et al.
Box 6.1 (continued)
into a single population once more, or they may co-exist as increasingly
distinct entities even if some interbreeding occurs. In this case, competition
between the two populations will lead to further divergence resulting in
ecological character displacement. In other words, the most similar individuals
of each species suffer the strongest competition, such that extreme phenotypes
are favored by selection and intermediate phenotypes are selected against
(Brown and Wilson 1956; Grant 1972). Two things are surprising regarding
this model: (1) how complete and specific it is and (2) how it was forgotten by
most evolutionary biologists in the ensuing decades (Grant 2000, 2001). The
deep insights of Perkins, including the central role of competition in driving
phenotypic divergence, are particularly impressive considering that his archipelago radiation model is very similar to the “ecological speciation model”
proposed in the twenty-first century (Rundle and Nosil 2005; Nosil 2012).
Pathways for speciation in oceanic archipelagos—using the Gulf of Guinea as an example.
In this schematic, the single endemic species on Annobón has always arisen by
allospeciation
In many archipelagos, speciation is achieved by divergence in isolation
(allospeciation: Mayr and Diamond 2001), the first step of the radiation model
(Panels 1 and 2 of figure above). This may even be the case for most
archipelagos, as recently confirmed for birds in a global analysis of diversification on islands (Valente et al. 2020). It may also be deemed the most passive,
or trivial, speciation mode as permanently isolated populations will always
follow distinct evolutionary paths. Phenotypic diversification is often limited
in this setting, especially when the mainland and island provide similar
habitats. At the other extreme, populations may diverge and speciate fully in
sympatry (Panel 4 of figure above; sympatric speciation). This mechanism is
not included in Perkins’ model and although much work has been devoted to
demonstrating speciation without any sort of geographic isolation, it has been
extremely difficult to find convincing cases in nature (Coyne and Orr 2004;
(continued)
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Box 6.1 (continued)
Coyne 2007; Bolnick and FitzPatrick 2007). Often, even the best candidates
have experienced an initial period of isolation—even a short one—just as in
the archipelago radiation model (Feder et al. 2003; Martin et al. 2015a).
The composition of the community across an archipelago can reveal which
of the above scenarios played a major role in the origin of endemic species. For
instance, the number of families represents the minimum number of colonizations from the mainland, whereas single representatives from mainland groups
provide unambiguous cases of allospeciation. The presence of sympatric
congeneric endemic species in an archipelago indicates the groups where
molecular-based studies are needed, as such species could be the result of
any of the speciation modes. There are several such instances in the Gulf of
Guinea oceanic islands that have not yet been investigated with molecular data
including among several groups of plants (Garcia and Shevock 2022; Stévart
et al. 2022), mollusks (Panisi et al. 2022), mushrooms (Desjardin and Perry
2022), arachnids (Crews and Esposito 2022), and insects Mendes and Bivarde-Sousa 2022; Nève et al. 2022). An important limitation of molecular
studies, however, is that they cannot account for the possibility that undetected
extinctions have removed the true sister species of extant species. In the
volcanic islands of the Gulf of Guinea, no suitable fossil ground has yet
been found and hence the extent to which extinctions may confound our
inferences of speciation mode is unknown.
Getting There: Modes of Active and Passive Dispersal
Although the location of the oceanic islands of the Gulf of Guinea is favorable to
colonization from the continent, it is still a considerable distance to travel for many
organisms. The task is made easier for active flyers, such as birds, bats, or large
insects. For organisms that disperse passively in the air—the aerial plankton—the
dominant wind currents determine the most likely sources of colonizers. In the Gulf
of Guinea, these are the southwestern monsoon winds, responsible for the high
precipitation that sustains the rainforests, and the northern dry harmattan winds
(Ceríaco et al. 2022c). It is the meeting of these two air masses that determines the
position of the meteorological equator. The southwestern winds are unlikely to have
dispersed colonizers from continental Africa but may have promoted inter-island
dispersal from the southwest to the northeast (i.e., Annobón to São Tomé to
Príncipe). Passive wind-dispersing organisms are therefore more likely to have
originated from West Africa, to the north of the archipelago, and this is indeed the
case for angiosperms (Exell 1973) and Simuliidae black-flies (Mustapha et al. 2006).
Dispersal via the northern harmattan winds is likely to have been more prominent
during glacial cycles, when they displaced the meteorological equator further south
(Lézine et al. 1994) and thus extending further into the Gulf. These hypotheses
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regarding both the direction, timing, and periodicity of colonization for winddispersed taxa can be tested with molecular phylogenetic analyses.
Ocean currents determine the most likely sources of aquatic organisms and of
terrestrial organisms that disperse in water, including some seed plants and marine
fishes that became secondarily adapted to the freshwater bodies of the islands (Costa
et al. 2022). These currents have also likely played a major role in facilitating the
arrival of many non-volant, non-swimming, and salt-intolerant animals via passive
dispersal on floating vegetation rafts (e.g., Ali and Fritz 2021). These include all
amphibians (Bell et al. 2022), several fossorial reptiles (Ceríaco et al. 2022b), and
the two species of endemic shrews (Rainho et al. 2022). Likewise, plants with low
dispersal ability also likely reached the islands via rafting, for instance, the unusual
plant Sciaphila ledermannii, a mycoheterotroph that obtains its nutrients by a
symbiotic relationship with fungi and lacks obvious structures for either wind or
animal dispersal of its seeds (Daniel 2010). Other species that likely reached the
islands in this way include species pairs with tight ecological associations unlikely to
be maintained by independent dispersal events, such as the hypothesized simultaneous colonization of São Tomé by the sheet-web tarantula Allothele and its
kleptoparasitic spider Isela (Charles Griswold, pers. comm.).
Several factors come together in the Gulf of Guinea to support the rafting
hypothesis (Measey et al. 2007; Ceríaco et al. 2022c). First, three large rivers
(from north to south: Niger, Ogooué, and Congo) drain into the Gulf of Guinea in
the vicinity of the islands. These rivers are among the largest in the world with
exceptional freshwater discharge during the rainy season. Second, tropical Africa
receives very high precipitation levels during the rainy season that can lead to
occasional downfalls of river margins, resulting in rafts of vegetation and soil—a
necessary requisite for different groups of animals and plants, such as fossorial
amphibians and reptiles that made it to the islands (Bell et al. 2022; Ceríaco et al.
2022b). During the rainy season, high freshwater discharge leads to a large outflow
of the rivers into the sea, creating extensive freshwater plumes that create a superficial low-salinity layer in the sea (Richardson and Walsh 1986; Jourdin et al. 2006),
and protect the rafts from the intrusion of saltwater. Finally, the dominant ocean
currents in the Gulf of Guinea direct the freshwater plumes of the Niger and Congo
rivers towards the islands. In summary, the ocean currents together with the top layer
of freshwater create “freshwater paths” that carry floating natural rafts from West
and Central African river drainages towards the islands (Measey et al. 2007).
The dispersal histories of island species can be inferred using molecular data to
build phylogenies and identify the most closely related species or populations on the
continent. For instance, a phylogeographic approach revealed that the Gray Parrot
Psittacus erithacus first reached Príncipe Island from West Africa (c. 1 Ma ago), and
that in contemporary times new colonizers arrived from Central African populations
(Melo and O'Ryan 2007). By contrast, phylogenetic studies of the endemic São
Tomé caecilians suggest they are the product of a single dispersal event (c. 1 Ma ago)
from East Africa (Loader et al. 2007). Likewise, the House Snakes Boaedon are the
product of a single dispersal event to the archipelago from Southern Africa (Ceríaco
et al. 2021). The rare instances of inter-island dispersal can be a bit more challenging
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to decipher from molecular data (e.g., Melo et al. 2011). Such studies will typically
require population-level genetic sampling to estimate patterns of genetic diversity for
each island (e.g., Bell et al. 2015b; Weinell et al. 2019) with the assumption that each
successive colonization event from the source population represents a bottleneck,
leading to sequential reductions in genetic diversity along the island chain (Clegg
et al. 2002). Thus far, such biogeographic studies have primarily been conducted for
many of the islands’ amphibians, reptiles, and birds with results supporting instances
of dispersal from West, Central, East, and Southern Africa, as well as some cases of
inter-island dispersal (Bell et al. 2022; Ceríaco et al. 2022b; Melo et al. 2022). As
more phylogenetic and population genetic studies become available from a greater
diversity of taxa, we will start to gain a better understanding of the dominant
continent-to-island and inter-island dispersal pathways and likely mechanisms.
The Temporal Setting
The oceanic islands of the Gulf of Guinea originated from the activity of the
Cameroon Volcanic Line, which began c. 30 my ago (Burke 2001). As such they
are a relatively old island system, with the age of Príncipe estimated at 31 Ma, São
Tomé at 15 Ma, and Annobón at 6 Ma (Ceríaco et al. 2022c). For comparison, the
ages of the islands of the Hawaiian archipelago range from 5 to 0.5 Ma (Carson and
Clague 1995) and the Galapagos from less than 0.5 to 3 Ma (Harpp and Geist 2018).
Thus, in theory, the islands of the Gulf of Guinea have had extensive evolutionary
time to accumulate species diversity and endemism. The tempo at which species
richness has accrued, however, may have been influenced by many global climatic
factors (e.g., changes in sea level and exposed coastline of the African continent), as
well as local geological factors (e.g., devastating volcanic eruptions). As the fossil
record in the region is poor, molecular clock approaches can be employed to estimate
divergence times between the island endemics and their closest mainland relatives.
In turn, these dated phylogenies can be used to infer the corresponding colonization
time frame for a given lineage (Fig. 6.1) and reconstruct the timeline of community
assembly.
The currently available divergence dating studies suggest that the old age of the
islands has not necessarily translated to an abundance of very old lineages. In plants,
although afromontane paleo-endemics are present, these co-exist with a large assemblage of neo-endemics (Figueiredo 1994). Likewise, for other groups, most molecular estimates of divergence times indicate that many endemics are much younger
than the ages of the islands. For example, from 22 divergence time estimates for
endemic birds, 18 occurred within the last 2 Ma, 3 within the last 3–5 Ma, and the
oldest dates to 8 Ma (Table 24.1 in Melo et al. 2022). The endemic fruit fly
Drosophila santomea (Llopart et al. 2002; Turissini and Matute 2017), caecilians
(Loader et al. 2007), and shrews (Nicolas et al. 2019) also represent recent colonization and speciation events within the last 2 Ma, while inferred colonization dates
for reed frogs (Bell et al. 2015a), the ridged frog Ptychadena newtoni (Zimkus et al.
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Fig. 6.1 The colonization date of an archipelago lies between the time of most ancient common
ancestor (MACA) and the time of most recent common ancestor (MRCA). Time of MACA assumes
that the appearance of the insular lineages was simultaneous with colonization. Time of MRCA
does not take into account post-colonization demographic effects on genetic diversity. Even if the
true MACA and/or MRCA went extinct (or were not sampled) they would be located within this
interval. Adapted from Vences (2005) and Hayward and Stone (2006)
2017), and skink Trachylepis thomensis (Weinell et al. 2019), date to the LateMiocene.
Although divergence estimates are not yet available for many groups on the
oceanic islands of the Gulf of Guinea, the emerging pattern supports high species
turnover. This turnover likely arises as a product of the small size of the islands,
moderate distances to the continental pool of new potential dispersers, and the
intense recent volcanism of the islands. Small island size is associated with high
extinction rates (MacArthur and Wilson 1967). Proximity to the mainland increases
colonization rates, in particular for more mobile organisms, such as birds, which is
expected to favor taxon cycle dynamics. According to the taxon cycle hypothesis,
successful colonizers tend to be generalists that will outcompete specialized
endemics, but these generalists then evolve into endemic specialists that will themselves be outcompeted when new generalists reach the island (Wilson 1961; Ricklefs
and Bermingham 1999, 2002). In the oceanic islands of the Gulf of Guinea, the
community assembly of avian blood parasites is concordant with the taxon cycle
hypothesis (Loiseau et al. 2017). This is particularly interesting as the
co-evolutionary arms race between pathogens and their hosts has been proposed as
a factor that could be driving taxon cycle patterns in the macro-fauna (Ricklefs and
Bermingham 1999, 2002; Ricklefs et al. 2016). It is unclear whether such a pattern is
present in other taxonomic groups in the Gulf of Guinea.
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Volcanism in the continental and oceanic sector of the Cameroon Volcanic Line
has been contemporaneous and more or less continuous since the Cretaceous (Fitton
1987; Lee et al. 1994; Burke 2001). Volcanic activity persisted until recently on the
islands (0.1 Ma: Lee et al. 1994; 0.036 Ma: Barfod and Fitton 2014—see also
Ceríaco et al. 2022c) and is still present for Mount Cameroon, and to a lesser extent,
Bioko. Only faint signatures of volcanic activity remain on São Tomé in the form of
hot springs (Henriques and Neto 2015), but the intensity of recent volcanic activity is
still clearly visible in the orography, which is marked by high mountains and steep
slopes, characteristic of young islands. For example, the peak of São Tomé, rising at
2024 m, was formed 1.5 Ma together with most of the central mountain massif of the
island (Caldeira et al. 2003). These major volcanic events have likely driven species
to extinction on multiple occasions, contributing to accelerating species turnover.
Volcanic eruptions could also contribute to diversification and speciation, however,
by dividing the ranges of previously panmictic populations with lava flows. The
distributions of the two endemic sister caecilian lineages—Schistometopum ephele
and S. thomense on São Tomé align with this hypothesis (Stoelting et al. 2014,
O’Connell et al. 2021), as do patterns of genetic variation in the skink Trachylepis
thomensis (Jesus et al. 2005).
The prevalence of species derived from recent speciation events attests to the Gulf
of Guinea islands being diversification centers rather than simple “museums” where
continental species found refuge from habitat changes associated with glacial cycles.
Yet, the presence of species whose arrivals date to earlier times of island formation,
and of Afromontane paleo-endemic plants in particular, supports the hypothesis that
the islands offered a stable climatic environment during glacial cycles (Plana et al.
2004). As more dated phylogenetic studies become available from a greater diversity
of taxa, we will start to gain a better understanding of the tempo of island colonization and in situ diversification.
Hybridization and Speciation in the Gulf of Guinea
The role of hybridization in evolution, and in speciation in particular, remains one of
the most fundamental questions in evolutionary biology (Abbott et al. 2013;
Seehausen et al. 2014; Taylor and Larson 2019). The consequences of hybridization
between two lineages range from the extinction of one lineage (via the fusion of the
two) to the origin of a new “hybrid” lineage. In between these extremes, hybridization can lead to different levels of genetic introgression across species boundaries,
with the potential of accelerating, rather than hindering, the evolutionary process
(Anderson and Stebbins 1954; Arnold and Emms 1998). In intermediate island
systems, such as the oceanic islands of the Gulf of Guinea, a mainland lineage
may colonize the islands more than once and at different points in time. Such cases
are likely to lead to hybridization between the diverging island and mainland
lineages. These rare and episodic hybridization events provide clear-cut models to
study the consequences of hybridization in lineage divergence and speciation. In the
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oceanic islands of the Gulf of Guinea, several examples of hybridization between
species have been detected. Interestingly, several of these cases were only detected
with molecular data, suggesting that several other cases are likely to be uncovered
with the increasing use of genetic data in the region. Here we highlight some of the
better studied examples.
The Drosophila santomea x D. yakuba Hybrid Zones The genus Drosophila,
with c. 1500 species, includes the most widely used model organism for the study of
genetics, D. melanogaster. Interestingly, up until the discovery and description of
the endemic species from São Tomé, D. santomea (Lachaise et al. 2000), stable
hybrid zones within the genus were unknown. The description of this hybrid zone in
Drosophila quickly led to the search, and discovery, of others such as on the island
of Bioko (Cooper et al. 2018) and the Seychelles (Matute and Ayroles 2014). On São
Tomé, the island endemic co-occurs with its sister species, the widespread
Sub-Saharan D. yakuba. The endemic species is mostly restricted to mist forest at
higher elevations, whereas the cosmopolitan species prefers more open habitats at
lower elevations. Although the two species diverged between c. 400,000 (Llopart
et al. 2002) and 1 million years ago (Turissini and Matute 2017), hybridization
occurs at a rate of about 1% where their ranges meet, at intermediate elevations
(Lachaise et al. 2000; Llopart et al. 2005a). This hybrid zone became an important
model for research on the genetic basis of phenotypic differences (Llopart et al.
2002); the evolution of reproductive barriers (Coyne et al. 2002; Moehring et al.
2006a, b; Turissini et al. 2015); the impacts of introgression on the genome,
including the replacement of the mitochondrial DNA of D. santomea by that of
D. yakuba (Llopart et al. 2005a; Turissini et al. 2015); and, more generally, on the
role of hybridization and introgression in speciation (Turissini and Matute 2017;
Matute et al. 2020). The hybrid zone is unusual in that a population of hybrid males
is restricted to the higher elevations of São Tomé, away from the ranges of both
parental species (Llopart et al. 2005b). The origins of this hybrid male population are
still unclear.
The Hyperolius thomensis x H. molleri Hybrid Zone Two endemic species of
reed frogs occur on São Tomé—H. thomensis mostly restricted to the native closedcanopy forests, and H. molleri associated with more open habitats, including human
modified ones (Bell et al. 2015b, 2022). Although closely related (c. 0.5–1.5 Ma;
Bell et al. 2015a), they are clearly phenotypically distinct species differing in size,
coloration, advertisement call, and reproductive biology (Drewes and Wilkinson
2004; Gilbert and Bell 2018; Bell and Irian 2019). In spite of this, hybridization
occurs where the two species meet at the interface of closed-canopy forest and more
open habitats, resulting in a mosaic hybrid zone (Bell et al. 2015b; Bell and Irian
2019). This hybrid zone is ripe for investigations of the genetic basis of phenotypic
differences, reproductive barriers, the scale and pattern of introgression across
species boundaries, and the impact of gene flow on genome architecture and
phenotypic evolution. Although the geographic and temporal extent of hybridization
between these species is incompletely understood, recent evidence suggests that
hybridization may be a direct result of human-driven habitat changes, and of
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deforestation in particular (Bell and Irian 2019). The hybrid zone of the two
Drosophila species from São Tomé also coincides with the transition from agricultural areas to native forest habitats, and therefore may also be a result of changes in
habitat structure (Lachaise et al. 2000).
Mitochondrial Introgression in Parrots and Pigeons Mitochondrial data used to
infer phylogenetic and phylogeographic relationships of most endemic bird species
in the archipelago (Melo 2007; Melo et al. 2022) uncovered several instances of
mitochondrial introgression (Box 21.1 in Melo et al. 2022): (1) the Gray Parrot
Psittacus erithacus, where a distinct Príncipe lineage hybridized with recent arrivals
from the mainland (Melo and O'Ryan 2007); (2) the Lemon Dove Columba larvata,
where, as with the parrot, a distinct island lineage was recently joined by a new wave
of mainland colonizers (Hugo Pereira and Martim Melo, unpublished data); (3) from
the Sao Tome Green-Pigeon Treron sanctithomae to the Príncipe subspecies of the
African Green-Pigeon Treron calvus virescens (Pereira 2013). These are all species
with strong flying abilities—making them typical oceanic island colonizers—and as
such, secondary contact and inter-island dispersal events are not surprising. Genomic
studies are required to better understand the extent of introgression derived from
interbreeding between the diverging lineages.
The Saga of the Canaries Crithagra concolor x C. rufobrunnea The islands of
Príncipe and São Tomé host two endemic canaries (Fringillidae: Crithagra). The
Principe Seedeater C. rufobrunnea is present on Príncipe, Boné de Jóquei Islet
(c. 2.5 km from Príncipe), and São Tomé. Gene flow between the three allopatric
populations is reduced and phenotypic differentiation has evolved, justifying their
current treatment as three distinct subspecies (Melo 2007). The Sao Tome Grosbeak
C. concolor is restricted to the primary forests of São Tomé, where it is the rarest or,
at least, the most difficult bird species to find. The São Tomé population of the
Principe Seedeater occurs across the entire island, from primary forest to urban
areas—whenever trees are present. The phenotype of the grosbeak has often misled
taxonomists, who episodically considered it to be a weaver (Ploceidae; cf. Melo et al.
2022). More recently, molecular evidence confirmed not only that it is a Crithagra
canary, but that it is sister to the Principe Seedeater (Melo et al. 2017). The surprising
twist to this story is that molecular data, from multiple loci (2 mitochondrial markers,
33 nuclear introns and exons, 34 microsatellites, and c. 10,000 single nucleotide
polymorphisms—SNPs) consistently indicated that the São Tomé population of the
seedeater is more closely related to the grosbeak than to its conspecific allopatric
populations on Príncipe and Boné de Jóquei Islet (Melo 2007; Stervander 2009,
2015). The paraphyly of the seedeater was concordant with the grosbeak and
seedeater having speciated in sympatry on São Tomé—a very unlikely scenario
for birds, with the only another potential case described in the Nesospiza buntings
(Thraupidae) from the Tristan da Cunha archipelago (Ryan et al. 2007). Clarification
of this pattern was only possible using a large-scale genomic approach (Stervander
2015; Stervander et al. 2022). Mapping of over 130,000 SNPs across the genome
revealed that the “sympatric speciation pattern” was the consequence of an extensive
degree of genetic introgression between the two species. For the subset of
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Fig. 6.2 Genomic patterns of differentiation and introgression between the Sao Tome Grosbeak
and the Principe Seedeater, exemplified by data from chromosome 14. Three classes of phylogenetic signatures are distributed across the genome: Chromosomal segments that are phylogenetically inconclusive are gray (“inconclusive”; 89.1% of all segments across the genome that were
assigned a local phylogeny); Segments representing a preserved phylogenetic signal (not
introgressed during secondary contact of the grosbeak and seedeater on São Tomé), where the
three seedeater populations are sister taxa and form a distinct lineage from the grosbeak, are blue
(“preserved” 4.6%); Segments representing introgression from the grosbeak to the São Tomé
population of Príncipe seedeater are red (“introgressed”; 6.3%). The latter suggest the sympatric
populations of the grosbeak and the seedeater on São Tomé are sister taxa, and divergent from the
other seedeater populations. Example topologies representative of each of the three genomic classes
are drawn in corresponding colors, with the three seedeater populations abbreviated as ST (São
Tomé; orange font; sympatric with the grosbeak), P (Príncipe; purple), and B (Boné de Jóquei;
green). Figure from Stervander et al. (2022)
phylogenetically informative SNPs, more SNPs supported the sympatric speciation
pattern (“introgressed markers”) than allopatric speciation (i.e., where the three
seedeater populations make a monophyletic group, sister to the grosbeak; “preserved
markers”; Fig. 6.2). Many of the SNPs supporting allopatric speciation were associated with coding regions, including those harboring genes underlying bill size and
shape, suggesting a strong role for natural selection against hybrids with intermediate bills (Stervander 2015; Stervander et al. 2022).
Evolution on Islands
The “Island Syndrome”
Island organisms often capture the imagination of scientists and non-scientists alike,
as “museums of curiosities.” They are lands of “dragons” (Komodo dragon Varanus
komodoensis) and of other fantastical creatures such as the Dodo Raphus cucullatus
(Hume 2012), a giant flightless pigeon encountered by Alice in her adventures in
wonderland (Carroll 1865). Naturalists noticed early on that organisms on islands
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across the world appear to have shared suites of unusual characteristics (Darwin
1859; Wallace 1880; Carlquist 1965; Grant 1998b; Whittaker 1998). These common
evolutionary paths have been described for many traits and grouped under the
“island syndrome” umbrella (Grant 1998b; Losos and Ricklefs 2009; Burns 2019;
Baeckens and Van Damme 2020). Such island syndrome traits include:
1. increased longevity and lower fecundity (e.g., Adler and Levins 1994; Covas
2012; Novosolov et al. 2013);
2. wider ecological niches (Grant 1965a, 1998b; Blondel 2000; Covas 2016; Scott
et al. 2003; Amorim et al. 2017);
3. small species becoming larger and large species becoming smaller (Grant 1965a;
Lomolino 2005; Clegg 2010; Lomolino et al. 2013; Novosolov et al. 2013;
Biddick et al. 2019; Benítez-López et al. 2021);
4. species becoming more sedentary, with the evolution of flightlessness in animals
(Diamond 1981; Wright et al. 2016; Leihy and Chown 2020) and the transition
away from wind-dispersal in plants (Cody and Overton 1996; Kavanagh and
Burns 2014);
5. animals becoming less territorial, allowing them to live in higher densities
(density compensation: MacArthur et al. 1972), which is also likely associated
with the evolution of increased “tameness” on islands;
6. birds losing colorful ornaments (Grant 1965b; Doutrelant et al. 2016).
Most of the hypotheses proposed to explain the convergent evolution of a wide
suite of traits on oceanic islands are linked to the defining abiotic factors of oceanic
islands: isolation, small size, and a stable and mild climate associated with the buffer
influence of the sea (Grant 1998a, b; Whittaker 1998; Blondel 2000; Covas 2016;
Baeckens and Van Damme 2020). Isolation and small size underlie the defining
biotic feature of oceanic islands: lower species richness relative to mainland areas of
equivalent size (MacArthur and Wilson 1967). This depauperate biota translates to
lower levels of inter-specific competition which contributes to ecological release
(Herrmann et al. 2020). Lower species richness also translates to fewer predators and
parasites, allowing species to evolve in ways that are generally not possible on the
mainland—including growing towards their metabolic optimum size or losing
dispersal abilities.
The Gulf of Guinea islands present several potential cases of the island syndrome
across different groups, albeit studies on this subject have focused primarily on birds
(Box 6.2). Gigantism is the most striking, with examples found in plants, amphibians, reptiles, and birds, and dwarfism in the only endemic bird descending from a
large continental species, the Sao Tome Ibis Bostrychia bocagei. Many of the island
syndromes can only be identified once the island endemics are placed in the
evolutionary context of the continental lineage they arose from. For instance, the
endemic giant lobelia, Lobelia barnsii, found near the peak of São Tomé, is most
likely part of the monophyletic clade that groups all giant Lobelia of the world
(Antonelli 2008, 2009: L. barnsii not included in the analyses) and, if so, the large
size of the island endemic will reflect shared history rather than convergent evolution
towards island gigantism. By contrast, the Principe Giant Tree Frog Leptopelis
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palmatus does not appear to be closely related to the largest continental species in the
genus and may therefore represent a true case of island gigantism (Jaynes et al.
2021). The house snakes, Boaedon bedriagae from São Tomé and B. mendesi from
Príncipe, may also be island giants as they are considerably larger than their
mainland relatives in the B. capensis complex in southern Africa (Ceríaco et al.
2021). Within an archipelago, selective pressures of the island condition may be
stronger in smaller islands. This likely applies to the gigantism and tameness of the
Tinhosa Grande islet population of Trachylepis adamastor. Recently described as a
unique species due to its large size and dark coloration (Ceríaco 2015), molecular
data indicate that the populations on Tinhosas and Príncipe are not genetically
differentiated (Ceríaco et al. 2016, 2020). Such rapid phenotypic changes have
been observed in just a few generations in other island lizards (e.g., Amorim et al.
2017). Likewise, out of the three populations of the endemic Principe Seedeater (São
Tomé, Príncipe, Boné de Jóquei Islet), it is the birds from the small 40 ha islet that
have evolved by far the largest body mass and bill and have lost more of their flying
abilities (sedentariness) and anti-predator behavior (tameness) (Box 6.3).
Box 6.2 The Island Syndrome in the Birds of the Gulf of Guinea Oceanic
Islands
Wider niches: Bird song is a trait directly linked to fitness for its role in mate
attraction and territory defense (Collins 2004). Hence, song is a signal under
strong selection for efficient transmission. In species-rich communities, competition for acoustic space is expected to be high—as overlap of different
songs masks the signals and impairs the efficacy of their transmission
(Wollerman and Wiley 2002). Thus, mainland species tend to partition the
acoustic space into narrow temporal and spatial (frequency bandwidth) windows to minimize interference (Planqué and Slabbekoorn 2008; Weir et al.
2012). By contrast, the acoustic space of species-poor islands is predicted to be
less saturated. Comparisons of bird communities of São Tomé and Cameroon
revealed that the species-poor island communities live in an acoustic environment with less acoustic interference (both from birds and insects) than those on
the mainland, that island species spend more time vocalizing alone, and that
acoustic overlap is lower (Robert et al. 2019, 2021). This lower competition
for acoustic space translates into the songs of island species occupying a
broader frequency bandwidth than the songs of their mainland counterparts
(Robert et al. 2021)—a pattern that is consistent with the character release
hypothesis predicted from the lower levels of inter-specific competition (Grant
1972; Herrmann et al. 2020).
Island rule: The trends of body size evolution in the endemic birds of the
Gulf of Guinea fit the predictions of the island rule very closely. Most small
and medium birds increased in size, with three “island giants” including the
world’s largest sunbird (Sao Tome Sunbird Dreptes thomensis), weaver (Giant
Weaver Ploceus grandis), and canary (Sao Tome Grosbeak Crithagra
(continued)
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Box 6.2 (continued)
rufobrunnea). The few exceptions where small birds decreased slightly in size
occur in those species that co-exist with a congeneric species and, therefore,
represent the few cases in which inter-specific competition is present and
character displacement may be at play (see main text and Fig. 6.3). The
exceptions to this rule appear to be limited to the Sao Tome ParadiseFlycatcher Terpsiphone atrochalybeia and the Sao Tome Short-tail Motacilla
bocagii, which are smaller than their mainland relatives but do not have any
close relatives on the island. By contrast, the only endemic derived from a
group of large birds, the Sao Tome Ibis Bostrychia bocagei, is the smallest
representative of its group and one of the smallest ibises in the world.
Dispersal loss: Darwin hypothesized that sedentariness on islands evolves
because dispersing individuals are unlikely to return (Darwin 1859). Under
this hypothesis, the smaller the island, the stronger the selection favoring
individuals that do not disperse. One study investigated the evolution of flying
potential among populations of the endemic Principe Seedeater Crithagra
rufobrunnea in the early stages of divergence. This species occurs in three
allopatric populations: Príncipe, Boné de Jóquei Islet (c. 2.5 km off Príncipe),
and São Tomé. Gene flow between the three populations is very restricted and
phenotypic differentiation is significant (Melo 2007). The population on the
smallest island (the 40 ha Boné de Jóquei Islet) had the lowest flying potential,
as inferred from its small wing length: body mass ratio (Melo 2007; Box 6.3).
Color loss: The loss of coloration, color patches, and even sexual dimorphism in island birds has long attracted the attention of ornithologists (Grant
1965b). This pattern is consistent across distinct taxonomic groups and island
systems (Doutrelant et al. 2016). A trend for increased melanism has also been
suggested for island birds (Uy and Vargas-Castro 2015)—and for reptiles
(Novosolov et al. 2013)—but has not yet been as extensively studied. As
with the island rule, color loss is on full display in the endemic birds of the
oceanic islands of the Gulf of Guinea. Lipochromes (yellow and green pigments) present in mainland relatives have mostly been lost in the island
endemics: Sao Tome Oriole Oriolus crassirostris, the five white-eye species
(Zosterops sp.; Melo et al. 2011), the Sao Tome Sunbird, and the Principe
Sunbird Anabathmis hartlaubi (Newton’s Sunbird A. newtonii being the
exception). Additionally, the male of the Sao Tome Paradise-Flycatcher is
entirely black, and melanin predominates in the plumage of the Principe
Seedeater and the endemic São Tomé subspecies of the Western Barn Owl
Tyto alba thomensis.
Several hypotheses have been put forward to explain the loss of color in
island birds including that (1) species-poor communities may relax the need
for elaborate signals used in species recognition (Martin et al. 2010, 2015a, b);
(2) long-lived species have higher levels of parental care, which is associated
with lower investment in sexual signals (Covas 2012); (3) sexual selection is
(continued)
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M. Melo et al.
Box 6.2 (continued)
relaxed as a consequence of both the reduced genetic diversity (Frankham
1997) and higher relatedness within island populations (Griffith 2000). Most
work on the Gulf of Guinea islands has focused on the hypothesis that colors in
birds are honest signals of immune condition as they often depend on the
acquisition of carotenoids from the diet, which are also essential co-adjuvants
of the immune system (Hamilton and Zuk 1982). From a pathogen perspective, islands are thought to be more benign environments because the decrease
in species richness is expected to also extend to parasites. If this expectation is
correct, the inter-individual variation in health condition on islands should be
very narrow, and hence color would no longer hold information regarding
individual condition.
A survey of avian blood parasites indicated that parasite diversity and
prevalence is lower on Príncipe and São Tomé relative to the adjacent mainland (Loiseau et al. 2017). Proxies of acquired immune function were lower on
islands (Lobato et al. 2017), and genes from the Major Histocompatibility
Complex (also involved in acquired immunity) were found to be under relaxed
selection (Barthe et al. 2022), consistent with low exposure to pathogens.
Other important genetic components of the immune system, however, were
impacted by small population sizes and drift rather than by relaxed selection
(Barthe et al. 2022). Demonstrating a direct link between the reduction in
parasites and color loss in the avian community is more challenging. Although
many of the island endemics have lost coloration and many of the more recent
arrivals have not, the birds of Príncipe and São Tomé do not provide enough
data points along the gradient of time since colonization to conclusively
support the Hamilton and Zuk hypothesis.
Box 6.3 Evolution on an Island of an Island
Boné de Jóquei Islet (1) is only about 600 x 900 m and lies c. 2.5 km off the
southeast coast of Príncipe (2), from which it has been separated since the last
glaciation, c. 10,000 years ago. It holds an endemic subspecies of the Principe
Seedeater Crithagra rufobrunnea fradei (3), which occurs at very high densities (4). Two other subspecies occur on Príncipe and on São Tomé Islands,
respectively. The birds from Boné have the smallest wing relatively to their
mass, indicating the loss of dispersal ability. They have evolved a high degree
of tameness, reflecting evolution in a predator-free environment. They have
stouter bills, which have likely evolved due to the reliance of their diet on the
resources provided by the oil palm Elaeis guineensis, which constitutes the
dominant vegetation. They feed both on the pollen of the male inflorescences
(continued)
6
Biogeography and Evolution in the Oceanic Islands of the Gulf of Guinea
159
Box 6.3 (continued)
(5) and on the fruit (6, 7). The oil palms of Boné produce giant fruits, which
appear to have no parallel worldwide—and are not found on neighboring
Príncipe, where both species also co-occur. The large fruits may have
co-evolved as a defense against the strong predation pressure exerted by the
seedeater, or as an adaptation against dispersal. (6) Large fruits from Boné oil
palms in comparison with typical fruits; 15 cm ruler shown. Photo credits:
Martim Melo.
Inter-Specific Competition Accelerates Phenotypic Evolution
Low levels of inter-specific competition characterize species-poor island assemblages, resulting in high levels of intra-specific competition. Both factors likely
contribute to the evolution of many traits associated with the island syndrome.
Research on bird speciation in the oceanic islands of the Gulf of Guinea (Melo
160
M. Melo et al.
2007; Melo et al. 2022), however, reveals an important role for rare cases of interspecific competition that occur when closely related lineages meet on the same island
(see also: Grant 1965c)—an event that may be not so infrequent in intermediate
island systems. Molecular phylogenies have shown that in most cases the most
phenotypically divergent species are those that (1) evolved in sympatry with a
close relative (both evolutionarily and ecologically) and (2) represent the most recent
speciation events, instead of deriving from the oldest colonization events as previously assumed (Melo et al. 2022). For example, the two most phenotypically
“aberrant” white-eyes, the Principe Speirops Zosterops leucophaeus and the São
Tomé Speirops Z. lugubris, are sister species derived from the most recent speciation
events in the Gulf of Guinea white-eye radiation (Box 21.2 in Melo et al. 2022).
Furthermore, in this radiation, when two species meet it is the newcomer that
changes the most (Melo et al. 2011), in a process of asymmetrical character
displacement that had been predicted by theory (Doebeli and Dieckmann 2000),
and confirmed in the radiation of Darwin’s finches (Petren et al. 2005).
The evolution of true giants among the Gulf of Guinea island birds seems to have
resulted from the sequential effects of character release (Herrmann et al. 2020) and
character displacement (Brown and Wilson 1956; Grant 1972). The three giant birds
(weaver, sunbird, canary) all evolved in sympatry with a closely related lineage (the
sister lineage in the case of the canary). This suggests the following history for the
evolution of gigantism in the Gulf of Guinea birds, as previously suggested by
Amadon (1953): (1) a colonizer arrives to an island; (2) with no direct competitors it
evolves towards a generalist diet (character release), which in birds is associated with
an increase in bill size and, correspondingly, body size (Grant 1965a; Blondel 2000);
(3) a related lineage colonizes the island and inter-specific competition ensues;
(4) for co-existence to be possible, selection drives a reduction in competition
through character displacement, (5) the larger species evolves to become even larger.
Morphometrics of the five-species radiation of the white-eyes of the oceanic islands
of the Gulf of Guinea is strongly suggestive of character displacement as a driver of
phenotypic differentiation, although in this case the larger species evolved from the
secondary arrivals (Fig. 6.3).
Collectively, these studies point to the importance of inter-specific competition in
driving and accelerating phenotypic divergence in island birds, and even in the
speciation process.
Concluding Remarks
The Gulf of Guinea oceanic islands are an exciting example of an intermediate island
system, such that they are close enough to the continent to receive a diverse array of
mainland dispersers but far enough away for these to diverge once they arrive to the
islands. Thus, the archipelago holds great potential for testing classic hypotheses of
island biogeography by providing a wide array of independent evolutionary replicates, something that is missing from more remote archipelagos dominated by few
6
Biogeography and Evolution in the Oceanic Islands of the Gulf of Guinea
161
Fig. 6.3 Evidence for character displacement? Morphometrics of the white-eyes (Zosteropidae) of
the Gulf of Guinea, including the five-species radiation of the oceanic islands and the three species
radiation of Bioko and Mount Cameroon. White-eyes generally occur as single allopatric species,
but in the Gulf of Guinea there are four instances of co-occurrence of two species. On Annobón
there is only one species, which has evolved a larger size than its mainland counterpart (broken line)
in accordance with the island rule. In all other cases, where two species meet in sympatry, the
secondary arrival (red) increased significantly in size, while the first colonizers (green) did not
change much or decreased in size relative to their closest mainland relatives (depicted, approximately, by the broken line). In addition, the secondary arrivals evolved strikingly different colors
from those of the typical white-eye template (Box 21.2 in Melo et al. 2022). These patterns of
phenotypic divergence in this group support the process of asymmetric character displacement. The
large phenotypic differences of the secondary arrivals led them to be originally placed in a separate
genus, Speirops
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M. Melo et al.
lineages, and for investigating the role of gene flow in speciation and diversification.
Likewise, the archipelago presents the opportunity to disentangle mechanisms of
community assembly in a setting that is intermediate between the complex communities of continents, with high phylogenetic diversity, and the simple communities of
more isolated archipelagos, in which most of the diversity is derived from a few
extensive radiations. Finally, the archipelago’s endemics exhibit many of the
unusual phenotypes that have long captured the attention of scientists and
non-scientists, alike. As taxonomic and systematic research advances for the archipelago’s lesser known groups, hypothesis-driven studies investigating speciation
and phenotypic evolution will be possible in a more representative subset of the
remarkable diversity of the Gulf of Guinea oceanic islands.
Acknowledgments MM was supported via the European Union’s Horizon 2020 research and
innovation programme under grant agreement 854248. Fundação para a Ciência e a Tecnologia
(FCT, Portugal) provided structural funding to CIBIO (UIDB/50027/2021). We thank the editor
Ricardo F. de Lima for his helpful comments and suggestions.
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Chapter 7
Species Ecology in the Gulf of Guinea
Oceanic Islands: Distribution, Habitat
Preferences, Assemblages, and Interactions
Filipa C. Soares, Joana M. Hancock, Jorge M. Palmeirim,
Hugulay Albuquerque Maia, Tariq Stévart, and Ricardo F. de Lima
Abstract The oceanic islands of the Gulf of Guinea (Príncipe, São Tomé, and
Annobón) are an exceptional centre of endemism for flora and fauna. Remarkable
progress has been made in biological research during the last few decades: from
species being described and reported for the first time, to general patterns of specieshabitat associations found across terrestrial, coastal, and marine taxa. Despite this
increase in knowledge, key aspects of Gulf of Guinea species ecology remain poorly
F. C. Soares (*) · J. M. Palmeirim
Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências,
Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon,
Portugal
J. M. Hancock
Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências,
Universidade de Lisboa, Lisbon, Portugal
MARE, Marine and Environmental Sciences Centre, ISPA, Instituto Universitário de Ciências
Psicológicas, Sociais e da Vida, Lisbon, Portugal
H. A. Maia
Departamento de Ciências Naturais, da Vida e do Ambiente, Faculdade de Ciências e
Tecnologias, Universidade de São Tomé e Príncipe, São Tomé, Sao Tome and Principe
T. Stévart
Africa and Madagascar Department, Missouri Botanical Garden, St. Louis, MO, USA
Herbarium et Bibliothèque de Botanique Africaine, Université Libre de Bruxelles, Brussels,
Belgium
Meise Botanic Garden, Meise, Belgium
R. F. de Lima
Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências,
Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon,
Portugal
Gulf of Guinea Biodiversity Centre, São Tomé, Sao Tome and Principe
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_7
171
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F. C. Soares et al.
understood. This chapter reviews existing knowledge on the biodiversity of the
islands, focusing on species distributions, population abundance estimates, traits,
habitat associations and interactions. To promote these islands as ecological models,
and to ensure the future of their endemic-rich biodiversity, it is essential to overcome
current knowledge gaps and reduce existing taxonomic, spatial, and temporal biases
in the information available. Therefore, future studies should favour systematic
island-wide surveys and prioritize understudied areas and taxonomic groups. Moreover, long-term monitoring studies are urgently needed to assess biodiversity trends
and to advise conservation actions. The future of ecological research and conservation of the unique biodiversity of these islands must increasingly rely on the
development of local biodiversity-focused scientific expertise, through outreach,
capacity building, and advanced training, paired with international collaborations
and the development of local organizations.
Keywords Annobón · Conservation · Exotic species · Príncipe · São Tomé ·
Seasonality
Introduction
The oceanic islands of the Gulf of Guinea (Príncipe, São Tomé, and Annobón) have
long been recognized for the high levels of endemism of their flora and fauna (Jones
1994). This in itself makes them an important model of ecological research, but
studying ecology in these unique islands may also provide invaluable insights into
evolutionary and ecological processes, since islands can be used as natural experiments to extrapolate to wider scales (Whittaker et al. 2017).
The description of the biodiversity in the archipelago began in the late eighteenth
century and was intensified during the late nineteenth and twentieth centuries
(Ceríaco et al. 2022b). Since then, the islands have captured the imagination and
efforts of biologists, prompting scientific studies across multiple disciplines, many of
which aim to clarify different aspects of ecology (e.g., Lima 2016), such as species
distributions and habitat associations. Up to the 1990s, virtually all zoological
publications focused on taxonomy (Gascoigne 1993), and this is still mostly the
case for plants (Stévart et al. 2022) and most invertebrates. Despite an increase in
ecological research over the last few decades, key aspects of the ecology of species
occurring in the Gulf of Guinea islands remain poorly documented, such as the
influence community diversity and composition has on ecosystem processes. Progress is often halted by major knowledge gaps in areas fundamental to ecology, such
as taxonomy. This has been the case for most invertebrates, as unresolved taxonomy
halts progress in other areas of research. Take the example of terrestrial molluscs, in
which an updated taxonomy opened the doors for several ecological studies (Panisi
et al. 2022).
Here, we review existing information on the ecology of species from the oceanic
islands of the Gulf of Guinea. Specifically, we address current knowledge on species
distributions, population abundance, traits, habitat associations and interactions. We
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Species Ecology in the Gulf of Guinea Oceanic Islands: Distribution,. . .
173
also provide key references for each island and taxonomic group and identify current
knowledge gaps to direct future research.
Distribution
Information on the distributions of species on the oceanic islands of the Gulf of
Guinea has been an important feature of initial studies. Some are even associated
with the first descriptions of the islands themselves: a report of São Tomé in 1506,
made by the Portuguese navigator Gonçalo Pires and written by Valentim
Fernandes, describes an abundance of kites and the occurrence of a crocodilian
that has since been extirpated from the island (Monod et al. 1951). However, much
of the data on species distributions available today is still limited to the brief reports
included in species descriptions (e.g. Ceríaco et al. 2015), species catalogues
(e.g. Stévart and de Oliveira 2000; Csuzdi 2005; Sérgio and Garcia 2011; Mendes
and Bivar-de-Sousa 2012), or studies focusing on various aspects of their biology
(e.g. Drewes and Stoelting 2004). These are usually based on opportunistic observations, rather than on systematic surveys of the islands, and often only mention the
islands where the species occur. When such studies provide details on the distribution of a given species, they tend to be biased towards well preserved accessible sites
(Atkinson et al. 1991, Stévart et al. 2022).
Few studies have compiled geographically explicit information on species locations. Some exceptions include pteridophytes (Figueiredo 2002), endemic plants
(Joffroy 2000; Stévart et al. 2022), land snails (Holyoak et al. 2020), and birds (Jones
and Tye 2006). In some cases, information and even maps are shown, but details on
how these were obtained are missing, as is the case for amphibians and reptiles
(Pollo 2017) and threatened endemic birds (IUCN 2020a).
Even fewer species assemblages have been systematically surveyed across any of
the islands. Some exceptions include plants (Fundação Príncipe 2019; Stévart et al.
2022), terrestrial snails (Tavares 2020), benthic reefs and fishes (Maia et al. 2018b),
sea turtles (Ribeiro 2018; Hancock 2019), birds (Fundação Príncipe 2019; Soares
et al. 2020), and bats (Rainho et al. 2010). Bird surveys informed some of the first
island-wide assessments of the distribution of community traits, such as species
richness, composition, and structure (e.g. Lima et al. 2013; Soares 2017; Fig. 7.1).
Documenting plant species assemblages to classify vegetation is ongoing (Dauby
et al. 2022), although the main gradients have been described (Monod 1960; Stévart
1998; Ogonovszky 2003).
The scarcity of historical records hampers the detection and quantification of
temporal changes in the distribution of species on the oceanic islands of the Gulf of
Guinea. However, sometimes even sporadic records allow assessing trends, such as
the retraction of native species and the expansion of introduced species. For instance,
localities linked to herbarium samples have provided convincing evidence for the
disappearance of many plant species from large portions of the north of São Tomé
and Príncipe, such as Aerangis flexuosa (Ridl.) Schltr, 1887. Interviews in rural and
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Fig. 7.1 Maps showing the distribution of (a) non-native bird species richness, (b) proportion of
native bird species (Soares et al. 2020), and (c) compositional dissimilarity (Soares 2017). There
was a clear opposing pattern in the distribution of non-native species richness and proportion of
native species: non-native bird species thrive particularly well in land use types most influenced by
humans (a), whereas native bird species dominate the best-preserved forests (b). Species composition largely coincides with the distinct land use types (c)
coastal communities suggest distribution areas for populations of giant land snails
(Panisi 2017) and fishes (Maia et al. 2018a) have shifted. Historical distribution data
reveal strong declines in the ranges of the endemic Obô Giant Land Snail
Archachatina bicarinata (Bruguière, 1792) (Dallimer and Melo 2010), of the
endemic São Tomé Shrew Crocidura thomensis (Bocage, 1887) (Lima et al.
2016), and of the number of beaches where sea turtles nest on São Tomé (Graff
1996; Ribeiro 2018). The number of recorded extinctions and extirpations is very
small, with the only documented cases being an unknown species of crocodile on
São Tomé (Ceríaco et al. 2018), an endemic subspecies of Olive Ibis on Príncipe
(Lima and Melo 2021), and two orchid species (IUCN 2020). However, as for most
other oceanic islands, vegetation clearance and the introduction of species are likely
to have caused extinctions and extirpations before taxonomic studies started, and
those may remain unknown, especially considering the poor fossil or subfossil
record of the islands.
Population Estimates
To date, there has not been an attempt to estimate plant population sizes. The first
attempts to characterize plant species abundance on Príncipe provided valuable
information on population dynamics of threatened species (Benitez et al. 2018).
This study also revealed a higher abundance of species than previously thought, with
high levels of regeneration for Grossera elongata Hutch, 1944, Santiria balsamifera
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Species Ecology in the Gulf of Guinea Oceanic Islands: Distribution,. . .
175
Oliv., 1886, and Mesogyne henriquesii Engl., 1894, and a lack of regeneration for
Strephonema sp. nov. and Carapa gogo A. Chev. ex Kenfack, 2011.
The scarcity of quantitative surveys has resulted in very few reliable population
size estimates for animal species. These include estimates made for birds (Dallimer
and King 2007; Dallimer et al. 2009, 2010, 2012; Fundação Príncipe 2019), particularly for species of conservation concern, such as the Critically Endangered Dwarf
Olive Ibis Bostrychia bocagei (Chapin, 1923) (Azevedo 2015), all pigeon species on
São Tomé (Carvalho 2014), the Endangered Grey Parrot Psittacus sp. on Príncipe
(Valle 2015), and the undescribed Príncipe Scops-Owl Otus sp. (Freitas 2019).
Recent studies have also attempted to estimate population sizes for the Hawksbill
Turtle Eretmochelys imbricata (Linnaeus, 1766) (Hancock 2019) and the Obô Giant
Land Snail (Panisi 2017; Fundação Príncipe 2019), both on Príncipe and on São
Tomé. On land, the difficult terrain and dense vegetation have greatly hampered the
use of methods to account for detectability, such as distance sampling (but see:
Dallimer and King 2007). In marine ecosystems abundances are even harder to
sample, partly because many of the important species in these environments are
migratory and have complex life cycles.
The very few long-term population studies that have been conducted include
attempts to determine population trends of reef fishes, sea turtles, seabirds, and the
Grey Parrot on Príncipe. The study of reef fish on São Tomé revealed worrisome
declines (Maia et al. 2018b). Underwater visual census and photo-quadrats across six
sites around São Tomé allowed researchers to explore the relative importance of
exposure, depth, and topographic complexity as drivers of fish and benthic reef
communities. Species richness, abundance, and biomass of reef fish were higher in
deeper sites, which suffer less influence from human activities and are under the
direct influence of a constant thermocline resulting from the intrusion of cold waters
from the Benguela current.
Breeding female sea turtles have been monitored on Príncipe and São Tomé since
the early 1990s (Ribeiro 2018; Hancock 2019). However, incomplete temporal and
spatial coverage has led to high levels of uncertainty and hindered the quantification
of critical parameters to estimate abundances. Recent advances in population modelling are overcoming this problem (Hancock et al. 2019), and standardized surveys
carried out on both islands since 2012 will allow even more accurate estimates in the
future. Techniques such as genetic analyses have also been used to estimate operational sex-ratios and assess population changes over time, such as reductions in
effective population sizes in the Olive Ridley Turtle Lepidochelys olivacea
(Eschscholtz, 1829), and migration rates in the Green Turtle Chelonia mydas
(Linnaeus, 1758) (Hancock et al. 2019).
Local seabird colonies are the most important in the tropical Eastern Atlantic
(BirdLife International 2020), primarily due to the large breeding colonies on the
Tinhosas islets (Monteiro et al. 1997; Valle et al. 2016; Bollen et al. 2018; Lima and
Martins 2020). These small islets (<25 ha) host around 140,000 breeding pairs of
Sooty Tern Onychoprion fuscatus (Linnaeus, 1766), 10,000 pairs of Brown Noddy
Anous stolidus (Linnaeus, 1758), and important breeding populations of Black
Noddy Anous minutus Boie, 1844, and Brown Booby Sula leucogaster (Boddaert,
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1783). Large population decreases have been reported for these colonies, but it is not
yet clear whether these represent real declines or natural variations between years.
Breeding and non-breeding seabird population sizes were first assessed in 1997, for
most islets and small islands around Príncipe and São Tomé (Monteiro et al. 1997).
More recently, the Tinhosas have been monitored quarterly to refine population
estimates and trends, and to gain a better understanding of the breeding seasonality
of these species (Valle et al. 2016; Bollen et al. 2018; Lima and Martins 2020).
Finally, the population of Grey Parrot on Príncipe has so far been the only one
targeted by a population viability analysis (Valle 2015). Counts suggest that the
species has recovered since the 2005 trade ban, now numbering around 8000
individuals, and that adult survivorship is critical to ensure population persistence,
since the species can sustain relatively high levels of chick harvesting.
Species Traits
From early on, researchers showed an interest in describing the temporal trends in
the evolution and selection of species traits (Hortal et al. 2015). Many initial
descriptions of biodiversity provided the first data on species traits that are vital
for ecological studies. Biological collections, in particular, play a fundamental role
in enriching trait databases, and can even lead to unexpected discoveries. In the
oceanic islands of the Gulf of Guinea, morphological analyses of more than 2500
plant specimens collected in 2019 and 2020 have yielded many new species, while
rediscovering rare species and finding new records for the islands (Stévart et al.
2022). Despite strong research effort in the 2000s (Figueiredo et al. 2011), ongoing
studies on orchids are still leading to the description of new species, especially for
the genus Tridactyle. Moreover, museum specimens allow the quantification of traits
and trait variability, which are key to understanding the ecological function of
species (e.g., Heleno et al. 2021). These collections are particularly relevant for
species that might be harder to find and offer a historical reference that allows an
assessment of temporal changes in traits, an aspect that remains poorly explored in
these and other islands.
Species traits can be measured not only on museum specimens but also in the
field, on living specimens that are not collected. This has begun to be carried out
extensively in plants, but the amount of information available varies greatly between
islands and specific groups (Exell 1944; Figueiredo et al. 2011; Sérgio and Garcia
2011; Klopper and Figueiredo 2013; Velayos et al. 2014), and, overall, information
about plant traits remains scarce. This is not surprising considering that much of the
plant taxonomy remains unresolved, and many species are still being reported and
described as new to the islands (Benitez et al. 2018; Stévart et al. 2022). Ongoing
work focused on threatened plant species has been collecting important information
on species traits (Stévart et al. 2019).
A new checklist of land snails of São Tomé and Príncipe provided some information on these species’ traits (Holyoak et al. 2020). Despite limitations, both on the
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Species Ecology in the Gulf of Guinea Oceanic Islands: Distribution,. . .
177
types of the traits characterized and on the number of species that have been assessed
(Tavares 2020), this remains one of the few studies providing species traits for
invertebrate taxa.
Sea turtle and bird traits have been studied much more extensively on the islands.
The long-term monitoring of sea turtles in Príncipe and São Tomé since the 1990s
collected data on female size that captured both spatial and temporal variation
(Ribeiro 2018; Hancock 2019). Bird banding activities on the islands, although
sporadic, have allowed collecting trait data, mostly on activity, morphometric
measurements, and coloration, which have improved our understanding of sexual
dimorphism, spatial trait variability, and daily and annual life cycles (King and
Dallimer 2003; Madeira 2018).
High endemism rates and island syndromes hinder the use of the increasingly
available global trait databases to assess species traits for island species, which have
to be gathered locally (e.g., Covas 2016). In addition, behavioural, physiological,
and life-history traits are often less easily recorded than morphological traits and
remain an important knowledge gap (Hortal et al. 2015). Finally, to interpret current
ecosystems under the lens of long-term ecology it is also vital to understand which
species are native (Nogué et al. 2017).
Habitat Associations
Until recently, local information on species-habitat associations was very scarce
(e.g., Exell 1944; de Naurois 1994), but the situation has greatly improved since the
1990s. Some of the first studies from this period reported associations between
species occurrence and local environmental variables, producing brief descriptions
of habitat preferences (e.g., Atkinson et al. 1991; Joffroy 2000; Jones and Tye 2006).
This was followed by more detailed and accurate descriptions for the best-studied
groups, such as mammals (e.g., Dutton and Haft 1996) and birds (e.g., Dallimer and
King 2007).
In recent years, a few studies have used geographically explicit information on
environmental variables to model the distribution of terrestrial snails and birds on
Príncipe (Fundação Príncipe 2019; Rebelo 2020) and on São Tomé (Lima et al.
2017; Panisi 2017; Soares 2017). Some of these studies have also assessed how local
variables, often related to the vegetation, affect the distribution of species and
species assemblages at smaller scales. Most of these have focused on vertebrates,
such as amphibians (e.g., Strauß et al. 2018) and birds (e.g., Lima et al. 2013;
Carvalho et al. 2015; Margarido 2015; Lewis et al. 2018; Alves 2019; Freitas 2019),
but also on land snails (Panisi 2017; Rebelo 2020; Tavares 2020).
Native species, and especially endemic and threatened species, tend to be strongly
associated with ecosystems that have been less disturbed by human activities. This
pattern is common to terrestrial, coastal, and marine realms, and to distinct groups,
including birds (Lima et al. 2013; Soares et al. 2020), tree frogs (Strauß et al. 2018),
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F. C. Soares et al.
sea turtles (Hancock 2019), land snails (Panisi 2017; Tavares 2020), and even
earthworms (Csuzdi 2005) in the Gulf of Guinea.
In terrestrial groups, species distributions are strongly determined by land use,
which in turn has been shaped mostly by topography (Jones et al. 1991; Norder et al.
2020). The best-preserved native forests, on which most native species depend, tend
to persist in rainy, remote, and rugged areas (e.g., Soares et al. 2020). However,
some native species, and even a few endemics, managed to adapt to novel ecosystems created by humans, including some birds (Dallimer et al. 2009; Lima et al.
2013; Carvalho 2014; Alves 2019), mammals (Rainho et al. 2010), frogs (Strauß
et al. 2018), and land snails (Tavares 2020). Among novel ecosystems, those that
maintain dense tree cover and mimic the structure of the native vegetation seem to be
preferred by native species (Jones and Tye 2006; Lima et al. 2014). These include
secondary forests, which result from vegetation regrowth after logging and agricultural abandonment, and agroforest systems, such as coffee and cocoa shade plantations, which integrate trees and agricultural crops (Jones et al. 1991; Oyono et al.
2014; Dauby et al. 2022). Unfortunately, it is also clear that many taxa do not cope
well in these novel ecosystems (e.g., Fundação Príncipe 2019; Soares et al. 2020). In
contrast with native terrestrial species, introduced species tend to be associated with
more intensive land uses, many of which are located in the drier lowlands (Jones
et al. 1991). On São Tomé, introduced birds are mainly small granivore species that
rely on anthropogenic land uses (Soares et al. 2020), while introduced mammals
seem to be less restricted to these environments (Dutton 1994).
Altitude might be less relevant to explain the distribution of mobile terrestrial
organisms with broad ecological niches, such as most birds (e.g., Soares et al. 2020;
but see: Dallimer et al. 2009; Lima et al. 2017), but it is crucial for other groups, such
as snails (Tavares 2020), and notably plants (Exell 1944; Monod 1960; Stévart et al.
2022). Since plants are key components of terrestrial ecosystems, altitude has thus
fundamental implications for how ecosystems are distributed across the islands
(Dauby et al. 2022).
In reef ecosystems, depth and wave exposure appear to be the most important
factors to explain changes in fish diversity (Tuya et al. 2018) and in the composition
of fish and benthic communities (Morais and Maia 2017; Maia et al. 2018b). For
highly mobile marine megafauna, such as sea turtles and cetaceans, species distributions vary among groups and appear to be related mostly to ecosystem type, food
availability, depth, and sea surface temperature. For example, species of cetaceans
that are quite similar, such as the Pantropical Spotted Dolphin Stenella attenuata
(Gray, 1846), and the Common Bottlenose Dolphin Tursiops truncatus (Montagu,
1821), show clearly distinct habitat preferences related with bathymetry (Picanço
et al. 2009). In the case of sea turtles, the habitat associations are strongly related to
life stage. Juvenile Green and Hawksbills sea turtles feed on seagrasses or algal beds
and coral and/or rocky reefs respectively, all year long (Monzón-Argüello et al.
2011; Ferreira et al. 2018; Hancock et al. 2018). By contrast, most adult turtles are
found in coastal waters only during the reproductive season and are seldom observed
feeding. The northern beaches of São Tomé are dominated by the Olive Ridley,
which is extremely rare in the south of the island and on the island of Príncipe
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Species Ecology in the Gulf of Guinea Oceanic Islands: Distribution,. . .
179
(Hancock et al. 2015). On the other hand, the Green Turtle is clearly the dominant
nesting sea turtle species on Príncipe, and on the eastern and southern shores of São
Tomé. This is linked to the preference of Green Turtle for narrow and steeper
beaches associated with strong erosive processes, while Olive Ridley prefers
unobstructed access to wide beaches with gentle slopes. The Hawksbill Turtle
typically prefers small, protected beaches composed mainly of coralline sand and
surrounded by vegetation, hence occurring mostly on the Rolas Islet off São Tomé,
and along the northern coast of Príncipe (Hancock 2019).
Species Interactions
Interactions between species are often complex, but they are the structure that
supports biodiversity, and thus their study is fundamental to understand ecosystem
functioning (Thébault and Fontaine 2010). Since they rely on detailed knowledge of
basic aspects of the ecology of species and are often difficult to quantify, few species
interactions have been studied in-depth on these islands, and the information available in the literature is often still limited to brief descriptions (e.g., Jones and Tye
2006; Wirtz and d’Udekem d’Acoz 2008; Vasco-Rodrigues et al. 2017).
We drafted a qualitative vertebrate food web for terrestrial ecosystems in São
Tomé and Príncipe, distinguishing native and non-native species (Fig. 7.2). This was
based solely on information on trophic interactions described for the islands for
introduced mammals (Dutton 1994), birds (Jones and Tye 2006), bats (Rainho et al.
2010), shrews (Ceríaco et al. 2015; Lima et al. 2016), amphibians and reptiles
(Ceríaco et al. 2018), the undescribed Príncipe Scops-Owl (Freitas 2019), and on
more generic sources for other species (IUCN 2020). Nevertheless, even this
simplistic approach, which excludes humans from the equation, illustrates major
disruptions of trophic interactions by non-native species. Beyond the obvious
changes in the topography of trophic interactions, the impact of introduced species
is further heightened by their distinctive traits (Capellini et al. 2015). This food web
provides a starting point for studies to deepen our understanding of trophic linkages
and how they may be disrupted by introduced species.
A more quantitative, community-level approach enabled building a multi-guild
seed dispersal network for São Tomé (Heleno et al. 2021). This showed that
non-native species can disrupt this important component of ecosystem functioning,
especially large mammals, which are seldom native on oceanic islands. Other
quantitative studies at the community level have assessed how reef microhabitats
mediate fish agonistic interactions (Canterle et al. 2020), and how land use and host
species influence richness, prevalence, and co-infection patterns of haemosporidian
bird parasites (Reis et al. 2021). A quantitative, species-specific study used stable
isotopes to reveal that juvenile São Tomé Green Turtles adapt their diet preferences
to the available food sources and, in contrast with expectations, are not strict
herbivores (Hancock et al. 2018). Further quantitative studies at the community
and species level across terrestrial and marine ecosystems are sorely needed.
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F. C. Soares et al.
Fig. 7.2 Generalized São Tomé and Príncipe terrestrial vertebrate food web. Each icon represents a
group of native or non-native species in the same trophic level. Arrows signal energy transfers
through trophic interactions. Green symbolizes native species and interactions, red symbolizes
non-native ones and grey symbolizes non-vertebrate components of the food web, namely plants
and invertebrates. Native herbivores include fruit bats, pigeons, and parrots, while non-native
include several ungulates, Rock Pigeon Columba livia J.F. Gmelin, 1789, and Laughing Dove
Streptopelia senegalensis (Linnaeus, 1766). Native omnivores include several species of pigeons
and perching bird species, while non-native include rodents, Mona Monkey Cercopithecus mona
(Schreber, 1775), African Civet Civettictis civetta (Schreber, 1776), Pig Sus scrofa Linnaeus, 1758,
fowls, and other bird species. Native insectivores include amphibians, geckos, skinks, shrews, bats,
and a few bird species, while non-native include geckos, skinks; the Palm Swift Cypsiurus parvus
(M.H.K.Lichtenstein, 1823), an insectivore that colonized the islands recently. Native carnivores
include Dwarf Olive Ibis Bostrychia bocagei (Chapin, 1923), owls, and Black Kite Milvus migrans
(Boddaert, 1783), while Cattle Egret Bubulcus ibis (Linnaeus, 1758) is the only non-native
carnivore bird. Snakes are the only native vertivores, while Cat Felis catus Linnaeus, 1758, Dog
Canis familiaris Linnaeus, 1758, and Least Weasel Mustela nivalis Linnaeus, 1766 are all
non-native vertivores. Humans have been omitted from the figure, but they participate in all trophic
levels that are represented. Decomposers have also been omitted
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Species Ecology in the Gulf of Guinea Oceanic Islands: Distribution,. . .
181
Concluding Remarks
Species are still being described from the Gulf of Guinea on a regular basis (Lima
2016), clearly showing that much taxonomic work is still needed to understand the
biodiversity of these islands. In recent years, careful reviews combined with intensive island surveys and advances in molecular analyses have led to the description of
several new endemic species. Terrestrial vertebrates are certainly the best-studied
taxa, but since 2000 two amphibians (Uyeda et al. 2007; Bell 2016), six reptiles
(Ceríaco et al. 2022a), and one mammal species (Ceríaco et al. 2015) have been
newly described as endemic to the islands. Many widespread species have also been
reported for the first time, including plants (Stévart et al. 2019), land snails (Holyoak
et al. 2020), fishes (Costa et al. 2022), and birds (Lima and Melo 2021). A few have
also regained species status (e.g., Melo et al. 2010), while many others remain
undescribed, even among plants (e.g. Stévart et al. 2022), land mammals (Rainho
et al. 2022), and birds (Melo et al. 2022). This incomplete knowledge is a serious
handicap to develop a more in-depth understanding of the ecology of the islands.
Furthermore, ecological studies have been biased towards certain groups, such as
terrestrial vertebrates, and notably birds. This bias occurs because the taxonomy of
these groups is mostly resolved, both locally (Jones and Tye 2006) and globally
(Billerman et al. 2020). Such studies have been particularly relevant for the recognition of the biological importance of these islands at the global scale (e.g. Le Saout
et al. 2013). Conversely, very few ecological studies have been dedicated to invertebrate groups, exceptions including very recent research on land snails (Panisi et al.
2022) and mosquitoes (Reis et al. 2021). Biases persist even within taxonomic
groups, since studies tend to focus on conspicuous and easily detectable species.
Even among birds, the existence of the Príncipe Scops-Owl was only confirmed in
2016 (Verbelen et al. 2016), and the taxonomy of the Gulf of Guinea Storm Petrel
remains uncertain (Flood et al. 2019). Although often rarer and harder to find,
threatened and endemic species are targeted by more studies than expected (Lima
et al. 2011), because they tend to be the focus of conservation studies (e.g., Lima
et al. 2017).
There are also important spatial research biases, within and across the islands.
The most evident is the scarcity of studies on Annobón, the smallest and least
accessible of the main islands. Within Príncipe and São Tomé, the most remote
areas have also been less surveyed. Marine species are often less known, simply
because they are more challenging to study. This is especially true for those living
away from the coast and at greater depths.
Finally, there are also multiple temporal biases. Certain groups tend to be studied
primarily during certain seasons, as it is the case for plants (e.g., Benitez et al. 2018)
and sea turtles (Ribeiro 2018; Hancock 2019), which are mostly monitored during
the breeding season. Out of convenience, many other taxa tend to be studied during
the dry seasons, such as birds (Lima et al. 2017), even though this is not their
breeding season (Madeira 2018). These biases may ultimately constrain the broader
182
F. C. Soares et al.
understanding of the ecology of the islands and a conscious effort to study species
throughout the year would help alleviate this bias.
Relatively few studies have addressed community ecology, focusing instead on
individual species, even when multiple species are included in the same study. In
some cases, this has resulted from methodological limitations to gather comparable
data from multiple species simultaneously. Nevertheless, in recent years, there have
been several community ecology studies, including birds (Lima 2012; Soares et al.
2020), land snails (Tavares 2020), plants (Fundação Príncipe 2019), and bird–plant
interactions (Heleno et al. 2021).
To promote these islands as models for understanding ecological processes, it is
necessary to overcome knowledge gaps and research biases, which generate uncertainty and limit extrapolation to broader contexts. To do so, future studies should
include systematic island-wide surveys, or prioritize understudied areas, such as
Annobón, less accessible areas within the islands, and marine environments. Likewise, research must focus on understudied taxonomic groups, such as invertebrates.
For most of these groups many fundamental ecological aspects, such as distribution
and environmental associations, remain fully unknown. Furthermore, studies at the
community level and focusing on species interactions are needed to understand the
functioning of ecosystems and ultimately help protect the unique biodiversity of
these islands.
To ensure the future of the endemic-rich biodiversity of these islands, it is evident
that protecting remaining natural ecosystems and preventing the degradation of
human-modified ecosystems, such as secondary forests, are key priorities. Additionally, the over-exploitation of native species and the introduction and spread of
non-native species must be curbed, and conservation strategies need to be continuously refined and implemented. These include Red Listing (IUCN 2020), speciesspecific action plans for threatened species (e.g., Ndang’ang’a et al. 2014a, b; Panisi
et al. 2020; Fundação Príncipe 2021), the expansion of the existing network of
protected areas (BirdLife International 2020), and their management plans. Longterm monitoring studies are urgently needed to assess biodiversity trends, promptly
identify declines, and inform conservation actions.
Finally, it is crucial to raise public awareness about the unique biodiversity of
these islands, both internationally and locally. Local biodiversity education has
greatly improved in recent years (Ayres et al. 2022), but the development of local
scientific expertise through outreach, capacity building, and advanced training is still
lacking and should be promoted through international collaborations.
Acknowledgments The Portuguese Government, through “Fundação para a Ciência e a
Tecnologia” (FCT/MCTES), supported RFL, JMH, and FCS by providing structural funds to
cE3c (UID/BIA/00329/2021), and JMH and FCS by funding their PhD grants ((PD/BD/52599/
2014 and PD/BD/140832/2018, respectively). TS’s work in São Tomé and Príncipe is supported
through the “Critical Ecosystem Partnership Fund (CEPF)” which is a joint initiative of l’Agence
Française de Développement, Conservation International, the European Union, the Global Environment Facility, the Government of Japan, and the World Bank. We thank the reviewers Peter
Jones and Mariana Carvalho for their helpful comments and suggestions that improved the chapter.
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183
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Chapter 8
Fungi of São Tomé and Príncipe Islands:
Basidiomycete Mushrooms and Allies
Dennis E. Desjardin and Brian A. Perry
Abstract Mushrooms and allies belong to the Agaricomycetes lineage of
Basidiomycota. A total of 260 species, belonging in 109 genera, 51 families and
13 orders have been reported from São Tomé and Príncipe between 1851 and 2020,
of which 66 were described as new species. They range in body forms from agarics
and boletes to polyporoid, clavarioid, coralloid, thelephoroid, stereoid, corticioid,
hydnoid, cantherelloid, gasteroid, and jelly fungi. The vast majority are saprotrophs,
a small number are plant pathogens, and a rare few may be ectomycorrhizal. Sixty
species, 23%, can be classified putative endemics. The current state of knowledge of
the Agaricomycetes from the nation is based on fewer than ten expeditions in the
past 170 years and represents only a snapshot of the actual diversity that is likely
present.
Keywords Agaricomycetes · Fungal diversity · Mycota · Taxonomy
Introduction
This chapter constitutes a preliminary accounting of the mushrooms and allied taxa
(Fungi, Basidiomycota) that occur in the West African island nation São Tomé and
Príncipe (ST&P). Herein, we treat only organisms currently recognized as belonging
to the Agaricomycetes lineage, comprising most mushroom-forming taxa. These
charismatic megafungi are recognized easily in the field although understudied in
tropical Africa. The names associated with each species are based historically on
morphological features of their sexual reproductive structures, i.e., the mushrooms,
supplemented now with molecular sequence data.
D. E. Desjardin (*)
Department of Biology, San Francisco State University, San Francisco, CA, USA
e-mail: ded@sfsu.edu
B. A. Perry
Department of Biological Sciences, California State University East Bay, Hayward, CA, USA
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_8
189
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D. E. Desjardin and B. A. Perry
The Agaricomycetes comprises organisms commonly called gilled fungi (agarics), boletes, polypores, club and coral fungi, thelephoroid and stereoid fungi,
corticioid fungi (resupinates), tooth fungi, cantherelloid fungi, gasteroid fungi (puffballs, stinkhorns, bird’s nest fungi, earthstars) and jelly fungi. They form sexual
reproductive structures (basidiomes) large enough to be observed with the naked eye
and broadly defined as mushrooms (¼ macrofungi). Their vegetative, mycelial stage
serves numerous ecological roles as saprotrophs, mixotrophs, pathogens, endophytes, and mycorrhizae, and aids in soil generation, erosion control, biofiltration,
nutrient retention and other important bioprocesses. Their sporulating stage, beyond
functioning as the dispersal and reproductive phase, serves as a food source for
myriad organisms. Many lineages produce basidiomes harvested by indigenous
cultures in West Africa (e.g., chanterelles, boletes, oyster mushrooms, wood ears,
etc.) and used for food, medicine, textile dyeing, a source of income and other
sociological aspects (entheogens) (Osarenkhoe et al. 2014). Although the mycota of
the region is diverse and abundant, only limited research has been published on the
fungi of ST&P, primarily because few mycologists have visited the islands. Several
expeditions in the late nineteenth century, a single excursion in the twentieth
century, and several in the twenty-first century constitute the total acquisitions
upon which our current knowledge of the diversity of Agaricomycetes from ST&P
is based.
History of Agaricomycetes Research
The first published account of Agaricomycetes from São Tomé was a report by Elias
M. Fries (1851) of six species collected by Krebs (no further collector information
was provided) in a paper entitled Novarum Symbolarum Mycologicarum Mantissa.
Four of these were described as new species, viz., Agaricus papularis Fr.,
A. macromastes Fr., Panus troglodytes Fr., and Lentinus flaccidus Fr., the first
three of which have not been treated since, and their taxonomic placement is
uncertain. This was followed by a more substantive contribution from G. Winter
(1886) based on his study of specimens collected from São Tomé in 1885 by
A. Moller, Inspector of the Botanical Garden of Coimbra, and Francisco A. Dias
Quintas and F. Newton, Portuguese botanists. Winter’s (1886) paper was an
accounting of 100 species of Fungi as part of the Flora de S. Thomé, Contribuições
para o Estudo da Flora d’Africa, compiled by J. Henriques (1886). Of these,
29 represented species of Basidiomycota; none were new species. Roumeguère
(1889) examined a number of the fungal specimens collected from São Tomé by
Moller, Quintas and Newton and reported four species of Basidiomycota, of which
one, Stereum amphirhytes Sacc. & Berl. was reported as new (published again that
same year by Saccardo and Berlese). The species has not been treated since.
Saccardo and Berlese (1889) also studied some Moller and Newton specimens
from ST&P and reported 13 species of Basidiomycota, of which six represented
new species. In a paper on Fungi from Cameroon, Bresadola (1890) reported three
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Fungi of São Tomé and Príncipe Islands: Basidiomycete Mushrooms and Allies
191
species of Polyporus from São Tomé, including one new species, P. squamulosus
Bres. The most significant early accounting of Fungi from ST&P were the papers by
Bresadola and Roumeguère (1890) and Bresadola (1891), which comprised a
re-examination of the material reported by Winter (1886) and inclusion of additional
taxa from specimens not treated by Winter. Collectively, these two papers reported
83 species of Basidiomycota from ST&P, of which 9 were new taxa. The specimens
reported from ST&P between 1886 and 1891, representing 113 species, were
deposited in the Herbarium of the Botanic Garden and Botanical Museum BerlinDahlem (B), but unfortunately were destroyed in a fire in 1943, making taxonomic
confirmation now impossible. Consequently, the taxonomic placement of the new
species is uncertain, and the occurrence on ST&P of many of the other species
reported, which were based primarily on European epithets, is questionable.
During the twentieth century, the only significant contribution to our knowledge
of Fungi from ST&P was that of António Xavier Pereira Coutinho, Professor of
Horticulture at the Instituto Superior de Agronomia, Universidade de Lisboa.
Coutinho (1925) reported 74 Basidiomycota and two Ascomycota from São
Tomé, based on material collected in 1920 by his son Martinho de França Pereira
Coutinho, and Professor Manuel de Sousa da Câmara, Head of Section and Director,
respectively, of the Laboratory of Plant Pathology at the same Institute. Eighty-two
percent of the species were collected at Água-Izé. Ten of the Basidiomycota
represented new species.
Contemporary treatments of Agaricomycetes from ST&P based on newly collected specimens and molecular systematic approaches did not begin until the early
twenty-first century. In 2001, Dr. Robert C. Drewes, Curator of Herpetology at the
California Academy of Sciences, led a multidisciplinary research expedition to
ST&P, the beginning of two decades of intensive exploration of the islands to
document their biodiversity (Drewes 2002). In April 2006 (2 weeks) Desjardin,
and in April 2008 (3 weeks), Desjardin and Perry conducted extensive fieldwork on
ST&P, documenting the diversity of macrofungi (fleshy Agaricomycetes, excluding
polypores and corticioid fungi). To honor Robert Drewes, who has dedicated more
than 40 years of his life to research in Africa, and who introduced us to the island
nation, we described Phallus drewesii Desjardin & B.A. Perry (Phallaceae, Fig. 8.1–
5) in our premier paper (Desjardin and Perry 2009). Subsequently, partial results of
these expeditions were published in nine additional papers (Desjardin and Perry
2015a, b, 2016, 2017, 2018, 2020; Desjardin et al. 2017; Cooper et al. 2018; Grace
et al. 2019), reporting 126 species of Agaricomycetes, including 36 new species.
This research is ongoing—78 additional specimens, representing approx. 50 species,
await publication. Several other researchers have documented macrofungi from the
region over the past decade. Decock (2011) described Truncospora oboensis Decock
(Polyporaceae, Fig. 8.1–4) and Coltricia oboensis Decock (2013)
(Hymenochaetaceae) as new from material collected from high elevation cloud
forests on São Tomé. Degreef et al. (2013) reported two rare Phallaceae, Blumenavia
angolensis (Welw. & Curr.) Dring and Mutinus zenkeri (Henn.) E. Fisch., from São
Tomé. Most of the species included in these contemporary publications are
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D. E. Desjardin and B. A. Perry
Fig. 8.1 Representative Agaricomycetes from São Tomé and Príncipe: (1) Marasmius laranja
(Agaricales); (2) Gymnopus rodhallii (Agaricales); (3) Cyathus poeppigii (Agaricales); (4)
Truncospora oboensis (Polyporales); (5) Phallus drewesii (Phallales); (6) Geastrum schweinitzii
(Geastrales); (7) Scytinopogon havencampii (Trechisporales); (8) Aphelaria subglobispora
(Cantharellales). Scale bar ¼ 10 mm. Photo credits: (1–3, 5, 6, 8) B. Perry, (4) C. Decock (7)
W. Eckerman
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193
represented by single or very few specimens, although the specimens are deposited
in herbaria and accessible for future studies.
Diversity and Endemism
Our knowledge of the diversity of fungi globally is incomplete due to their unique
biology (cryptic mycelium producing often inconspicuous, short-lived sporulating
structures upon which their names are based) and difficulty in identification (Willis
2018). In ST&P, documentation of the diversity of Agaricomycetes is rather depauperate as a direct result of limited fieldwork conducted there to date. Fungal species
reported prior to 1925 is a reflection of the peregrinations of itinerant botanists, not
the result of a concerted effort to document the fungi from the region. Their
serendipitous encounters with mushrooms produced exsiccati that were often
squashed between paper and blotters in plant presses and dried amongst the plant
specimens that were the focus of early expeditions. Subsequent research in the
twentieth century (Coutinho 1925) produced better quality specimens, but as with
earlier expeditions, focused primarily on easily collected and preserved polypores
and allies. It was not until the twenty-first century that a concerted effort was made to
document the Agaricomycetes from the nation, supported by well documented
fungarium specimens and molecular data (research of Desjardin, Perry and colleagues). Combining the unsubstantiated early reports with new vouchered reports,
we account for 260 species of Agaricomycetes from ST&P, representing 109 genera,
51 families and 13 orders (Appendix).
It is difficult to compare these numbers with those of Agaricomycetes recorded
from neighboring countries of West Africa (Piepenbring et al. 2020). We recognize
that what we are presenting herein is only a snapshot of the actual mushroom
diversity from the islands. More effort needs to be focused on documenting the
polypores and similar taxa with persistent basidiomes whose early reports are not
vouchered, and continued work on taxa with fleshy, putrescent basidiomes in
understudied lineages.
Determining the distribution status of fungi is fraught with difficulties. Many
areas of the world have not been explored for fungi, and documentation from tropical
Africa is especially limited. It is premature to state unequivocally that any species is
“endemic” until we have more data on the diversity of fungi from understudied
areas. For this treatise, if a species was described as new from São Tomé or Príncipe
and it has not yet been reported from elsewhere, we recognize the taxon as a putative
endemic and annotate as such in the Appendix. Under this scenario, 66 new species
have been described from material collected on ST&P, of which six species have
been reported as occurring elsewhere. Hence, 60 species can be considered as
putative endemics, or a 23% level of endemism in the Agaricomycetes from ST&P.
Species reports, where identification was based on molecular phylogenetic data,
indicate that ST&P mushrooms or their closest relatives occur in neighboring West
and Central African countries (Cameroon, Sierra Leone, DR Congo), other parts of
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continental Africa and Madagascar, South East and South-Central Asia, and tropical
America (pers. obs.). No attempt was made to rate species as resident, migrant,
vagrant or introduced as such categorizations would be only speculative. We
recognize that the mushrooms commonly collected in habitats dominated by introduced plants, such as coastal cacao-banana groves, coffee plantations and other
agricultural sites, most likely represent introduced species, however, we have not
annotated them as such. Interestingly, a number of the species that we encountered in
human-altered lowland habitats, either also occur in or have their closest known
relatives in the Caribbean region. This could indicate unidirectional or bidirectional
introduction of fungal species associated with aspects of the slave or agricultural
trade.
Ecology and Conservation
The macrofungi of ST&P are primarily saprotrophic, decomposing leaf litter and
woody substrates. A number of species may be pathogens, associated with root or
heart rot of woody plants (e.g., Bjerkandera, Fomes), while a rare few are biotroph
associates of mosses (Cotylidia). The ectomycorrhizal status of ST&P fungi is
unknown, but we suspect that there are very few because of the paucity of ectotrophic host plant genera. A cross-reference of the annotated list of Angiosperms for
ST&P (Figueiredo et al. 2011) with a list of global ectotrophic host plant genera
(Brundrett 2009), yielded only six potential ectotrophic host plant genera in ST&P,
viz., Casuarina (Casuarinaceae), Lonchocarpus and Acacia (Fabaceae), Eucalyptus
and Melaleuca (Myrtaceae), and Manilkara (Sapotaceae), which include only ten
local species. Of these ten, six are introduced species, and only four may represent
native species, viz., Lonchocarpus sericeus (Poir.) Kunth, Acacia kamerunensis
Gand., Acacia pentagona (Schumach.) Hook. and Manilkara obovata (Sabine &
G. Don) J.H. Hemsl. Whether these potential plant host species are ectotrophic has
not been determined.
Mushrooms and allies require adequate moisture and appropriate nutritional
substrates for survival. Many species, whether saprotrophic, pathogenic, or mycorrhizal, are host specific (at various levels of specificity). When their habitats change
due to changes in water availability (rain, humidity), anthropogenic disturbance, or
an alteration in plant community structure, the abundance and diversity of fungi
changes as well. Conservation efforts focused on fungi are in their infancy globally.
Of the 135,000 species of fungi described to date (Kirk 2019), as noted by
Piepenbring et al. (2020), only 91 have been evaluated for the global Red List
established by the International Union for Conservation of Nature (IUCN). None
of the species reported from ST&P are included in the list.
8
Fungi of São Tomé and Príncipe Islands: Basidiomycete Mushrooms and Allies
195
Agaricomycetes of São Tomé and Príncipe
An accounting of the history and diversity of ST&P mushrooms in each order is
presented below, organized in accordance with the phylogenetic tree of
Agaricomycetes adapted from Varga et al. (2019) (Fig. 8.2).
Order Agaricales
Approximately half of the known Agaricomycetes from ST&P belong to the
Agaricales, this accounting primarily the result of recent research published by
Desjardin and Perry. To date, 133 species of Agaricales have been reported from
ST&P, belonging to 46 genera in 24 families. This order is comprised mainly of
Fig. 8.2 Phylogenetic tree of Agaricomycetes adapted from Varga et al. (2019). Orders containing
taxa reported from São Tomé and Príncipe are in bold
196
D. E. Desjardin and B. A. Perry
gilled mushrooms, i.e., basidiomes with the hymenium (spore-producing tissue)
located on radiating plate-like structures (gills ¼ lamellae) suspended under a cap
(pileus), and together typically elevated by a stem (stipe). A few families in the order
contain species with clavarioid (club-shaped), coralloid (branched, coral-shaped),
gasteroid (enclosed, puffball-like) or corticioid (crust-like, with smooth, resupinate
hymenophores) basidiomes. These mushrooms are typically putrescent, lasting from
only a few hours to a few days, then wither and disappear. They form only after
abundant moisture is available, usually during the wet season, and encountering
them is often serendipitous. To obtain quality specimens for study and determination, basidiomes must be collected fresh, their taxonomically important features
documented, and then dried immediately for long-term preservation. This procedure
presents many difficulties in understudied tropical habitats and most likely accounts
for the limited number of early reports. Between 1851 and 1891, only 19 species of
Agaricales were reported from ST&P, four of which were new species, and two of
the latter remain incertae sedis (Fries 1851; Winter 1886; Roumeguère 1889;
Saccardo and Berlese 1889; Bresadola and Roumeguère 1890; Bresadola 1891).
Coutinho (1925) reported 17 gilled mushroom species from São Tomé, of which six
were new species and two of these are currently of unknown taxonomic placement.
Most of the known Agaricales from ST&P were reported by Desjardin, Perry and
colleagues, viz., 101 species of which 32 were new to science. They provided
comprehensive coverage of clavarioid and gasteroid species in the Clavariaceae,
Lycoperdaceae and Nidulariaceae (Desjardin and Perry 2015b), dark-spored species
in the Bolbitiaceae, Crepidotaceae, Hymenogastraceae, Psathyrellaceae and
Strophariaceae (Desjardin and Perry 2016), gymnopoid species in the Agaricaceae,
Catathelasmataceae, Hydropoid clade, Hygrophoraceae, Marasmiaceae,
Mycenaceae, Omphalotaceae, Physalacriaceae and Tricholomataceae (Desjardin
and Perry 2017, Desjardin et al. 2017), species of Pluteus of Pluteaceae (Desjardin
and Perry 2018), mycenoid species in the Hydropoid clade and Mycenaceae (Cooper
et al. 2018), marasmioid species in the Marasmiaceae (Grace et al. 2019), and
hygrophoroid species in the Hygrophoraceae (Desjardin and Perry 2020). Additional
specimens collected during the 2008 expedition await diagnosis.
Order Boletales
Most members of order Boletales are ectomycorrhizal and require specific plant
hosts to support their mutualistic symbiosis. As noted in the section on ecology, few
ectotrophic plant species occur on ST&P, and accordingly, ectomycorrhizal
Agaricomycetes are rare. Most Boletales form putrescent basidiomes with a thick
fleshy cap supporting a tubular hymenophore with the hymenium lining the inside of
the vertically oriented tubes, and all elevated on a stipe—a body form known as a
bolete. A few lineages form gasteroid basidiomes, while others form corticioid
(crust-like, resupinate with smooth or wrinkled hymenophore) basidiomes. Only a
single species of Boletales has been reported from Príncipe, the gasteroid
8
Fungi of São Tomé and Príncipe Islands: Basidiomycete Mushrooms and Allies
197
Scleroderma dictyosporum Pat. (Sclerodermataceae) (Desjardin and Perry 2015b).
We are aware of several boletes that occur on São Tomé, although official reports
have not yet been published. Desjardin and Perry (unpubl.) have collected a single
specimen of a Tylopilus sp. (deposited in SFSU) and have seen photographs of a
probable Phlebopus sp. (no specimens retained). Whether these taxa are
ectomycorrhizal or saprotrophic is currently unknown.
Order Stereopsidales
Members of order Stereopsidales form corticioid or thelephoroid (tough, with a
smooth or wrinkled hymenophore) basidiomes. Only a single species from the
order, the thelephoroid Stereopsis radicans (Berk.) D.A. Reid (Stereopsidaceae)
has been reported, apparently collected twice on São Tomé, once on wood by
F. Quintas in 1885 (Bresadola and Roumeguère 1890), and once on soil in 1920
(Coutinho 1925).
Order Polyporales
The first fungi collected and repeatedly reported from West African countries were
mostly polypores, belonging mainly to the Polyporales and Hymenochaetales
(Piepenbring et al. 2020). This is because of their persistent basidiomes, which
may be encountered throughout the year when fleshy species are not apparent, and
due to the ease of collecting, drying and transporting specimens. Basidiomes are
typically tough and woody, with a tubular hymenophore, lack a stem, and grow on
woody substrates as saprotrophs or pathogens. Seventy-one species of order
Polyporales have been documented from ST&P; 55 of these were reported prior to
1925, of which six represented new species, viz., Daedalea newtonii Bres. & Roum.
(Fomitopsidaceae), Tyromyces squamulosus (Bres.) Ryvarden (Incrustoporiaceae),
and Favolus jacobeus Sacc. & Berl., Polyporus torquescens Sacc. & Berl. and
Trametes discolor Sacc. & Berl. (Polyporaceae) (Saccardo and Berlese 1889;
Bresadola 1890; Bresadola and Roumeguère 1890). Stereum pulchellum Sacc. &
Berl. was described as new from Príncipe, but is currently accepted as a synonym of
Podoscypha involuta (Klotsch ex Fr.) Imazeki (Podoscyphaceae). Apparently, the
specimen vouchers of these 55 species were destroyed in the 1943 fire at the Berlin
Herbarium. Coutinho (1925) added another 16 species to the list, including two new
species, Fomes ferrugineobrunneus Cout. and Lentinus thomensis Cout.
(Polyporaceae). Since then, only a single species of Polyporales has been reported
from São Tomé, the new species Truncospora oboensis Decock (Polyporaceae,
Fig. 8.1–4) (Decock 2011). Although many species of polypores were observed on
ST&P during the expeditions by Desjardin and Perry (in 2006 and 2008), this fungal
group was not the focus of their research and no specimens were collected. Future
198
D. E. Desjardin and B. A. Perry
research should focus on documenting order Polyporales from ST&P, to verify early
reports with vouchered material and to clarify polypore diversity for the region.
Order Thelephorales
Members of this order form tough, stipitate basidiomes with a smooth hymenophore
(thelephoroid) and stipitate or sessile basidiomes with a toothed hymenophore
(hydnoid). Only a single species has been reported from São Tomé, the new sessile
hydnoid taxon Phaeodon thomensis Cout. (Bankeraceae) (Coutinho 1925). The
species is known from a single collection made in 1920 and has not been reported
since from West Africa.
Order Russulales
Species of order Russulales are quite common and abundant in Africa. They develop
basidiomes with a great variety of body forms, from gilled and poroid to hydnoid,
corticioid, clavarioid and coralloid. Many are ectomycorrhizal, while others are
saprotrophs or plant pathogens. Unfortunately, the speciose ectomycorrhizal genera
Russula and Lactarius, so common in the miombo woodlands of Western Africa, are
lacking in ST&P because of the near absence of ectotrophic host plants. Only
14 species of Russulales have been documented from ST&P, all but one species
reported before 1925 (Winter 1886; Saccardo and Berlese 1889; Bresadola and
Roumeguère 1890). Most of these represent saprotrophic or pathogenic taxa with
corticioid or stereoid (sessile, with a cap and smooth hymenophore) basidiomes in
the Hericiaceae, Peniophoraceae and Stereaceae, although two Lentinellus species
are gilled fungi in Auriscalpiaceae. Only two species were described as new from
São Tomé, the corticioid Scytinostroma quintasianum (Bres. & Roum.) Nakasone
(Peniophoraceae), named after the early Portuguese collector F. Quintas (Bresadola
and Roumeguère 1890), and the stereoid Stereum amphirhytes Sacc. & Berl.
(Stereaceae) (Saccardo and Berlese 1889).
Order Hymenochaetales
Similar to the Polyporales, the ST&P representatives of order Hymenochaetales
form primarily persistent basidiomes with tubular hymenophore and saprotrophic
or pathogenic ecology (Hymenochataceae), but the order also contains an unusual
lineage with small, fleshy basidiomes with gilled or smooth hymenophore
(Rickenellaceae) that are associated with mosses. Twelve species have been
documented from São Tomé, ten of which were reported prior to 1925 (Winter
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Fungi of São Tomé and Príncipe Islands: Basidiomycete Mushrooms and Allies
199
1886; Roumeguère 1889; Bresadola and Roumeguère 1890), whose material has
been lost, although four of these species were recollected and reported again by
Coutinho (1925). Two lignicolous species were described as new, Polystictus
albocinereus Cout. (Coutinho 1925) and Coltricia oboensis Decock
(Hymenochaetaceae) (Decock 2013). This is another group that needs attention
from contemporary researchers.
Order Phallales
The Phallales constitute the “stinkhorns,” a lineage of bizarrely-shaped mushrooms
with a dispersal strategy symbiotic with insects. All basidiomes are initially globose
or egg-shaped with the hymenophore enclosed (gasteroid), and as they mature, the
outer peridium layer ruptures, and the inner sporulating structure erupts into a
plethora of shapes, allowing for common names like octopus stinkhorn, basket
stinkhorn, Devil’s horn, etc. The spores are produced in a gelatinous, putrid-scented
mass on the elevated structure. The often carrion-like odor attracts insects, primarily
flies, who lay their eggs in the stinkhorn to provide a food source for their larvae, and
the adults also consume the spores which pass through their digestive system and
when defecated, aid in stinkhorn dispersal. Six species belonging to the Phallaceae
have been documented from ST&P. The first reported was a new species, Clathrus
parvulus Bres. & Roum., a very small (<20 mm diam), reddish basket stinkhorn that
has not been reported since first discovery (Bresadola and Roumeguère 1890). The
remaining five species are recent reports (Degreef et al. 2013; Desjardin and Perry
2015b), including a new species, Phallus drewesii (Fig. 8.1–5).
Order Gomphales
Three families comprise the order Gomphales, but only members of the
Gomphaceae have been reported from ST&P. The family contains species with
funnel-shaped basidiomes with wrinkled to venous or gilled hymenophore
(cantharelloid) and coralloid basidiomes. Only a single genus of coralloid species
has been reported from São Tomé, representing three species of Ramaria. Two
represent new species described in 1890 that have not been recollected, viz.,
Ramaria henriquesii (Bres. & Roum.) Corner (ut Clavaria), and Ramaria
mollerianum (Bres. & Roum.) Corner (ut Lachnocladium) (Bresadola and
Roumeguère 1890), both named after the early Portuguese botanists who conducted
fieldwork on São Tomé. The genus Ramaria is ectomycorrhizal in other parts of the
world, but the nutritional status of the São Tomé species is unknown.
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D. E. Desjardin and B. A. Perry
Order Geastrales
The order Geastrales, with the single family Geastraceae, are commonly known as
the “Earthstars.” The basidiomes, initially fully enclosed (gasteroid), rupture, and the
outer layers split and fold back into ray-shaped arms (star-like), exposing the interior
puffball, which opens by a central apical pore to passively release the internal spores.
Three species of Geastrum were recently reported from ST&P (Desjardin and Perry
2015b), the most unusual being Geastrum schweinitzii (Berk. & M.A. Curtis) Zeller
(Fig. 8.1–6), which forms very small earthstar basidiomes that arise from a thick
membranous sheet of mycelium (subiculum) that covers the substrate.
Order Trechisporales
Members of this order form corticioid basidiomes (type genus Trechispora) or
coralloid basidiomes (Scytinopogon). Only a single species from the group has
been recently reported, the new species Scytinopogon havencampii Desjardin &
B.A. Perry (Fig. 8.1–7), described from material collected on Príncipe (Desjardin
and Perry 2015a). Although it grows from the soil, we suspect that it is a saprotroph.
The genus Scytinopogon with coralloid basidiomes was recently accepted as a
synonym of Trechispora, a genus composed primarily of corticioid species, based
on multi-gene analyses (Meiras-Ottoni et al. 2021).
Order Auriculariales
The “jelly fungi” is a heterogeneous assemblage of fungi representing numerous
lineages, wherein the basidiomes are rubbery-gelatinous and hydrophilic/hygroscopic. Order Auriculariales comprises a number of families, several of which
contain species that form such basidiomes. Members of the Auriculariaceae often
form lignicolous, ear-shaped basidiomes that are commonly known as “wood ear”
mushrooms, which are edible and both wild-harvested and artificially cultivated.
Three species of Auricularia were documented early from São Tomé (Winter 1886;
Bresadola and Roumeguère 1890; Bresadola 1891) and reported again by Coutinho
(1925) from additional specimens. We have no information on whether local
cultures consume these commonly encountered mushrooms.
Order Cantharellales
Basidiome morphology is quite variable in order Cantharellales, and includes
clavarioid, coralloid, cantharelloid (funnel-shaped with decurrent gills or veins),
8
Fungi of São Tomé and Príncipe Islands: Basidiomycete Mushrooms and Allies
201
and hydnoid body forms. Three species, one from each of three families
(Aphelariaceae, Cantharellaceae, Hydnaceae), have been reported from ST&P. The
earliest report was for Craterellus crispus (Bull.) Berk. (Bresadola 1891), accepted
now as a synonym of Pseudocraterellus undulatus (Pers.) Rauschert. This species is
considered ectomycorrhizal, and given the paucity of ectotrophic plant species on
São Tomé, we question the original identification by Bresadola (1891). The two
additional reports of Cantharellales are from recently collected specimens, viz.,
Aphelaria subglobispora P. Roberts (Fig. 8.1–8) and Clavulina vanderystii (Bres.)
Corner (Desjardin and Perry 2015b).
Summary and Future Research
Although the Gulf of Guinea oceanic islands of São Tomé (13+ my) and Príncipe
(31+ my) are volcanic in origin and have never been part of or connected by a land
bridge to continental Africa (Lee et al. 1994), they are rich in Agaricomycetes
diversity. The fungal species or their ancestors reached the islands by wind, avian
or human-mediated dispersal, or on flotsam. Only a handful of expeditions have
been conducted since 1851, which produced specimens of Agaricomycetes that
allowed documentation of mushroom diversity from the islands. To date, 260 species, belonging in 109 genera, 51 families and 13 orders have been reported from
ST&P, providing only a snapshot of the estimated actual diversity of this important
fungal group. Twenty-three percent of these may represent endemic species.
Reported taxa represent myriad body forms, from agarics and boletes, to polypores,
club and coral fungi, thelephoroid, stereoid, corticioid, hydnoid and cantherelloid
fungi, puffballs, stinkhorns, bird’s nest fungi, earthstars, and jelly fungi. Nearly half
(113 spp.) of the recorded 260 species are known only from published reports, as
their vouchered specimens were destroyed during World War II, and hence the
accuracy of their determinations is questionable. The majority of reported species are
saprotrophic, functioning as important litter and wood decomposers, while a number
are plant pathogens and a rare few are putatively ectotrophic. The islands provide a
wide variety of native and human-disturbed habitats that undoubtedly house hidden
Agaricomycetes diversity. Future research should focus on recollecting the lineages
containing unvouchered species reports (polypores, thelephoroid, stereoid, corticioid
fungi), on identifying available specimens belonging to difficult taxonomic groups
(e.g., lepiotoid, entolomatoid, hemimycenoid taxa), and on further intensive fieldwork conducted monthly in undisturbed native forests. Our knowledge of the
mushrooms and allies from ST&P is in its infancy, and additional field and lab
work will surely yield surprises, new distribution records and new taxa.
202
D. E. Desjardin and B. A. Perry
Acknowledgments We thank Dr. Robert C. Drewes (California Academy of Sciences) who
continues to initiate, coordinate and lead multi-organism biotic surveys on São Tomé and Príncipe;
Eng. Arlindo de Ceita Carvalho, Director General of the Ministry of Environment, Victor Bonfim,
Salvador Sousa Pontes and Danilo Barbero for permission to collect and export specimens for
study. We are indebted to Société de Conservation et Développement for logistics and housing
support, especially the wonderful staff of Omali Lodge and Bom Bom Island. We are grateful for
the support and cooperation of Bastien Loloumb of Zuntabawe and Faustino Oliveira, former
Director of the botanical garden at Bom Sucesso. We were assisted in the field by José Ramos
Maria Vital Pires on Príncipe and by Quintino Quade Cabral, Martinho Nascimento and José Clara
on São Tomé. For continuing support, we are most grateful to Ned Seligman, Quintino Quade
Cabral and Roberta dos Santos of STePUP. We are grateful to the College of Science and
Engineering at San Francisco State University for partial funding to support travel to São Tomé
and Príncipe, and to the G. Lindsay Field Research Fund of the California Academy of Sciences
(CAS) for financially supporting the expedition in 2006 and the Hagey Research Venture Fund
(CAS) in 2008. We thank Cony Decock and Wes Eckerman for the use of their photos of
Truncospora oboensis and Scytinopogon havencampii, respectively. Lastly, we are especially
grateful to Roderick C.M. Hall, Coleman P. Burke and William K. Bowes Jr. whose generous
philanthropy has supported our research on São Tomé and Príncipe.
Appendix
List of Agaricomycetes reported from Príncipe (P) and São Tomé (ST). Author
abbreviations and nomenclature are according to Index Fungorum (www.
indexfungorum.org). Phylogenetic placement and synonymy are based on current
literature, or as reported in Species Fungorum (www.speciesfungorum.org) and
Mycobank (www.mycobank.org). E—putative endemic
Currently accepted name
ORDER AGARICALES
Agaricaceae
Agaricus subflabellatus Cout.
Agaricus sylvaticus Schaeff.
Phellorinia herculeana (Pers.) Kreisel
Ripartitella brasiliensis (Speg.) Singer
Tulostoma mollerianum Bres. & Roum.
Bolbitiaceae
Conocybe zeylanica (Petch) Boedijn
Catathelasmataceae
Callistosporium cystidiatum (T.J. Baroni,
Lodge & D.L. Lindner) Vizzini, Consiglio
& M. Marchetti
Callistosporium elegans Desjardin &
B.A. Perry
Callistosporium praemultifolium (Murrill)
Vizzini, Consiglio & M. Marchetti
Name reported in literature
Citation
P
Agaricus subflabellatus Cout.
Psalliota sylvatica (Schaeff.)
P. Kumm.
Phellorinia delestrei (Durieu
& Mont.) E. Fisch.
Ripartitella brasiliensis
(Speg.) Singer
Tylostoma mollerianum Bres.
& Roum.
Coutinho (1925)
Coutinho (1925)
E
X
Coutinho (1925)
X
Desjardin and Perry (2017)
X
Bresadola and
Roumeguère (1890)
E
Conocybe zeylanica (Petch)
Boedijn
Desjardin and Perry (2016)
X
Pleurocollybia cystidiata
T.J. Baroni, Lodge &
D.L. Lindner
Callistosporium elegans
Desjardin & B.A. Perry
Pleurocollybia praemultifolia
(Murrill) Singer
Desjardin and Perry (2017)
X
Desjardin and Perry (2017)
E
Desjardin and Perry (2017)
ST
X
(continued)
8
Fungi of São Tomé and Príncipe Islands: Basidiomycete Mushrooms and Allies
Currently accepted name
Clavariaceae
Clavaria phoenicea Zoll. & Moritzi
Clavulinopsis amoena (Zoll. & Moritzi)
Corner
Crepidotaceae
Crepidotus hemiphlebius (Berk. &
M.A. Curtis) Murrill
Crepidotus kangoliformis Desjardin &
B.A. Perry
Crepidotus nephrodes (Berk. &
M.A. Curtis) Sacc.
Simocybe centunculus (Fr.) P. Karst.
Cyphellaceae
Chondrostereum purpureum (Pers.)
Pouzar
Entolomataceae
Entoloma mammosum (L.) Hesler
Entoloma papillatum (Bres.) Dennis
Hydropoid Clade
Clitocybula intervenosa A.C. Cooper,
Desjardin & B.A. Perry
Hydropus globosporus A.C. Cooper,
Desjardin & B.A. Perry
Hydropus murinus A.C. Cooper,
Desjardin & B.A. Perry
Trogia anthidepas (Berk. & Broome)
Corner
Trogia aff. brevipes Corner
Trogia buccinalis (Mont.) Pat.
Trogia delicata Corner
Trogia aff. furcata Corner
Trogia infundibuliformis Berk. & Broome
Hygrophoraceae
Arrhenia cystidiata Desjardin
& B.A. Perry
Cuphophyllus laranja Desjardin
& B.A. Perry
Cuphophyllus pratensis (Fr.) Bon
Hygrocybe macambrarensis Desjardin
& B.A. Perry
Hygrocybe aff. miniata (Fr.) P. Kumm.
Hygrocybe sp.
Hymenogastraceae
Galerina makereriensis Pegler
203
Name reported in literature
Citation
P
Clavaria phoenicea Zoll. &
Moritzi
Clavulinopsis amoena (Zoll.
& Moritzi) Corner
Desjardin and Perry
(2015b)
Desjardin and Perry
(2015b)
X
Agaricus hemiphlebius Berk.
& M.A. Curtis
Crepidotus kangoliformis
Desjardin & B.A. Perry
Crepidotus nephrodes (Berk.
& M.A. Curtis) Sacc.
Simocybe centunculus (Fr.)
P. Karst.
Coutinho (1925)
X
Desjardin and Perry (2016)
E
Desjardin and Perry (2016)
X
Stereum purpureum Pers.
Bresadola and
Roumeguère (1890)
X
Hyporrhodius mammosus
(L.) J. Schröt.
Nolanea papillata Bres.
Coutinho (1925)
X
Bresadola (1891)
X
Clitocybula intervenosa
A.C. Cooper, Desjardin
& B.A. Perry
Hydropus globosporus
A.C. Cooper, Desjardin
& B.A. Perry
Hydropus murinus
A.C. Cooper, Desjardin
& B.A. Perry
Trogia anthidepas (Berk.
& Broome) Corner
Trogia aff. brevipes Corner
Cantharellus
buccinalis Mont.
Trogia delicata Corner
Trogia aff. furcata Corner
Trogia infundibuliformis
Berk. & Broome
Cooper et al. (2018)
E
Cooper et al. (2018)
E
Cooper et al. (2018)
E
Arrhenia cystidiata Desjardin
& B.A. Perry
Cuphophyllus laranja
Desjardin & B.A. Perry
Cuphophyllus pratensis (Fr.)
Bon
Hygrocybe macambrarensis
Desjardin & B.A. Perry
Hygrocybe aff. miniata (Fr.)
P. Kumm.
Hygrocybe sp.
Desjardin and Perry (2017)
E
Desjardin and Perry (2020)
E
Galerina makereriensis
Pegler
ST
X
Desjardin and Perry (2016)
Desjardin and Perry (2017)
Desjardin and Perry (2017)
Bresadola and
Roumeguère (1890)
Cooper et al. (2018)
Desjardin and Perry (2017)
Desjardin and Perry (2017)
Desjardin and Perry (2020)
X
X
X
X
X
X
X
X
Desjardin and Perry (2020)
E
Desjardin and Perry (2020)
X
Desjardin and Perry (2020)
X
Desjardin and Perry (2016)
X
(continued)
204
D. E. Desjardin and B. A. Perry
Currently accepted name
Name reported in literature
Citation
Galerina physospora Singer
Gymnopilus aculeatus (Bres. & Roum.)
Singer
Galerina physospora Singer
Pholiota aculeata Bres.
& Roum.
X
E
Gymnopilus aureobrunneus (Berk. &
M.A. Curtis) Murrill
Naucoria aureobrunnea
(Berk. & M.A. Curtis) Cout.
Gymnopilus aureobrunneus
(Berk. & M.A. Curtis) Murrill
Naucoria delipis (Berk. &
Broome) Cout.
Gymnopilus
purpureosquamulosus
Høiland
Naucoria brevipes Cout.
Naucoria chrysotricha (Berk.
& M.A. Curtis) Cout.
Naucoria fusco-olivacea
Bres. & Roum.
Naucoria papularis
(Fr.) Sacc.
Desjardin and Perry (2016)
Bresadola and
Roumeguère (1890),
Coutinho (1925)
Coutinho (1925)
Desjardin and Perry (2016)
X
Coutinho (1925)
X
Gymnopilus delipis (Berk. & Broome)
Singer
Gymnopilus purpureosquamulosus
Høiland
Naucoria brevipes Cout.
Naucoria chrysotricha (Berk. &
M.A. Curtis) Cout.
Naucoria fusco-olivacea Bres. & Roum.
Naucoria papularis (Fr.) Sacc.
P
Desjardin and Perry (2016)
X
X
E
X
Bresadola and
Roumeguère (1890)
Coutinho (1925)
E
Coutinho (1925)–doubtful
(see Desjardin and Perry
(2016))
Coutinho (1925)–doubtful
(see Desjardin and Perry
(2016))
E
X
Inocybe hystrix (Fr.) P. Karst.
Inocybe reticulata Cout.
Inocybe reticulata Cout.
Lycoperdaceae
Lycoperdon molle Pers.
Lycoperdon molle Pers.
Desjardin and Perry
(2015b)
X
Campanella buettneri Henn.
Campanella burkei Desjardin
& B.A. Perry
Lactocollybia variicystis
D.A. Reid & Eicker
Marasmius albisubiculosus
C.L. Grace, Desjardin &
B.A. Perry
Marasmius aff. apatelius
Singer
Collybia collina (Scop.)
P. Kumm.
Marasmius colorimarginatus
Antonín
Marasmius corrugatiformis
Singer
Marasmius diversus
C.L. Grace, Desjardin &
B.A. Perry
Marasmius
elaeocephaliformis
C.L. Grace, Desjardin &
B.A. Perry
Marasmius elaeocephalus
Singer
Desjardin et al. (2017)
Desjardin and Perry (2017)
X
E
Marasmius aff. apatelius Singer
Marasmius collinus (Scop.) P. Kumm.
Marasmius colorimarginatus Antonín
Marasmius corrugatiformis Singer
Marasmius diversus C.L. Grace, Desjardin
& B.A. Perry
Marasmius elaeocephaliformis
C.L. Grace, Desjardin & B.A. Perry
Marasmius elaeocephalus Singer
X
Coutinho (1925)
Coutinho (1925)
Inocybaceae
Inocybe hystrix (Fr.) P. Karst.
Marasmiaceae
Campanella buettneri Henn.
Campanella burkei Desjardin &
B.A. Perry
Lactocollybia variicystis D.A. Reid &
Eicker
Marasmius albisubiculosus C.L. Grace,
Desjardin & B.A. Perry
ST
E
Desjardin and Perry (2017)
X
Grace et al. (2019)
E
Grace et al. (2019)
X
Bresadola and
Roumeguère (1890)
Grace et al. (2019)
X
X
Grace et al. (2019)
X
Grace et al. (2019)
E
Grace et al. (2019)
E
Grace et al. (2019)
X
(continued)
8
Fungi of São Tomé and Príncipe Islands: Basidiomycete Mushrooms and Allies
Currently accepted name
Name reported in literature
Citation
Marasmius grandisetulosus Singer
Marasmius grandisetulosus
Singer
Marasmius aff.
guyanensis Mont.
Marasmius haediniformis
Singer
Marasmius laranja
C.L. Grace, Desjardin &
B.A. Perry
Marasmius leptocephalus
C.L. Grace, Desjardin &
B.A. Perry
Marasmius aff. megistus
Singer
Marasmius nodulocystis
Pegler
Marasmius palmivorus
Sharples
Marasmius paratrichotus
C.L. Grace, Desjardin &
B.A. Perry
Marasmius rotalis Berk. &
Broome
Marasmius segregatus
C.L. Grace, Desjardin &
B.A. Perry
Marasmius subarborescens
Singer
Marasmius subruforotula
Singer
Marasmius suthepensis
Wannathes, Desjardin &
Lumyong
Marasmius tenuisetulosus
(Singer) Singer
Grace et al. (2019)
Marasmius aff. guyanensis Mont.
Marasmius haediniformis Singer
Marasmius laranja C.L. Grace, Desjardin
& B.A. Perry
Marasmius leptocephalus C.L. Grace,
Desjardin & B.A. Perry
Marasmius aff. megistus Singer
Marasmius nodulocystis Pegler
Marasmius palmivorus Sharples
Marasmius paratrichotus C.L. Grace,
Desjardin & B.A. Perry
Marasmius rotalis Berk. & Broome
Marasmius segregatus C.L. Grace,
Desjardin & B.A. Perry
Marasmius subarborescens Singer
Marasmius subruforotula Singer
Marasmius suthepensis Wannathes,
Desjardin & Lumyong
Marasmius tenuisetulosus (Singer) Singer
Mycenaceae
Favolaschia auriscalpium (Mont.) Henn.
Filoboletus pallescens (Boedijn) Maas
Geest.
Heimiomyces tenuipes (Schwein.) Singer
Mycena alphitophora (Berk.) Sacc.
Mycena antennae A.C. Cooper, Desjardin
& B.A. Perry
Mycena breviseta Höhnel
Mycena brunneoviolacea A.C. Cooper,
Desjardin & B.A. Perry
Mycena aff. discobasis Métrod
Mycena discogena Singer
Mycena galopus (Pers.) P. Kumm.
Laschia auriscalpium Mont.
Filoboletus pallescens
(Boedijn) Maas Geest.
Heimiomyces tenuipes
(Schwein.) Singer
Mycena alphitophora
(Berk.) Sacc.
Mycena antennae
A.C. Cooper, Desjardin &
B.A. Perry
Mycena breviseta Höhnel
Mycena brunneoviolacea
A.C. Cooper, Desjardin &
B.A. Perry
Mycena aff. discobasis
Métrod
Mycena discogena Singer
Mycena galopus (Pers.)
P. Kumm.
205
P
ST
X
Grace et al. (2019)
X
Grace et al. (2019)
X
Grace et al. (2019)
E
Grace et al. (2019)
E
Grace et al. (2019)
X
Grace et al. (2019)
X
X
Desjardin and Perry (2017)
X
Grace et al. (2019)
X
Grace et al. (2019)
X
Grace et al. (2019)
E
Grace et al. (2019)
X
Grace et al. (2019)
X
Grace et al. (2019)
X
Grace et al. (2019)
X
Winter (1886), Bresadola
and Roumeguère (1890)
Cooper et al. (2018)
X
X
Desjardin and Perry (2017)
X
Cooper et al. (2018)
X
Cooper et al. (2018)
E
Cooper et al. (2018)
Cooper et al. (2018)
X
E
Cooper et al. (2018)
Cooper et al. (2018)
Cooper et al. (2018)
X
X
X
(continued)
206
D. E. Desjardin and B. A. Perry
Currently accepted name
Name reported in literature
Citation
Mycena aff. holoporphyra (Berk. &
M.A. Curtis) Singer
Mycena lamprospora (Corner) E. Horak
Mycena aff. holoporphyra
(Berk. & M.A. Curtis) Singer
Mycena lamprospora (Corner) E. Horak
Mycena lasiopus Maas Geest.
& de Meijer
Mycena longinqua
A.C. Cooper, Desjardin &
B.A. Perry
Mycena oboensis
A.C. Cooper, Desjardin &
B.A. Perry
Mycena phaeonox
A.C. Cooper, Desjardin &
B.A. Perry
Agaricus roseus Schaeff.
Mycena solis A.C. Cooper,
Desjardin & B.A. Perry
Mycena tintinnabulum
(Paulet) Quél.
Cooper et al. (2018)
Mycena lasiopus Maas Geest. & de Meijer
Mycena longinqua A.C. Cooper,
Desjardin & B.A. Perry
Mycena oboensis A.C. Cooper, Desjardin
& B.A. Perry
Mycena phaeonox A.C. Cooper, Desjardin
& B.A. Perry
Mycena rosea Gramberg
Mycena solis A.C. Cooper, Desjardin &
B.A. Perry
Mycena tintinnabulum (Paulet) Quél.
Nidulariaceae
Cyathus limbatus Tul. & C. Tul.
Cyathus poeppigii Tul. & C. Tul.
Omphalotaceae
Gymnopus billbowesii Desjardin &
B.A. Perry
Gymnopus aff. brunneigracilis (Corner)
A.W. Wilson & Desjardin
Gymnopus cervinus (Henn.) Desjardin &
B.A. Perry
Gymnopus gibbosus (Corner)
A.W. Wilson, Desjardin & E. Horak
Gymnopus hirtelloides Desjardin &
B.A. Perry
Gymnopus hirtellus (Berk. & Broome)
Desjardin & B.A. Perry
Gymnopus irresolutus Desjardin &
B.A. Perry
Gymnopus melanopus A.W. Wilson,
Desjardin & E. Horak
Gymnopus mustachius Desjardin &
B.A. Perry
Gymnopus ocellus Desjardin & B.A. Perry
Gymnopus ocior (Pers.) Antonín &
Noordel.
Gymnopus pleurocystidiatus Desjardin &
B.A. Perry
P
ST
X
Cooper et al. (2018)
X
Cooper et al. (2018)
X
Cooper et al. (2018)
E
X
Cooper et al. (2018)
E
Cooper et al. (2018)
E
Coutinho (1925)
Cooper et al. (2018)
X
E
Bresadola and
Roumeguère (1890)
X
Cyathus limbatus Tul. &
C. Tul.
Cyathus poeppigii Tul. &
C. Tul.
Desjardin and Perry
(2015b)
Desjardin and Perry
(2015b)
X
Gymnopus billbowesii
Desjardin & B.A. Perry
Gymnopus aff.
brunneigracilis (Corner)
A.W. Wilson & Desjardin
Gymnopus cervinus (Henn.)
Desjardin & B.A. Perry
Gymnopus gibbosus (Corner)
A.W. Wilson, Desjardin &
E. Horak
Gymnopus hirtelloides
Desjardin & B.A. Perry
Gymnopus hirtellus (Berk. &
Broome) Desjardin &
B.A. Perry
Gymnopus irresolutus
Desjardin & B.A. Perry
Gymnopus melanopus
A.W. Wilson, Desjardin &
E. Horak
Gymnopus mustachius
Desjardin & B.A. Perry
Gymnopus ocellus Desjardin
& B.A. Perry
Agaricus xanthopus Fr.
Desjardin and Perry (2017)
X
Desjardin and Perry (2017)
X
Gymnopus pleurocystidiatus
Desjardin & B.A. Perry
X
Desjardin and Perry (2017)
X
Desjardin and Perry (2017)
X
X
Desjardin and Perry (2017)
E
Desjardin and Perry (2017)
X
Desjardin and Perry (2017)
E
Desjardin and Perry (2017)
X
Desjardin and Perry (2017)
E
Desjardin and Perry (2017)
E
Coutinho (1925)
X
Desjardin and Perry (2017)
E
(continued)
8
Fungi of São Tomé and Príncipe Islands: Basidiomycete Mushrooms and Allies
207
Currently accepted name
Name reported in literature
Citation
Gymnopus aff. polygrammus (Mont.)
J.L. Mata
Gymnopus quercophilus (Pouzar) Antonín
& Noordel.
Gymnopus rodhallii Desjardin &
B.A. Perry
Gymnopus ugandensis (Pegler) Desjardin
& B.A. Perry
Gymnopus aff. polygrammus
(Mont.) J.L. Mata
Marasmius splachnoides
(Hornem.) Fr.
Gymnopus rodhallii
Desjardin & B.A. Perry
Gymnopus ugandensis
(Pegler) Desjardin &
B.A. Perry
Marasmius amadelphus
(Bull.) Fr.
Desjardin and Perry (2017)
X
Bresadola and
Roumeguère (1890)
Desjardin and Perry (2017)
X
Marasmiellus ramealis (Bull.) Singer
Mycetinis ignobilis (Berk. & Broome)
Desjardin & B.A. Perry
Setulipes afibulatus Antonín
Physalacriaceae
Cyptotrama asprata (Berk.) Redhead &
Ginns
Pleurotaceae
Pleurotus tuber-regium (Fr.) Singer
Pluteaceae
Pluteus albidus Beeli
Pluteus albostipitatus (Dennis) Singer
Pluteus chrysaegis (Berk. & Broome)
Petch
Pluteus hirtellus Desjardin & B.A. Perry
Pluteus losulus Justo
Pluteus thomensis Desjardin & B.A. Perry
Psathyrellaceae
Candolleomyces albipes (Murrill)
Wächter & A. Melzer
Candolleomyces cacao (Desjardin &
B.A. Perry) Wächter & A. Melzer
Coprinellus aureogranulatus (Uljé &
Aptroot) Redhead, Vilgalys & Moncalvo
Coprinellus disseminatus (Pers.)
J.E. Lange
Coprinopsis afronivea Desjardin &
B.A. Perry
Coprinopsis cinerea (Schaeff.) Redhead,
Vilgalys & Moncalvo
Mycetinis ignobilis (Berk. &
Broome) Desjardin &
B.A. Perry
Setulipes afibulatus Antonín
P
E
ST
E
Desjardin and Perry (2017)
X
Bresadola and
Roumeguère (1890),
Coutinho (1925)
Desjardin and Perry (2017)
X
Desjardin and Perry (2017)
X
X
X
Cyptotrama asprata (Berk.)
Redhead & Ginns
Desjardin and Perry (2017)
Lentinus tuber-regium (Fr.)
Fr.
Lentinus descendens Afzel ex
Fr.
Coutinho (1925)
X
Bresadola and
Roumeguère (1890),
Coutinho (1925)
X
Pluteus albidus Beeli
Pluteus albostipitatus
(Dennis) Singer
Pluteus chrysaegis (Berk. &
Broome) Petch
Pluteus hirtellus Desjardin &
B.A. Perry
Pluteus losulus Justo
Pluteus thomensis Desjardin
& B.A. Perry
Desjardin and Perry (2018)
Desjardin and Perry (2018)
X
X
Desjardin and Perry (2018)
X
Desjardin and Perry (2018)
E
Psathyrella albipes (Murrill)
A.H. Sm.
Psathyrella cacao Desjardin
& B.A. Perry
Coprinellus aureogranulatus
(Uljé & Aptroot) Redhead,
Vilgalys & Moncalvo
Coprinellus disseminatus
(Pers.) J.E. Lange
Coprinarius disseminatus
(Pers.) P. Kumm.
Psathyrella disseminata
(Pers.) Quél.
Coprinopsis afronivea
Desjardin & B.A. Perry
Coprinus cinereus (Schaeff.)
Gray
Desjardin and Perry (2016)
X
Desjardin and Perry (2016)
E
Desjardin and Perry (2016)
X
Desjardin and Perry (2016)
X
Coutinho (1925)
X
Bresadola and
Roumeguère (1890)
Desjardin and Perry (2016)
X
Saccardo and Berlese
(1889)
X
Desjardin and Perry (2018)
Desjardin and Perry (2018)
X
X
E
E
(continued)
208
D. E. Desjardin and B. A. Perry
Currently accepted name
Name reported in literature
Citation
Psathyrella oboensis Desjardin &
B.A. Perry
Pterulaceae
Pterulicium xylogenum (Berk. & Broome)
Corner
Schizophyllaceae
Schizophyllum commune Fr.
Psathyrella oboensis
Desjardin & B.A. Perry
Desjardin and Perry (2016)
E
Pterula subaquatica Bres.
& Roum.
Bresadola and
Roumeguère (1890)
X
Schizophyllum commune Fr.
Schizophyllum commune var.
multifidum (Batsch) Cooke
Schizophyllum alneum (L.)
J. Schröt.
Winter (1886)
Bresadola and
Roumeguère (1890)
Coutinho (1925)
X
X
X
Deconica overeemii
(E. Horak & Desjardin)
Desjardin & B.A. Perry
Deconica protea (Kalchbr.)
Desjardin & B.A. Perry
Hypholoma aff. subviride
(Berk. & M.A. Curtis) Dennis
Desjardin and Perry (2016)
X
Desjardin and Perry (2016)
X
Desjardin and Perry (2016)
X
Tricholomopsis aurea (Beeli)
Desjardin & B.A. Perry
Desjardin and Perry (2017)
X
Scleroderma dictyosporum
Pat.
Desjardin and Perry
(2015b)
ORDER STEREOPSIDALES
Stereopsidaceae
Stereopsis radicans (Berk.) D.A. Reid
Thelephora radicans Berk.
Bresadola and
Roumeguère (1890),
Coutinho (1925)
X
ORDER POLYPORALES
Cerrenaceae
Cerrena hydnoides (Sw.) Zmitr.
Trametes hydnoides (Sw.) Fr.
Bresadola and
Roumeguère (1890)
X
Trametes sepium Berk.
Daedalea newtonii Bres.
& Roum.
Coutinho (1925)
Bresadola and
Roumeguère (1890),
Coutinho (1925)
Bresadola and
Roumeguère (1890)
Bresadola and
Roumeguère (1890)
Strophariaceae
Deconica overeemii (E. Horak &
Desjardin) Desjardin & B.A. Perry
Deconica protea (Kalchbr.) Desjardin &
B.A. Perry
Hypholoma aff. subviride (Berk. &
M.A. Curtis) Dennis
Tricholomataceae s.l.
Tricholomopsis aurea (Beeli) Desjardin &
B.A. Perry
ORDER BOLETALES
Sclerodermataceae
Scleroderma dictyosporum Pat.
Fomitopsidaceae
Antrodia albida (Fr.) Donk
Daedalea newtonii Bres. & Roum.
Daedalea quercina (L.) Pers.
Daedalea quercina (L.) Pers.
Ranadivia modesta (Kunze ex Fr.) Zmitr.
Polyporus atypus Lév.
Incrustoporiaceae
Tyromyces albogilvus (Berk. &
M.A. Curtis) Murrill
Tyromyces squamulosus (Bres.) Ryvarden
Irpicaceae
Flavodon flavus (Klotzsch) Ryvarden
Polyporus albogilvus Berk. &
M.A. Curtis
Polyporus squamosus Bres.
Winter (1886), Coutinho
(1925)
Bresadola (1890)
Irpex flavus Klotzsch
Bresadola and
Roumeguère (1890),
Coutinho (1925)
P
ST
X
E
X
E
X
X
X
E
X
(continued)
8
Fungi of São Tomé and Príncipe Islands: Basidiomycete Mushrooms and Allies
209
Currently accepted name
Name reported in literature
Citation
Meripilaceae
Rigidoporus lineatus (Pers.) Ryvarden
Polyporus zonalis Berk.
Rigidoporus microporus (Sw.) Overeem
Polyporus auberianus Mont.
Bresadola and
Roumeguère (1890),
Coutinho (1925)
Winter (1886), Bresadola
and Roumeguère (1890),
Coutinho (1925)
Meruliaceae
Steccherinum rawakense (Pers.) Banker
Hydnum rawakense Pers.
Saccardo and Berlese
(1889)
X
Polyporus adusta (Willd.) Fr.
Polyporus imberbis (Bull.)
Fr.
Stereum spadiceum var.
venosum Quél.
Corticium caeruleum
(Schrad. ex Lam.) Fr.
Bresadola (1890)
Bresadola (1890)
X
X
Bresadola and
Roumeguère (1890)
Bresadola and
Roumeguère (1890)
X
Stereum involutum Klotzsch
ex Fr.
Stereum pulchellum Sacc.
& Berl.
Bresadola and
Roumeguère (1890)
Saccardo and Berlese
(1889)
Lentinus sprucei
(Berk.) Cout.
Panus sprucei Berk.
Coutinho (1925)
X
Bresadola and
Roumeguère (1890)
Bresadola and
Roumeguère (1890)
Coutinho (1925)
X
Phanerochaetaceae
Bjerkandera adusta (Pers.) P. Karst.
Bjerkandera fumosa (Pers.) P. Karst.
Porostereum spadiceum (Pers.) Hjortstam
& Ryvarden
Terana caerulea (Schrad. ex Lam.)
Kuntze
Podoscyphaceae
Podoscypha involuta (Klotzsch ex Fr.)
Imazeki
Polyporaceae
Asterotus dealbatus (Berk.) Singer
Coriolopsis badia (Berk.) Murrill
Trametes badia Berk.
Coriolopsis occidentalis (Klotzsch)
Murrill
Coriolus sprucei (Berk.) G. Cunn.
Earliella scabrosa (Pers.) Gilb. &
Ryvarden
Polystictus occidentalis
(Klotzsch) Sacc.
Trametes sprucei Berk.
Trametes sanguinea
(Klotzsch) Pat.
Daedalea sanguinea
Klotzsch
Favolus multiplex Lév.
Favolus grammocephalus (Berk.) Imazeki
Favolus jacobeus Sacc. & Berl.
Favolus platyporus Berk. & M.A. Curtis
Favolus tenuiculus P. Beauv.
Fomes amboinensis (Lam.) Cooke
Polyporus
grammocephalus Berk.
Favolus jacobeus Sacc.
& Berl.
Favolus platyporus Berk. &
M.A. Curtis
Favolus tesselatus Mont.
Hexagonia tenuicola
(P. Beauv.)
Favolus brasiliensis (Fr.) Fr.
Fomes amboinensis (Lam.)
Cooke
P
ST
X
X
X
X
X
X
X
Coutinho (1925)
Coutinho (1925)
X
X
Winter (1886)
X
Bresadola and
Roumeguère (1890),
Coutinho (1925)
Winter (1886)
X
Saccardo and Berlese
(1889), Bresadola and
Roumeguère (1890)
Bresadola and
Roumeguère (1890)
Coutinho (1925)
Bresadola and
Roumeguère (1890)
Bresadola (1891)
Coutinho (1925)
X
E
E
X
X
X
X
X
(continued)
210
D. E. Desjardin and B. A. Perry
Currently accepted name
Name reported in literature
Citation
Fomes ferrugineobrunneus Cout.
Fomes
ferrugineobrunneus Cout.
Ganoderma fulvellum Bres.
Coutinho (1925)
E
Bresadola and
Roumeguère (1890)
Winter (1886)
X
Fomes fulvellus (Bres.) Sacc.
Funalia caperata (Berk.) Zmitr. &
Malysheva
Ganoderma amboinense (Lam.) Pat.
Ganoderma applanatum (Pers.) Pat.
Ganoderma australe (Fr.) Pat.
Ganoderma lucidum (Curtis) P. Karst.
Ganoderma multiplicatum (Mont.) Pat.
Ganoderma ochrolaccatum (Mont.) Pat.
Ganoderma oerstedii (Fr.) Torrend
Hexagonia cucullata (Mont.) Murrill
Polyporus caperatus Berk.
Ganoderma amboinense
(Lam.) Pat.
Fomes applanatus (Pers.) Fr.
Ganoderma australe (Fr.)
Pat.
Polyporus australis Fr.
Ganoderma lucidum (Curtis)
P. Karst.
Fomes lucidus (Curtis) Sacc.
Polyporus lucidus (Curtis) Fr.
Ganoderma multiplicatum
(Mont.) Pat.
Fomes multiplicatus
(Mont.) Sacc.
Ganoderma ochrolaccatum
(Mont.) Pat.
Fomes ochrolaccatus (Mont.)
Pat.
Fomes oerstedii (Fr.) Cooke
Favolus cucullatus Mont.
Hexagonia purpurascens (Berk. &
M.A. Curtis) Murrill
Leiotrametes menziesii (Berk.) Welti &
Courtec.
Favolus purpurascens Berk.
& M.A. Curtis
Polystictus kurzianus Cooke
Lentinus striatulus Lév.
Lentinus thomensis Cout.
Lentinus villosus Klotzsch
Lentinus flaccidus Fr.
Lentinus thomensis Cout.
Lentinus villosus Klotzsch
Lenzites applanatus (Klotzsch) Fr.
Lenzites applanatus
(Klotzsch) Fr.
Lenzites asperus (Klotzsch) Fr.
Lenzites asperus (Klotzsch)
Fr.
Lenzites deplanatus Fr.
Lenzites repandus Fr.
Lenzites deplanatus Fr.
Lenzites repandus Fr.
Lopharia cinerascens (Schwein.)
G. Cunn.
Microporus affinis (Blume & T. Nees)
Kuntze
Lopharia lirellosa Kalchbr. &
MacOwen
Polystictus affinis (Blume &
T. Nees) Fr.
Polyporus flabelliformis
Klotzsch
Polystictus flabelliformis Fr.
P
ST
X
X
Bresadola and
Roumeguère (1890)
Coutinho (1925)
Bresadola and
Roumeguère (1890)
Winter (1886)
Bresadola and
Roumeguère (1890)
Coutinho (1925)
Winter (1886)
Bresadola and
Roumeguère (1890)
Coutinho (1925)
X
X
X
X
X
X
X
X
Bresadola and
Roumeguère (1890)
Coutinho (1925)
X
Coutinho (1925)
Bresadola and
Roumeguère (1890)
Winter (1886)
X
X
Bresadola and
Roumeguère (1890),
Coutinho (1925)
Fries (1851)
Coutinho (1925)
Winter (1886), Bresadola
and Roumeguère (1890)
Bresadola and
Roumeguère (1890),
Coutinho (1925)
Winter (1886), Bresadola
and Roumeguère (1890),
Coutinho (1925)
Winter (1886)
Winter (1886), Coutinho
(1925)
Coutinho (1925)
X
X
X
X
X
E
X
X
X
X
X
X
Roumeguère (1889)
X
Winter (1886)
X
Bresadola and
Roumeguère (1890),
Coutinho (1925)
X
(continued)
8
Fungi of São Tomé and Príncipe Islands: Basidiomycete Mushrooms and Allies
Currently accepted name
Microporus xanthopus (Fr.) Kuntze
Panus neostrigosus Drechsler-Santos &
Wartchow
Perenniporia ohiensis (Berk.) Ryvarden
Polyporus amboinensis Fr.
Polyporus dictyopus Mont.
Polyporus philippinensis Berk.
Polyporus rugulosus Lév.
Polyporus torquescens Sacc. & Berl.
Polyporus venezuelae Berk. &
M.A. Curtis ex Cooke
Pseudofavolus polygrammus (Mont.)
G. Cunn.
Pycnoporus sanguineus (L.) Murrill
Szczepkamyces campestris (Quél.) Zmitr.
Name reported in literature
Citation
P
Polystictus carneoniger
(Berk. ex Cooke) Cooke
Polystictus xanthopus (Fr.)
Fr.
Bresadola and
Roumeguère (1890)
Saccardo and Berlese
(1889), Bresadola and
Roumeguère (1890)
Bresadola and
Roumeguère (1890)
Coutinho (1925)
Winter (1886)
Bresadola and
Roumeguère (1890)
Coutinho (1925)
X
Lentinus strigosus Fr.
Trametes ohiensis Berk.
Polyporus amboinensis Fr.
Polyporus dictyopus Mont.
Favolus philippinensis
(Berk.) Sacc.
Polyporus rugulosus Lév.
Polyporus torquescens Sacc.
& Berl.
Polyporus venezuelae Berk.
& M.A. Curtis ex Cooke
Hexagonia polygramma
(Mont.) Fr.
Polystictus sanguineus (L.)
G. Mey.
Trametes campestris Quél.
Trametes cubensis (Mont.) Sacc.
Trametes cubensis
(Mont.) Sacc.
Trametes discolor Sacc. & Berl.
Trametes discolor Sacc.
& Berl.
Trametes gibbosa (Pers.) Fr.
Polystictus hirsutus (Wulfen)
Fr.
Trametes gibbosa (Pers.) Fr.
Trametes hirsuta (Wulfen) Lloyd
Trametes meyenii (Klotzsch) Lloyd
Trametes pubescens (Schumach.) Pilát
Daedalea ochracea Kalchbr.
Polystictus velutinus
(Pers.) Sacc.
Trametes strumosa (Fr.) Zmitr., Wasser &
Ezhov
Trametes versicolor (L.) Lloyd
Polyporus strumosus Fr.
Trametes villosa (Sw.) Kreisel
Truncospora oboensis Decock
Polystictus pinsitus (Fr.) Fr.
Truncospora oboensis
Decock
Xenasmataceae
Xenasmatella vaga (Fr.) Stalpers
ORDER THELEPHORALES
Bankeraceae
Phaeodon thomensis Cout.
ORDER RUSSULALES
211
Polysticus versicolor (L.) Fr.
ST
X
X
X
X
X
X
X
Bresadola and
Roumeguère (1890),
Coutinho (1925)
Saccardo and Berlese
(1889)
Winter (1886)
X
Winter (1886)
X
Coutinho (1925)
X
Bresadola and
Roumeguère (1890)
Bresadola and
Roumeguère (1890),
Coutinho (1925)
Saccardo and Berlese
(1889)
Coutinho (1925)
Bresadola and
Roumeguère (1890),
Coutinho (1925)
Coutinho (1925)
Saccardo and Berlese
(1889), Bresadola and
Roumeguère (1890),
Coutinho (1925)
Coutinho (1925)
X
E
X
E
X
X
X
X
X
X
Bresadola and
Roumeguère (1890)
Fries (1851)
Decock (2011)
X
E
Phlebia vaga Fr.
Coutinho (1925)
X
Phaeodon thomensis Cout.
Coutinho (1925)
E
(continued)
212
Currently accepted name
Auriscalpiaceae
Lentinellus cochleatus (Pers.) P. Karst
Lentinellus flabelliformis (Bolton) S. Ito
Hericiaceae
Laxitextum bicolor (Pers.) Lentz
Peniophoraceae
Scytinostroma duriusculum (Berk. &
Broome) Donk
Scytinostroma quintasianum (Bres. &
Roum.) Nakasone
Stereaceae
Stereum amphirhytes Sacc. & Berl.
Stereum bellum (Kunze) Sacc.
Stereum hirsutum (Willd.) Pers.
Stereum kalchbrenneri Sacc.
D. E. Desjardin and B. A. Perry
Name reported in literature
Citation
Lentinus cochleatus var.
occidentalis (Pers.) Fr.
Lentinus flabelliformis (Bolton) Fr.
Fries (1851)
X
Coutinho (1925)
X
Stereum bicolor (Pers.) Fr.
Bresadola and
Roumeguère (1890)
X
Stereum duriusculum Berk. &
Broome
Corticium quintasianum
Bres. & Roum.
Bresadola and
Roumeguère (1890)
Bresadola and
Roumeguère (1890)
X
Stereum amphirhytes Sacc.
& Berl.
Saccardo and Berlese
(1889), Roumeguère
(1889)
Winter (1886), Bresadola
and Roumeguère (1890)
Bresadola and
Roumeguère (1890)
Saccardo and Berlese
(1889), Bresadola and
Roumeguère (1890)
Winter (1886), Bresadola
and Roumeguère (1890),
Coutinho (1925)
Bresadola and
Roumeguère (1890)
Winter (1886), Bresadola
and Roumeguère (1890),
Coutinho (1925)
Winter (1886)
Winter (1886), Bresadola
and Roumeguère (1890)
Stereum bellum
(Kunze) Sacc.
Stereum hirsutum
(Willd.) Pers.
Stereum kalchbrenneri Sacc.
Stereum lobatum (Kunze ex Fr.) Fr.
Stereum lobatum (Kunze ex
Fr.) Fr.
Stereum obliquum Mont. & Berk.
Stereum obliquum Mont.
& Berk.
Stereum fasciatum (Schwein.)
Fr.
Stereum ostrea (Blume & T. Nees) Fr.
Stereum versicolor (Sw.) Fr.
Xylobolus subpileatus (Berk. &
M.A. Curtis) Boidin
ORDER HYMENOCHAETALES
Hymenochaetaceae
Coltricia oboensis Decock
Fuscoporia ferruginosa (Schrad.) Murrill
Stereum versicolor (Sw.) Fr.
Stereum subpileatum Berk. &
M.A. Curtis
Coltricia oboensis Decock
Poria ferruginosa (Schrad.)
P. Karst.
Fuscoporia senex (Nees & Mont.) Gohb.Nejh.
Fomes senex (Nees & Mont.)
Cooke
Hydnoporia tabacina (Sowerby) Spirin,
Miettinen & K.H. Larss.
Hymenochaete damicornis (Link) Lév.
Hymenochaete tabacina
(Sowerby) Lév.
Hymenochaete damicornis
(Link) Lév.
Hymenochaete
tenuissima Berk.
Polystictus sideroides (Lév.)
Cooke
Polyporus gilvus (Schwein.)
Fr.
Hymenochaete tenuissima Berk.
Inonotus sideroides (Lév.) Ryvarden
Phellinus gilvus (Schwein.) Pat.
Decock (2013)
Bresadola and
Roumeguère (1890),
Coutinho (1925)
Bresadola and
Roumeguère (1890),
Coutinho (1925)
Bresadola and
Roumeguère (1890)
Bresadola and
Roumeguère (1890)
Bresadola and
Roumeguère (1890)
Coutinho (1925)
Roumeguère (1889),
Saccardo and Berlese
P
ST
E
E
X
X
X
X
X
X
X
X
X
E
X
X
X
X
X
X
X
(continued)
8
Fungi of São Tomé and Príncipe Islands: Basidiomycete Mushrooms and Allies
Currently accepted name
Name reported in literature
Polyporus gilvus var.
scruposus (Fr.) Henn.
Polyporus scruposus Fr.
Polyporus scruposus var.
isidioides (Berk.) Cooke
Polyporus licnoides Mont.
Phellinus igniarius (L.) Quél.
Polyporus igniarius (L.) Fr.
Fomes igniarius (L.) Fr.
Phylloporia pectinata (Klotzsch)
Ryvarden
Fomes pectinatus (Klotzsch)
Gillet
Polystictus albidocinereus Cout.
Polystictus
albidocinereus Cout.
Polyporus
russogramme Berk.
Polystictus russogramme (Berk.) Cooke
Rickenellaceae
Cotylidia aurantiaca (Pat.) A.L. Welden
Thelephora aurantiaca Pers.
Thelephora affinis Berk. &
M.A. Curtis
ORDER PHALLALES
Phallaceae
Blumenavia angolensis (Welw. & Curr.)
Dring
Clathrus parvulus Bres. & Roum.
Mutinus bambusinus (Zoll.) E. Fisch.
Mutinus zenkeri (Henn.) E. Fisch.
Phallus drewesii Desjardin & B.A. Perry
Blumenavia angolensis
(Welw. & Curr.) Dring
Clathrus parvulus Bres.
& Roum.
Mutinus bambusinus (Zoll.)
E. Fisch.
Mutinus zenkeri (Henn.)
E. Fisch.
213
Citation
P
(1889), Bresadola and
Roumeguère (1890)
Bresadola and
Roumeguère (1890)
Winter (1886)
Winter (1886)
ST
X
X
X
Bresadola and
Roumeguère (1890)
Winter (1886)
Bresadola and
Roumeguère (1890),
Coutinho (1925)
Bresadola and
Roumeguère (1890),
Coutinho (1925)
Coutinho (1925)
X
X
X
X
E
Winter (1886)
X
Bresadola and
Roumeguère (1890)
Winter (1886)
X
X
Degreef et al. (2013),
Desjardin and Perry
(2015b)
Bresadola and
Roumeguère (1890)
Desjardin and Perry
(2015b)
Degreef et al. (2013),
Desjardin and Perry
(2015b)
Desjardin and Perry (2009)
Phallus indusiatus Vent.
Phallus drewesii Desjardin &
B.A. Perry
Phallus indusiatus Vent.
ORDER GOMPHALES
Gomphaceae
Ramaria henriquesii (Bres. & Roum.)
Corner
Ramaria molleariana (Bres. & Roum.)
Corner
Ramaria polypus Corner
Clavaria henriquesii Bres.
& Roum.
Lachnocladium mollerianum
Bres. & Roum.
Ramaria polypus Corner
Bresadola and
Roumeguère (1890)
Bresadola and
Roumeguère (1890)
Desjardin and Perry
(2015b)
ORDER GEASTRALES
Geastraceae
Geastrum fimbriatum Fr.
Geastrum fimbriatum Fr.
Desjardin and Perry
(2015b)
Desjardin and Perry
(2015b)
X
E
X
X
X
E
X
X
X
X
X
(continued)
214
D. E. Desjardin and B. A. Perry
Currently accepted name
Name reported in literature
Citation
P
ST
Geastrum schweinitzii (Berk. &
M.A. Curtis) Zeller
Geastrum velutinum Morgan
Geastrum schweinitzii (Berk.
& M.A. Curtis) Zeller
Geastrum velutinum Morgan
Desjardin and Perry
(2015b)
Desjardin and Perry
(2015b)
X
X
Scytinopogon havencampii
Desjardin & B.A. Perry
Desjardin and Perry
(2015a)
E
Auricularia auricula-judae
(Bull.) Quél.
Hirneola auricula-judae
(Bull.) Berk.
Laschia tremellosa Fr.
Auricularia fuscosuccinea
(Mont.) Henn.
Hirneola fuscosuccinea
(Mont.) Sacc.
Auricularia polytricha
(Mont.) Sacc.
Hirneola polytricha (Mont.)
Fr.
Coutinho (1925)
X
Bresadola (1891)
X
Winter (1886)
Coutinho (1925)
X
X
Bresadola and
Roumeguère (1890)
Coutinho (1925)
X
Bresadola and
Roumeguère (1890)
X
ORDER TRECHISPORALES
Hydnodontaceae
Trechispora havencampii (Desjardin &
B.A. Perry) Meiras-Ottoni & Gibertoni
ORDER AURICULARIALES
Auriculariaceae
Auricularia auricula-judae (Bull.) Quél.
Auricularia fuscosuccinea (Mont.) Henn.
Auricularia nigricans (Sw.) Birkebak,
Looney & Sánchez-García
ORDER CANTHARELLALES
Aphelariaceae
Aphelaria subglobispora P. Roberts
Cantharellaceae
Pseudocraterellus undulatus (Pers.)
Rauschert
Hydnaceae
Clavulina vanderystii (Bres.) Corner
Aphelaria subglobispora
P. Roberts
Desjardin and Perry
(2015b)
Craterellus crispus
(Bull.) Berk.
Bresadola (1891)
Clavulina vanderystii (Bres.)
Corner
INCERTAE SEDIS—insufficient data, problematic nomenclature
Agaricus (Collybia) diffractus Cout. nom. Competing epithet; not
illeg.
treated since publication
Agaricus (Galera) macromastes Fr.
Not treated since publication
Agaricus (Mycena) rufescens Cout. nom.
illeg.
Agaricus (Naucoria) papularis Fr.
Competing epithet; not
treated since publication
Not treated since publication
Panus troglodytes Fr.
Polystictus affinis var. cyathoidea Sacc.
& Berl.
Not treated since publication
Not treated since publication
Polystictus mollerianus Sacc., Berl.
& Roum.
Not treated since publication
Desjardin and Perry
(2015b)
X
X
X
X
X
Coutinho (1925)
E
Fries (1851) (see Desjardin
and Perry (2016))
Coutinho (1925) (see
Cooper et al. (2018))
Fries (1851) (see Desjardin
and Perry (2016))
Fries (1851)
Saccardo and Berlese
(1889), Roumeguère
(1889)
Saccardo and Berlese
(1889)
E
E
E
E
E
E
8
Fungi of São Tomé and Príncipe Islands: Basidiomycete Mushrooms and Allies
215
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Open Access This chapter is licensed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits use, sharing,
adaptation, distribution and reproduction in any medium or format, as long as you give appropriate
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statutory regulation or exceeds the permitted use, you will need to obtain permission directly from
the copyright holder.
Chapter 9
The Bryophyte Flora of São Tomé
and Príncipe (Gulf of Guinea): Past, Present
and Future
César Garcia, Cecília Sérgio, and James R. Shevock
Abstract This chapter aims to present a review of the knowledge of the bryological
flora for the São Tomé and Príncipe Islands (Gulf of Guinea). An updated catalogue
is presented, as well as a brief overview of the first expeditions conducted by the
University of Coimbra. The labels of the historical herbarium collections and
correspondence were analyzed, which provides an important source of data contributing toward research in taxonomy and conservation of these oceanic islands. Since
2007, exploratory fieldwork was carried out in different habitats of this archipelago
along an altitudinal gradient, aiming to improve the knowledge of the ecology and
distribution patterns of its bryophyte flora. A total of 304 taxa of bryophytes
(133 mosses, 164 liverworts and seven hornworts) are currently reported, of which
21 are endemic to São Tomé and Príncipe and 144 species are shared endemics with
the African continent. Several vouchers, especially in the herbaria of the University
of Lisbon and of the California Academy of Sciences, are still under study and will
likely provide further insights and new discoveries.
Keywords Africa · Biodiversity · Bryophytes · Conservation · Expeditions ·
Herbaria
Introduction
Bryophytes are a group of land plants that includes mosses, liverworts, and hornworts, and with over 20,000 described species, they are the second most speciose
group of higher plants, after angiosperms (Patiño and Vanderpoorten 2018; Song
C. Garcia (*) · C. Sérgio
Museu Nacional de História Natural e da Ciência, Universidade de Lisboa, Lisbon, Portugal
Centre for Ecology, Evolution and Environmental Changes (cE3c), CHANGE Associated
Laboratory - Global Change and Sustainability Institute, Faculdade de Ciências, Universidade
de Lisboa, Lisbon, Portugal
e-mail: cgarcia@fc.ul.pt
J. R. Shevock
California Academy of Sciences, Department of Botany, San Francisco, USA
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_9
217
218
C. Garcia et al.
et al. 2021). Bryophytes are a common component of tropical forests and provide
important ecosystem functions. In tropical regions during rainstorms numerous
bryophyte species can quickly absorb (and retain) many times their dry weight in
water. The absorbed water is then slowly released over time back into the environment, thereby reducing the erosive effects of heavy rain and allowing other plants
and animals to benefit from the rain and the humid environment for a longer period
(Pócs 1982). Bryophytes are widely distributed in terrestrial ecosystems (St Martin
and Mallik 2017), and islands provide an exceptional natural laboratory for ecological and evolutionary research in this group of terrestrial plants that is often poorly
studied. Oceanic tropical islands usually host amazing bryophyte diversity, including endemic species, especially in the montane forests favoured by ideal climatic
conditions, such as frequent rainfall and permanent fog (Ah-Peng et al. 2012).
The first known bryophyte collections of São Tomé and Príncipe were made by
Friedrich Welwitsch (1806–1872) in 1853 and 1860, as part of the expeditions
supported by the Portuguese government to Angola (Dolezal 1974), followed by
Charles Barter (1821–1859) and Gustav Mann (1836–1916), botanists with special
interest in vascular flora (Sérgio and Garcia 2011). One of the greatest Portuguese
mentors of Botany in Africa was Júlio Augusto Henriques (1838–1928) and he
outlined a plan for studying the flora of São Tomé and Príncipe (Coutinho 1929–30).
Throughout his life, Henriques remained deeply invested in understanding the
botanical diversity of the archipelago, which motivated his tireless research as
professor and director of the Botanical Garden of the University of Coimbra for
more than 50 years. His initial interest in the botanical study of São Tomé and
Príncipe was likely related to cultivation of the Cinchona tree (Chinchona spp.) and
other medicinal plants at the Coimbra Botanical Garden (Perpétuo et al. 2012). At
the age of 65, Henriques led an expedition to the island of São Tomé to study the
island’s flora, departing from Lisbon on June 23, 1903. The research based on this
visit culminated in an important publication (Henriques 1917). During his stay in the
archipelago, Henriques was received by the owners of many farms (roças), taking
notes and obtaining important data on the natural history of the island. Fernandes
(1980, 1986) noted that when Henriques planned the study of the flora of São Tomé
and Príncipe in the 1880s, he implemented a set of measures that proved to be
extremely important for the enrichment of the University of Coimbra herbarium
(currently, Herbário do Instituto Botânico de Coimbra, Coimbra, Portugal - COI).
First, he promoted and intensified the development of the Coimbra herbarium and
trained qualified botany specialists. It was to this end that he appointed Adolpho
Frederico Möller (1842–1920), a renowned collector of flora in Portugal and later in
São Tomé and Príncipe (four months in 1885), and in turn Francisco Joaquim Dias
Quintas (1864–1909) in botanical field studies in São Tomé and Príncipe. Second,
Henriques sent material collected on these expeditions to the greatest bryologists at
the time. Their results were published in the “Boletim da Sociedade Broteriana”, a
scientific journal dedicated to Botany and co-published by the University of Coimbra and the Broterian Society (Sociedade Broteriana).
9
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Herbarium Specimens and Associated Documentation
Numerous naturalists passing through or purposefully visiting São Tomé and
Príncipe gathered biological collections, some of which were then published in
different scientific outlets. The Austrian naturalist and explorer Friedrich Welwitsch
visited São Tomé in 1853 and 1860, during stopovers at the beginning and end of his
botanical survey of Angola (Sérgio and Garcia 2011). The major scientific expeditions during the nineteenth century were performed by Adolpho Möller in 1885
(Henriques 1917; Sérgio and Garcia 2011), Francisco Quintas from 1888 to 1889,
and Francisco Newton (1864–1909) between 1885 and 1895 (Sérgio and Garcia
2011). Casual collections were made by different naturalists, for example, the French
botanist Auguste Jean Baptiste Chevalier (1873–1956) in 1905 (Exell 1944).
In all these field studies, botanical collections were organized, and duplicates
were distributed to different herbaria. These included COI, and the herbaria of the
Museu Nacional de História Natural e da Ciência da Universidade de Lisboa,
Lisbon, Portugal (LISU), of the Natural History Museum, London, United Kingdom
(BM), of the Muséum National d’Histoire Naturelle de Paris, France (PC), of the
Instituto de Investigação Científica Tropical - ULisboa (LISC), and of the Conservatoire et Jardin botaniques de la Ville de Genève, Geneve Switzerland (G), and the
Brotherus Herbarium (H-BR) of the Finnish Museum of Natural History University
of Helsinki, Finland (H) (Herbaria acronyms according to Thiers 2016). The original
herbarium collections, details presented in field notes, draft descriptions of species,
and the extensive correspondence between the collectors and the specialists that
studied the biological material are a valuable source of data and a base for modern
studies regarding São Tomé and Príncipe flora.
Presently, COI and LISU herbaria hold most of the bryophyte specimens cited in
the bibliography for São Tomé and Príncipe, corresponding mostly to the collections
of Friedrich Welwitsch, Möller, Quintas and Newton, in addition to the smaller
collections of Júlio Henriques. However, duplicates of these collections are also
found in other European herbaria (Sérgio and Garcia 2011). The bryological collections resulting from the expeditions organized by Júlio Henriques were studied by
several experts. The liverworts were sent to Franz Stephani (1842–1927) between
1886 and 1913. The mosses were first sent to Carl Müller (1818–1889) in Halle
(between 1885 and 1887) and later to Viktor Ferdinand Brotherus (1849–1929) in
Helsinki (between 1889 and 1904). The letters that Henriques sent to Stephani and
Brotherus (Biblioteca Digital de Botânica da Universidade de Coimbra 2021) list all
the specimens exchanged. Thus, specimens originating from these collections were
progressively divvied up and disseminated by several international herbaria at the
discretion of the authors who studied them.
In this study, by cross-checking the LISU database referring to the aforementioned studied herbaria, we were able to confirm where the reference material and
most of the respective nomenclatural types are currently located (Sérgio and Garcia
2011). Additionally, we also gathered and compared all available information on
220
C. Garcia et al.
Fig. 9.1 Two specimens (1, 2) of Bryum coronatum Schwägr., corresponding to the same
Welwitsch specimen (n 126, Insula de S. Thomé loco called Monte Caffé) collected in December
1860, and (3, 4) Sendtnera mollis Steph. Typus, Slopes of Pico de São Tomé, 1500-2100 m, 1885,
Adolpho Möller 23. (1) At BM herbarium with “Inter Angolense” labels, with original iconography;
(2) At LISU herbarium without iconography but with a handwritten label by Welwitsch; (3) At COI
herbarium with the Möller label; (4) At BM herbarium (BM000745048) of Stephani’s herbarium
and handwritten data by the same author
where the voucher specimens from São Tomé and Príncipe are currently housed
(e.g., Figs. 9.1 and 9.2).
Most of the material of each specimen in the COI herbarium is abundant and
generally corresponds to isotypes found also in BM, G, H or PC. The labels in COI
are generally not the original and must have been written by Möller or Quintas
(Fig. 9.2), who organized the collections, with many duplicates sent to other
herbaria. Arthur Wallis Exell (1901–1993) first landed on São Tomé Island in
October 1932 to initiate a botanical expedition of the islands of the Gulf of Guinea
(e.g., Fig. 9.3.1–2). He visited the four principal islands (São Tomé, Príncipe, Bioko
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Fig. 9.2 Brotherus specimen identifications. Two specimens of Ectropothecium drepanophyllum
corresponding to the same specimen from Quintas, n 23: (1) Holotypus in H herbarium
(H-BR1415–022) with Brotherus handwriting; (2) Isotypus in COI herbarium with a handwritten
label from Quintas
and Annobón), and the results of this expedition were published in 1944, in the
Catalogue of the Vascular Plants of São Tomé (Exell 1944).
There are also numerous other specimens with labels based on the printed text of
the work published by Carl Müller (1886a), such as the mosses collected by Adolpho
Frederico Möller in 1885 and published in the Boletim da Sociedade Broteriana. We
also verified the presence of specimens with original handwritten labels by Stephani
and Brotherus in COI herbarium collections (Fig. 9.3.3–4), although some labels
have two handwritings with the numbering of localities corresponding to Adolpho
Möller manuscripts and the identifications handwritten by Stephani (Figs. 9.3.3–4
and 9.4) or Carl Müller.
The historical specimens from São Tomé and Príncipe archived in the Stephani
collection in the herbarium of Genève (G) (Geissler 1982) have duplicates at COI.
However, some taxa collected by Newton and Quintas were not returned to Coimbra,
at least those studied after 1900. These correspond to the specimen references
indicated in the most recent volumes of the Index Hepaticarum (Stephani
1901–1906, 1905–1909, 1909–1912, 1912–1917, 1917–1925). Likewise, there are
a considerable number of specimens collected during Júlio Henriques career in the
herbarium of Paris (PC), either included in the collections of Jules Cardot
(1860–1934), Ferdinand Renauld (1837–1910) or Robert Potier de La Varde
(1878–1961), that are often cited in revisionary studies of bryophyte genera.
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C. Garcia et al.
Fig. 9.3 Arthur Exell (1, 2) and Francisco Quintas specimens (3, 4). (1) Octoblepharum albidum,
Esperança, circa 350 ft., 1932, Exell 675 in the herbarium of Coimbra (COI); (2) Hygrolejeunea
pulcherrima, Santa Maria, circa 4200 ft., 1932, Exell 197 in the London (BM) collections; (3)
Isotypus of Metzgeria thomeensis (BM); (4) The same material in COI, isotypes. Both labels (3, 4)
correspond to Stephani’s manuscripts
At the Helsinki herbarium (H), a significant part of material from São Tomé was
found in the Brotherus (H–BR) collections, particularly type specimens collected in
this archipelago (Sérgio and Garcia 2011), corresponding almost exclusively to
Quintas and Möller collections. However, some of the specimens originally studied
by Brotherus are now at BM, PC or COI herbaria and were not found at H herbarium
(e.g., Leucobryum homalophyllum Broth.). It should be noted that, contrary to
Stephani, Brotherus returned all the material he studied to Coimbra, mostly with
handwritten labels.
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Fig. 9.4 (1) Original description of Lejeunea ramosissima Steph. included in the archives of the
Botanical Institute of Coimbra Library as part of the letter dated 25 February 1886, and (2)
Iconography of several species, including L. ramosissima Steph. (33 and 34) and Sendtneria mollis
Steph. (22 and 23) by Stephani (1886)
Historical Correspondence
The correspondence between naturalists who studied bryophyte specimens collected
by Möller, Quintas and Newton, is largely housed in the archives of the University of
Coimbra at present. The documentation referring to Welwitsch’s correspondence,
currently in Lisbon at the Museu Nacional de História Natural e da Ciência
(MUHNAC) of the University of Lisbon, does not provide any mention of bryophytes, despite the existence of bryophyte herbarium specimens of Welwitsch’s
expeditions in LISU herbarium (MUHNAC). Among this documentation are lists
of the identified species and, in some cases, the original descriptions of species are
also included.
Although it was not possible to study all Júlio Henriques’ correspondence in
some foreign institutions (except for the one in the library of the University of
Helsinki and in the Botanical Garden of Geneva), we analyzed the correspondence
exchanged between him and several specialists that is filed at the University of
Coimbra (Biblioteca Digital de Botânica da Universidade de Coimbra). Some
important parts of this correspondence are transcribed below.
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C. Garcia et al.
Correspondence from Júlio Henriques to Franz Stephani
Henriques’ first letter referring sending material to Stephani, was on 8 January 1885.
The first publication of Stephani concerning the liverworts of São Tomé (Stephani
1886) refers to the A. Moller 1885 collections, so the specimen identifications must
have been rather hasty. It describes 19 new species, in addition to other taxa, such as
those already described by Mitten from the Cameroon Mountains (Mitten 1863)
(e.g., Radula bipinnata Mitt.). Among the first records for São Tomé and Príncipe
there was, for example, Lejeunea ramosissima Steph. (Fig. 9.4), Plagiochila
integerrima Steph., Sendtnera mollis Steph. and Anthoceros pinnatus Steph., all
currently still considered as distinct species with valid names. In the letter of
25 February 1886, Stephani sent along a list referencing the figures with the
iconographies that were included in the same publication of Stephani (1886).
Correspondence from Júlio Henriques to Carl Müller
The correspondence sent by C. Müller from Halle to Henriques is very sparse and
consists only of four letters between 1885 and 1887. C. Müller’s second letter, dated
21 March 1886 (UC Digitalis 2021), is the most important as it includes a list of
about 50 taxa, corresponding to the identification of the specimens cited in Müller
(1886a, b). These specimens include more than 25 new species, some of them still
recognized as species, as in the case of Funaria acicularis Müll.Hal and Leucobryum
leucophanoides Müll.Hal.
Correspondence from Júlio Henriques to Viktor Ferdinand
Brotherus
Sérgio and Garcia (2011) analyzed much of the correspondence between Henriques
and Brotherus. Henriques’ first letter dated 31 January 1889, refers to sending
(on 24 January 1889) a package including mosses from São Tomé to Copenhagen
and then to Helsinki. The exchange of bryological material continued and Henriques
must have sent a second package that also included material from Portugal. In
Brotherus’s letter to Coimbra, sent on 19 August 1889, he states “J’ai reçu en bon
état, il ya quelque jours, la quaisse avec des mousses du Portugal et j’irais à leurs
déterminations et révision aussitôt qu’il me sera possible. Les mousses de l’île
S. Thomé de votre second envoi j’ai déjà examinés et vous communique le nom
des espèces. Sont-elles aussi recueillies par M. Quintas”? [“I received in good
condition, a few days ago, the case with mosses from Portugal and I will make
their identifications and revision as soon as possible. The mosses of the island
S. Thomé of your second shipment I have already examined and communicated to
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you the names of the species. Were they also collected by Mr. Quintas”?]
(UC Digitalis 2021).The reprints referenced in these letters correspond to the 1890
article, published in the “Boletim da Sociedade Broteriana” (Brotherus 1890), where
29 new species are described, some still considered valid species, including several
endemics, such as Leucobryum homalophyllum Broth. and Ectropothecium
drepanophyllum Broth (Fig. 9.2).
Correspondence from Júlio Henriques to Francisco Quintas
Although there are no extant records of correspondence from Möller to Henriques, a
set of letters from Quintas sent from São Tomé to Henriques in Coimbra are still
extant (Biblioteca Digital de Botânica da Universidade de Coimbra 2021). From
most of this correspondence, it is evident that Quintas kept Henriques apprised of his
research and situation on the island, attaching lists of the material he sent to Coimbra.
Although there is no specific numbering for the bryophyte specimens, there were
indications of the boxes that contained cryptogams. For instance, the attachment to
the letter issued on 21 July 1888 (UC Digitalis 2021). In that same letter, he also
mentioned that mushroom specimens were listed separately. There are many bryophyte specimens collected by Quintas, which correspond to about 70 different
bryophyte taxa, some of them corresponding to new species, such as Plagiochila
flabellata Steph., P. amplifolia Steph. Among the liverworts and numerous species
of mosses (ca. 31) described as new by Brotherus in 1890, we have the examples of
Pilotrichella calomicra Broth., Porotrichum quintasii Broth., P. caudatum Broth.,
Trichosteleum dicranelloides Broth., among other new taxa.
Correspondence from Francisco Newton to Júlio Henriques
Some correspondence between Henriques and Newton is available in the historical
archives of MUHNAC, but none of these letters has any reference to bryophytes. In
Coimbra University, there is a letter sent by Newton to Henriques about his 1885
upcoming mission to Africa. Based on this letter, dated 23 August 1885, Newton
makes Henriques aware of certain material from Angola (UC Digitalis 2021). He
also confirms in that letter that he proposed to make a stop at Príncipe Island and then
São Tomé. Ultimately, Newton arrived in São Tomé on 24 September 1885 (Guedes
2021).
Strangely, most of the bryophyte material collected by Newton and found in the
different herbaria (BM, FH, G, JE and M herbaria) corresponds to specimens
collected in 1887 on Príncipe and only a few are indicated to be from São Tomé.
In fact, in the different publications concerning Newton, specimens correspond to
Príncipe Island, excluding two references corresponding to São Tomé, in Angolares
(Stephani 1888a, b). It is also interesting to note that the bryophyte specimens
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C. Garcia et al.
collected on Príncipe Island were only shipped in September of 1885 (Newton
1885), after this letter, but Newton should have sent more material later.
Apparently, Newton did not organize the numbering of his bryophyte specimens
and the labels are very uninformative. The numbering of specimens was made when
the plants arrived in Coimbra. However, it should be noted that based on Newton’s
collections, some liverwort species were described by Stephani (1888a, b), as
Microlejeunea africana Steph., Lejeunea newtonii Steph. (now included in
Cheilolejeunea newtonii Steph. ex Schiffn.), Plagiochila thomeensis Steph. (currently a synonym for Plagiochila terebrans Nees et Mont. ex Lindenb);
Cheilolejeunea principensis Steph. (synonymized to Cheilolejeunea serpentina
(Mitt.) Mizut.), and Lophocolea newtonii Steph. (synonymized to Lophocolea
martiana Nees).
Historical Collecting Localities
Based on the data associated with the aforementioned collections, the location (exact
or approximate) of the historical collecting activities by the first naturalists dedicated
to the study of bryophytes in São Tomé Island was georeferenced (Fig. 9.5), and
used as a starting point for the most recent fieldwork performed by the authors.
Exell’s 1944 plant catalogue (Exell 1944) includes all the species known at the
time and new reports of some taxa for the islands (Figueiredo 1994, 2005; Figueiredo and Gascoigne 2001), including diverse bryophytes. He was based in Vanhulst
(Macambrará), in the Roça Zampalma and collected most of the bryophyte material
in this region. This bryophyte collection was the basis for two publications, in which
about 40 taxa of liverworts and mosses are listed (Exell 1944). Most of Exell’s
specimens are stored in BM, except for some specimens that are kept at COI.
After the Exell expedition, other collections were obtained in 1956 by the French
naturalist Théodore Monod (1902–2000) and C. A. Thorold (1906–1998) in São
Tomé and Príncipe, mainly in Pico de Príncipe, during the “6th Conférence
lnternationale des Africanistes de I’Ouest” (Monod 1960). Most of this material is
hosted in PC and was the basis of the publication of Potier de la Varde (1959).
Arnaldo Roseira also collected in the islands between 1954 and 1958, corresponding
to 79 specimens of three taxa in the PO herbarium (Universidade do Porto) (Costa
2020).
Recent Studies
Since the middle of the twentieth century and after the works of Exell, the study of
bryophytes of São Tomé and Príncipe came to a halt. Only more recently has a new
effort emerged through the project Bryotome (Sérgio and Garcia 2011). During this
project, the first author carried out fieldwork in São Tomé and Príncipe in 2007 and
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Fig. 9.5 Historical collecting localities of naturalists who collected bryophytes specimens on São
Tomé Island from the mid-nineteenth century to mid-twentieth century: (1) Auguste Jean Baptiste
Chevalier (1873–1956), (2) Arthur Wallis Exell (1901–1993), (3) Gustav Mann (1836–1916), (4)
Adolpho Frederico Möller (1842–1920), (5) Théodore Monod (1902–2000), (6) Francisco Newton
(1864–1909), (7) Francisco Joaquim Dias Quintas (1864–1909), (8) Charles Aubrey Thorold
(1906–1998), (9) Friedrich Welwitsch (1806–1872)
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C. Garcia et al.
Fig. 9.6 Study localities in 2007, 2008, 2010, 2013 and 2016 for the enrichment of the University
of Lisbon (LISU) and the California Academy of Science (CAS) herbaria
2008, collecting about 6000 specimens at various altitudes, including Pico de São
Tomé. This project enabled the study of herbarium specimens, georeferencing
historical specimens, planning new fieldwork more effectively, and studying different substrates (epiphytic, epiphyllous, rupicolous, terricolous and humicolous) to
better determine specific microhabitats of species across the islands. In 2010, 2013
and 2016, expeditions sponsored by the California Academy of Sciences were
carried out (Fig. 9.6). During these new expeditions, several species were discovered, including new records for the archipelago and the African continent, as well as
species new to science (Figs. 9.7 and 9.8). One of the new species discovered was
particularly interesting: Dendroceros paivae is distinct from most other species of
the genus in its ecology, gametophyte, and sporophyte characters, resembling only
the Bornean D. foliicola J. Haseg. In comparison to the type material of D. foliicola,
D. paivae has a narrower sporophyte diameter. The thallus of D. paivae does not
form rosettes, the cuticle is weakly papillose, and apices are plane to undulate, while
D. foliicola forms rosette-like patches with strong crispate margins, even at branches
apices, and the cuticle is slightly papillose (Garcia et al. 2012).
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Fig. 9.7 Liverworts and hornworts from São Tomé and Príncipe: (1, 2) Dendroceros paivae
C.A. Garcia, Sérgio & J. C. Villarreal. (hornworts) at the type locality (LISU 237201) (Garcia
et al. 2012); (3, 4) Megaceros flagellaris (Mitt,) Steph. (hornworts) growing on a tree trunk in the
first known locality in São Tomé and Príncipe and the second one reported for the African Continent
(LISU 237200); (5) Anthoceros pinnatus Steph. (hornworts); (6) Phaeoceros carolinianus (Michx.)
Prosk. (hornworts); (7) Colura sp. (liverworts); (8) Cyathodium cavernarum Kunze (liverworts)
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C. Garcia et al.
Fig. 9.8 Liverworts and mosses from São Tomé and Príncipe. (1) Marchantia pappeana Lehm.
subsp. pappeana (liverworts). (2), Plicanthus hirtellus (F. Weber) R.M. Schust. (liverworts). (3),
Calymperes lonchophyllum Schwägr. (mosses). (4), Octoblepharum albidum Hedw. (mosses). (5),
Orthostichella sp. (mosses). (6), Trematodon longicollis Michx. (mosses). (7), Macromitrium
sulcatum var. sulcatum (Hook.) Brid. (mosses). (8), Calymperes palisotii Schwägr. (mosses)
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Diversity, Composition and Endemism
In recent years, several papers resulting from these last expeditions have been
published. These included the study of secondary metabolism compounds
(Figueiredo et al. 2010) and the description of new species and new genera of
bryophytes (Enroth and Shevock 2011; Müller et al. 2011; Garcia and Sérgio
2012a, b, c, d, e; Shevock et al. 2013; Pócs et al. 2015; Sollman et al. 2016; Enroth
and Shevock 2017a, b; Müller and Shevock 2018; Müller et al. 2019).
These works allowed revising the number of species and endemics for each island
individually and for the two islands combined (Table 9.1 and Appendix). One
hundred and forty-four species of bryophytes occurring on the islands are currently
considered endemic to Africa, 21 of which are endemic to the archipelago, including
seven liverworts or hornworts and 14 mosses. One of these species is the hornwort
Dendroceros paivae C.A. Garcia, Sérgio & J. C. Villarreal. (hornworts), endemic to
São Tomé Island (Garcia et al. 2012) and found only in a single location, in a very
restricted area.
The known bryophyte species diversity of the islands has increased markedly as
specimens of various families are critically examined. For example, prior to fieldwork by the authors, only three species of the moss genus Fissidens (Fissidentaceae)
were reported (O’Shea 2006). Now, Fissidens Hedw. is the most species-rich
bryophyte genus in the archipelago with 24 known species (Shevock et al. 2013).
The liverwort genera, Lejeunea Lib. and Plagiochila (Dumort.) Dumort. are also
quite diverse with 19 and 18 species respectively (Müller et al. 2011; Pócs et al.
2015). A similar story of species additions for the islands was provided in a recent
study of the moss families Neckeraceae (Enroth and Shevock 2011, 2017a, b) and
Table 9.1 Bryophyte species
diversity and endemism for
each island individually and
for the two islands combined
Príncipe
São Tomé
P&ST
MARCHANTIOPHYTA and ANTHOCEROTOPHYTA
Liverworts and hornworts
Total species/taxa
108
138
171
Island endemism
4
4
7
African endemism
52
65
80
DIVISION BRYOPHYTA
Mosses
Total species/taxa
41
114
133
Island endemism
1
13
14
African endemism
16
59
64
TOTAL BRYOPHYTES
Liverworts, hornworts and mosses
Total species/taxa
149
252
304
Island endemism
5
17
21
African endemism
68
124
144
Liverworts and hornworts, according to Wigginton (2018), and
mosses, according to O’Shea (2006)
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C. Garcia et al.
Pottiaceae (Sollman et al. 2016). Ongoing work on the moss family Calymperaceae
also has discovered several new species for these islands. We anticipate species
additions for these islands will continue for many years to come. Most studies were
carried out on existing trails to reach higher areas, and several regions have not yet
been surveyed (Figs. 9.5 and 9.6) due to the difficult terrain. Additional species will
likely be documented and discovered as more remote cloud forest environments can
be systematically surveyed. Our updated summary for the bryoflora of the islands
reveals the documented diversity has increased significantly since the last reports of
the mosses (O’Shea 2006) and of the liverworts and hornworts (Wigginton 2018).
Thus, the 304 bryophytes documented for the archipelago at this time are likely a
vast underestimate of the true diversity (Appendix).
The species catalogue of the bryophyte flora of the islands of São Tomé and
Príncipe presented in this work (Appendix) is based on all known published literature. All the literature on bryophytes of São Tomé and Príncipe Islands was
surveyed, including liverworts, hornworts, and mosses. The delimitation of families
follows the latest version of the Checklist of sub-Saharan Africa of Wigginton
(2018) for liverworts and hornworts and O’Shea (2006) for mosses. Taxa are
presented in alphabetical order of all the accepted names (including subspecies
and varieties). Taxa with synonymies (homotypic and heterotypic synonyms)
whose type locality corresponds to São Tomé and Príncipe are designated in a
second column with respective authors and the year of publication for São Tomé
and Príncipe. The most accurate information about the original description, as well
as the relevant synonyms, were considered with general taxonomic criteria. The
present table includes only records published up until June 2020 (unpublished data
of the authors, including new species and localities, are not included). The catalogue
is not a taxonomic document, and no new taxonomic nor nomenclatural acts are
published here. Synopses of families and genera are placed alphabetically within
each order.
Final Remarks
The known bryoflora of São Tomé and Príncipe includes at least 304 species. Based
on our ongoing studies and the number of specimens still awaiting critical study, this
number will increase in the coming years as the diversity of this group becomes more
comprehensively documented. The apparently low number of known species may be
explained by the logistical and practical difficulties of carrying out fieldwork in
dense forests and in areas of rough terrain, a reality that affects most of the scientists
working in the region. Bryophytes are also generally very small plants, and many
species occur in small populations. Therefore, during fieldwork some species can
easily be overlooked or may occupy exceedingly specialized microhabitats that are
difficult to find (e.g., fine twigs in the tree canopy). Further difficulty originates from
the fact that the taxonomy of different bryophyte families is not well developed in
the tropics, and world experts in bryophyte taxonomy are also starting to become
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scarce, especially those dedicated to the study of tropical species. Many bryophyte
species reported from Africa are known only from type specimens or based on a
handful of collections. Almost 45 bryophyte taxa reported for São Tomé and
Príncipe have not been resampled since the nineteenth century. For a large number
of bryophyte species, the ecology and habitat specificity are not well known or not
known at all, and also the distribution patterns, elevational range, and abundance for
most species remain to be determined.
The threats affecting forest habitats in São Tomé and Príncipe, such as habitat
destruction or competition by invasive species, may affect the survival of bryophytes. One major threat to biodiversity conservation in the archipelago, particularly
to the cryptogamic communities, forest structure, and habitat diversity along the
altitudinal gradients is deforestation, especially that associated with the plantations
of oil palm Elaeis guineesis Jacq. In the Emolve region (southern region of São
Tomé), there is a monoculture of more than 600 ha of oil palm that is expected to
continue growing, which would result in a significant loss in biodiversity (bryophytes and other taxonomic groups), especially to forests at lower elevations. By
contrast, ancestral roças (old colonial farms), with Cofeea spp. and Theobroma
cacao L. plantations, seem to preserve a high diversity of bryophyte species, mainly
epiphytic taxa.
New bryological studies are urgently needed, especially in areas that have never
been surveyed. Together with the recently collected material that is currently being
studied by the coauthors and other colleagues, these new surveys will continue to
increase our knowledge of distributions, species diversity and the particularities of
bryophyte endemism in the country. A more comprehensive and updated species list
will be essential to inform a future IUCN Red List assessment of bryophytes from
São Tomé and Príncipe and to designate priority areas for conservation.
Acknowledgments The present study was partly supported by “Fundação para a Ciência e a
Tecnologia” (POCTI/AFR/58699/2004 and SFRH/BPD/22304/2005) and by California Academy
of Sciences Gulf of Guinea Funds (the expedition of 2016 performed by the first author and all those
carried out by the last author). We are grateful to the curators of the following herbaria for kindly
allowing us to study in situ the plant material and for the loan of specimens, including types: BM, G,
H; PC, NICH and VIT. The authors are grateful to the são-tomenses, Eng. Salvador Pontes,
Aurélio Espirito-Santo ({), Francisco Alamô, Estevão Soares, Mr. Lagoas ({), Sátiro Raúl José da
Costa, Ostelino Conceição Rocha (Balú) e Júlio da Conceição Rocha for their help during the
fieldwork. Thanks also to expedition photographer Andrew Stanbridge.
234
C. Garcia et al.
Appendix
Updated catalogue of bryophytes from São Tomé and Príncipe Islands. A: African
endemics. E: Island endemism.
Synonyms (basionyms) based in
São Tomé and Príncipe collections
Taxon species/subspecies/variety
DIVISIONS
Marchantiophyta and Anthocerotophyta
Liverworts and Hornworts
Acrolejeunea emergens (Mitt.)
Steph. var. emergens
Aneura pinguis (L.) Dumort. sens.
lat.
Aneura latissima Spruce
Anthoceros pinnatus Steph.
Bazzania decrescens subsp. molleri
(Steph.) E.W.Jones
Bazzania nitida (F.Weber) Grolle
Brachiolejeunea laxifolia (Taylor)
Schiffn.
Calypogeia fissa (L.) Raddi
Calypogeia peruviana Nees
et Mont.
Caudalejeunea africana (Steph.)
Schiffn.
Caudalejeunea dusenii Steph.
Caudalejeunea hanningtonii (Mitt.)
Schiffn.
Caudalejeunea lehmanniana
(Gottsche) A.Evans
Ceratolejeunea cornuta (Lindenb.)
Steph.
Ceratolejeunea floribunda Steph.
Cheilolejeunea intertexta
(Lindenb.) Steph.
Cheilolejeunea montagnei
(Gottsche) R.M.Schust.
Cheilolejeunea rigidula (Nees ex
Mont.) R.M.Schust.
Cheilolejeunea surrepens (Mitt.) E.
W.Jones
Anthoceros pinnatus Steph. 1886
Mastigobryum molleri Steph. 1886
P
ST
X
X
X
X
X
X
X
A
X
X
X
2015/
2011
1956/
1886
1888/
2011
1886
2015/
1886
2011
1912
X
X
1970
1976
X
X
2011
A
A
A
2015
2000/
2000
2015
X
E
1960/
2015
1913
X
2015/
1893
1863
Brachiolejeunea thomeensis Steph.
1912
X
X
Ceratolejeunea floribunda Steph.
2013 1913
Cheilolejeunea newtonii Steph. ex
Schiffn. 1893
Euosmolejeunea thomeensis Steph.
1914
Cheilolejeunea principensis Steph.
ex Paris 1888
Year of
first ref.
P/ST
X
X
1888
X
2015
(continued)
9
The Bryophyte Flora of São Tomé and Príncipe (Gulf of Guinea): Past,. . .
Taxon species/subspecies/variety
Cheilolejeunea trifaria (Reinw.
et al.) Mizut.
Chiloscyphus difformis (Nees) J.J.
Engel et R.M.Schust.
Cololejeunea africana (Steph.) R.
M.Schust.
Cololejeunea cuneifolia Steph.
Cololejeunea iradieri Infante et
Heras
Cololejeunea lanceolata E.W.Jones
Cololejeunea leloutrei (E.W.Jones)
R.M.Schust.
Cololejeunea mocambiquensis S.
W.Arnell
Cololejeunea obliqua (Nees et
Mont.) Schiffn.
Cololejeunea obtusifolia (E.W.
Jones) Tixier
Cololejeunea papilliloba Steph.
Cololejeunea platyneura (Spruce)
A.Evans
Cololejeunea pusilla Steph.
Cololejeunea zenkeri (Steph.) E.W.
Jones
Colura calderae Pócs
Colura digitalis (Mitt.) Steph.
Synonyms (basionyms) based in
São Tomé and Príncipe collections
Lejeunea grandistipula Steph.
1886
Lophocolea molleri Steph. 1886
Physocolea africana Steph. 1915
X
Year of
first ref.
P/ST
2015/
1886
1886
A
1916
A
2015
2015
A
2015
1960
ST
X
A
A
A
Cololejeunea crenatiflora Steph.
1891
X
2015
X
A
X
X
2011/
1891
2015
2015
2015
A
A
A
A
A
A
A
X
A
A
X
E
E
Lophocolea devexa Mitt. 1863
X
X
Lophocolea newtonii Steph. 1907
X
X
2015
2000/
2015
2011
1958/
1953
2015
2015
2015/
1958
2015/
2011
2015/
1863
1953
X
X
A
E
1952
1863
2010
2012
Colura hattoriana Pócs
Colura obesa Jovet-Ast
Colura tenuicornis (A.Evans)
Steph.
Colura thomeensis Pócs
Conoscyphus trapezioides (Sande
Lac.) Schiffn.
Cryptolophocolea martiana (Nees)
L.Söderstr., Crand.-Stotl. et Stotler
subsp. martiana
Cyathodium cavernarum Kunze
Dendroceros crispatus Nees
Dendroceros herasii M.Infante
Dendroceros paivae C.Garcia,
Sérgio & J.C. Villarreal
P
X
235
(continued)
236
Taxon species/subspecies/variety
Dibrachiella africana (Steph.) X.Q.
Shi, R.L.Zhu et Gradst.
Dibrachiella autoica (Vanden
Berghen) X.Q.Shi, R.L.Zhu et
Gradst.
Diplasiolejeunea cavifolia Steph.
Drepanolejeunea capulata (Taylor)
Steph.
Drepanolejeunea cultrella (Mitt.)
Steph.
Drepanolejeunea physifolia
(Gottsche) Pearson
Dumortiera hirsuta (Sw.) Nees
Folioceros incurvus (Steph.) D.C.
Bharadwaj
Fossombronia indica Steph.
Fossombronia sp.
Frullania angulata Mitt. var.
angulata
Frullania apicalis Mitt.
Frullania apiculata (Reinw. et al.)
Nees
Frullania caffraria Steph.
C. Garcia et al.
Synonyms (basionyms) based in
São Tomé and Príncipe collections
Frullania purpurea Steph.
Frullania rio-janeirensis (Raddi)
Ångstr.
Frullania serrata Gottsche var.
serrata
Frullania spongiosa Steph.
Fuscocephaloziopsis connivens
subsp. fissa (Steph.) Váňa et L.
Soderstr.
Herbertus dicranus (Taylor ex
Gottsche, Lindenb. et Nees) Trevis.
ST
A
Lejeunea cavifolia Steph. 1886
Drepanolejeunea molleri Steph.
1913
Prionolejeunea fissistipula Steph.
1913
2015
X
A
1886
2011
A
A
A
A
X
X
A
A
2015/
1913
1960/
1913
1960/
1886
1888/
1889
2019
2011
1863
X
X
Frullania angulata Mitt. 1863; F.
subatrata Steph. 1911;
F. cordifolia Steph. 1911
Frullania laceriloba Steph. 1911
A
A
X
2015/
1911
2011
X
1894
X
A
X
X
X
X
X
X
X
1886
1886/
1863
1910
2015/
2004
1976
1976/
1891
1886
Frullania molleri Steph. 1894
(Probably synonym)
Frullania diptera (Lehm.) Drège
Frullania ericoides (Nees) Mont.
Frullania obscura (Sw.) Mont.
Frullania obscurifolia Mitt.
P
A
Frullania thomeensis Steph. 1910
Frullania africana Steph. 1891
A
X
Sendtnera mollis Steph. 1886
Year of
first ref.
P/ST
2000
X
X
X
X
X
X
2011/
2011
1988/
1988
2011/
1886
(continued)
9
The Bryophyte Flora of São Tomé and Príncipe (Gulf of Guinea): Past,. . .
Taxon species/subspecies/variety
Heteroscyphus dubius (Gottsche)
Schiffn.
Heteroscyphus spectabilis (Steph.)
Schiffn.
Synonyms (basionyms) based in
São Tomé and Príncipe collections
237
Year of
first ref.
P/ST
1888
P
X
ST
A
A
2015/
1886
Lejeunea abyssinica (Gola) Cufod.
A
A
Lejeunea acuta Mitt.
A
A
Lejeunea anisophylla Mont.
X
X
2015/
2015
2019/
1960
2011/
2011
2015
2011
2011
2015
1888/
1960
1896
Isotachis perfoliata Steph. 1886
Chiloscyphus thomeensis Steph.
1893 nom. nud.?
Lejeunea brenanii E.W.Jones
Lejeunea cf. obtusata Gottsche
Lejeunea conformis Nees et Mont.
Lejeunea eckloniana Lindenb.
Lejeunea flava (Sw.) Nees
Lejeunea grossecristata (Steph.) E.
W.Jones
Lejeunea helenae Pearson
Lejeunea ibadana A.J.Harr. et E.W.
Jones
Lejeunea jungneri (Steph.) Steph.
Lejeunea lyratiflora Steph.
Lejeunea papilionacea Prantl
Lejeunea phyllobola Nees et Mont.
Lejeunea pulchriflora (Pearson)
G.E. Lee, Bechteler, Pócs, SchäfVerw. & Heinrichs
Lejeunea ramosissima Steph.
A
X
A
X
X
X
A
Hygrolejeunea grossecristata
Steph. 1896; Taxilejeunea
longirostris Steph. 1914
X
A
A
A
A
X
X
X
Lejeunea ramosissima Steph. 1886
X
X
Lejeunea setacea (Steph.) Steph.
A
A
Lejeunea tuberculosa Steph.
Lepidozia succida Mitt.
X
A
A
Lepidozia ubangiensis Steph.
Leptolejeunea astroidea (Mitt.)
Steph.
Leptolejeunea epiphylla (Mitt.)
Steph.
Leptolejeunea maculata (Mitt.)
Schiffn.
A
A
A
X
X
X
X
Leptolejeunea quintasii Steph.
1891
Lejeunea thomeensis Steph. 1886;
Drepanolejeunea gomphiae Steph.
1913
2015
2015/
2015
1901
2015
2011
2011
2015
1996/
1886
1969/
1969
2011
2011/
1891
2015
2015
2015/
1891
2015/
1886
(continued)
238
Taxon species/subspecies/variety
Lopholejeunea nigricans (Lindenb.)
Schiffn.
Lopholejeunea subfusca (Nees)
Schiffn.
Marchantia debilis Goebel
Marchantia pappeana Lehm.
subsp. pappeana
Marchesinia excavata (Mitt.)
Schiffn.
Marchesinia principensis Frank
Müll. et Shevock
Mastigophora diclados (Brid. ex F.
Weber) Nees
Megaceros flagellaris (Mitt.) Steph.
Metalejeunea cucullata (Reinw.
et al.) Grolle
Metzgeria furcata (L.) Dumort.
Metzgeria leptoneura Spruce
Metzgeria lindbergii Schuffn.
Microlejeunea africana Steph.
Microlejeunea ankasica E.W. Jones
Microlejeunea kamerunensis Steph.
Neurolejeunea breutelii (Gottsche)
A.Evans var. africana Pócs
Notoscyphus lutescens (Lehm. et
Lindenb.) Mitt.
Odontolejeunea lunulata (F.Weber)
Schiffn.
Pallavicinia lyellii (Hook.) Carruth.
Phaeoceros carolinianus (Michx.)
Prosk.
Plagiochila barteri Mitt.
Plagiochila barteri var. valida
(Steph.) Vanden Berghen
Plagiochila brunneola Steph.
Plagiochila divergens var. capensis
(Steph.) E.W. Jones
Plagiochila flabellata Steph.
Plagiochila fusifera Taylor
C. Garcia et al.
Synonyms (basionyms) based in
São Tomé and Príncipe collections
A
A
Year of
first ref.
P/ST
2011/
2011
2015/
2011
2011
1886
A
1886
P
X
ST
X
X
X
Marchantia planiloba Steph. 1886
Homalolejeunea henriquesii
Steph. 1888
A
X
2018
X
X
X
Metzgeria thomeensis Steph. 1891
X
X
Metzgeria recurva Steph. 1886
X
X
X
A
A
A
A
A
A
Microlejeunea africana Steph.
1888
Microlejeunea cochlarifolia Steph
1888 (probably synonymy)
E
Odontolejeunea thomeensis Steph.
1912
Pallavicinia pilifera Steph. 1891
Plagiochila triangularis Steph.
1886; P. quintasii Steph. 1904
Plagiochila flabellata Steph. 1886;
P. molleri Steph. 1886
Plagiochila amplifolia Steph. 1901
2015
X
2004/
1912
1891
2011
A
A
A
A
A
X
A
2004/
1891
2004/
1886
2015
1888/
1891
2015
1990/
1888
2015
X
X
X
Plagiochila brunneola Steph. 1904
2015/
1886
2012
2015
A
X
1962/
1886
1981/
1981
1904
1962
2011/
1886
1901
(continued)
9
The Bryophyte Flora of São Tomé and Príncipe (Gulf of Guinea): Past,. . .
Taxon species/subspecies/variety
Plagiochila gibbiflora Steph.
Plagiochila heterostipa Steph.
Plagiochila integerrima Steph.
Synonyms (basionyms) based in
São Tomé and Príncipe collections
Plagiochila gibbiflora Steph. 1904
P
239
ST
E
A
X
X
A
A
Plagiochila moenkemeyeri Steph.
A
A
Plagiochila neckeroidea Mitt.
A
A
Plagiochila pectinata Willd. ex
Lindenb.
Plagiochila pinniflora Steph.
Plagiochila praemorsa Steph.
A
A
X
A
X
A
A
A
A
Plagiochila loloensis Steph.
Plagiochila integerrima Steph.
1886
Plagiochila rotundifolia Steph.
1904
Plagiochila cacuminis Steph. 1918
Plagiochila sarmentosa (Lehm. et
Lindenb.) Lindenb.
Plagiochila strictifolia Steph.
Requires confirmation
Plagiochila terebrans Nees et
Mont. ex Lindenb.
Pleurozia gigantea (F.Weber)
Lindb.
Plicanthus hirtellus (F.Weber) R.M.
Schust.
Porella abyssinica var. hoehnelii
(Steph.) Pócs.
Porella subdentata (Mitt.) E.W.
Jones var. subdentata
Porella subdentata var.
camerunensis E.W.Jones
Prionolejeunea grata (Gottsche)
Schiffn.
Prionolejeunea principensis
Vanden Berghen
Radula ankefinensis Gottsche ex
Steph.
Radula appressa Mitt.
Plagiochila thomeensis Steph.
1886
Radula boryana (F.Weber) Mont.
Radula flaccida Lindenb. et
Gottsche
Madotheca thomeensis Steph.
1910
A
X
1962/
1962
2011/
1886
1863
X
1886
A
2011
A
1963/
1910
2011
A
X
X
1960/
1960
1960
A
A
A
A
X
X
X
X
2011/
2015
1910/
1886
1996/
1863
1939/
1939
E
Radula angustata Steph. 1886;
R. molleri Steph. 1910
Radula tamariscina Mitt. 1863;
R. bipinnata Mitt. 1863
Year of
first ref.
P/ST
1904
2015
2011/
1886
2011/
1904
2011/
1960
2011/
1904
2011/
1960
2011
1888/
1918
(continued)
240
Taxon species/subspecies/variety
Radula fulvifolia (Hook.f. et Taylor)
Gottsche et al.
Radula stenocalyx Mont.
Riccardia amazonica (Spruce)
Schiffn. ex Gradst. et Hekking
Riccardia erosa (Steph.) E.W.Jones
Riccardia limbata (Steph.) E.W.
Jones
Riccardia longispica (Steph.)
Pearson
Riccia congoana Steph.
Riccia discolor Lehm. et Lindenb.
Riccia lanceolata Steph.
Riccia moenkemeyeri Steph.
Riccia stricta (Lindenb.) Perold
Schiffneriolejeunea occulta (Steph.)
Gradst.
Schiffneriolejeunea pappeana
(Nees) Gradst. var. pappeana
Schiffneriolejeunea polycarpa
(Nees) Gradst.
Solenostoma borgenii (Gottsche ex
Pearson) Steph.
Solenostoma dusenii (Steph.) Váňa,
Hentschel et Heinrichs.
Spruceanthus abbreviatus (Mitt.) X.
Q.Shi, R.L.Zhu et Gradst.
Spruceanthus floreus (Mitt.)
Sukkharak et Gradst.
Stictolejeunea balfourii (Mitt.) E.
W.Jones
Symphyogyna podophylla (Thunb.)
Mont. et Nees
Syzygiella manca (Mont.) Steph.
Telaranea coactilis (Spruce) J.J.
Engel et G.L.Merr.
Telaranea nematodes (Gottsche ex
Austin) M.Howe
Thysananthus auriculatus (Wilson)
Sukkharak et Gradst. var.
auriculatus
C. Garcia et al.
Ptychocoleus quintasii Steph. 1912
A
Year of
first ref.
P/ST
2001/
2011
2015/
1910
2015/
2011
2011/
1891
2011/
1891
2015/
2011
2012
2015
2015
2012
2012
2015/
2011
1912
Phragmicoma amplectens Steph.
1886 ¼ P. molleri Steph. 1886
X
1886
A
1974
X
X
2019/
1974
2015
A
1891
X
2015
Synonyms (basionyms) based in
São Tomé and Príncipe collections
P
X
ST
X
X
X
X
X
Aneura erosa Steph. 1891
A
A
Aneura reticulata Steph. 1891
A
A
A
A
X
X
A
A
X
Jungermannia geminiflolia Mitt.
1863
Lepidozia quintasii Steph. 1922
X
A
X
A
X
2011
X
1863
X
2011
X
1922
X
2011/
1949
(continued)
9
The Bryophyte Flora of São Tomé and Príncipe (Gulf of Guinea): Past,. . .
Taxon species/subspecies/variety
Thysananthus humilis (Gottsche)
Sukkharak et Gradst.
Thysananthus nigrus (Steph.)
Sukkharak et Gradst.
Thysananthus turgidus (Steph.)
Sukkharak et Gradst.
DIVISION Bryophyta
Mosses
Afrothamnium stipitatum (Mitt.)
Enroth
Anoectangium aestivum
(Hedw.) Mitt.
Anoectangium stracheyanum Mitt.
Barbula cf. seramensis H.Akiyama
Brachymenium leptophyllum
(Bruch & Schimp. ex Müll.Hal.)
Bruch & Schimp. ex A.Jaeger
Brachymenium nepalense Hook.
Brachymenium subuliferum (Mitt.)
A.Jaeger
Brachymitrion moritzianum (Müll.
Hal.) A.K.Kop.
Bryum apiculatum Schwägr.
Bryum argenteum Hedw. var.
argenteum
Bryum coronatum Schwägr.
Bryum huillense Welw. & Duby
Bryum thomeanum P. de la Varde
Caduciella mariei (Besch.) Enroth
Callicostella brevipes (Broth.)
Broth.
Callicostella chionophylla (Müll.
Hal.) Broth.
Callicostella fissidentella (Besch.)
Kindb.
Callicostella perpapillata Broth. &
P.de la Varde
Callicostella salaziae (Besch.)
Broth.
Calymperes afzelii Sw.
Calymperes lonchophyllum subsp.
saxatile (Müll. Hal. ex Besch.)
S.R. Edwards
Synonyms (basionyms) based in
São Tomé and Príncipe collections
241
P
X
ST
X
Mastigolejeunea nigra Steph. 1891
A
X
Mastigolejeunea turgida Steph.
A
X
Bryum subuliferum Mitt. 1863;
Bryum molleri Müll.Hal. 1886
Orthodon thomeanus Broth. 1890;
Tayloria thomeana Broth. 1903
Bryum areoblastum Müll.Hal.
1886
Bryum squarripilum Müll.Hal.
1886
Bryum erythrostegum Müll.Hal.
1886
Bryum quintasii Broth.1890
Bryum thomeanum P.de la Varde
1959
X
1982
X
2016
X
X
X
2016
2016
1972
X
A
1972
1863
X
1890
X
1886
X
1886
X
1886
X
E
1890
1959
A
2017
1952
E
1886
A
1890/
1890
1944
A
1890
X
1863
1944
X
Hookeria chionophylla Müll.Hal.
1886
Hookeria thomeana Broth. 1890
A
X
Hookeria quintasi Broth. 1890
Calymperes quintasi Broth. 1890
A
Year of
first ref.
P/ST
2014/
1888
2015/
1891
1983/
1917
(continued)
242
Taxon species/subspecies/variety
Calymperes palisotii Schwägr.
Calymperes pintasii Müll.Hal. ex
Besch.
Calymperes tenerum Müll.Hal.
Calyptothecium acutifolium var.
breviusculum (Müll.Hal. ex Dusén)
Argent
Campylopus flexuosus (Hedw.) Brid
var. flexuosus.
Campylopus savannarum (Müll.
Hal.) Mitt.
Chionoloma bombayense (Müll.
Hal.) P. Sollman
Cyclodictyon filicuspis P.de la
Varde
Cyclodictyon laetevirens (Hook. &
Taylor) Mitt.
Deslooveria quintasii (Broth.)
Enroth
Deslooveria saotomensis (Enroth &
Shevock) Enroth
Dicranella falcularia Müll.Hal. ex
Dusén
Ectropothecium brevifalcatum
(Müll.Hal.) Kindb.
Ectropothecium diffusum (Mitt.) A.
Jaeger
Ectropothecium drepanophyllum
Broth.
Fissidens asplenioides Hedw.
Fissidens borgenii Hampe
C. Garcia et al.
Synonyms (basionyms) based in
São Tomé and Príncipe collections
P
X
ST
A
Calymperes principis Broth. 1890
X
Campylopus quintasii Broth. 1890
Dicranum divaricatum Mitt. 1863;
Campylopus erythrocaulon Broth.
1890
X
X
A
1890/
1959
2011
X
1890
X
1890/
1863
X
2016
X
1944
X
1944
Porotrichum quintasii Broth. 1890
A
1890
Porotrichum saotomense Enroth
and Shevock (2011)
E
2011
A
Hypnum brevifalcatum Müll.Hal.
1886
Stereodon diffusus Mitt. 1863
1944
A
A
E
1890
A
X
X
X
X
2013
2013/
2013
2013/
2013
2013/
2013
2013
2013
2013/
2013
2013/
2013
1890/
1890
Ectropothecium drepanophyllum
Broth. 1890
X
X
A
X
A
A
Fissidens flaccidus Mitt.
X
X
A
A
Fissidens subglaucissimus Broth.
1890
1888
1863
Fissidens crispulus Brid. var.
crispulus
Fissidens crispulus var. robinsonii
(Broth.) Z. Iwats.& Z.-H. Li
Fissidens crispus Mont.
Fissidens darntyi Schimp.
Fissidens enervis Sim
Fissidens glaucissimus Welw. &
Duby
Year of
first ref.
P/ST
1987
1896
(continued)
9
The Bryophyte Flora of São Tomé and Príncipe (Gulf of Guinea): Past,. . .
Taxon species/subspecies/variety
Fissidens intramarginatus (Hampe)
A.Jaeger
Fissidens metzgeria (Müll.Hal.)
Broth.
Fissidens microcarpus Mitt.
Fissidens ovatus Brid.
Fissidens pallidinervis Mitt.
Fissidens palmatus Hedw
Fissidens pellucidus Hornsch.
Synonyms (basionyms) based in
São Tomé and Príncipe collections
P
243
ST
X
Year of
first ref.
P/ST
2013
A
2013
A
A
X
X
X
X
Fissidens porrectus Mitt.
A
A
Fissidens punctulatus Sande Lac.
Fissidens ramulosus Mitt.
A
X
A
A
A
Fissidens sciophyllus Mitt.
Fissidens serratus Müll.Hal. var.
serratus
Fissidens submarginatus Bruch
Fissidens usambaricus Broth.
Fissidens zollingeri Mont.
Floribundaria floribunda (Dozy &
Molk.) M.Fleisch.
Floribundaria vaginans (Welw. &
Duby) Broth.
Funaria acicularis Müll.Hal.
Funaria hygrometrica Hedw. var.
hygrometrica
Gymnostomiella erosula (Müll.Hal.
ex Dusén) Arts
Gymnostomiella vernicosa (Hook.)
M.Fleisch.
Hydrogonium consanguineum
(Thwaites & Mitt.) Hilp.
Hydrogonium orientale (F. Weber)
Kucera
Hymenostylium recurvirostrum
(Hedw.) Dixon var. recurvirostrum
Hyophila involuta (Hook.) A.Jaeger
Hypopterygium tamarisci (Sw. ex
Sw.) Brid. ex Müll.Hal.
Isopterygium nanoglobum (Müll.
Hal.) Paris
Fissidens purpureocaulis Müll.
Hal. 1900
X
X
A
X
2013
2013
2013
2011
A
1886
E
X
1886
1901
A
2016
X
2016
X
2016/
2016
2016/
1987?
2016
X
Papillaria patentissima Müll.Hal.
1886
Funaria acicularis Müll.Hal. 1886
X
X
X
Hypopterygium brevifolium Broth.
1890
Hypnum nanoglobum Müll.Hal.
1886
2013
2013
2013
2013
2013/
2013
2013/
2013
1890
2013/
2013
2013/
2013
2013
X
X
X
X
E
2016/
2016
1997/
1863
1886
(continued)
244
Taxon species/subspecies/variety
Lepidopilum lastii Mitt.
Lepidopilum niveum (Müll.Hal.)
Kindb.
Leptodontium viticulosoides (P.
Beauv.) Wijk & Margad. var.
viticulosoides
Leucobryum fouta-djalloni Paris &
Cardot
Leucobryum homalophyllum Broth.
Leucobryum leucophanoides Müll.
Hal.
Leucoloma gracilescens Broth.
Leucoloma secundifolium Mitt.
Leucomium strumosum
(Hornsch.) Mitt.
Leucophanes molleri Müll.Hal.
Leucophanes unguiculatum Mitt.
Lopidium struthiopteris (Brid.) M.
Fleisch.
Macromitrium sulcatum (Hook.)
Brid. var. sulcatum
Mesonodon flavescens (Hook.)
W.R. Buck
Mittenothamnium leptoreptans
(Broth.) Cardot
Neckeromnion lepineanum (Mont.)
S.Olsson, Enroth, Huttunen & D.
Quandt
Neckeropsis disticha (Hedw.)
Kindb.
Octoblepharum albidum Hedw.
Orthostichella rigida (Müll. Hal.)
B.H.Allen & Magill
Orthostichella versicolor (Müll.
Hal.) B.H. Allen & W.R. Buck
Orthostichidium involutifolium
subsp. thomeanum (Broth.) Argent
Orthostichidium involutifolium
(Mitt.) Broth. subsp. involutifolium.
C. Garcia et al.
Synonyms (basionyms) based in
São Tomé and Príncipe collections
P
Hookeria niveum Müll.Hal. 1886
Leucobryum homolophyllum
Broth. 1890
Leucobryum leucophanoides Müll.
Hal. 1886
Leucoloma gracilescens Broth.
1890
Leucoloma secundifolium
Mitt.1863
Leucophanes molleri Müll.Hal.
1886
Leucophanes unguiculatum
Mitt.1863
Hypopterygium subtrichocladum
Broth. 1890
Macromitrium undatifolium Müll.
Hal. 1886
ST
A
A
Year of
first ref.
P/ST
1944
1886
X
2016
A
1959
E
1890
E
1886
A
1890
A
1863
X
1944
X
1886
A
1863
X
X
X
X
1890/
1997
1917/
1886
2011
E
1890
X
X
2017/
2017
X
X
X
X
X
2011/
1993
1944/
1959
1886
X
1886
A
1996/
1890
A
1959
X
Microthamnium leptoreptans
Broth. 1890
Pilotrichella leptoclada Müll.Hal.
1886; P. calomicra Broth. 1890
Pilotrichella inflatifolia Müll.Hal.
1886
Hildebrandtiella thomeana
Broth.1890; Orthostichidium
thomeanum (Broth.) Broth. 1906
A
(continued)
9
The Bryophyte Flora of São Tomé and Príncipe (Gulf of Guinea): Past,. . .
Taxon species/subspecies/variety
Philonotis nanothecia (Müll.Hal.)
Kindb.
Philonotis trichodonta (Müll.Hal.)
Kindb.
Pinnatella minuta (Mitt.) Broth.
Pinnatidendron piniforme (Brid.)
Enroth
Plagiomnium rhynchophorum
(Hook.) T.J.Kop. var.
rhynchophorum.
Pogonatum gracilifolium Besch.
Pogonatum usambaricum (Broth.)
Paris
Pyrrhobryum spiniforme
(Hedw.) Mitt.
Racopilum orthocarpioides Broth.
Racopilum thomeanum Broth.
Radulina borbonica (Bél.) W.R.
Buck
Rhacopilopsis trinitensis (Müll.
Hal.) E.Britton ex Dixon
Rhizofabronia persoonii (Schwägr.)
M.Fleisch var. persoonii.
Rhynchostegium hopfferi (Welw. &
Duby) A.Gepp
Scabrellifolium elongatum (Welw.
& Duby) Enroth
Scabrellifolium substriatum
(Hampe) Enroth
Sematophyllum amblystegiocarpum
(Müll.Hal.) Broth.
Splachnobryum obtusum (Brid.)
Müll.Hal.
Symphyodon pygmaeus (Broth.) S.
He & Snider
Syrrhopodon gardneri (Hook.)
Schwägr.
Syrrhopodon lamprocarpus Mitt.
Tayloria solitaria (Hedw.) T.J.Kop.
& W.Weber
Synonyms (basionyms) based in
São Tomé and Príncipe collections
Bartramia nanothecia Müll.Hal.
1886
Bartramia trichodonta Müll.Hal.
1886
Hypnum africanum Welw. & Duby
1872
245
ST
A
Year of
first ref.
P/ST
1886
E
1886
X
X
X
X
1917/
1872
2011/
2011
1944
P
X
Polytrichum rubentiviride Müll.
Hal. 1886; P. molleri Müll.Hal.
1886
Racopilum orthocarpioides Broth.
1890
Rhacopilum thomeanum Broth.
1890
Trichosteleum
subpycnocylindricum Broth. 1890
Microthamnium subelegentulum
Broth. 1890
Hypnum hopfferi Welw. & Duby
1872
Hypnum molleri Müll.Hal. 1886
Porotrichum caudatum Broth.
1890
Hypnum amblystegiocarpum Müll.
Hal. 1886
Syrrhopodon quintasii Broth. 1890
A
A
1944/
1886
A
1989
X
1886
A
1890
A
1890
X
1890
X
1890
A
1863
E
1872
A
1886
X
1890
E
1886
X
2016
X
2011
X
1890
A
A
1886
1972
(continued)
246
Taxon species/subspecies/variety
Thamnobryum corticola (Kindb.)
De Sloover
Thuidium involvens subsp.
thomeanum (Broth.) Touw
Trachypodopsis serrulata (P.
Beauv.) M.Fleisch. var. serrulata
Trachypus bicolor var. viridulus
(Mitt.) Zanten
Trematodon divaricatus Bruch
Trematodon longicollis Michx.
Trichosteleum dicranelloides Broth.
Vesicularia glaucula (Broth.)
Broth.
Vesicularia scaturigina (Brid.)
Broth.
Vesicularia strephomischos (Welw.
& Duby) Broth.
Wijkia monodii (P.de la Varde) H.
Akiyama
Wijkia trichocoleoides (Müll.Hal.)
H.A.Crum
C. Garcia et al.
ST
A
Year of
first ref.
P/ST
1902
Thuidium thomeanum Broth. 1890
A
1890
Trachypodopsis quintasiana
Broth. 1909
Papillaria molleri Müll.Hal. 1886
A
1909
X
1886
A
1886
X
1886
A
1890
A
1890
A
1863
A
1872
E
1959
A
1886
Synonyms (basionyms) based in
São Tomé and Príncipe collections
Trematodon flexifolius Müll.Hal.
1886??
Trematodon flexifolius Müll.Hal.
1886
Trichosteleum dicranelloides
Broth. 1890
Ectropothecium glauculum Broth.
1890
Hypnum strephomischos Welw. &
Duby 1872
Gollania monodii P.de la Varde
1959
Hypnum trichocoleoides Müll.Hal.
1886
P
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Open Access This chapter is licensed under the terms of the Creative Commons Attribution 4.0
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Chapter 10
Diversity of the Vascular Plants of the Gulf
of Guinea Oceanic Islands
Tariq Stévart, Gilles Dauby, Davy U. Ikabanga, Olivier Lachenaud,
Patricia Barberá, Faustino de Oliveira, Laura Benitez,
and Maria do Céu Madureira
T. Stévart (*)
Missouri Botanical Garden, Africa and Madagascar Department, St. Louis, USA
Herbarium et Bibliothèque de Botanique africaine, Université Libre de Bruxelles, Brussels,
Belgium
Meise Botanic Garden, Meise, Belgium
e-mail: tariq.stevart@mobot.org
G. Dauby
AMAP, botAnique et Modélisation de l’Architecture des Plantes et des végétations, Université
Montpellier, CIRAD, CNRS, INRAE, IRD, Montpellier, France
D. U. Ikabanga
Missouri Botanical Garden, Africa and Madagascar Department, St. Louis, USA
Laboratoire d’Ecologie Végétale et de Biosystématique, Département de Biologie, Faculté des
Sciences, Université des Sciences et Techniques de Masuku, Franceville, Gabon
O. Lachenaud
Herbarium et Bibliothèque de Botanique africaine, Université Libre de Bruxelles, Brussels,
Belgium
Meise Botanic Garden, Meise, Belgium
P. Barberá
Missouri Botanical Garden, Africa and Madagascar Department, St. Louis, USA
F. de Oliveira
Direção das Florestas e da Biodiversidade, São Tomé, Sao Tome and Principe
Herbário Nacional de São Tomé e Príncipe (STPH), Centro de Investigação Agronómica e
Tecnológica, Alto Potó, Sao Tome and Principe
L. Benitez
Fauna & Flora International, Cambridge, UK
Fundação Príncipe, Santo António, Sao Tome and Principe
M. do Céu Madureira
Centre for Functional Ecology, Departamento de Ciências da Vida, Universidade de Coimbra,
Coimbra, Portugal
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_10
249
250
T. Stévart et al.
Abstract Despite a long history of botanical collecting in the three oceanic islands
of the Gulf of Guinea, no recent studies have documented floristic patterns. This
chapter summarizes information on the vascular plants of the islands, including
inventories conducted on Príncipe and São Tomé since 2017, as well as two recent
expeditions to Annobón. An updated database of the vascular flora was compiled,
which includes 14,376 records representing 1285 species and infraspecific taxa
(1028 native). Príncipe has 445 species and infraspecific taxa (394 native), São
Tomé has 1044 (842 native), and Annobón has 344 (274 native). Recent inventory
work has generated collections of more than 90% of the endemic woody species.
Several very rare taxa were rediscovered, including Balthasaria mannii (Oliv.)
Verdc., 1969 (Pentaphylacaceae) and Psychotria exellii R. Alves, Figueiredo and
A.P. Davis, 2005 (Rubiaceae), neither of which had been seen for more than
50 years. At least 17 species new to science were also discovered on Príncipe and
São Tomé. Of the 1028 indigenous taxa, 164 (16%) are currently considered
endemic to the islands. Of the 285 species evaluated according to the IUCN Red
List criteria, 2 (0.7%) were Data Deficient, 226 (79.3%) Least Concern or Near
Threatened, 55 (19.3%) threatened (including 3 Critically Endangered, 21 Endangered, and 31 Vulnerable), and 2 (0.7%) Extinct. On São Tomé and Príncipe,
325 plant species are used in traditional medicine, 37 of which are endemic. These
results should be used to identify new priority sites for conservation, including on
Annobón, where priority sites are less well defined.
Keywords Collecting effort · Endemism · Flora · IUCN red list · Species richness
Despite a long history of collecting in the three oceanic islands of the Gulf of Guinea
(Príncipe, São Tomé, and Annobón), no recent studies have documented their
floristic patterns. In this chapter, we synthesize current knowledge on their diversity
of vascular plants: (1) briefly reviewing the history of botanical exploration,
(2) documenting the spatial distribution of sampling, species richness, and endemism within and between the islands, (3) reviewing risk of extinction assessments
for plant species, using the IUCN Red List criteria, and (4) providing an account of
plants used in traditional medicine in São Tomé and Príncipe.
Sampling Efforts Through Time
São Tomé
Despite the relatively small area occupied by São Tomé and Príncipe compared to
other African countries, their flora has been the subject of many publications
(Figueiredo 1994b; Figueiredo et al. 2011; Droissart et al. 2018). The first comprehensive studies of the flora of São Tomé and Príncipe, primarily focused on São
Tomé, were undertaken by Júlio Henriques from the University of Coimbra (e.g.,
10
Diversity of the Vascular Plants of the Gulf of Guinea Oceanic Islands
251
Fig. 10.1 Collecting effort in the oceanic islands of the Gulf of Guinea, showing numbers of
species and records accumulated through time. Insert figure shows the number of species newly
recorded per year. Specimens were excluded if they had an estimated georeferencing precision
greater than or equal to 4 km. A total of 2600 records were excluded because they lacked
information on the year of collection
Henriques 1892, 1917), who worked on the collections made during the 1880s by
Francisco Newton, Adolfo Moller and Francisco Quintas (Figueiredo and Smith
2019; Ceríaco et al. 2022). In 1932–1933, Arthur Wallis Exell visited the three
islands, collecting extensively and publishing the seminal catalogue of vascular
plants (Exell 1944), in which many new species were described and several new
records noted. Exell subsequently published a few additional papers (e.g., Exell
1956, 1959; Exell and Rozeira 1958), and finally produced a preliminary checklist of
the Angiosperms of the islands (Exell 1973). Fieldwork largely stopped for the next
20 years, followed by an extensive period of collecting (Fig. 10.1), supported for the
first 10 years by the ECOFAC project, which was funded by the European Commission. The Bom Sucesso Botanical Garden and the National Herbarium (STPH)
were established on São Tomé during this period, and a few papers were published
on the flora of the islands (e.g., Stévart et al. 2000; Stévart and Oliveira 2000; Stévart
and Cribb 2004). In 2011, a new checklist was published, providing a good synthesis
of the history of botanical studies, and the current state of knowledge of the flora
with citations of herbarium specimens (Figueiredo et al. 2011). A significant
collecting effort since 2016 justifies a new synthesis on the diversity of vascular
plants of these islands (Fig. 10.1).
252
T. Stévart et al.
Príncipe
The history of floristic surveys on Príncipe is largely similar to that of São Tomé.
During the nineteenth and twentieth century, Príncipe was visited by several collectors during expeditions to São Tomé or Annobón (Exell 1944; Figueiredo 1994a;
Figueiredo and Smith 2019, 2020; Ceríaco et al. 2022). The flora of Príncipe was
included in several checklists and publications (Exell 1944, 1956, 1959, 1973; Exell
and Rozeira 1958; Figueiredo et al. 2011). A few collecting expeditions were
conducted in the late 1990s with support from the ECOFAC project, followed by
sporadic collections during the subsequent 20 years. In 2016, a project aiming to
describe the tree diversity of Príncipe was initiated, which included exhaustive
collecting, especially in the southern part of the island, and the production of the
first forest classification ever proposed for Príncipe (Benitez et al. 2018). This
initiative also supported the creation of an unofficial herbarium at the Príncipe
Natural Park headquarters, built local botanical capacity, conducted Red List assessments, and made floristic data available online (Tropicos 2021).
Annobón
An account of the history of botanical studies on Annobón was presented in its most
recent checklist (Velayos et al. 2013a). The oldest collections from the island are
probably those made during the nineteenth century by the British botanists Andrew
B. Curror (1839–1843) and Richard Burton (1861–1864). The first study specifically
dealing with the flora of Annobón was published by the German botanist Johannes
Mildbraed from the Botanical Garden of Berlin, based on his collection made in
1911 (Mildbraed 1937) during the 1910–1911 Deutsche Zentral-Afrika-Expedition.
As mentioned above, Exell also published on its flora (Exell 1944, 1956, 1963,
1973), including ca. 40 specimens he collected in 1933. Luís G. Sobrinho studied the
material collected by Francisco Newton between November 1892 and January 1893
(Sobrinho 1953). Finally, in 2010 and 2011, botanists of the Real Jardín Botánico
Madrid and the Universidad Nacional de Guinea Ecuatorial collected exhaustively
on the island, subsequently publishing an updated catalogue of the plants of
Annobón with citations of herbarium specimens (Velayos et al. 2013a).
Spatial Distribution of Collecting Effort
The Database
Recent data on the flora of Príncipe, São Tomé, and Annobón were included in an
updated version of the RAINBIO database (Dauby et al. 2016). The quality and
10
Diversity of the Vascular Plants of the Gulf of Guinea Oceanic Islands
253
accuracy of georeferencing of all specimen records were assessed first by verifying
whether they fell within the limits of the islands and, if not, at what distance from the
coast, using the CoordinateCleaner R package (Zizka et al. 2019). When errors or
inaccuracies were detected, or when coordinates were entirely missing,
georeferencing was corrected or added manually using the locality information
indicated on specimen labels. A scale from one to nine was used to indicate the
precision of the georeferencing of each record, assigned based on label coordinates,
either manually or automatically (Dauby et al. 2016). When the elevation was
provided on the specimen label, it was recorded in the database, otherwise it was
retrieved from an elevation raster based on the geo-coordinates. The resulting
database includes 14,376 records, among which 12,077 represent collections identified to the species level, and 12,790 are georeferenced, constituting the largest and
most comprehensive dataset ever compiled for the islands.
Collecting Effort
Collecting effort is highly heterogeneous on all islands (Fig. 10.2). In Príncipe, most
fieldwork has been concentrated at higher elevations, centered on Pico Papagaio and
near Pico do Príncipe. The same is true for São Tomé, where they are concentrated
around Pico de São Tomé and between Bom Sucesso and Lagoa Amélia. In
Annobón, they have focused around Lake Apot, but also on the coast near Punta
Yalba. All of these locations but the last are at higher altitudes and harbor relatively
intact vegetation (Dauby et al. 2022). When standardized by area (Fig. 10.3),
highlands clearly appear as the most intensely collected, while the lowlands and
the rugged central portions of the islands are the most under-collected (Fig. 10.2).
This pattern of collection suggests that botanists tend to conduct fieldwork in
accessible areas that have less impacted vegetation, while more heavily impacted
areas at lower elevations or very remote locations remain undersampled.
Species richness has a bimodal distribution with respect to elevation gradient on
São Tomé. It should be stated that this decrease is only due to the fact that elevated
areas are much less extensive. In fact, when you look at areas of comparable size
(Fig. 10.2) the diversity is higher in elevated areas. Species richness is, however,
also well correlated with sampling effort, so it is not clear to what extent these
patterns are biased by sampling. The second explanation is obviously the
correct one: 1100–1200 m is the area where lowland and montane species overlap,
hence the higher diversity.
On Príncipe, Pico de Príncipe was relatively less well collected than Pico
Papagaio because it is less accessible, the trail being uncovered by the first modern
field surveys during the ECOFAC project in the 1990s (Baillie 1999). The southern
part of the island was poorly collected until recently because it is usually accessed by
boat. The recent field expedition conducted as part of the Global Tree Campaign
allowed surveying the flora around Rio Porco, where the last remaining example of
original littoral forest can be found on the islands (Benitez et al. 2018).
254
T. Stévart et al.
Fig. 10.2 Maps of Príncipe, São Tomé, and Annobón, showing the number of specimens, number
of species, and proportion of endemic species per 1 km-sided hexagon. The proportion of endemic
species is only shown in hexagons with at least 25 specimen records for Annobón and 20 elsewhere.
Specimens whose estimated georeferencing precision is greater than 4 km were excluded. The red
outline demarks the boundaries of Natural Parks
On São Tomé, some lowland areas have been relatively well explored, namely
around São Miguel, São João dos Angolares, and the mouths of Xufe-Xufe or Iô
Grande River. These have been less sampled than the highlands, thus remaining
10
Diversity of the Vascular Plants of the Gulf of Guinea Oceanic Islands
255
Fig. 10.3 (a, c, e) Number of species and (b, d, f) sampling effort relative to area along 100 m
elevational bands for (a, b) São Tomé, (c, d) Príncipe and (e, f) Annobón. Sampling effort was
obtained from specimen density per unit of area, and numbers indicate the area covered by each
elevational band in km2. The color scale represents the proportion of endemic species. Specimens
whose estimated georeferencing precision is greater than 4 km were excluded. When available,
elevation was retrieved from the specimen label, otherwise it was estimated from the elevation raster
based on coordinates
overall poorly sampled given their much larger area (Fig. 10.3). Observed species
richness on São Tomé (Fig. 10.2b) is particularly high around the Pico de São Tomé,
Lagoa Amélia, and Bom Sucesso, but is also highly correlated with specimen density
256
T. Stévart et al.
(Pearson correlation R ¼ 0.94) and is therefore certainly underestimated in most
other parts of the island.
On Annobón, the number of species per 1 km-sided hexagons is also correlated
with collecting effort (Fig. 10.2g–h), but the proportion of endemic plants is higher
in the elevated area of the island (Figs. 10.2i and 10.3).
Floristic Diversity
The numbers of vascular plant taxa recorded from São Tomé and Príncipe were
indicated in the most recent checklist (Figueiredo et al. 2011): 135 families (of which
29 are introduced), 624 genera (172 introduced), and 1104 species (301 introduced),
along with 12 infraspecific taxa, including 119 endemic taxa (107 species and
12 infraspecific taxa). However, these figures only concern São Tomé and Príncipe,
and extensive inventories have since been conducted on Príncipe (Benitez et al.
2018) and on São Tomé (Flora Ameaçada 2021). An updated calculation indicates
that 1285 species and infraspecific taxa (1028 native) are known to occur on the three
islands (Table 10.1). Príncipe has 445 species and infraspecific taxa (394 native),
São Tomé has 1044 (842 native), and Annobón has 344 (274 native). Príncipe has
the highest proportion of native flora (88.5%), followed by São Tomé (80.7%), while
Annobón has the lowest (79.7%).
The three most species-rich families are Orchidaceae (163 taxa), Rubiaceae
(94 taxa), and Fabaceae (86 taxa); however, many of the Fabaceae are not native
(Table 10.2). Euphorbiaceae s.l., as previously delimited, was one of the most
speciose families, but its members have recently been divided among Euphorbiaceae
s.str. (44 taxa) and Phyllanthaceae (27 taxa).
The genera with the most species and infraspecific taxa are Asplenium L. (28),
Bulbophyllum Thouars (27), and Polystachya Hook. (26) (Table 10.3), all of which
are wind-dispersed.
Table 10.1 Family, genus, species, and infraspecific taxon richness on each of the three oceanic
islands of the Gulf of Guinea
Families
Genera
Species and infraspecific taxa richness (SR)
SR native
% of the flora which is native
Individuals
Príncipe
94
264
445
394
88.5
1876
São Tomé
143
561
1044
842
80.7
8182
Annobón
90
241
344
274
79.7
773
Total
155
627
1285
1028
80.0
11,388
The number of native species or infraspecific taxa is given as well as the native proportion of each
island’s flora
10
Diversity of the Vascular Plants of the Gulf of Guinea Oceanic Islands
257
Table 10.2 The most species-rich families on the oceanic islands of the Gulf of Guinea
Orchidaceae
Rubiaceae
Fabaceae
Poaceae
Euphorbiaceae
Cyperaceae
Asteraceae
Aspleniaceae
Phyllanthaceae
Malvaceae
SR
163
94
86
46
44
34
31
28
27
26
Príncipe
85
46
14
4
14
8
2
14
14
1
São Tomé
125
73
70
40
32
25
28
25
20
21
Annobón
25
18
38
24
12
14
9
5
6
12
Grand total
235
137
122
68
58
47
39
44
40
34
Numbers indicate specific and infraspecific taxon richness (SR) for all islands taken together and for
each individual island. The grand total represents the total number of species-presences recorded
across the islands
Table 10.3 The most species-rich genera on the oceanic islands of the Gulf of Guinea
Asplenium
Bulbophyllum
Polystachya
Cyperus
Psychotria
Ipomoea
Begonia
Ficus
Pteris
Desmodium
SR
28
27
26
22
13
12
11
11
11
10
Príncipe
14
14
12
2
4
2
5
3
7
1
São Tomé
25
20
21
16
12
8
10
10
9
9
Annobón
5
4
6
11
2
4
2
3
1
9
Grand total
44
38
39
29
18
14
17
16
17
19
Numbers indicate specific and infraspecific taxon richness (SR) for all islands taken together and for
each individual island. The grand total represents the total number of species-presences recorded
across the islands
Main Findings of the Botanical Expeditions on São Tomé
and Príncipe, 2019–2020
To improve the documentation of the current floristic diversity of São Tomé and to
identify conservation priorities, several botanical expeditions were undertaken
between 2019 and 2021 (Flora Ameaçada 2021). Various localities across the island
were visited, from the dry North to the wet South, and from the coast to the summit
of the Pico de São Tomé at 2024 m, covering most vegetation types. More than 90%
of the endemic woody species were seen during this fieldwork. Some very rare
species were rediscovered, including Balthasaria mannii (Oliv.) Verdc., 1969
(Pentaphylacaceae) (Fig. 10.4.2–4), and Psychotria exellii R. Alves, Figueiredo
and A.P. Davis, 2005 (Rubiaceae), both restricted to near the summit of the Pico
258
T. Stévart et al.
Fig. 10.4 Species endemic to São Tomé and Príncipe: (1) Santiria balsamifera Oliv., 1887
(Burseraceae); (2–4) Balthasaria mannii (Oliv.) Verdc., 1969 (Theaceae); (5) Cleistanthus
sp. nov. (Euphorbiaceae); (6) Impatiens manteroana Exell, 1944 (Balsaminaceae). Photos credits:
(1, 6) Tariq Stévart, (3–5) Olivier Lachenaud, (2) Gilles Dauby
10
Diversity of the Vascular Plants of the Gulf of Guinea Oceanic Islands
259
de São Tomé and not seen for more than 50 years. Even more interesting is the
finding of at least 17 species new to science—a number likely to increase as the
ongoing identification of specimens continues. The most remarkable of these is a
new species of Cleistanthus Hook. f. ex Planch., 1848 (Phyllanthaceae)
(Fig. 10.4.5), which is the dominant tree of dry forest remnants in the North of the
island. Several earlier collections of this species are deposited in herbaria, but they
had not yet been identified. Although locally abundant, the new species of
Cleistanthus is highly threatened by wood exploitation and charcoal production,
and its habitat is in need of protection. In addition, 42 species represent new country
records for São Tomé and Príncipe, most of which are widespread on the mainland.
One of them, Phyllocosmus sessiliflorus Oliv., 1868 (Ixonanthaceae), is the first
record of its family from the islands. Other species previously known from the
country are new island records, namely five for São Tomé and 26 for Príncipe.
Complementing the efforts undertaken since 2016 to understand tree diversity in
the southern forests of Príncipe (Benitez et al. 2018), since 2019, several botanical
expeditions have focused on the drier North (Flora Ameaçada 2021). This work
included areas of secondary or presumably degraded forest, extending from coastal
and lowland forests to the northern plateau of the island, but also involved collecting
in areas in the south that had not been assessed during previous years, such as the
summit of Pico do Príncipe (947 m). These inventories resulted in the discovery of
eight species new to science, six of which are only known from Príncipe.
Endemism
The flora of the Gulf of Guinea Islands comprises approximately 1700 indigenous
species of angiosperms (Figueiredo 1994b), and is well known for its high level of
endemism. Bioko is a continental island, while Príncipe, São Tomé and Annobón are
oceanic, never having been connected to the mainland or to one another. It is
therefore not surprising that Bioko has a more speciose flora (1558 species, Velayos
et al. 2013b), but exhibits much lower levels of endemism (3.6% according to Exell
1973).
Of the 1028 indigenous species and infraspecific taxa documented from Príncipe,
São Tomé, and Annobón, approximately 164 are endemic (Table 10.4, Figs. 10.4,
10.5, 10.6 and 10.7), yielding a rate of endemism of about 16%. Estimates for
endemism on Príncipe have varied significantly over the years, from 12.7% (Exell
1944), to 9.9% (Exell 1973), and to the current 14.7% for vascular plants
(Table 10.4). Calculations of endemism in São Tomé have decreased from 19.4%
(Exell 1944) to 15.4% (Exell 1973) and the current 14.5% (Table 10.4). On
Annobón, they are estimated to be at 6.9% (Table 10.4).
The families with the largest numbers of endemic taxa are Orchidaceae (30),
Rubiaceae (29), and Euphorbiaceae s.str. (15) (Table 10.5). The genera Polystachya
(Orchidaceae), Begonia L., 1753 (Begoniaceae) and Psychotria L., 1759
(Rubiaceae) have the largest numbers of endemic species (Table 10.6). Some
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T. Stévart et al.
Table 10.4 Plant endemism in the oceanic islands of the Gulf of Guinea (including 17 putative
new species)
Single-island endemic species
Shared endemics between islands
Total endemics
Indigenous species
Endemic rate (3 islands)
Endemic rate (strict)
Príncipe
28
30
58
394
14.7
7.6
São Tomé
90
32
122
842
14.5
3.8
Annobón
14
5
19
274
6.9
1.8
Total
132
32
164
1028
16.0
3.1
emblematic endemic species are the gigantic species Begonia baccata Hook.f., 1866
and Begonia crateris Exell, 1944, which can reach a height of 4 m. Afrocarpus
mannii (Hook.) C.N. Page, 1988 (Podocarpaceae), the only native gymnosperm, is
endemic to São Tomé and is widely grown in many botanic gardens around the
world. The proportion of endemic species tends to increase with elevation with an
endemic rate between 20 and 25% in the highlands of the three islands (Fig. 10.3).
Conservation
From 1998 to 2020, risk of extinction assessments were performed for 285 native
and introduced plant species from Príncipe, São Tomé, and Annobón Islands (IUCN
2021). These taxa belonged to 207 genera and 86 families, and over 13% are
endemic to São Tomé and Príncipe. Cyperus L., 1753 (Cyperaceae) is the bestrepresented genus, with twelve species assessed; the remaining genera are
represented by between one and four species each. Seven families have more than
ten species assessed: Orchidaceae (34.9% of all species assessed), Fabaceae
(29.1%), Cyperaceae (24.4%), Rubiaceae (23.3%), Euphorbiaceae (17.4%),
Apocynaceae and Phyllanthaceae (11.6% each). Thirty-two assessments were
made in 1998 and 62 more were done between 2000 and 2017. The number of
species assessed has more than doubled between 2018 and 2020 (Fig. 10.8). Of the
285 species evaluated to date, 0.7% are Data Deficient, 19.3% are threatened
(3 Critically Endangered, 21 Endangered, and 31 Vulnerable), and 78.3% are
Least Concern or Near Threatened. Two Orchidaceae species (Angraecopsis
dolabriformis (Rolfe) Schltr., 1918 and Angraecum astroarche Ridl., 1887) are considered Extinct (Simo et al. 2018a, b), since they were not recorded after intensive
surveys in the locations where they had previously been documented. The number of
species assessed as threatened per year has decreased over time, even though the
total number of assessments performed each year has increased: 22 of 32 species
were assessed as threatened in 1998, compared to just 21 of 191 assessments done
over the last three years (Fig. 10.7; Table 10.7). This is partly due to numerous recent
assessments on widespread non-threatened tree species (e.g., Symphonia globulifera
L. f., 1782, Xylopia aethiopica (Dunal) A. Rich., 1845, Cola digitata W. Mast.,
10
Diversity of the Vascular Plants of the Gulf of Guinea Oceanic Islands
261
Fig. 10.5 Species endemic to São Tomé and Príncipe: (1) Carapa gogo A. Chev. ex Kenfack, 2011
(Meliaceae); (2–3) Palisota pedicellata K.Schum., 1897 (Commelinaceae); (4) Polystachya
expansa Ridl., 1887 (Orchidaceae); (5) Pandanus thomensis Henriq., 1887 (Pandanaceae); (6–7)
Lobelia barnsii Exell, 1944 (Campanulaceae); (8–9) Impatiens buccinalis Hook.f., 1864
(Balsaminaceae). Photo credits: (all, except 6) Tariq Stévart, (6) Gilles Dauby
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T. Stévart et al.
Fig. 10.6 Species endemic to São Tomé and Príncipe: (1) Thunbergianthus quintasii Engl., 1897
(Scrophulariaceae); (2) Costus giganteus Welw. ex Ridl., 1887 (Costaceae); (3) Rhipidoglossum
pendulum (la Croix & P.J.Cribb) Farminhão & Stévart, 2018 (Orchidaceae); (4) Dicranolepis
thomensis Engl. & Gilg, 1894 (Thymelaeaceae); (5) Tabernaemontana stenosiphon Stapf, 1895
(Apocynaceae); (6) Leea tinctoria Lindl. ex Baker, 1868 (Leeaceae); (7) Elatostema thomense
Henriq., 1892 (Urticaceae); (8) Begonia crateris Exell, 1944 (Begoniaceae); (9) Erica thomensis
(Henriq.) Dorr & E.G.H.Oliv., 1999 (Ericaceae). Photo credits: (all, except 8) Tariq Stévart, (8)
Olivier Lachenaud
10
Diversity of the Vascular Plants of the Gulf of Guinea Oceanic Islands
263
Fig. 10.7 Species endemic to São Tomé and Príncipe: (1) Erica thomensis (Henriq.) Dorr & E.G.
H.Oliv., 1999 (Ericaceae); (2) Chytranthus mannii Hook.f., 1867 (Sapindaceae); (3) Strephonema
sp. nov. (Combretaceae). Photo credits: (1) Davy Ikabanga, (2) Laura Benitez, (3) Tariq Stévart
1868, and Santiria trimera (Oliv.) Aubrév., 1948) (Fig. 10.4.1). Some species
require better knowledge before they can be assessed (e.g., Santiria trimera) or are
outside of their native range (Coffea arabica L., 1753), and therefore their presence
264
Table 10.5 The ten families
with the largest number of
endemic species and infraspecific taxa on the three oceanic
islands of the Gulf of Guinea
T. Stévart et al.
Family
Orchidaceae
Rubiaceae
Euphorbiaceae
Begoniaceae
Melastomataceae
Sapotaceae
Violaceae
Acanthaceae
Aspleniaceae
Balsaminaceae
Príncipe
10
10
6
2
2
1
1
1
São Tomé
22
21
11
5
5
2
3
3
2
2
Annobón
2
3
2
2
1
Total
30
27
15
6
6
4
4
3
3
3
Numbers indicate specific and infraspecific taxon richness (SR)
Table 10.6 The ten genera
with the largest number of
endemic species and infraspecific taxa on the three oceanic
islands of the Gulf of Guinea
Genus
Polystachya
Psychotria
Begonia
Diaphananthe
Rinorea
Tristemma
Asplenium
Cassipourea
Chassalia
Dryopteris
Príncipe
4
2
2
1
1
1
2
São Tomé
5
8
4
2
3
3
2
1
2
2
Annobón
1
1
1
1
1
Total
8
8
6
4
4
4
3
3
3
3
Numbers indicate specific and infraspecific taxon richness (SR)
on these islands is irrelevant for Red Listing, and they were not included in this
analysis. For example, a recent taxonomic revision of Santiria Blume, 1850, in
Africa revealed that a threatened species (S. balsamifera Oliv., 1886) occurs on São
Tomé and Príncipe (Ikabanga et al. 2019). Additional efforts will be needed to assess
other endemic and range-restricted species to enable a more accurate assessment of
the true proportion of threatened plant species on the oceanic islands of the Gulf of
Guinea.
Recent Red List activities and field expeditions have shown that the flora of São
Tomé and PrÚncipe is highly threatened, in addition to historical threats that have
ceased, such as large-scale plantations that profoundly changed the natural vegetation of the two islands (Muñoz-Torrent et al. 2022). On Príncipe, current threats are
relatively limited and not clearly defined, but certainly include the development of
infrastructure for tourism (Lima et al. 2022), whose impact on the flora remains to be
quantified. The development of human activities adds pressure on the remaining
forests in the north, which are already threatened by small-scale agriculture, charcoal
production, firewood collection, and logging (D’Avis 2022). The collection and use
of medicinal plants are also subjecting some species to the risk of local extinction.
Diversity of the Vascular Plants of the Gulf of Guinea Oceanic Islands
265
90
100 %
80
90 %
70
80 %
70 %
60
60 %
50
50 %
40
40 %
30
30 %
20
20 %
10
10 %
0
Cumulative frequency
Number of assessments
10
0%
1998 2000 2004 2010 2011 2012 2013 2014 2015 2016 2017 2018 2019 2020
Years
Number of assessments
Cumulative frequency
Fig. 10.8 Progress of the number of risk of extinction assessments made for species occurring on
Príncipe, São Tomé, and Annobón islands from 1998 to 2020
Table 10.7 Number of
threatened species recorded on
Príncipe, São Tomé, and
Annobón islands from 1998
to 2020
Threatened species
CR
EN
Years
1998
0
1
2000
1
0
2004
0
2
2013
0
1
2014
0
1
2018
2
9
2019
0
1
2020
0
6
Total threatened species
VU
21
0
4
1
3
0
1
1
Total
22
1
6
2
4
11
2
7
55
Indeed, most of the plants harvested by traditional healers and by commercial sellers
who collect medicinal plants for alcoholic beverages come from forests, and very
few plants are cultivated for medicinal purposes. On São Tomé, threats include local
logging around the parks, and the widespread presence of invasive species (Lima
et al. 2022). These threats do not affect most species directly, but they impact the
quality of their habitat. The most severe current threats on São Tomé are, however,
the presence of an oil palm plantation in the southwest of the island, and charcoal
production is also an important threat, especially in the north (Oyono et al. 2014).
These activities have expanded in recent years and directly impact populations of
plant species. On Annobón, plants occurring in almost all parts of the island are
threatened by small-scale agriculture. The dry northern part of the island, from the
sea to Lake Apot, is particularly heavily impacted by agriculture, urbanization, and
infrastructure construction (Norder et al. 2020).
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T. Stévart et al.
The Medicinal Plants of São Tomé and Príncipe
Many medicinal plants have been used for centuries on São Tomé and Príncipe and
are often the only available therapeutic agents. Until the end of the twentieth century,
uses were not well documented, and few ethnopharmacological studies had been
conducted on the medicinal plants used by the population of the two islands.
Between 1993 and 2001, an exhaustive collection of the medicinal flora was
conducted to record ethnomedical information from the most renowned local traditional healers. More than 350 taxa were identified, for which voucher specimens
were deposited at the University of Coimbra herbarium (COI), and more than 1000
traditional preparation procedures and their respective uses were recorded
(Madureira et al. 2003). Exhaustive bibliographic research was also conducted,
resulting in a monograph for each species containing traditional uses and scientific
data (Madureira et al. 2003; Madureira 2006, 2010).
These investigations show a strong correlation between the traditional use of most
medicinal plants and their proven pharmacological activity, demonstrating that many
of them have a recognized efficacy: e.g., Spermacoce verticillata L., 1753,
Desmodium adscendens (Sw.) DC., 1825, Dracaena arborea (Willd.) Link, 1821,
Phyllanthus amarus Schumach. & Thonn., 1827, Phyllanthus urinaria L., 1753,
Piper capense L.fil., 1781, Scoparia dulcis L. 1753 (Madureira 2006, 2008), along
with Tithonia diversifolia (Hemsl.) A. Gray, 1883, an introduced species that has
antimalarial activity and could be a very interesting alternative to commercially
available antimalarials (Madureira 2010). An analysis of the composition of essential
oils from eighteen species widely used in traditional medicine for the treatment of
infections was carried out, and the preliminary study of the antibacterial and
antifungal activities of these essential oils proved their activity, highlighting the
oils of Cymbopogon citratus (DC.) Stapf, 1906, Ocimum gratissimum l., 1753,
Santiria balsamifera and Zingiber officinale Roscoe, 1807, which showed the best
activities (Martins 2002). Some of these medicinal plants have been studied for their
antiviral properties (Phyllanthus amarus, Scoparia dulcis, Momordica charantia L.,
1753, and Margaritaria discoidea (Baill.) G.L. Webster, 1967). Other species have
shown some promising results regarding their antitumor activity, such as
Desmodium adscendens, Piper capense, and Momordica charantia (Madureira
2008), and more recently the identification of natural compounds from Voacanga
africana Stapf, 1894, that show multiple biological activities of interest for
Alzheimer’s disease (Currais et al. 2014).
The families with the largest numbers of species used for medicinal purposes are
Euphorbiaceae (13 species), Asteraceae (12), Rubiaceae (11), Moraceae (10),
Malvaceae (9), Rutaceae (8), and Apocynaceae (7). The fact that many families
(57) and genera (134) are represented on the list of medicinal species illustrates the
high level of knowledge of the flora among traditional healers, and it is possible to
infer that there are a great variety of chemical structures and pharmacological
activities among the medicinal plants collected in the region.
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Diversity of the Vascular Plants of the Gulf of Guinea Oceanic Islands
267
The traditional uses of the medicinal plants are highly diverse: analgesic, antiinflammatory or anti-rheumatic action represent the main group of traditional records
(218), followed by diseases of the digestive system (204); diseases related to the
respiratory system represent the third group with 179 traditional records; genitourinary system (134); skin diseases (97); traditional medicines for the treatment of
febrile conditions (38) and malaria (23); diseases of the cardiovascular system (43);
14 preparations for the treatment and control of diabetes, and 16 indications for
diseases of the central nervous system. Finally, on São Tomé and Príncipe, many
medicinal plants are also used for food, representing about 15.0% of the total species
collected for medicinal purposes (Madureira 2012).
Among the 350 medicinal species used, 37 are endemic to the islands of the Gulf
of Guinea (e.g., Tabernaemontana stenosiphon, Begonia baccata, Croton stellulifer
Hutch. 1944, Hernandia beninensis Welw. ex Henriq., 1892, Staudtia pterocarpa
Warb., 1897, Pandanus thomensis Henriq., 1887, Afrocarpus mannii, Chytranthus
mannii Hook.f., 1867, and Costus giganteus Welw. ex Ridley, 1887), which indicates an evident dynamism of the local traditional medicine, with traditional healers
maintaining and perfecting their traditional therapeutic wisdom, and taking advantage of the native available resources of São Tomé and Príncipe.
Improving Local Botanical Practices and Knowledge
The literature review for this chapter revealed a heavy reliance on a few key
publications for the identification of medicinal plant species based on local vernacular names (Rozeira 1958; Roseira 1984; Figueiredo 2002; Figueiredo et al. 2011),
the majority of which lack the citation of voucher specimens. Vernacular names are
important for identification of plants locally, but to be reliable and of use for
scientific studies, they must be unambiguously linked to scientific names, which
requires the collection and storage of voucher specimens. This need is particularly
pressing considering that local names vary from region to region, sometimes multiple species having the same name, or multiple names referring to a single species
(e.g., Figueiredo et al. 2011). This is especially true in the case of medicinal plant
parts that are sold in the markets, for which accurate identification to species is even
more difficult, but also for ecological studies such as tree inventories, which have so
far mostly used local names (e.g., Salgueiro and Carvalho 2001).
Basic botanical skills are also largely lacking, especially with respect to plant
taxonomy and botanical nomenclature. The correct botanical name of an individual
plant, linked to a voucher specimen, is the sine qua non of phytomedical research.
Without the unique taxonomic identifier, research cannot accurately be linked to the
existing literature. This uncertainty, thus obstructs the accuracy and reproducibility
of results—a cornerstone of science. It is therefore vital to increase local scientific
literacy, and continue training local botanists with different skills, from field identification, to the management of herbarium specimens, and more advanced scientific
capacities to ensure increased local autonomy for research and conservation. To
268
T. Stévart et al.
overcome these handicaps, the publication of a practical field guide to facilitate plant
identification and stimulate the interest for botany is highly recommended.
Concluding Remarks
Significant collecting effort, especially since 2016, has created a huge updated
wealth of information for the islands, which is readily available online (Tropicos
2021). Nevertheless, this information is still being compiled and will require extensive taxonomic work and numerous publications until it can produce an updated
vascular plant checklist for the islands. The same is true for Red List assessments,
many of which seem to be focusing on species that are widespread, while endemic
and range-restricted species that are more likely to be threatened remain unassessed.
This calls for a major, consolidated focus on conservation assessments, which are
currently being conducted through several mostly uncoordinated projects. The
results of this work could and should then be used to identify new priority sites for
conservation (D’Avis 2022; Lima et al. 2022), including on Annobón, where priority
sites are less well defined.
Acknowledgments This work was supported by the Critical Ecosystem Partnership Fund, a joint
initiative of l’Agence Française de Développement, Conservation International, the European
Union, the Global Environment Facility, the Government of Japan and the World Bank, through
the project CEPF-104130. Data collection on Príncipe was conducted by Fauna & Flora International, Fundação Príncipe, the Missouri Botanical Garden, and the University of Coimbra,
supported by the Global Tree Campaign through multiple grants. We are also grateful to Ricardo
F. de Lima, Roy Gereau, and Porter P. Lowry II for editing the manuscript and for their constructive
comments and suggestions.
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Chapter 11
A Checklist of the Arachnids from the Gulf
of Guinea Islands (Excluding Ticks
and Mites)
Sarah C. Crews and Lauren A. Esposito
Abstract While historic efforts to document the arachnofauna of the Gulf of Guinea
islands have primarily been the result of fortuitous collecting by non-specialists,
recent efforts have been made to provide a more thorough documentation using
systematic, targeted collecting methods. Results from those preliminary efforts
indicate that the current formal scientific knowledge of the fauna is significantly
underreported. Here, we present the first checklist of all arachnid species, excluding
mites and ticks, for the Gulf of Guinea islands. We hope that this will serve as a
guide to begin the immense work of documenting the true diversity represented in
this unique archipelago.
Keywords Diversity · Scorpion · Spider · Survey
Introduction
This chapter provides a preliminary account of the arachnids that occur on the
islands of Bioko, Príncipe, São Tomé, and Annobón. We treat our assessment as
preliminary because to comprehensively determine which arachnids inhabit a place,
systematic, multi-year, seasonal surveys are critical. For many arachnid species, the
annual lifecycle is temporal, often with adult males and females more common at
particular times of the year (Cardoso et al. 2009). Standardized collecting methods
have been proposed for arachnids, which allow for a more effective estimate of
species richness when collecting efforts are limited (e.g., Malumbres-Olarte et al.
2016). To date, however, this type of surveying for arachnids has not been undertaken on any of the Gulf of Guinea islands. In fact, nearly all of the historical
collectors of arachnids in the region, including West and Central Africa, collected
them opportunistically while making general collections of flora and fauna or
targeting other organisms. The lack of methodical collecting across much of the
S. C. Crews · L. A. Esposito (*)
Institute for Biodiversity Science and Sustainability, California Academy of Sciences, San
Francisco, USA
e-mail: lesposito@calacademy.org
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_11
273
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S. C. Crews and L. A. Esposito
African continent and the monumental work needed for subsequent taxonomic
investigation also hinders our ability to discern whether species recorded from the
islands are endemic or are also present on the mainland. Consequently, our current
knowledge of the arachnid fauna of the islands is far from complete given the few
historical or contemporary surveys dedicated to documenting arachnid diversity and
minimal taxonomic study of most major groups. Here we summarize what is (and
likely is not) known about the arachnid diversity of the Gulf of Guinea archipelago in
the hopes that it will inspire and guide future research on this understudied group.
Arachnids are a diverse and ancient group (>430 my old) of primarily terrestrial
arthropods. There are 11 extant orders, all of which are known from mainland
Africa, with 8 known from the Gulf of Guinea islands. While Acari, or ticks and
mites, are present, we do not discuss them here. They are typically treated separately
in arachnid faunal overviews and surveys because, although they are arachnids, they
are extremely diverse and even more poorly known than other arachnids. Their life
histories and habits differ greatly from the other arachnids in that many are plant or
animal parasites or live in soil.
There are three orders of arachnids that have not yet been found on the Gulf of
Guinea islands, although they are known from the adjacent mainland. One of these
orders is the Palpigradi, or microwhip scorpions, which are very small, pale, eyeless
animals that live interstitially in leaf litter, caves, or cracks deep in the ground. They
are found worldwide, but due to their cryptic habits and small size, fewer than
100 species have been described (Harvey 2013a). The other two orders, however, are
not minute. These are the Solifugae, or sun spiders, and the Thelyphonida, or whip
scorpions. The former consists of about 1000 species that are primarily found in dry
habitats, while the latter has only about 100 species described from a wide variety of
tropical and sub-tropical ecosystems (Harvey 2013e; Murienne et al. 2013).
Although they are not small, whip scorpions are burrowers, thus not easily detected,
and there is only a single species known from Africa (Huff and Prendini 2009).
Below, we discuss the seven other orders: Amblypygi or whip spiders, Opiliones or
harvestmen, Pseudoscorpiones or pseudoscorpions, Ricinulei or hooded tickspiders,
Schizomida or short-tailed whip scorpions, Scorpiones or scorpions, and include a
focused discussion of the most diverse group, the Araneae or spiders.
A Brief History of Arachnological Research
In the 1700s and 1800s, most arachnid collecting in the Gulf of Guinea was done by
naturalists making general collections of extant flora and fauna as well as fossils. The
specimens were then sold or donated to European museums, where they were
divvied up and given to experts on the various groups, who then described new
species and/or published a species list. Ferdinand Karsch (1884) was likely the first
arachnologist to focus specifically on arachnids from the Gulf of Guinea islands. He
received the specimens for his study from Professor Richard Greeff of Marburg, who
had lived on São Tomé and Príncipe islands for several months in 1879–1880.
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275
Greeff made some of the first maps of the islands and collected everything from
crinoids (echinoderms) to sipunculids (peanut worms) to geckos and published his
results in 1884. Other authors published smaller works on the island fauna, including
Vieira (1893) and Pocock (1900), the latter of whom described some theraphosid
spiders that had been purchased by trustees of the British Museum.
Leonardo Fea from the Museum of Natural History in Genoa, Italy made trips to
Asia and Africa in the late 1800s to the early 1900s, spending 1900–1902 on São
Tomé and Príncipe, Bioko, and Annobón, and 1902 in Cameroon and the French
Congo (now the Republic of Congo, Gabon, and Central African Republic).
Although primarily collecting specimens for his malacological and geological
research, he also collected several arachnids. These specimens eventually made
their way to perhaps the most prolific arachnologist of all time, Eugene Simon
from the Natural History Museum in Paris. In the early 1900s, Simon began
describing and cataloging a large collection that comprises the most comprehensive
arachnid publications of the region (1907, 1909–1910), where he included a brief
tribute to Fea who had died in 1904.
Following Simon’s work, there were a number of important publications in the
1900s. Hansen (1921) described harvestmen and other small arachnid groups primarily from the Fea collection. Roewer later described many of the harvestmen from
Fea’s collection in a series of papers (1927, 1942, 1949). Additional research was
conducted by Amélia Bacelar (1956), the first woman to formally study Gulf of
Guinea arachnids, and also by Otto Kraus (1960). The latter was on an expedition to
the “Gulf of Guinee” led by Herrn P. Viette on the Calypso (The Calypso was owned
by Jacques Cousteau, purchased in 1950, so he also was likely on this trip, but there
is no mention of him specifically). Prieto more recently published on the harvestmen
of Bioko and Annobón (Prieto 1999). In 1998, arachnologist Darrell Ubick of the
California Academy of Sciences (CAS) visited Bioko. Ubick’s 1998 collection from
Bioko was the first targeted collection of arachnids in the region, resulting in over
5000 specimens that are deposited at CAS. A preliminary report published on the
material identified 372 morphospecies, with 9 families and 5 genera otherwise
undocumented from the region (Griswold et al. 1999). A series of trips to São
Tomé and Príncipe have been made by other CAS arachnologists, including Charles
Griswold and Joel Ledford in 2001, Tamas Szűts in 2013, and Lauren Esposito in
2016, and will likely yield undescribed species.
Arachnids of the Gulf of Guinea Islands
Here we have compiled a list of spider, scorpion, whip spider, harvestmen, hooded
tickspider, pseudoscorpion, and short-tailed whipscorpion species from the Gulf of
Guinea islands based on the published works mentioned above, community science
observations documented using iNaturalist (iNaturalist 2021), the World Spider
Catalog (WSC 2021), and the Western Australian Museum catalogs for the smaller
arachnid groups (Harvey 2013a, b, c, d, e, f). The majority of specimens mentioned
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S. C. Crews and L. A. Esposito
or described in publications are singletons—single individuals from unique localities. However, there are many caveats. For example, in Simon’s papers, specimens
are listed as being from specific localities (i.e., a particular island), whereas in the
WSC, the available information is provided at the country level without further
specificity, with Bioko often included only as Guinea. Two of the species described
from Fea’s material were not associated with any locality data beyond the region as a
whole; consequently, due to the large geographic scope of his surveys, they could
have originated from any of the islands and/or the mainland. Given the paucity of
data from the region, we chose to err on the side of inclusion for compiling a list of
arachnids from the Gulf of Guinea oceanic islands. In particular, we include taxa
reported from the land-bridge island in the archipelago, Bioko, because species
reported from this island may also occur on the oceanic islands. We have also
analyzed publication information to assess the quantity of research conducted on
arachnid fauna of the area as a way of beginning a conversation on the remaining
work required before major evolutionary questions (i.e., biogeography) can be
addressed within these diverse lineages.
Order Amblypygi
The amblypygids or whip spiders are a modestly diverse group of predatory arachnids with approximately 150 extant species found in tropical and sub-tropical
regions around the world (Harvey 2013f). All amblypygids lack silk glands and
are not venomous. Their first pair of legs are highly modified sensory organs that
give the appearance of antennae or whips, and their chelicerae are modified into
raptorial claw-like structures (Fig. 11.1). Amblypygids are often found in leaf litter
and caves, and all species are nocturnal. Four species in two genera (Charinus,
Damon) are known from the Gulf of Guinea islands, three of which (all Damon) are
confirmed to also occur in continental Africa (Appendix) (Harms 2018).
Order Araneae
The Araneae or spiders are the most diverse arachnid group, with nearly 50,000
described species (WSC 2021). Spiders have chelicerae with fangs, and most species
use these to inject venom into their prey, which range from insects to other spiders
and small vertebrates (Fig. 11.1). Although the venom of some species can be
dangerous to humans, most species do not pose a risk. Spiders also have spinnerets
that extrude silk, which is used to build webs for prey capture, make retreats and egg
sacs, for mating purposes, as well as dispersal via ballooning.
A total of 213 spider species have been recorded from the Gulf of Guinea islands,
encompassing 48 families and 136 genera (Appendix). The most speciose spider
families from the islands are Araneidae (40 species), Salticidae (33), Tetragnathidae
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277
Fig. 11.1 Representative Arachnids from the Gulf of Guinea islands: (1) Hysterocrates sp.
(spider); (2) Gasteracantha thomasinsulae (spider); (3) Assamiidae (harvestman); (4) Damon
medius (whip spider); (5) Nilus sp. (spider) predating on frog; (6) pseudoscorpion; (7) Pandinus
imperator (scorpion); (8) Ricinoides sp. (hooded tickspider). Photo credits: (1) Guy Tansley, (2)
Brian Simison, (3, 6) Gonzalo Giribet, (4) John Sullivan, (5) Andrew Stanbridge, (7) Nik Borrow,
(8) Beat Akeret
278
S. C. Crews and L. A. Esposito
(15), and Lycosidae (12). All other families have fewer than ten recorded species,
which likely reflects poor collecting of several groups, including good dispersers or
those with cryptic ecologies. Singleton families (families from which only a single
species is known) make up 35% of the familial diversity on the islands. Several
dozen species were described based on material collected from the oceanic islands in
the archipelago and are not known to occur in continental Africa, suggesting they
may be island endemics.
Order Opiliones
The Opiliones are commonly referred to as harvestmen and contain over 6500
described species distributed worldwide. Although they appear superficially similar
to spiders (Araneae), they are not closely related and do not possess venom glands
(Fig. 11.1). They also do not have silk glands and thus do not build webs. Collectively, 34 species in 7 families are known from the Gulf of Guinea islands, 10 of
which are confirmed to also occur in continental Africa (Appendix).
Order Pseudoscorpionida
Pseudoscorpionida, commonly known as pseudoscorpions, are small arachnids,
typically around 3 mm in length, with pincer-like pedipalps similar to those of
scorpions (Fig. 11.1); however, unlike scorpions, some pseudoscorpions deliver
venom with their pedipalps rather than a stinger on a tail, which they lack. This
group includes over 3300 described species that occur in many kinds of environments, but they are often overlooked due to their size (Harvey 2013b). Pseudoscorpions spin silk from a specialized gland in their jaws to produce a cocoon. Thirteen
species in four families are known from the Gulf of Guinea islands, eight of which
are confirmed to also occur in continental Africa (Appendix).
Order Ricinulei
The Ricinulei are commonly known as hooded tickspiders but are not true spiders
(Fig. 11.1). This group is not very diverse, with ~75 extant species described from
tropical Africa and the Neotropics (Harvey 2013c). One species, Ricinoides
crassipalpe, is documented from Bioko Island, and it is also found in continental
Africa (Appendix). It is unclear whether any representatives of this enigmatic order
occur on the oceanic islands in the Gulf of Guinea.
11
A Checklist of the Arachnids from the Gulf of Guinea Islands (Excluding. . .
279
Order Scorpiones
The Scorpiones, commonly known as scorpions, are easily recognized by their
grasping pincers and curved, segmented tail with a stinger (Fig. 11.1). This group
includes over 2500 described species that can be found in a variety of habitats around
the globe (Fet et al. 2000). Because their exoskeletons contain fluorescent compounds, scorpions glow under ultraviolet light, facilitating detection at night.
Although all scorpions produce venom, most species do not pose a risk to humans.
Three species in two families are known from the Gulf of Guinea islands (Appendix), all of which are also found in continental Africa. The only species known from
an oceanic island in the archipelago is Isometrus maculatus, which is introduced on
São Tomé (see below).
Order Schizomida
The Schizomida, commonly known as short-tailed whipscorpions, superficially
resemble true scorpions but have a short tail that lacks a stinger, and their first pair
of legs is antenniform. This group includes over 230 described species that can be
found in tropical and sub-tropical habitats worldwide, with a few species occupying
temperate habitats (Harvey 2013d). Only one species is known from the Gulf of
Guinea islands, Schizomus parvus, which is documented from both São Tomé and
Bioko islands (Appendix).
Diversity, Endemism, and Introduced Species
Based on the current literature, araneids are the most species-rich arachnid group in
the Gulf of Guinea. Araneidae are the most diverse spider lineage on many tropical
islands (e.g., Caribbean: Crews et al. 2015; Crews and Yang 2016), though some
studies of tropical island spider diversity have found higher numbers of salticid
species (Caribbean: Crews et al. 2019; Southeast Asia: Ponce et al. 2021). Salticids
and some araneids (e.g., Gasteracantha, nephilines) are diurnal, the latter often with
large aerial webs that would be more obvious to a non-spider specialist, whereas
many of the other families have species that are nocturnal or that do not build aerial
webs. Thus, for the Gulf of Guinea, it is difficult to know whether the large number
of salticid and araneid species reported is due to a collecting artifact (i.e.,
non-targeted collecting) or if it is representative of the true diversity. For instance,
sub-tropical island surveys employing standardized collecting have reported the
highest species diversity of small and cryptic linyphiid spiders, underscoring the
limitations of extrapolating from opportunistic sampling efforts (Macaronesia:
Malumbres-Olarte et al. 2016, 2020). Likewise, although crab spiders (Thomisidae)
280
S. C. Crews and L. A. Esposito
and lynx spiders (Oxyopidae) are diurnal, they are generally cryptic or ground-living
and easily overlooked. Targeted collecting methods to comprehensively survey
arachnid diversity include vegetation beating, leaf litter sifting combined with
malaise or Winkler traps, visual night searching for nocturnal arachnids using
white and ultraviolet light, turning rocks and logs, and pitfall traps.
Of particular note in the Gulf of Guinea archipelago is the high diversity of
tetragnathid species, likely owing to their relatively good dispersal ability and the
extremely high humidity and abundance of freshwater on the islands, and
mygalomorph families (Barychelidae, Cyrtaucheniidae, Ischnothelidae, Migidae,
Theraphosidae). A preliminary report on a targeted spider collection on Bioko
identified 81 theridiid morphospecies, 45 salticid morphospecies, 39 araneid
morphospecies, and 32 linyphiid morphospecies. This far exceeds the 8, 14,
25, and 5 species, respectively, that have been formally documented from the island
(Griswold et al. 1999).
The total number of spider species on each island is somewhat unclear because
the literature and WSC often provide the country or general region rather than a
specific island. What we do know is that São Tomé and Príncipe together have
130 recorded species, and that 33 (33%) of the 101 species that have specific locality
data are from Príncipe and 51 (50%) from São Tomé. Ten species are known from
Annobón and 91 from Bioko. Of the 211 species documented from the archipelago,
113 also occur on the mainland. The remaining ~100 species may be endemic to one
or more of the islands, but more comprehensive sampling of continental diversity is
needed to confirm their endemic status.
Based on the available records, however, Príncipe has 20 endemic species in
13 families (17 genera), and 61% of the families and 82% of the genera are
represented from singletons. São Tomé has 23 endemic species (only slightly
more than Príncipe based on the depauperate data) in 9 families and 13 genera,
and 69% of the families and 82% of the genera are singletons. Bioko has 27 endemic
species in 16 families and 27 genera, with 69% of families and 93% of genera
represented by singletons. Annobón has two endemic species recorded: Thoriosa
taurina (Simon 1909) (Ctenidae) and Hogna furva cingulipes (Simon 1909)
(Lycosidae).
We can also examine the arachnid fauna of each island for instances of multiple
closely related endemic species, which may point to within-island species radiations
and provide further evidence that the taxa are indeed island and/or archipelago
endemics. The only (non-introduced) genera shared between São Tomé, Príncipe,
and Bioko are Castianeira (Corinnidae) (São Tomé and Bioko), Mallinella
(Zodariidae) (Príncipe and Bioko), and Tetragnatha and Leucauge (Tetragnathidae)
(São Tomé, Príncipe and Bioko). Genera with multiple species on a single island
occur in the salticids Maltecora (2 in Príncipe, 1 on São Tomé) and Belippo (3 on
São Tomé), and the theraphosid Hysterocrates (3 on São Tomé, 1 on Bioko). A
number of (likely) introduced species are also documented in the literature, many of
them cosmopolitan or cosmotropical, and almost all are associated with human
construction or agriculture (indicated in Appendix). Most of the introduced species
11
A Checklist of the Arachnids from the Gulf of Guinea Islands (Excluding. . .
281
were collected from multiple localities, and some mentions date back to at least the
1800s, indicating that the introductions are not recent.
What We Know of the Arachnid Fauna, and Likely Do Not
To gauge the level of scientific activity on the Gulf of Guinea arachnid taxa through
time, we used publication data and taxonomic changes as a proxy (i.e., the number of
years from original description that a species has been idle). Because spiders are the
most speciose arachnid group present on the islands, our conclusions are drawn from
spider-specific taxonomic data. The average number of years since a species had
been studied was 83.4, with the most recent being within the past year (Araneus
apricus (Karsch 1884), Peplometus biscutellatus (Simon 1887)) (DippenaarSchoeman et al. 2020; Wesołowska et al. 2020). The two species with the longest
period of inactivity (137 years) were both described by Karsch (1884): Singa
concinna (Araneidae), described from an immature specimen but still considered
valid, and Philodromus morsus (Philodromidae). At least 55 (of 210) species are
only known from the original description (26.2%), with 22 (10.5%) having been
mentioned in publications from the past 10 years, 70 (33.3%) in the past 50 years,
and 88 (41.9%) in more than 50 years. The majority of species (58%) are known
from both sexes, which is surprisingly high and could be explained by some of the
most prolific collectors having spent long periods of time on the islands. The
remaining species (41.3%) are known only from female (31.9%), immature
(1.4%), or male specimens (8.1%). These differences are likely because males are
often only active for part of the year.
Although our knowledge is incomplete, there are some interesting emerging
patterns for arachnid diversity on the Gulf of Guinea islands. For one, three orders
of arachnids appear to be entirely missing from the fauna, though all are present on
the mainland: Thelyphonida (whip scorpions), Palpigradi (micro whip scorpions),
and Solifugae (wind scorpions). Two additional orders are apparently absent from
the oceanic islands: Ricinulei (hooded tickspiders) and Scorpiones (aside from an
introduced species). The absence of some of these groups is unexpected for islands
of this size and age (scorpions, whip scorpions), while the absence of others may be
attributable to a gap in collecting effort (e.g., microwhip scorpions).
A thorough understanding of arachnids on the Gulf of Guinea islands is still
severely lacking. The majority of species descriptions were made in the first half of
the twentieth century, there have been very few collections made by arachnologists,
and none made using standardized methods of collection that would allow for a
better assessment of the proportion of described versus undescribed fauna (Cardoso
et al. 2009). Additionally, nearly all of the arachnid research to date has focused on
alpha taxonomy and has not included the use of any modern tools or technologies to
expedite the rate of discovery and description (i.e., molecular methods). Taxonomic
training programs for local naturalists or students and partnerships with global
experts would likely go a long way in closing this knowledge gap.
282
S. C. Crews and L. A. Esposito
Appendix
Checklist of the arachnids of the Gulf of Guinea: including the three oceanic islands,
the land-bridge island (Bioko), and the adjacent mainland
SPECIES
ORDER AMBLYPYGI
Family Charinidae
Charinus africanus Hansen 1921
Family Phrynichidae
Damon johnstonii (Pocock 1894)
Damon medius (Herbst 1797)
Damon tibialis (Simon 1876)
ORDER ARANEAE
Family Agelenidae*
Agelenidae sp.
Family Anapidae*
Anapidae sp.
Family Araneidae
Aetrocantha falkensteini Karsch 1879
Agalenatea redii (Scopoli 1763)
Araneus aethiopissa Simon 1907
Araneus apricus (Karsch 1884)
Araneus catospilotus Simon 1907
Araneus cereolus (Simon 1886)
Araneus principis Simon 1907
Aranoethra cambridgei (Butler 1873)
Argiope flavipalpis (Lucas 1858)
Argiope lobata (Pallas 1772)
Argiope trifasciata (Forsskål 1775)
Caerostris sexcuspidata (Fabricius 1793)
Cyclosa circumlucens Simon 1907
Cyclosa formosa Karsch 1879
Cyrtarachne bigibbosa Simon 1907
Cyrtarachne nodosa Thorell 1899
Cyrtophora citricola (Forsskål 1775)
Gasteracantha curvispina (Guérin 1837)
Gasteracantha sanguinolenta C.L. Koch 1844
Gasteracantha thomasinsulae Archer 1951
Megaraneus gabonensis (Lucas 1858)
Metepeira labyrinthea (Hentz 1847)
Neoscona chiarinii (Pavesi 1883)
Neoscona moreli (Vinson 1863)
Neoscona novella (Simon 1907)
SEX
A
ST
P
X
STP
B
MA
X
X
X
X
X
X
X
*
*
MF
MF
MF
F
F
MF
F
MF
MF
MF
MF
MF
F
F
F
F
X
I
X
X
X
X
E
X
X
X
X
X
I
X
X
X
X
X
I
MF
MF
F
MF
MF
MF
MF
F
X
I
X
I
X
X
X
I
X
?
?
X
X
?
X
X
I
X
X
X
X
X
X
X
I
X
X
X
X
X
X
X
X
X
X
E
X
X
I
X
X
(continued)
11
A Checklist of the Arachnids from the Gulf of Guinea Islands (Excluding. . .
SPECIES
Neoscona penicillipes (Karsch 1879)
Neoscona rufipalpis (Lucas 1858)
Neoscona simoni Grasshoff 1986
Neoscona subfusca C.L. Koch 1837
Nephila constricta Karsch 1879
Nephilingis cruentata (Fabricius 1775)
Pararaneus perforatus (Thorell 1899)
Poltys caelatus Simon 1907
Poltys fornicatus Simon 1907
Pseudartonis semicoccinea Simon 1907
Singa concinna Karsch 1884
Singafrotypa acanthopus (Simon 1907)
Trichonephila clavipes (Linnaeus 1767)
Trichonephila fenestrata venusta (Blackwall 1865)
Trichonephila turneri (Blackwall 1833)
Family Barychelidae
Cyphonisia manicata Simon 1907
Cyphonisia nesiotes Simon 1907
Cyphonisia obesa Simon 1889
Family Cheiracanthiidae
Cheiracanthium furculatum Karsch 1879
Cheiracanthium joculare Simon 1909
Family Clubionidae
Clubionidae sp.
Clubiona haplotarsa Simon 1909
Family Corinnidae
Castianeira formosula Simon 1909
Castianeira thomensis Simon 1909
Creugas gulosus Thorell 1878
Procopius ensifer Simon 1909
Procopius gentilis Simon 1909
Procopius granulosus Simon 1903
Procopius laticeps Simon 1909
Pseudocorinna septemaculeata Simon 1909
Pseudocorinna ubicki Jocqué and Bosselaers 2011
Family Ctenidae
Africactenus fernandensis (Simon 1909)
Anahita mamma Karsch 1884
Ctenus potteri Simon 1901
Ctenus capulinus (Karsch 1879)
Thoriosa fulvastra Simon 1909
Thoriosa spadicea (Simon 1909)
Thoriosa spinivulva (Simon 1909)
SEX
MF
MF
F
MF
MF
MF
MF
F
F
F
Imm.
MF
MF
MF
MF
A
ST
P
X
STP
X
X
I
I
X
X
X
X
E
E
X
X
X
X
X
E
283
B
X
X
I
X
X
?
X
X
I
X
X
Imm.
MF
MF
X
X
MA
X
X
X
I
X
X
X
X
X
I
X
X
X
E
MF
F
E
X
X
X
X
X
*
M
M
MF
MF
F
MF
F
F
F
MF
F
MF
F
MF
F
F
MF
E
X
E
I
X
I
E
X
X
X
E
X
E
X
X
X
X
X
X
X
X
X
X
E
X
E
X
X
X
X
X
(continued)
284
SPECIES
Thoriosa taurina (Simon 1909)
Family Cyatholipidae
Buibui kankamelos Griswold 2001
Wanzia fako Griswold 1998
Family Cyrtaucheniidae
Acontius humiliceps (Simon 1907)
Family Deinopidae
Deinopis anchietae Brito Capello 1867
Family Dictynidae
Dictynidae sp.
Anaxibia difficilis (Kraus 1960)
Family Dipluridae*
Dipluridae sp.
Family Gnaphosidae
Gnaphosidae sp.
Aphantaulax ensifera Simon 1907
Echemus lacertosus Simon 1907
Poecilochroa haplostyla Simon 1907
Family Hahniidae
Hahnia eidmanni (Roewer 1942)
Family Hersiliidae
Hersilia occidentalis Simon 1907
Family Ischnothelidae
Lathrothele catamita (Simon 1907)
Family Linyphiidae
Afroneta sp.
Araeoncus femineus (Roewer 1942)
Hypomma clypeatum Roewer 1942
Linyphia karschi Roewer 1942
Mecynidis sp.
Microlinyphia sp.
Family Liocranidae*
Hortipes sp.
Family Lycosidae
Arctosa bacchabunda (Karsch 1884)
Alopecosa sublimbata Roewer 1960
Edenticosa edentula (Simon 1909)
Geolycosa minor (Simon 1909)
Hogna ferox (Lucas 1838)
Hogna furva (Thorell 1899)
Hogna furva cingulipes (Simon 1909)
Hogna karschi (Roewer 1951)
Hogna principum (Simon 1909)
S. C. Crews and L. A. Esposito
SEX
MF
A
E
ST
P
STP
B
MA
MF
MF
X
X
X
X
F
E
MF
X
M
E
X
X
*
*
*
MF
F
MF
E
E
E
X
X
X
F
E
MF
X
F
X
?
X
E
*
E
E
F
F
MF
E
*
*
*
F
MF
F
F
MF
MF
F
F
MF
E
E
E
E
I
X
I
X
E
E
X
X
(continued)
11
A Checklist of the Arachnids from the Gulf of Guinea Islands (Excluding. . .
SPECIES
Hogna thetis (Simon 1909)
Loculla rauca Simon 1909
Loculla rauca minor Simon 1909
Family Migidae
Moggridgea anactenidia Griswold 1987
Moggridgea occidua Simon 1907
Family Mimetidae
Mimetidae sp.
Anansi insidiator (Thorell 1899)
Kratochvilia pulvinata (Simon 1907)
Family Miturgidae*
Miturgidae sp.
Family Mysmenidae*
Mysmenidae sp.
Family Nesticidae
Nesticidae sp.
Nesticus inconcinnus Simon 1907
Family Ochyroceratidae*
Ochyroceratidae sp.
Family Oonopidae
Triaeris equestris Simon 1907
Xestaspis parmata Thorell 1890
Xestaspis sertata Simon 1907
Family Oxyopidae
Oxyopes brachiatus Simon 1909
Oxyopes campestratus Simon 1909
Oxyopes obscurifrons Simon 1909
Family Palpimanidae
Palpimanus hesperius Simon 1907
Sarascelis luteipes Simon 1887
Scelidocteus baccatus Simon 1907
Scelidocteus pachypus Simon 1907
Family Philodromidae
Philodromus morsus Karsch 1884
Philodromus albofrenatus Simon 1907
Family Pholcidae
Artema atlanta Walckenaer 1837
Leptopholcus obo Huber 2011
Leptopholcus tipula (Simon 1907)
Pholcus batepa Huber 2011
Pholcus circularis Kraus 1960
Pholcus moca Huber 2011
Smeringopina fon Huber 2013
SEX
F
F
F
A
ST
P
E
STP
X
X
X
E
X
E
X
X
E
E
F
285
B
MA
*
X
*
MF
F
E
X
*
*
*
F
E
X
F
F
MF
MF
MF
MF
F
F
MF
F
MF
*
E
I
X
I
E
X
E
X
X
E
X
E
X
X
X
X
F
F
X
MF
MF
MF
MF
MF
MF
MF
I
E
X
X
X
X
?
X
?
X
X
E
X
X
X
X
X
E
E
X
(continued)
286
SPECIES
Smeringopus principe Huber 2012
Smeringopus thomensis Simon 1907
Family Pisauridae
Dolomedes fernandensis Simon 1909
Nilus curtus O. Pickard-Cambridge 1876
Tetragonophthalma vulpina (Simon 1898)
Family Salticidae
Baryphas eupogon Simon 1902
Belippo anguina Simon 1909
Belippo calcarata (Roewer 1942)
Belippo nexilis (Simon 1909)
Belippo viettei (Kraus 1960)
Bokokius penicillatus Roewer 1942
Cosmophasis tricincta Simon 1909
Heliophanus congolensis Giltay 1935
Holcolaetis vellerea Simon 1909
Hyllus holochalceus Simon 1909
Hyllus leucomelas (Lucas 1858)
Maltecora chrysochlora Simon 1909
Maltecora divina Simon 1909
Maltecora janthina Simon 1909
Menemerus bivittatus (Dufour 1831)
Myrmarachne confusa Wanless 1978
Myrmarachne eidmanni Roewer 1942
Myrmarachne hesperia (Simon 1887)
Myrmarachne nigeriensis Wanless 1978
Natta horizontalis Karsch 1879
Nigorella albimana (Simon 1902)
Pachyballus flavipes Simon 1909
Peplometus biscutellatus (Simon 1887)
Plexippus paykulli (Audouin 1826)
Pochyta insulana Simon 1909
Portia africana (Simon 1886)
Thiratoscirtus capito Simon 1903
Thyene hesperia (Simon 1909)
Thyene ocellata (Thorell 1899)
Thyene sexplagiata (Simon 1909)
Thyenillus fernandensis Simon 1909
Tomomingi silvae Szűts & Scharff 2009
Viciria scintillans Simon 1909
Family Scytodidae
Scytodes longipes Lucas 1844
Scytodes punctipes Simon 1907
S. C. Crews and L. A. Esposito
SEX
MF
MF
A
MF
MF
P
STP
E
X
X
X
X
X
E
E
X
X
E
E
X
E
E
F
MF
MF
M
F
MF
MF
M
M
MF
MF
MF
M
MF
M
M
MF
MF
M
M
MF
MF
MF
MF
MF
MF
MF
MF
MF
MF
MF
MF
F
MF
M
MF
ST
B
E
?
X
MA
X
X
X
E
E
X
X
X
X
E
E
E
X
X
X
X
X
X
X
I
X
X
X
X
X
X
X
E
X
X
X
X
X
E
X
I
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
E
E
X
X
X
X
E
X
X
E
X
I
X
I
(continued)
11
A Checklist of the Arachnids from the Gulf of Guinea Islands (Excluding. . .
SPECIES
Scytodes velutina Heineken & Lowe 1832
Family Segestriidae
Ariadna laeta Thorell 1899
Ariadna rapinatrix Thorell 1899
Family Selenopidae
Selenops intricatus Simon 1910
Selenops radiatus Latreille 1819
Family Sparassidae
Barylestis insularis Simon 1909
Heteropoda venatoria (Linnaeus 1767)
Thelcticopis scaura (Simon 1909)
Thelcticopis truculenta Karsch 1884
Family Symphytognathidae*
Symphytognathidae sp.
Family Telemidae*
Telemidae sp.
Family Tetragnathidae
Dolichognatha petiti (Simon 1884)
Leucauge argenteanigra (Karsch 1884)
Leucauge cabindae (Brito Capello 1866)
Leucauge isabela Roewer 1942
Leucauge nigrocincta Simon 1903
Leucauge opiparis Simon 1907
Leucauge thomeensis Kraus 1960
Leucauge undulata (Vinson 1863)
Leucauge ungulata (Karsch 1879)
Mecynometa argyrosticta Simon 1907
Tetragnatha clavigera Simon 1887
Tetragnatha filum Simon 1907
Tetragnatha hastula Simon 1907
Tetragnatha macrops Simon 1907
Tylorida seriata Thorell 1899
Family Theraphosidae
Hysterocrates apostolicus Pocock 1900
Hysterocrates didymus Pocock 1900
Hysterocrates ederi Charpentier 1995
Hysterocrates greeffi (Karsch 1884)
Hysterocrates scepticus Pocock 1900
Phoneyusa manicata Simon 1907
Phoneyusa principium Simon 1907
Family Theridiidae
Achaearanea sp.
Argyrodes argyrodes (Walckenaer 1841)
SEX
MF
A
ST
X
F
F
MF
MF
287
P
STP
X
B
X
MA
X
X
X
E
?
?
X
X
I
F
MF
F
MF
E
I
X
X
X
I
E
E
*
F
MF
F
F
M
MF
MF
M
MF
MF
F
MF
MF
MF
F
F
MF
F
MF
MF
F
MF
F
MF
*
X
X
E
X
X
E
E
X
X
X
X
X
X
X
X
X
X
X
E
E
X
X
X
E
X
X
X
E
X
X
X
X
X
X
X
X
X
X
X
X
X
E
E
E
E
X
X
X
X
X
*
X
X
(continued)
288
SPECIES
Argyrodes zonatus (Walckenaer 1841)
Latrodectus hesperus Chamberlin & Ivie 1935
Nesticodes rufipes (Lucas 1836)
Rhomphaea nasica (Simon 1873)
Steatoda carbonaria (Simon 1907)
Steatoda rubrocalceolata (Simon 1907)
Theridion derhami Simon 1895
Theridion eugeni Roewer 1942
Theridion fernandense Simon 1907
Tidarren scenicum (Thorell 1899)
Family Theridiosomatidae
Theridiosomatidae sp.
Wendilgarda atricolor (Simon 1907)
Family Thomisidae
Ansiea tuckeri thomensis (Bacelar 1958)
Borboropactus noditarsis (Simon 1903)
Diaea puncta Karsch 1884
Holopelus albibarbis Simon 1895
Runcinia tropica Simon 1907
Stiphropus dentifrons Simon 1895
Synema jaspideum Simon 1907
Thomisops sulcatus Simon 1895
Thomisus tripunctatus Lucas 1858
Tmarus cancellatus Thorell 1899
Family Trachelidae
Orthobula sp. Simon, 1897
Family Udubidae
Raecius asper (Thorell 1899)
Family Uloboridae
Uloboridae sp.
Zosis geniculata (Olivier 1789)
Family Zodariidae
Mallinella leonardi (Simon 1907)
Mallinella octosignata (Simon 1903)
Mallinella submonticola (Van Hove & Bosmans 1984)
Systenoplacis septemguttatus Simon 1907
ORDER OPILIONES
Family Assamiidae
Bueana quadridentata Prieto 1999 nomen nudem?
Cerea feai Roewer 1927
Chilon horridus (Roewer 1912)
Chilon robustus Sørensen 1896
Eupodauchenius luteocruciatus (Loman 1910)
S. C. Crews and L. A. Esposito
SEX
MF
F
MF
MF
MF
F
F
MF
F
F
A
ST
X
P
I
I
X
X
STP
X
I
I
I
X
B
X
X
E
X
E
E
X
MA
X
I
I
X
X
X
*
F
M
Imm.
MF
MF
MF
F
M
MF
MF
M
MF
E
X
E
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
E
MF
*
MF
MF
F
MF
MF
I
I
E
I
X
E
X
X
X
E
X
X
X
X
X
X
X
X
(continued)
11
A Checklist of the Arachnids from the Gulf of Guinea Islands (Excluding. . .
SPECIES
Euselenca feai Roewer 1927
Henriquea spinigera Roewer 1927
Izea pectinata Roewer 1927
Musola longipes Roewer 1927
Palmanella tigrina Roewer 1927
Selencasta minuscula (Roewer 1927)
Selencula filipes (Roewer 1927)
Thomecola quadrispina (Roewer 1927)
Family Biantidae
Biantomma nigrospinosum Roewer 1942
Lacurbs fernandopoensis Prieto 1999 nomen nudem
Lacurbs nigrimana Roewer 1912
Metabiantes insulanus (Roewer 1949)
Metabiantes pumilio Roewer 1927
Family Ogoveidae
Ogovea nasuta Hansen 1921
Family Neogoveidae
Paragovia sironoides Hansen 1921
Family Phalangiidae
Dacnopilio insularis Hansen 1921
Megistobunus longipes Hansen 1921
Family Pyramidopidae
Conomma annobonum Roewer 1949
Conomma feae Roewer 1927
Conomma fortis Loman 1902
Conomma minima Roewer 1912
Conomma oedipus Roewer 1949
Conomma principeum Roewer 1949
Conomma sorianoi Prieto 1999 nomen nudem
Opconomma hirsuta Roewer 1927
Pyramidops albimana Roewer 1927
Pyramidops biseriata Roewer 1949
Pyramidops raptator (Sørensen 1896)
Family Samoidae
Microconomma armatipes Roewer 1915
ORDER PSEUDOSCORPIONIDA
Family Atemnidae
Cyclatemnus equestroides (Ellingsen 1906)
Micratemnus pusillus (Ellingsen 1906)
Parachernes cocophilus (Simon 1901)
Paratemnoides pallidus (Balzan 1892)
Tamenus camerunensis (Tullgren 1901)
Tamenus insularis Beier 1932
SEX
A
ST
P
STP
289
B
X
MA
X
E
E
E
E
E
E
E
E
E
X
X
E
E
X
E
E
E
E
E
E
X
X
X
X
X
E
X
X
E
E
E
X
X
X
X
E
E
X
X
X
X
X
X
X
?
X
X
E
X
X
(continued)
290
SPECIES
Titanatemnus sjoestedti (Tullgren 1901)
Titanatemnus thomeensis (Ellingsen 1906)
Family Olpiidae
Minniza vermis Simon 1881
Family Tridenchthoniidae
Ditha (Paraditha) sinuata (Tullgren 1901)
Tridenchthonius addititius Hoff 1950
Family Withiidae
Stenowithius angulatus (Ellingsen 1906)
Withius simoni (Balzan 1892)
ORDER RICINULEI
Family Ricinoididae
Ricinoides crassipalpe (Hansen and Sørensen 1904)
ORDER SCORPIONES
Family Buthidae
Isometrus maculatus (De Geer 1778)
Family Scorpionidae
Opisthacanthus lecomtei (Lucas 1858)
Pandinus dictator (Pocock 1888)
ORDER SCHIZOMIDA
Family Hubbardiidae
Schizomus parvus (Hansen 1921)
S. C. Crews and L. A. Esposito
SEX
A
ST
P
STP
B
X
MA
X
E
?
X
X
X
X
E
X
I
X
X
X
X
X
I
I
X
X
X
X
X
X
A: Annobón - ST: São Tomé - P: Príncipe - STP: locality given as “São Tomé and Príncipe” - B:
Bioko - MA: Mainland Africa. X: present; I: introduced; E: endemic: ? the literature is unclear; *: a
morphospecies has been reported (Griswold et al. 1999). The sex of the collected or photographed
specimens is given (F: female; M: male)
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Chapter 12
The Beetles (Coleoptera) of Príncipe, São
Tomé and Annobón
Gabriel Nève, Patrick Bonneau, Alain Coache, Artur Serrano,
and Gérard Filippi
Abstract The known beetle fauna of Príncipe, São Tomé, and Annobón amounts to
403 species and subspecies, of which 190 (47%) are endemic. The most diverse
families of beetles are the Cerambycidae (61 species), the Tenebrionidae (57 species), the Carabidae (45 species), the Scarabaeidae (34 species), and the
Coccinellidae (31 species). Most records come from São Tomé, with 297 species.
In comparison, Príncipe, with 151 recorded species, and especially Annobón, with
16 recorded species, still require extensive faunistic investigations. The families
Staphylinidae and Curculionidae probably hold numerous undescribed species and
should be the focus of future research. Most of the endemic species live in forests.
Therefore, the continued conservation of large forest areas on the islands is key to the
long-term survival of their unique beetle fauna. As elsewhere, the beetle fauna will
likely suffer from the effects of climatic change, and high-altitude species are likely
to be the most severely affected.
Keywords Biodiversity · Checklist · Coleoptera · Conservation · Endemism · Gulf
of Guinea
G. Nève (*)
Aix Marseille Université, Avignon Université, CNRS, IRD, IMBE, Marseille, France
e-mail: gabriel.neve@imbe.fr
P. Bonneau
OPIE, Office Pour les Insectes et leur Environnement de Provence-Alpes-du-Sud, Muséum
d’Histoire Naturelle de Marseille, Marseille, France
A. Coache
Impasse de l’Artémise, La Brillanne, France
A. Serrano
cE3c, Centre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências,
Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon,
Portugal
G. Filippi
MICROLAND, Maison de la vie associative, Aix-en-Provence, France
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_12
295
296
G. Nève et al.
Introduction
The islands of Príncipe, São Tomé, and Annobón, in the equatorial Atlantic ocean,
have a volcanic origin and have never been connected to the African continent
(Fitton and Dunlop 1985). Their isolation led to the evolution of numerous endemic
species, but also to a fauna that is less diverse than that of continental Africa, lacking
many continental species that were unable to cross the stretch of Atlantic ocean
isolating the islands. Before human colonization, which started in the late fifteenth
century, the islands were almost entirely covered by forests (Jones et al. 1991).
Entomological research in the islands started in the beginning of the nineteenth
century, with the first descriptions of endemic species by Hope (1833) and Klug
(1835). The fauna was subsequently investigated by entomologists from various
European countries who later published their findings in journals from their respective countries, making it difficult to produce a synthesis. The main additions to the
knowledge of the local beetle fauna came in waves (Fig. 12.1). Karsch (1881)
mentioned 53 species, including 21 he described as new to science. The Italian
explorer and zoologist Leonardo Fea (1852–1903) collected extensively on São
Tomé and Príncipe in 1900–1901, and 12 beetle species from the archipelago still
bear his name, such as Pseudammus feae (Fig. 12.2.3). The French entomologist
Léon Fairmaire (1820–1906) published revisions of the fauna of São Tomé (1891,
1892, 1902). The Portuguese botanist Júlio Augusto Henriques (1838–1928)
published an important geographical description of São Tomé (1917) that included
a list of all species then known to the island, unfortunately mentioning several
species based on dubious identification or with erroneous names. Later publications
were usually focused on a single family, such as Tenebrionidae (Gebien 1921, 1942)
and Coccinellidae (Fürsch 1974). Castel-Branco (1963) studied the insects feeding
Fig. 12.1 Number of named beetle species added per decade to the fauna of Príncipe, São Tomé,
and Annobón
12
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
297
Fig. 12.2 Photos of charismatic beetle fauna from the oceanic islands of the Gulf of Guinea.
Cerambycidae: (1–2) Macrotoma hayesii; (3) Pseudammus feae; (4) Acutandra delahayi; (5)
Sternotomis ducalis; (6) Sternotomis rufozonata. Brentidae: (7) Cerobates sennae. Mordellidae:
(8) Ophthalmoglipa horaki. Dynastinae: (9) Rhizoplatys cedrici (insert: genitalia). Photo credits: (1,
3–5, 7–9) Patrick Bonneau, (2) Gabriel Nève, (6) Artur Serrano
298
G. Nève et al.
on Theobroma cacao, and listed a series of predators, including several labybirds
(Coccinellidae).
Several expeditions to the islands were completed in the 1900s. Sousa da Camara
visited São Tomé in 1920 (Seabra 1922); Fernando Frade (Missão Científica a São
Tomé) visited São Tomé in November and December 1954 (Gomes Alves 1956);
Pierre Viette, from the Muséum National d’Histoire Naturelle (Paris) visited the
three islands in June and July 1956 (Viette 1956); and Guy Schmitz from the Royal
Museum of Central Africa (Tervuren, Belgium) visited São Tomé in October and
November 1973 (Basilewsky 1975). A zoological mission by entomologists and
ornithologists from the Faculdade de Ciências and Museu Nacional de História
Natural (Lisboa) took place in São Tomé and Príncipe in June and July 1984
(Mendes et al. 1988; Rocha Pité 1993; Serrano 1995; Zuzarte and Serrano 1996a).
Charles E. Griswold and Joel M. Ledford from the California Academy of Sciences
visited São Tomé and Príncipe in 2001 (Kavanaugh 2005), Clive R. Turner and
Tõnis Tasane from the African Natural History Research Trust (Herefordshire,
England) and the Natural History Museum (London) visited São Tomé in 2016
(Darby 2020). Several other entomologists visited the islands since 1980, and
published descriptions of their findings, notably Jean-Guy Canu from Príncipe
between 1989 and 1991 (Allard 1990; Antoine 1992) and Norbert Delahaye between
2013 and 2016 (Delahaye and Camiade 2016). The French NGO Microland also
visited São Tomé in February and October 2019, the latter expedition including a
week on Príncipe, and whose results on Coleoptera are published here for the
first time.
The local Brigada de Fomento Agro-Pecuário, and later the Centro de
Investigação Agronómica e Tecnológica de São Tomé e Príncipe (CIAT-STP)
commissioned numerous entomological studies, mostly related to agriculture
(Fürsch 1974). CIAT-STP holds a collection of insects mainly obtained between
the 1950s and 1975, when the former Portuguese colony gained independence.
Otherwise, specimens from São Tomé and Príncipe are now deposited in several
European and American institutions, as well as in numerous private collections.
The aim of this chapter is to compile a list of all Coleoptera species known from
the islands of Príncipe, São Tomé, and Annobón. For this, we relied on indexes of
entomological publications, and, for Cerambycidae, on the TITAN database
(Tavakilian and Chevillotte 2020). Drawing from published material and our experience on the islands, we analyze this list highlighting the distinctiveness of the
beetle fauna, possible threats, and main gaps in knowledge. Coleoptera families
followed recent publications (Bouchard et al. 2011; López-López and Vogler 2017),
and species nomenclature followed recent revisions (Appendix). Nomenclature for
Carabidae follows Lorenz (2005).
12
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
299
Diversity of the Beetle Fauna
The fauna that we find today in the archipelago is the result of successive colonization and extinction events throughout geological time. Colonization can be active, in
which flight has a dominant role, or passive, such as on floating rafts, or carried by
other animals or by air currents. Extinction can be derived from natural physical
mechanisms, such as catastrophic volcanism, or by ecological processes, such as
predation and competition between species, and in more recent history by anthropogenic actions, such as the destruction of habitats. In the last 500 years, since the
Portuguese first arrived on these islands, we cannot neglect the accidental introduction of exotic species through human activity, namely on the ballast of boats, through
the introduction of plant species of agricultural interest, or on imported goods.
The beetle fauna of Príncipe, São Tomé, and Annobón currently includes 403 species and subspecies (Appendix), which is certainly an underestimate of the richness
of the local fauna. A total of 297 species are known from São Tomé, while only half
of this number (151) has been listed for Príncipe, which most likely remains
understudied. For example, 20 species of Curculionidae are known from São
Tomé, but only 1 from Príncipe and 1 from Annobón. Only 16 Coleoptera species
have been reported for the latter island, which is clearly in need of further
investigations.
The most diverse families of beetles on Príncipe, São Tomé, and Annobón are the
Cerambycidae (61 species), the Tenebrionidae (57 species), the Carabidae (45 species), the Scarabaeidae (34 species), and the Coccinellidae (31 species) (Fig. 12.3).
The Cerambycidae, Carabidae, and Scarabaeidae have been actively studied by
numerous collectors over several decades and there are recent syntheses by Serrano
(1995, 2008, 2010), and Zuzarte and Serrano (1996b), while the Tenebrionidae have
been the subject of an in-depth study by Gebien (1921, 1942), and the Coccinellidae
by Fürsch (1974). The high number of Coccinellidae, 31 species, 8% of the known
beetles on the islands, is probably the result of two factors: (1) the family has been
the subject of a systematic study on the archipelago, and (2) their flight ability
facilitates colonization from continental Africa, compared to other beetle families
(half of the species known on the islands also occur on the African mainland).
The Staphylinidae has only 11 species recorded on the islands, accounting to less
than 3% of their known beetle fauna, but are likely more diverse than the current
estimates. For instance, Réunion, a partly forested equatorial island in the Indian
ocean, has 206 species listed, which amounts to one-fifth of the local beetle fauna,
about half of which are endemic (Gomy et al. 2016; Fig. 12.3). Two species of
Dytiscidae are known from São Tomé, which is most certainly an underestimate
since this family has not been the subject of a specialized study. Again, for comparison, this group is represented by 19 species on Réunion Island. Since Gebien (1921,
1942) listed 46 species of Tenebrionidae, only seven were added by Ardoin (1958,
1962) and Robiche (2000), plus two linked with imported goods (Luna de Carvalho
1984) and one newly found on São Tomé in 2019 (Laurent Soldati, pers. comm.).
300
G. Nève et al.
Fig. 12.3 Left: Distribution of known species of beetles from São Tomé, Príncipe, and Annobón, with the proportion in each family; families with less than six
species are grouped as “Others.” Right: distribution of species known on Réunion Island among the same families (Gomy et al. 2016). Note the differences in
scale between the two graphs
12
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
301
Distinctiveness of the Beetle Fauna
Out of 403 species recorded, 190 (47%) are known only from these islands and are
therefore considered endemic (Table 12.1). The Cerambycidae has 40 endemic
species, the highest number of all beetle families, followed by the Tenebrionidae
(32) and the Carabidae (24).
Lycidae (2 species) is the only family that is fully composed of endemic species
on the islands. The families that have the highest numbers of endemic species,
Tenebrionidae and Cerambycidae, occur mainly in forests (Barclay 2006; Rejzek
2006), which remain abundant on the islands.
The endemicity of several species has been recognized in their names; 16 species
bear the adjective thomensis, saotomense or one of their derivatives, 7 bear the
adjective principis, principensis or principiensis, and 3 bear the adjective
annobonae. The genus Saotomia was given to an endemic species of weevil
(Curculionidae), and the adjective amadori was recently given to a ground beetle
(Carabidae) to honor Rei Amador, a hero in São Tomé history.
Knowledge Gaps
The assignment of species to a particular island is sometimes problematic. For
example, Karsch (1882) described Apogonia insulana based on a specimen collected
by Erdmann in Príncipe. Kolbe (1899) doubted the locality and suggested it came
from the coast of Guinea. This uncertainty could only be solved when the species
was rediscovered on Príncipe in 2019 (Patrick Bonneau and Marc Lacroix,
unpublished; Fig. 12.4.1). In addition, some species mentioned in old references
were likely based on misidentifications (Table 12.2). The compilation of all Coleoptera species listed for the islands by various authors over two centuries also led to
numerous synonymies, some of which remain unresolved, as no systematic revision
has been done. This is the case of Grammopyga marginicollis, described as endemic
for São Tomé, but which may be a synonym of G. cincticollis, mentioned for
Príncipe and widely distributed in Africa. Biphilidae, Limnichidae, and
Ptilodactylidae are known to occur on the islands but the material has not yet been
identified at the species level (Appendix). Other poorly known families are also
likely present, such as Scydmaenidae.
In total, 37 families of beetles are known from Príncipe, São Tomé, and Annobón
whereas 70 are known from Réunion Island, which is larger (2511 km2) but also far
more distant from continents (Gomy et al. 2016). The known beetle fauna of
Reunion Island holds 1128 species, of which 428 (38%) are endemic (Gomy et al.
2016). Thus, there seems to be a gap in the knowledge of the Gulf of Guinea beetle
families that are studied by few entomologists. Focused research by specialist
entomologists, training local scientists, and conducting comprehensive surveys
with multiple trapping methods will be necessary to close this gap. For instance,
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G. Nève et al.
Table 12.1 Number of known named Coleoptera species in each family for the islands of Príncipe,
São Tomé, and Annobón (All: All species; END: Endemics)
Family
Anthribidae
Biphyllidae
Bostrichidae
Brentidae
Buprestidae
Carabidae
Cerambycidae
Chrysomelidae
Cicindelidae
Ciidae
Cleridae
Coccinellidae
Curculionidae
Dryophthoridae
Dytiscidae
Elateridae
Endomychidae
Gyrinidae
Histeridae
Hybosoridae
Hydrophilidae
Laemophloeidae
Limnichidae
Lucanidae
Lycidae
Lymexylidae
Mordellidae
Mycteridae
Nitidulidae
Oedemeridae
Passalidae
Ptiliidae
Ptilodactylidae
Ptinidae
Scarabaeidae
Silvanidae
Staphylinidae
Tenebrionidae
Trogossitidae
Zopheridae
TOTAL
Príncipe
All
END
São Tomé
ALL
END
Annobón
All
END
Total
All
END
7
0
4
10
2
19
18
19
2
0
0
6
1
0
2
2
0
0
6
0
3
0
0
5
1
0
1
0
0
0
1
0
0
0
16
0
0
24
0
2
151
7
?
5
7
4
32
45
16
2
1
1
27
20
4
1
8
1
1
8
1
3
7
?
4
1
1
2
1
3
3
2
2
?
2
20
3
11
37
3
1
297
0
0
2
0
0
0
7
0
0
0
0
0
1
0
0
0
0
0
0
0
1
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
4
0
0
16
9
?
8
11
5
45
61
28
3
1
1
31
21
4
2
9
1
1
9
1
6
7
?
9
2
1
3
1
3
3
2
2
?
2
34
3
11
57
3
3
403
6
?
1
2
1
24
40
11
0
0
0
16
11
0
0
6
0
0
2
0
2
0
?
5
2
0
2
0
0
2
1
0
?
0
20
0
3
32
1
0
190
5
0
1
1
1
10
9
8
0
0
0
2
0
0
0
1
0
0
2
0
1
0
0
2
1
0
1
0
0
0
1
0
0
0
8
0
0
11
0
0
65
5
?
0
2
0
14
27
7
0
0
0
14
10
0
0
6
0
0
1
0
1
0
?
2
1
0
1
0
0
2
1
0
?
0
12
0
3
21
1
0
131
0
0
0
0
0
0
5
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
2
0
0
9
Doubtful species and genera with unnamed species (Chrysomelidae: Longitarsus sp. and Manioba sp. and
Curculionidae: Sternuchopsis sp.) are not listed. Families with unnamed species are indicated by ‘?’
Subfamily
Brachininae
Carabidae
Harpalinae
Carabidae
Lebiinae
Cerambycidae
Cerambycinae Philematium festivum
(Fabricius, 1775)
Lamiinae
Ceroplesis bicincta
(Fabricius, 1798)
Parandrinae
Acutandra gabonica
Parandra gabonica
(Thompson, 1858)
Thompson, 1857
Cicindelinae
Habrodera nidula (Dejean,
1825)
Coccinellinae Cheilomenes lunata
(Fabricius, 1775)
Dytiscinae
Hydaticus capricula Anlar.
Cerambycidae
Cerambycidae
Cicindelidae
Coccinellidae
Dytiscidae
Lymexylidae
Scarabaeidae
Species
Synonyms
Pheropsophus angolensis
(Erichson, 1843)
Selenophorus atratus Klug, Progonochaetus caffer
(Boheman, 1848)
1862
Pentagonica conradti
Kolbe, 1898
Atractocerinae Atractocerus brasiliensis
Lepeletier de Saint Fargeau
& Audinet-Serville, 1825
Dynastinae
Oryctes obuncus Karsch
Revision
reference
Present
revision
Henriques 1917
Present
revision
Straneo, 1945
Straneo’s specimen could Serrano,
1995
not be assigned unambiguously to this species
Henriques, 1917
Probable confusion with Present
Philematium greeffi
revision
Henriques, 1917
Unconfirmed record
Present
revision
Hintz, 1919; Villiers,
Probable confusion with Bouyer
other Acutandra species et al. (2012)
1957
Unconfirmed record
Present
Henriques, 1917
revision
Henriques 1917; Seabra
Probable confusion with Fürsch,
1922; Castel-Branco 1963 C. sulphurea
1974
Henriques, 1917
No other reference to this Nilsson &
Hájek, 2018
name found. Nomen
nudum.
Seabra, 1922
Probable confusion with Present
Atractocerus brevicornis revision
References
Henriques, 1917
Comment
Probable confusion with
Pheropsophus amadori
Unconfirmed record
Henriques, 1917
No other reference to this Endrődi,
name found. Nomen
1985
nudum.
303
(continued)
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
Family
Carabidae
12
Table 12.2 List of species mentioned in old references that were most likely mistakenly reported for the islands
Family
Scarabaeidae
Tenebrionidae
Tenebrionidae
Subfamily
Dynastinae
Species
Synonyms
Temnorhynchus coronatus Temnorhynchus diana
diana (Palisot de Beauvois,
1805)
Tenebrioninae Gonocephalum aequale
Opatrum aequale
(Erichson, 1843)
Tenebrioninae Gonocephalum granicolle
Gebien, 1920
304
Table 12.2 (continued)
References
Henriques, 1917
Comment
Probable confusion with
T. tridentatus
Henriques, 1917
Dubious record
Gebien, 1942
Dubious record
Revision
reference
Present
revision
Iwan et al.,
2010
Iwan et al.,
2010
G. Nève et al.
12
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
305
we are currently working on the description of new species of Curculionidae from
São Tomé, and a revision of this family on the islands will probably yield several
new species. The Hydrophilidae, quite common in forest pools probably include
more than the six currently recognized species, and a revision of these would likely
reveal local endemism, as has been shown recently in the Neotropics (Smith and
Short 2020).
Soil Coleoptera
The soil fauna includes both endogean and epigean Coleoptera. The former spend all
or most of their life cycle within the soil, are not very conspicuous and in most cases
are poorly or almost entirely unknown due to their small size (mainly <2 mm) and
secretive way of life. Epigean beetles live on the ground, and are active mainly by
night or at twilight, while during the day they rest or hide in the litter, under rocks
and logs, sometimes burying themselves in the soil. The endogean beetles of
Príncipe, São Tomé, and Annobón, are completely unknown to science, hence the
absence of records of Scydmaenidae and Pselaphiinae. We do not know of any
research directed to their collection and study on the islands.
Most epigean beetles are predators such as Cicindelidae (e.g., Myriochila
melancholica), some ground Carabidae (e.g., Notiobia sanctithomae and Scarites
fatuus) and Staphylinidae. Many epigean beetles are saprophagous, such as
Tenebrionidae, or leaf litter dwellers (e.g., Curculionidae: Titilayo spp.). On the other
hand, the dung beetle fauna of the islands includes only four Onthophagini species
despite being extremely biodiverse in the continent. Other groups that have not yet been
reported from the islands include carrion (Silphidae), hide (Dermestidae), and skin
(Trogidae) beetles, as well as some families that have representatives that typically
occur on the ground (e.g., Cucujidae, Cryptophagidae, Latridiidae, Mycetophagidae,
etc.). Considering that this fauna is closely associated with substrate, vegetation cover,
and abiotic factors, such as humidity and temperature, we foresee that this group
contains an enormous component of undocumented diversity in these islands.
Epiphytic Coleoptera
The aerial parts of plants constitute an enormous spatial matrix, varying through time
in their different components (stems, leaves, inflorescences, and fruits). A high
percentage of the known beetles, both larval and adult, are phytophagous in the
broad sense of the term. Since São Tomé and Príncipe maintain almost 30% of the
original forest cover (Jones et al. 1991), it is not surprising that they host a rich
and diverse fauna of Coleoptera associated with the vegetation, including the
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G. Nève et al.
subterranean and the aerial parts of plants. Most Chrysomelidae and Curculionidae
species are phytophagous, sometimes having numerous species within a genus,
probably linked to different host species, as in the case of the six species of
Aspidomorpha (Curculionidae) recently recorded on Príncipe (Coache and Rainon
2020). Nitidulidae (Carpophilus spp.) and Bruchinae species are found in abundance
on flowers and mainly on fruits. Plant saps attract a multiplicity of species belonging
to different families, such as adults of Lucanidae (e.g., Prosopocoilus downesi,
Figs. 12.4.5–6), Cetoniinae (e.g., Chlorocala viridicyanea, Pachnoda spp.) and
Cerambycidae (e.g., Macrotoma hayesii, Sternotomis spp.). Finally, some species
are predators of other insects dwelling on vegetation, of which the Coccinellidae are
the best known and richest family in São Tomé and Príncipe.
Coleoptera Associated with Decaying Wood
Woodborer Coleoptera larvae and adults that live within the wood (xylophages) or
under bark (subcortical) can be predators, saprophagous or even phytophagous species
that seek refuge there. These are surely one of the most diverse and abundant ecological
Coleoptera groups in São Tomé and Príncipe, as almost all Coleoptera families present
species in these biotopes. Woodborer larvae include numerous species of Anthribidae,
Bostrichidae, Brentidae, Buprestidae, Cerambycidae, Curculionidae, Elateridae,
Lucanidae, Scarabaeidae, Tenebrionidae, among others. Adult beetles found in this
habitat encompass most of the endemic Carabidae (e.g., Metagonum insulanum,
Pseudobatenus straneoi, Abacetus spp., Camptogenys trisetosa), as well as Histeridae,
Laemophloeidae (e.g., Cryptolestes spp., Placonotus spp.) and Staphylinidae (e.g.,
Afrosorius spp.). It is sometimes possible to find numerous species of most families
mentioned above side-by-side in the same tree trunk.
Freshwater Coleoptera
São Tomé and Príncipe exhibit a wide range of freshwater biotopes, including
streams, rivulets, lagoons, pools, and phytotelmata, which are habitat to several
families of beetles (e.g., Gyrinidae, Haliplidae, Hygrobiidae, Dytiscidae,
Hydrophilidae and Hydraenidae). So far, only a few species of Gyrinidae,
Dytiscidae, and Hydrophilidae have been recorded from Príncipe, São Tomé, and
Annobón, but considering the abundance of freshwater biotopes on the islands,
many more likely remain to be discovered.
12
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
307
Coleoptera of Agricultural Importance
A few beetle species are known to be of agricultural importance, either as pests
of cultivated species, or as predators of pests. Lamprocopa occidentalis
(Chrysomelidae), which we documented in 2019 on both São Tomé and Príncipe,
is known as a serious pest on several cultivated Cucurbitacae (Adja et al. 2014).
Some species were deliberately introduced for the control of aphids and other insects
that are detrimental to agriculture. Among these, the Coccinellidae Rodolia
cardinalis was introduced by Castel-Branco (1963) specifically to control the
aphid Toxoptera aurantii (Boyer de Fonscolombe, 1841), which feeds on
Theobroma cacao, and seems now to have been extirpated. Other introduced pest
predators became established, such as Cryptognatha nodiceps, which feeds on the
Cottony Cushion Scale Icerya puchasi Makell, 1878 (Hemiptera) (Fürsch 1974).
Remarkably, the endemic ladybird species Chilocorus pilosus, Nephus derroni,
and N. theobromae were also found on cultivated plants, notably Coffea arabica,
Theobroma cacao and Cocos nucifera (Fürsch 1974). This must be the result of local
adaptations of either the ladybird species or of their prey, since the host plants are
introduced to cultivated plants. The natural habitat and feeding habits of these
species are not known.
Some Charismatic Species
The Príncipe endemic Macrotoma hayesii (Figs. 12.2.1–2) is the largest
Cerambycidae species in Africa (up to 12 cm), occurring in forests, where
Pentaclethra macrophylla has been described as its host plant (Tordo 1956).
Macrotoma hayesi is always rare, and the size of its imago, the adult life stage of
beetles, suggests a life cycle lasting several years. Its conservation requires
maintaining old growth forests with decaying trees in the Príncipe Natural Park,
including Azeitona. Another Cerambycidae, Ceratocentrus oremansi, reported in
1998 (Delahaye and Camiade 2016), is much smaller (3.2 to 5.5 cm) and has been
found in several forest areas on São Tomé Island.
The Lucanidae fauna of São Tomé and Príncipe is well known and includes nine
species and subspecies. Prosopocoilus antilopus has a distinct endemic subspecies
on each oceanic island: P. antilopus insulanus on São Tomé, P. antilopus beisa on
Príncipe and P. antilopus amicorum on Annobón. Eight additional subspecies have
been described from Senegal to the Democratic Republic of Congo (Bartolozzi and
Werner 2004). Prosopocoilus downesii is known from São Tomé, Príncipe and
Bioko. Specimens of Prosopocoilus, especially males, are known to vary in size
(Fig. 12.4), depending on larval growth conditions (Bartolozzi and Werner 2004),
with large males sometimes having proportionally long mandibles, as in the case of
“mesodonte” P. antilopus males (Gomes Alves 1956).
308
G. Nève et al.
Fig. 12.4 Photos of charismatic beetle fauna from the oceanic islands of the Gulf of Guinea (cont.).
Scarabaeidae: (1) Apogonia insulana; (2) Apogonia tomeensis (insert: genitalia); (3) Apogonia
decellei; (4) Clastocnemis quadrimaculatus oremansi. Lucanidae: (5) Prosopocoilus downesi (left:
female, right: male, mesodonte form); (6) Prosopocoilus downesi (male, prosodonte form); (7)
Prosopocoilus antilopus insulanus; (8) Figulus decipiens. Photo credits: (1–5, 7–8) Patrick
Bonneau, (6) Gabriel Nève
12
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
309
The Cetoniinae Uloptera canui (Scarabaeidae) is a typical example of a remarkable species that has a restricted distribution. It was described in 1992 based on a few
specimens from two areas in Príncipe at ca. 500 m altitude: Pico Mesa and Pico Dois
Irmãos. Given the peculiar ecological conditions of these locations, it is unlikely that
the species occurs at lower altitudes. Of the other 12 Cetoniinae species known from
São Tomé and Príncipe, 8 are endemic, either at the species or sub-specific level
(Table 12.1). Their poor ability to fly long distances likely explains why there are so
few species on the islands. One of these, the São Tomé endemic Stenosternus
costatus, is thought to be the result of an ancient colonization from the Neotropics,
since it is the only African species of the tribe Orphnini (Orphninae, Scarabaeidae –
Frolov 2013).
Carabidae are generally predators of smaller insects and other arthropods, and
sometimes of mollusks. Forty-five species are known from São Tomé and Príncipe.
The genus Pseudobatenus illustrates an interesting biogeography, since it is only
represented by the São Tomé endemic Pseudobatenus straneoi and two other
species, P. camerunicus (Burgeon, 1942) and P. longicollis Basilewsky, 1951,
which are restricted to Mt. Cameroon (Basilewsky 1975). These three species are
most likely altitudinal relicts of a widespread ancestral species. The Cerambycidae
Bangalaia thomensis has a similar distribution, being found only on São Tomé and
in Cameroon, although it occurs at low altitudes (Lepesme and Breuning 1956).
Concluding Remarks
Príncipe, São Tomé, and Annobón host 403 named species and subspecies of
beetles, plus an unknown number of undescribed species. Many of these species
are endemic and very little is known about them. For instance, several endemics,
such as Nesopatrum josephii (Tenebrionidae) and Panoptes convexus
(Curculionidae), were described from Ilhéu das Rolas by Karsch (1881), and there
are no records from São Tomé Island itself. Given the development of touristic
infrastructure and overall environmental degradation on Ilhéu das Rolas, it is not
known if these species persist. An improved knowledge of the fauna of the archipelago would require a variety of sampling techniques deployed in a wide range of
habitats, including some low-cost canopy trapping (Bar-Ness et al. 2011). The main
task, however, would be identification, which would require engaging specialists of
the various families. The establishment of a local reference collection would be an
important asset to train and raise awareness of the beetle fauna.
The long-term conservation of the beetle fauna, as for most of the endemic
terrestrial fauna of Príncipe, São Tomé, and Annobón relies on effective conservation of native forests. These still cover about 30% of the islands, an unusually high
percentage that is linked to the rugged topography (Norder et al. 2020). The capture
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G. Nève et al.
and export of beetles should also be controlled, namely of endemic species that
might be particularly vulnerable, such as the endemic as Macrotoma hayesii
(Fig. 12.2.1–2), which occurs at low densities. This and several other endemic beetle
species, such Rhizoplatys canui and Figulus decipiens (Figs. 12.4.4 and 12.4.8) are
emblematic and could serve as flagship species for the conservation of their habitats,
especially old growth forests, where standing dead old trees are key habitat for the
larvae. Visits to the forests and producing conservation educational material using
beetle fauna may play an important role in educating the public about the uniqueness
and exceptional biodiversity of the islands.
Acknowledgments We thank the authorities of the Príncipe Natural Park for their help in the field
and sampling permit. The Centro de Investigação Agronómica e Tecnológica de São Tomé e
Príncipe (CIAT-STP) authorized the export of specimens (permit N 011/2019). Laurent Soldati,
Marc Lacroix, and Yves Gomy identified specimens of Tenebrionidae, Melolonthinae, and
Histeridae, respectively. Roberto Poggi, Honorary Curator of Museo Civico di Storia Naturale
“Giacomo Doria” in Genoa (Italy), offered many works based on Leonardo Fea’s expeditions.
Comments from Dave Kavanaugh greatly improved this chapter.
Supplementary Material
A full text format of Appendix and Table 12.2, with references to the occurrence of all species in
Príncipe, São Tomé, and Annobón, together with the main synonyms is available on https://doi.org/
10.5281/zenodo.5151308.
Appendix
Appendix List of Coleoptera taxa known from the islands of Príncipe, São Tomé,
and Annobón. “Microland” refers to species added to the known São Tomé and
Príncipe fauna during our two expeditions in February and October 2019. E:
endemic species, I: introduced species, R: resident on the islands, *: species recorded
during the 2019 Microland expeditions (ML)
Litocerus Schönherr, 1833
Phloeobius Schönherr, 1823
Xylinada Berthold, 1827
Subfamily Choraginae Kirby, 1819
Araecerus Schönherr, 1823
P
Acorynus benitensis Jordan, 1903
Apateni benina Jordan, 1920
Cenchromorphus fulvum Jordan,
1903
Gynandrocerus thomensis Jordan,
1911
Litocerus beninus Jordan, 1920
Phloeobius hypoxanthus Jordan,
1911
Xylinada princeps Jordan, 1920
Xylinada thomasius Jordan, 1911
R
E
Araecerus fasciculatus (Degeer,
1775)
R
ST
A
Reference
ML
E
R
Jordan, 1920
Jordan, 1920
Jordan, 1920
E
E
Jordan, 1911
E
E
E
E
Jordan, 1920
Jordan, 1911
E
Jordan, 1920
Jordan, 1911
R
Jordan, 1920
R?
Microland
*
R
R
R
Microland
Lesne, 1906
Lesne, 1906
Lesne, 1906
Lesne, 1906
*
E
Synonyms
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
Gynandrocerus Lacordaire, 1866
Species
12
Higher taxonomy
Family Anthribidae Billberg, 1820
Subfamily Anthribinae Billberg, 1820
Acorynus Schönherr 1833
Apatenia Pascoe 1859
Cenchromorphus Fairmaire, 1893
Derographium fulvum
Xylinades princeps
Xylinades thomasius
Family Biphyllidae Le Conte, 1861
Unidentified species
Family Bostrichidae Latreille, 1802
Subfamily Apatinae Jacquelin du Val, 1861
Apate Fabricius, 1775
Apate cephalotes (Olivier, 1790)
Apate degener Murray, 1867
Apate monachus Fabricius, 1775
Apate terebrans (Pallas, 1772)
Phonapate discreta Lesne, 1906
Phonapate Lesne, 1895
R
R
E
R
Phonapate frontalis
*
(continued)
311
Species
ST
A
R
R
R
ML
Lesne, 1906
Luna de
Carvalho, 1984
Calabresi, 1920
*
R
R
Calabresi, 1920
Calabresi, 1920
*
E
Calabresi, 1920
R
Calabresi, 1920
*
R
Calabresi, 1920
*
R
R
R
R
E
E
Damoiseau,
1963
Karsch, 1881
R
R
Calabresi 1920
R
Synonyms
Lesne, 1906
R
R
Reference
Calabresi, 1920
Mygaleicus vittipennis;
Mygaleicus vittipennis nitida
Ceocephalus georgei
*
G. Nève et al.
Bostrychoplites cornutus (Olivier,
1790)
Xylionulus Lesne, 1901
Xylionulus transvena (Lesne,1900)
Subfamily Dinoderinae C.G. Thomson, 1863
Rhyzopertha Stephens, 1830
Rhyzopertha dominica (Fabricius,
1792)
Family Brentidae Billberg, 1820
Subfamily Brentinae Billberg, 1820
Adidactus Senna, 1894
Adidactus striolatus (Fairmaire,
1897)
Cerobates Schönherr, 1840
Cerobates sennae Calabresi, 1920
Cerobates sulcatus sulcirostris
Thomson, 1858
Eumecopodus Calabresi, 1920
Eumecopodus fuliginosus
Calabresi, 1920
Gynandrorhynchus Lacordaire, 1866
Gynandrorynchus vittipennis
(Fåhraeus, 1871)
Microtrachelizus Senna, 1893
Microtrachelizus aethiopicus
Calabresi, 1920
Orphanobrentus Damoiseau, 1962
Orphanobrentus picipes (Olivier,
1791)
Pseudomygaleicus de Muizon, 1960
Pseudomygaleicus georgei
(Karsch, 1881)
Rhinopteryx Lacordaire, 1865
Rhinopteryx foveipennis (J.Thomson, 1858)
Spatherhinus longiceps Kolbe,
Spatherhinus Power, 1879
1888
P
312
Higher taxonomy
Subfamily Bostrichinae Latreille, 1802
Bostrychoplites Lesne, 1899
Megactenodes Kerremans, 1893
R
Agrilus feae Kerremans, 1906
E
Chrysobothris dorsata (Fabricius,
1787)
Megactenodes westermanni (Gory
et Laporte, 1838)
R
Family Carabidae Latreille, 1802
Subfamily Brachininae Bonelli, 1810
Brachinulus Basilewsky, 1958
Pheropsophus Solier, 1833
Subfamily Harpalinae Bonelli, 1810
Idiomela Tschitscherine, 1900
Notiobia Perty, 1830
R
Parataenia chrysochlora (Palisot
de Beauvois, 1805)
R
Brachinulus viettei Basilewsky,
1958
Pheropsophus (Stenaptinus)
amadori Lassalle & Roux, 2021
Pheropsophus (Stenaptinus)
fastigiatus (Linnaeus, 1764)
E
Idiomelas (Egaploa) crenulatus
(Dejean, 1829)
Notiobia (Diatypus) sanctithomae
(Serrano, 1995)
Calabresi, 1920
Usambius conradti
Kerremans,
1906
R
Subfamily Chrysochroinae Laporte, 1835
Lampetis Dejean, 1833
Lampetis zona (Thomson, 1858)
Parataenia Kerremans, 1892
R
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
Subfamily Buprestinae Leach, 1815
Chrysobothris Eschscholtz, 1829
Usambius advena (Pascoe, 1866)
12
Usambius Kolbe, 1892
Family Buprestidae Leach, 1815
Subfamily Agrilinae Laporte, 1835
Agrilus Curtis, 1825
R
E
R
R
E
Kerremans,
1906
Kerremans,
1906
Kerremans,
1914
Kerremans,
1906
Damarsila zona
Basilewsky,
1958
Lassalle &
Roux, 2021
Basilewsky,
1975
Basilewsky,
1975
Serrano, 1995
Egaploa crenulata
313
(continued)
Siopelus Murray, 1859
Stenolophus Dejean, 1821
Subfamily Lebiinae Bonelli, 1810
Anaulacus W.S. MacLeay, 1825
Calleida Latreille, 1824
Dromius Bonelli, 1810
Pentagonica Schmidt-Göbel, 1846
Perigona Laporte de Castenau, 1835
P
Anaulacus (Microus) mocqueryzi
(Chaudoir, 1878)
Calleida (Stenocallida) ruficollis
(Fabricius, 1801)
Dromius (Klepterus) basilewskyi
(Serrano, 1995)
Pentagonica boavistensis Serrano,
1995
Pentagonica nigritula Straneo,
1943
Perigona (Euripogena) congoana
Burgeon, 1935
Perigona (Perigona) pallida
Laporte, 1835
Perigona (Perigona) parallela
Chaudoir, 1878
Perigona (Perigona) principensis
Serrano, 2008
Perigona (Trechicus) nigriceps
(Dejean, 1831)
Perigona (Trechicus) schmitzi
(Basilewsky, 1989)
R
ST
R
R
R
A
Reference
Basilewsky,
1975
Basilewsky,
1975
Basilewsky,
1975
R
Serrano, 1995
R
Serrano, 1995
E
Serrano, 1995
E
Serrano, 1995
E
Straneo, 1943
R
Basilewsky,
1989
Basilewsky,
1975
Basilewsky,
1989
Serrano, 2008
R
R
R
E
R
R
Basilewsky,
1975
Basilewsky,
1989
ML
Synonyms
Dichaetochilus planicollis
Aulacoryssus pulchellus
Stenolophus scapulare
Microus mocqueryzi
Trechicus nigriceps
Trechicus schmitzi
G. Nève et al.
Species
Progonochaetus (Progonochaetus)
planicollis (Putzeys, 1882)
Siopelus (Pseudosiopelus)
pulchellus (Dejean, 1829)
Stenolophus (Egadroma)
scapularis (Dejean, 1831)
314
Higher taxonomy
Progonochaetus G. Müller, 1938
Subfamily Panagaeinae Bonelli, 1810
Euschizomerus Chaudoir, 1850
Microcosmodes Strand, 1936
Subfamily Paussinae Latreille, 1807
Carabidomemnus Kolbe, 1924
Sphaerostylus Chaudoir, 1848
Subfamily Platyninae Bonelli, 1810
Euplynes Schmidt-Gobel, 1846
Metagonum Jeannel, 1948
Pseudobatenus Basilewsky, 1951
Straneoa Basilewsky, 1953
Chlaenius (Lissauchenius) assecla
Laferté-Senectere, 1851
Melanchiton laevisulcis Straneo,
1950
R
Euschizomerus buquetii Chaudoir,
1850
Microschemus vicinus (Murray,
1857)
R
Carabidomemnus
(Carabidomemnus) feae (Gestro,
1902)
Sphaerostylus (Afrozaena) feai
(Basilewsky, 1949)
Sphaerostylus (Afrozaena)
insularis (Basilewsky, 1949)
E
Euplynes brunneus Straneo, 1943
Metagonum insulanum
Basilewsky, 1948
Pseudobatenus straneoi
Basilewsky, 1957
Straneoa collatata (Karsch, 1881)
E
Straneoa seligmani Kavanaugh,
2005
R
R
Basilewsky,
1975
Basilewsky,
1975
R
Serrano, 1995
R
Basilewsky,
1975
Melanchiton laeviscus
Microcosmodes vicinus
Gestro, 1902
E
E
E
E
E
E
Basilewsky,
1949
Basilewsky,
1949
Straneo, 1943
Basilewsky,
1948
Basilewsky,
1957
Karsch, 1881
Pseudozaena insularis
Euplynes bruneus
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
Melanchiton Andrewes, 1940
12
Subfamily Licininae Bonelli, 1810
Chlaenius Bonelli, 1810
Zargus collatatus; Platynus
opacipennis; Straneoa
opacipennis
Kavanaugh,
2005
315
(continued)
Caelostomus MacLeay, 1825
Camptogenys Tschitscherine, 1899
Dromistomus Jeannel, 1948
Monodryxus Straneo, 1941–1942
Morion Latreille, 1810
Pachyroxochus Straneo, 1941–1942
Platyxythrius Straneo, 1941–1942
Subfamily Scaritinae Bonelli, 1810
Dyschirius Bonneli, 1810
Scarites Fabricius, 1775
P
Abacetus amplithorax Straneo,
1940
Abacetus feai Straneo, 1940
Caelostomus (Caelostomus)
striatocollis (Dejean, 1831)
Caelostomus (Drimostomellus)
punctifrons (Chaudoir, 1850)
Camptogenys trisetosa (Serrano,
1995)
Dromistomus complanatus
levistriatus (Straneo, 1941–1942)
Monodryxus crassus (Straneo,
1941–1942)
Morion guineensis Imhoff, 1843
E
Pachyroxochus subquadratus
Straneo, 1941–1942
Platyxythrius insularis Straneo,
1956
ST
R
E
E
E
R
R
E
E
Dyschirius (Dyschiriodes)
zanzibaricus palmeni Kult, 1954
Scarites fatuus Karsch, 1881
Scarites feanus Bänninger, 1937
E
Tachyta subvirens Chaudoir, 1878
R
Reference
ML
Synonyms
Straneo, 1940
E
R
R
A
R
E
Straneo, 1940
Straneo, 1941–
1942
Basilewsky,
1975
Serrano, 1995
Straneo, 1941–
1942
Straneo, 1941–
1942
Henriques,
1917
Straneo, 1941–
1942
Straneo, 1941–
1942
Basilewsky,
1975
Karsch, 1881
Bänninger,
1937
Serrano, 2008
*
Drimostomellus punctifrons
*
Caelostomus (Camptogenys)
trisetosus
Caelostomus complanatus var.
levistriatus
Morion guineense
Platyxythrius laevicollis
Dyschirius palmeni
G. Nève et al.
Subfamily Trechinae Bonelli, 1810
Tachyta Kirby, 1837
Species
316
Higher taxonomy
Subfamily Pterostichinae Bonelli, 1810
Abacetus Dejean, 1828
Diaspila Jordan, 1903
Neoplocaederus Sama, 1991
Philematium Thomson, 1864
Philomeces Kolbe, 1893
Phrosyne Murray 1870
Xylotrechus Chevrolat, 1860
Xystrocera Audinet-Serville, 1834
Subfamily Lamiinae Latreille, 1825
Acmocera Dejean, 1835
Chromalizus (Callichromalizus)
fragrans aldbaueri Delahaye &
Juhel, 2018
Chromalizus (Chromalizus)
rhodoscelis (Jordan, 1903)
Diaspila periscelis Jordan, 1903
Neoplocaederus fucatus (Thomson,
1858)
Philematium greeffi Karsch, 1881
Philomeces thomensis (Aurivillius,
1910)
Phrosyne brevicornis (Fabricius,
1775)
Xylotrechus aedon Jordan, 1903
Xystrocera interrupta Jordan, 1903
Xystrocera nigrita AudinetServille, 1834
I
I
E
I
I
E
R
Zuzarte & Serrano, 1996
Aurivillius,
1910
Henriques,
1917
Delahaye &
Juhel, 2018
E
Jordan, 1903
R
R
Jordan, 1903
Villiers, 1957
E
E
Karsch, 1881
Aurivillius,
1910
Henriques,
1917
Jordan, 1903
Jordan, 1903
Zuzarte & Serrano, 1996
R
E
R
R
R
Acmocera insularis Breuning, 1940
Acmocera lutosa Jordan, 1903
E
E
Henriques,
1917
Breuning, 1940
Jordan, 1903
*
Callichroma festivum
Cloniophorus rhodoscelis;
Callichroma rhodoscelis
*
Euporus brevicornis
*
Hystrocera interrupta
Achmocera anthriboides
317
Acmocera conjux Thomson, 1858
*
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
Chromalizus Schmidt, 1922
12
Family Cerambycidae Latreille, 1802
Subfamily Cerambycinae Latreille, 1802
Achryson Audinet-Serville, 1833
Achryson surinamum (Linnaeus,
1767)
Calanthemis Thomson, 1864
Calanthemis thomensis Aurivillius,
1910
Chlorida Miers, 1880
Chlorida festiva (Linnaeus, 1758)
(continued)
Ancylonotus Dejean, 1835
Bangalaia Duvivier, 1890
Coptops Serville, 1835
Eunidia Erichson, 1843
Frea Thomson, 1858
Glenea Newman, 1842
Insulochamus Dillon & Dillon, 1961
Jordanoleiopus Lepesme & Breuning,
1955
Monochamus Dejean, 1821
Species
Acridoschema thomense Jordan,
1903
Ancylonotus tribulus (Fabricius,
1775)
Bangalaia thomensis Breuning,
1947
Coptops aedificator (Fabricius,
1793)
Coptops annobonae Aurivillius,
1910
Coptops hypocrita Lameere, 1892
ST
E
A
Synonyms
Acridoschema thomensis
Jordan, 1903
R
Breuning, 1947
R
Jordan, 1903
Coptops fusca; Lamia fusca
Aurivillius,
1910
Aurivillius,
1910
Breuning, 1970
Lepesme, 1948
Jordan, 1903
Breuning, 1958
Aurivillius,
1928
Jordan, 1903
Pterolophia annobonae
R
E
R
E
E
E
E
E
R
ML
R
E
R
Reference
Jordan, 1903
Monochamus thomensis
Breuning, 1955
Jordan, 1903
R
E
E
Hintz, 1919
Breuning, 1956
E
Fairmaire, 1892
Monohommus rubigineus
G. Nève et al.
Eunidia thomensis Breuning, 1970
Frea maculicornis Thomson, 1858
Frea puncticollis Jordan, 1903
Glenea thomensis Breuning, 1958
Insulochamus annobonae
(Aurivillius, 1928)
Insulochamus thomensis (Jordan,
1903)
Jordanoleiopus (Polymitoleiopus)
feai Breuning, 1955
Monochamus (Ethiopiochamus)
ruspator (Fabricius, 1781)
Monochamus nubilosus Hintz,
1919
Monochamus principis Breuning,
1956
Monochamus rubiginosus Teocchi,
Sudre & Jiroux, 2014
P
318
Higher taxonomy
Acridoschema Thomson, 1858
Protonarthron Thomson, 1858
Pseudhammus Kolbe, 1894
Pterolophia Newman, 1842
Ropica Pascoe, 1858
Steirastoma Lepeletier & AudinetServille, 1830
Sternotomis Percheron, 1836
Villiers, 1957
Villiers, 1957
Phryneta vietti
E
Jordan, 1903
Pachystola trituberculata
thomensis
E
Breuning, 1936
R
Jordan, 1903
E
Aurivillius,
1910
Aurivillius,
1910
E
E
E
Zuzarte & Serrano, 1996
Zuzarte & Serrano, 1996
Aurivillius,
1910
Breuning, 1943
E
Breuning, 1938
E
I
Breuning, 1970
Zuzarte & Serrano, 1996
Fairmaire, 1902
E
E
E
R
R
Henriques,
1917
Plectonarthron microps
*
*
*
Pseudolemur rufozonata
*
Ultiolemur ducalis
319
Sternotomis (Pseudolemur)
rufozonata Fairmaire, 1902
Sternotomis (Ultiolemur) ducalis
(Klug, 1835)
I
E
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
Prosopocera Dejean, 1835
Phryneta verrucosa (Drury, 1773)
Phrynetopsis thomensis principis
Breuning, 1952
Phrynetopsis thomensis thomensis
(Jordan, 1903)
Prosopocera (Alphitopola)
insularis Breuning, 1936
Protonarthron microps (Jordan,
1903)
Pseudhammus (Litigiosus) feae
Aurivillius, 1910
Pterolophia
(Annobonaepraonetha) annobonae
Aurivillius, 1910
Pterolophia (Insularepraonetha)
ferrugineotincta Aurivillius, 1926
Pterolophia (Insularepraonetha)
insularis Breuning, 1938
Pterolophia (Principipraonetha)
principis Aurivillius, 1910
Pterolophia (Principipraonetha)
pseudoprincipis Breuning, 1943
Pterolophia (Pterolophia)
thomensis Breuning, 1938
Ropica thomensis Breuning, 1970
Steirastoma stellio Pascoe, 1866
12
Phryneta Dejean, 1835
Phrynetopsis Kolbe, 1894
(continued)
Subfamily Parandrinae Blanchard, 1845
Acutandra Santos-Silva, 2002
Subfamily Prioninae Latreille, 1802
Ceratocentrus Aurivillius, 1903
Macrotoma Audinet-Serville, 1832
Mallodon Lacordaire, 1869
Sarothrogastra Karsch, 1881
Acutandra barclayi Bouyer,
Drumont & Santos-Silva, 2012
Acutandra dasilvai Bouyer,
Drumont & Santos-Silva, 2012
Acutandra delahayei Bouyer,
Drumont & Santos-Silva, 2012
Acutandra oremansi Bouyer,
Drumont & Santos-Silva, 2012
Ceratocentrus oremansi Delahaye
& Camiade, 2016
Ceratocentrus principiensis
(Nýlander, 2000)
Macrotoma hayesii Hope, 1833
Macrotoma palmata (Fabricius,
1793)
Mallodon downesii Hope, 1843
Sarothrogastra edulis (Karsch,
1881)
Sarothrogastra feai (Lameere,
1912)
Callosobruchus maculatus
(Fabricius, 1775)
P
ST
R
A
E
Bouyer et al.,
2012
Bouyer et al.,
2012
Bouyer et al.,
2012
Bouyer et al.,
2012
E
E
E
E
E
R
ML
Synonyms
*
Villiers, 1957
E
E
R
Reference
Lepesme &
Breuning, 1950
Acanthophorus spinicornis
Nýlander, 2000
Tordo, 1956
Tordo, 1956
*
R
R
E
Fairmaire, 1891
Karsch, 1881
*
E
I
Telotoma hayesi
Macrotoma edulis
Lameere, 1912
Luna de
Carvalho, 1984
G. Nève et al.
Family Chrysomelidae Latreille, 1802
Subfamily Bruchinae Latreille, 1802
Callosobruchus Pic, 1902
Species
Tragocephala guerinii White, 1856
320
Higher taxonomy
Tragocephala Dejean, 1835
Subfamily Cassidinae Chapuis, 1875
Aspidomorpha Hope, 1840
Chiridopsis Spaeth, 1922
Laccoptera Boheman, 1855
Subfamily Criocerinae Latreille, 1804
Hatita Fairmaire, 1891
Lema Fabricius, 1798
Subfamily Eumolpinae Hope, 1840
Afroeurydemus Selman, 1965
Cheiridella Jacoby, 1904
Aspidimorpha (Afroaspidimorpha)
nigromaculata (Herbst, 1799)
Aspidimorpha (Aspidimorpha)
isparetta Boheman, 1854
Aspidimorpha (Aspidimorpha)
obovata (Klug, 1835)
Aspidimorpha (Aspidimorpha)
quinquefasciata (Fabricius, 1801)
Aspidimorpha (Aspidimorpha)
submutata Weise, 1899
Aspidimorpha (Aspidocassis)
confinis (Klug, 1835)
Chiridopsis aubei (Boheman,
1855)
Laccoptera (Orphodella)
corrugata (Sahlberg, 1823)
I
I
R
R
Coache &
Rainon, 2020
Coache &
Rainon, 2020
Coache &
Rainon, 2020
Henriques,
1917
Coache &
Rainon, 2020
Coache &
Rainon, 2020
Coache &
Rainon, 2020
Microland
E
R
Fairmaire, 1891
Jordan, 1903
E
E
Berlioz, 1919
E
E
Zoia, 2017
R
R
R
R
R
R
R
Hatita limbatella Fairmaire, 1891
Lema rubricollis Klug, 1835
Afroeurydemus variicolor (Berlioz,
1919)
Cheiridella principis Zoia, 2017
Castel-Branco,
1966
Luna de
Carvalho, 1984
Pachymerus lacerdae
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
Zabrotes Horn, 1885
Pachymerus nucleorum (Fabricius,
1792)
Zabrotes subfasciatus (Boheman,
1833)
12
Pachymerus Thunberg, 1805
*
*
Laccoptera corrugata
*
321
(continued)
Rhembastus Harold, 1877
Subfamily Galerucinae Latreille, 1802
Lamprocopa Hincks, 1949
Longitarsus Latreille, 1829
Manobia Jacoby, 1885
Nisotra Baly, 1864
Notomela Jacoby, 1899
Subfamily Hispinae Gyllenhal, 1813
Dactylispa Weise, 1897
Platypria Guérin-Méneville, 1840
Lamprocopa delata (Erichson,
1843)
Lamprocopa occidentalis Weise,
1895
Longitarsus sp.
Manobia sp.
Nisotra theobromae Laboissière,
1920
Notomela joliveti Biondi &
D’Alessandro, 2015
Dactylispa aculeata (Klug, 1835)
Dactylispa cavicollis Gestro, 1905
Dactylispa incredula Gestro, 1905
Dactylispa nigricornis Gestro,
1905
Platypria (Dichirispa)
paucispinosa Gestro, 1905
Thomispa feae (Gestro, 1906)
P
E
R
ST
E
A
Reference
Zoia, 2017
Zoia, 2017
ML
Synonyms
Zoia, 2017
R
Jordan, 1903
R
R
Microland
*
E
R?
R?
E
Microland
Microland
Laboissière,
1920
Biondi &
D’Alessandro,
2015
*
*
*
E
R
E
E
Gestro, 1905
Gestro, 1905
Gestro, 1905
Gestro, 1905
R
R
Gestro, 1905
E
E
Gestro, 1905
E
Anlacophora delata; Aulacophora
delata
Platypria feae
*
Trichispa feae
G. Nève et al.
Thomispa Würmli, 1975
Species
Paraivongius (Micromenius) sp.
Paraivongius (Paraivongius)
inexspectatus Zoia, 2017
Rhembastus piceus Zoia, 2017
322
Higher taxonomy
Paraivongius Pic, 1936
Myriochila Motschulsky, 1862
Cylindera (Ifasina) octoguttata
(Fabricius, 1787)
Lophyra neglecta (Dejean, 1825)
R
Myriochila melancholica
(Fabricius, 1798)
R
Serrano, 2008
R
R
Gomes Alves,
1956
Jordan, 1903
Xylographus nitidissimus Pic, 1916
R
Pic 1916
Necrobia rufipes (De Geer, 1775)
I
Luna de
Carvalho, 1984
Family Coccinellidae Latreille, 1807
Subfamily Chilocorinae Mulsant, 1846
Chilocorus Leach, 1815
Chilocorus cacti (Linnaeus, 1767)
R
Chilocorus pilosus Sicard, 1920
Endochilus plagiatus Sicard, 1920
Endochilus styx Sicard, 1911
Exochomus flavipes (Thunberg,
1781)
Exochomus nigrifrons Gerstäcker,
1871
E
E
R
Castel-Branco,
1963
Sicard, 1920
Sicard, 1920
Sicard, 1911
Sicard, 1920
R
Fürsch, 1974
R
Henriques,
1917
Endochilus Weise, 1898
Exochomus Redtenbacher, 1843
Subfamily Coccinellinae Latreille, 1807
Cheilomenes Mulsant, 1850
Cheilomenes sulphurea (Olivier,
1791)
E
R
Myriochile melancholica;
Cicindela melancholica
Exochomus nigromaculatus
insulicola
Brumus nigrifrons
(continued)
323
Family Ciidae Leach, 1819
Subfamily Ciinae Leach, 1819
Xylographus Melli‚, 1849
Family Cleridae Latreille, 1802
Subfamily Korynetinae Laporte, 1836
Necrobia Olivier, 1800
Lophyra discoidea
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
Lophyra Motschulsky, 1861
12
Family Cicindelidae Latreille, 1802
Subfamily Cicindelinae W. Horn, 1926
Cylindera Westwood, 1831
Micraspis Chevrolat in Dejean, 1836
Species
Coccinella intermedia (Crotch,
1874)
Micraspis striata (Fabricius, 1792)
Oenopia Mulsant, 1850
Oenopia doderoi (Sicard, 1911)
E
Hounkpati et al.,
2020
Sicard, 1911
Thea Mulsant, 1846
Subfamily Epilachninae Mulsant, 1846
Chnootriba Dejean, 1835
Thea moniqueae Fürsch, 1974
E
Fürsch, 1974
Chnootriba elaterii (Rossi, 1794)
R
Hounkpati et al.,
2020
Aulis nigricordis Fürsch, 1974
E
Fürsch, 1974
Scymnomorphus minuta Fürsch,
1974
Scymnomorphus principiensis
Gomes Alves & Castel-Branco,
1962
E
Fürsch, 1974
Subfamily Exoplectrinae Crotch, 1874
Aulis Mulsant, 1850
Subfamily Microweiseinae Leng, 1920
Scymnomorphus Weise, 1897
Subfamily Ortaliinae Mulsant, 1850
Rodolia Mulsant, 1850
Nephus Mulsant, 1846
ST
E
R
E
A
Reference
Gordon, 1987
Synonyms
Alesia striata
Coccinella doderoi; Synharmonia
doderoi
Sukunahikona minuta
Gomes Alves &
Castel-Branco,
1962
Rodolia cardinalis (Mulsant, 1850)
I
Rodolia seabrai Sicard, 1920
Rodolia vulpina Fürsch, 1974
E
E
Castel-Branco,
1963
Sicard, 1920
Fürsch, 1974
E
E
Castel-Branco,
1963
Fürsch, 1974
Fürsch, 1974
Cryptognatha nodiceps Marschall,
1912
Nephus derroni Fürsch, 1974
Nephus theobromae Fürsch, 1974
ML
I
G. Nève et al.
Subfamily Scymninae Mulsant, 1846
Cryptognatha Mulsant, 1850
P
324
Higher taxonomy
Coccinella Linnaeus, 1758
Scymnus oblongoides Fürsch, 1974
Scymnus scapuliferus Mulsant,
1850
Scymnus senegalensis Mader, 1955
Stethorus Weise, 1885
Subfamily Sticholotidinae Weise, 1901
Pharoscymnus Bedel, 1906
R
R
R
R
Family Curculionidae Latreille, 1802
Subfamily Conoderinae Schönherr, 1833
Panoptes Gerstaecker, 1860
Panoptes convexus Karsch, 1881
Subfamily Cryptorhynchinae Schönherr, 1825
Cyamobolus Schönherr, 1837
Cyamobolus greeffi Karsch, 1881
Mechistocerus Fauvel, 1862
Mechistocerus nubeculosus
Fairmaire, 1891
Subfamily Entiminae Schönherr, 1823
Phyllobius Germar, 1824
Phyllobius verruculatus Karsch,
1881
R
Gomes Alves,
1973
Fürsch, 1974
E
Fürsch, 1974
E
Karsch, 1881
E
R
Karsch, 1881
Fairmaire, 1891
E
Karsch, 1881
E
R
R
Stethorus chazeaui Fürsch, 1974
Pharoscymnus exiguus Weise,
1913
Pharoscymnus tetrastictus Sicard,
1930
Pharoscymnus tomeensis Fürsch,
1974
E
Fürsch 1974
Fürsch, 1974
Hounkpati et al.,
2020
Fürsch, 1974
Gomes Alves,
1973
Hounkpati et al.,
2020
Fürsch, 1974
R
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
Platynaspis capicola Crotch, 1874
Scymnus levaillanti Mulsant, 1850
Scymnus nubilus Mulsant, 1850
12
Platynaspis Redtenbacher, 1843
Scymnus Cuvier, 1816
Scymnus canariensis
Cyanobulus greeffi
Mecictocerus nubeculosus
(continued)
325
Subfamily Molytinae Schönherr, 1823
Aethiopacorep Voisin, 1992
Sternuchopsis Heller, 1917
Titilayo Cristóvão & Lyal, 2018
Subfamily Platypodinae Shuckard, 1839
Chaetastus Nunberg 1953
Costaroplatus Nunberg, 1963
Doliopygus Browne, 1962
P
Aethiopacorep africanus
(Hustache, 1932)
Sternuchopsis sp.
Titilayo barclayi Cristóvão & Lyal,
2018
Titilayo perrinae Cristóvão & Lyal,
2018
Titilayo saotomense Cristóvão &
Lyal, 2018
Titilayo turneri Cristóvão & Lyal,
2018
ST
E
R?
E
E
E
E
Chaetastus tuberculatus (Chapuis,
1865)
R
Costaroplatus pernix (Schedl,
1941)
Doliopygus erichsoni (Chapuis,
1865)
E
Doliopygus ibex Schedl, 1941
E
Periommatus excisus Strohmeyer,
1912
R
R
R
A
Reference
Borovec &
Anderson, 2021
E
Cristóvão &
Lyal, 2018
Microland
Cristóvão &
Lyal, 2018
Cristóvão &
Lyal, 2018
Cristóvão &
Lyal, 2018
Cristóvão &
Lyal, 2018
Beaver &
Löyttyniemi,
1985
Wood & Bright,
1992
Beaver &
Löyttyniemi,
1985
Wood & Bright,
1992
Wood & Bright,
1992
ML
Synonyms
*
Platyscapus pernix
Crossotarsus erichsoni
G. Nève et al.
Periommatus Chapuis, 1866
Species
Saotomia tuberculata Borovec &
Anderson, 2021
326
Higher taxonomy
Saotomia Borovec & Anderson, 2021
Xyleborus Eichhoff, 1864
I
Platypus intermedius (Schedl,
1937)
Platypus parallelus (Fabricius,
1801)
R
Stenoplatypus intermedius
R
I
Medler, 1980
Kaden, 1930
Hylesinopsis dubius
Stephanoderes hampei
I
Luna de
Carvalho 1984
R
Jordan, 1903
I
Luna de
Carvalho, 1984
R
Microland
R
Henriques,
1917
I
Hapalogenius dubius Eggers, 1920
Hypothenemus hampei (Ferrari,
1867)
Xyleborus ferrugineus (Fabricius,
1801)
Family Dryophthoridae Schönherr, 1825
Subfamily Dryophthorinae Schönherr, 1825
Cosmopolites Chevrolat, 1885
Cosmopolites sordidus (Germar,
1824)
Sitophilus Schönherr, 1838
Sitophilus oryzae (Linnaeus, 1763)
Subfamily Rhynchophorinae Schönherr, 1833
Metamasius Horn, 1873
Metamasius hemipterus Linnaeus,
1758
Temnoschoita Chevrolat, 1885
Temnoschoita quadrimaculata
Csiki, E., 1936
Family Dytiscidae Leach, 1815
Subfamily Copelatinae Van den Branden, 1885
Copelatus Erichson, 1832
Copelatus pallidus Régimbart,
1895
Wood & Bright,
1992
Wood & Bright,
1992
Wood & Bright,
1992
R
Régimbart,
1904
Sphenophorus sordidus;
Sphenophorus striatus
*
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
Subfamily Scolytinae Latreille, 1804
Hapalogenius Hagedorn, 1912
Hypothenemus Westwood, 1836
Platypus hintzi Schaufuss, 1897
12
Platypus Herbst, 1793
*
(continued)
327
Family Elateridae Leach, 1815
Subfamily Agrypninae Candèze, 1857
Calais Laporte de Castelnau, 1836
Elasmosomus Schwarz, 1903
Species
P
ST
Cybister (Melanectes) vulneratus
Klug, 1834
R
R
Jordan, 1903
E
Karsch, 1881
E
Girard, 2017
Calais controversa (Karsch, 1881)
E
R
Reference
Girard, 2017
ML
Synonyms
Trogus binotatus; Melanectes
vulneratus; Cybister binotatus
*
Ctenicera controversa; Alaus
chalcolepidinus
*
Lanelater substriatus
R
Girard, 2017
R
Fairmaire, 1891
E
Fairmaire, 1891
E
Fairmaire, 1891
E
Girard, 2017
E
Karsch, 1881
*
R
Microland
*
Psephus athoides
G. Nève et al.
Elasmosomus mocquerysi
(Fleutiaux, 1902)
Lanelater Arnett, 1952
Lanelater glabratus (Gyllenhall,
1817)
Subfamily Denticollinae Stein & Weise, 1877
Melanoxanthus Dejean, 1833
Melanoxanthus inaequalis
Candèze, 1881
Subfamily Elaterinae Leach, 1815
Propsephus Hyslop, 1921
Propsephus athoides (Candèze,
1881)
Propsephus campyloides (Candèze,
1897)
Propsephus melanotoides
(Fairmaire, 1891)
Propsephus scitulus Schwarz, 1909
Subfamily Lissominae Laporte, 1835
Lissomus Dalman, 1824
Lissomus francisci Karsch, 1881
Family Endomychidae Leach, 1815
Subfamily Lycoperdininae Bromhead, 1838
Ancylopus Costa, 1854
Ancylopus meridionalis Stroheker,
1962
A
328
Higher taxonomy
Subfamily Dytiscinae Leach, 1815
Cybister Curtis, 1827
Subfamily Histerinae Gyllenhal, 1808
Apobletes Marseul, 1861
Corticalinus Gomy, 2004
Hololepta Paykull, 1811
Pachycraerus Marseul, 1854
Platylister Lewis, 1892
Teretrius Erichson, 1834
Family Hybosoridae Erichson, 1847
Subfamily Hybosorinae Erichson, 1847
Hybosorus MacLeay, 1819
Family Hydrophilidae Latreille, 1802
Subfamily Sphaeridiinae Latreille, 1802
Coelostoma Brullé, 1835
Orectogyrus (Lobogyrus) lionotus
Régimbart, 1884
R
Régimbart,
1904
Platylomalus digitatus (Wollaston,
1867)
Platylomalus longicornis (Lewis,
1906)
R
Gomy, 2004
E
E
Lewis, 1906
E
R
R
Lewis, 1906
Gomy, 2004
R
R
R
Lewis, 1900
Lewis, 1900
*
R
R
Gomy, 2004
*
R
R
Gomy, 2004
*
R
Lewis, 1900
R
Kuijten, 1983
Apobletes macer (Lewis, 1906)
Corticalinus minusculus (Schmidt,
1893)
Hololepta syntexis Lewis, 1900
Pachycraerus chlorites Lewis,
1900
Pachycraerus cyanescens
Erichson, 1834
Platylister (Ricinodendrus)
foliaceus (Paykull, 1811)
Teretrius braganzae Lewis, 1900
Hybosorus illigeri Reiche, 1853
R
Platysoma macer
Régimbart,
1907
(continued)
329
Coelostoma rufitarse (Boheman,
1851)
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
Family Histeridae Gyllenhal, 1808
Subfamily Dendrophilinae Reitter, 1909
Platylomalus Cooman, 1948
12
Family Gyrinidae Latreille, 1810
Subfamily Gyrininae Latreille, 1810
Orectogyrus Régimbart, 1884
Megasternini Mulsant, 1844
Pachysternum Motschulsky, 1863
Pelosoma Mulsant, 1844
Species
Dactylosternum abdominale
(Fabricius, 1792)
Dactylosternum intermedium
Régimbart, 1907
Dactylosternum profundum
Régimbart, 1907
Unidentified species
Pachysternum capense (Mulsant,
1844)
Pelosoma buccalis (Régimbart,
1907)
ST
R
R
E
R
R?
R
E
R
I
I
R
R
I
R
R?
A
Reference
Régimbart,
1907
Régimbart,
1907
Régimbart,
1907
Microland
Régimbart,
1907
Régimbart,
1907
ML
*
Lefkovitch,
1962
Luna de
Carvalho, 1984
Luna de
Carvalho, 1984
Lefkovitch,
1962
Lefkovitch,
1962
Luna de
Carvalho, 1984
Lefkovitch,
1962
Microland
Synonyms
*
G. Nève et al.
Family Laemophloeidae Ganglbauer, 1899
Subfamily Laemophloeinae Ganglbauer, 1899
Cryptolestes Ganglbauer, 1899
Cryptolestes atulus Lefkovitch,
1962
Cryptolestes ferrugineus (Stephens,
1831)
Cryptolestes pusillus (Schönherr,
1817)
Placonotus Mac Leay, 1871
Placonotus bolivari (Grouvelle,
1905)
Placonotus politissimus (Wollaston, 1867)
Placonotus testaceus (Fabricius,
1787)
Xylolestes Lefkovitch, 1962
Xylolestes unicolor (Grouvelle,
1908
Family Limnichidae Erichson, 1846
Unidentified species
P
330
Higher taxonomy
Dactylosternum Wollaston, 1854
12
Figulus anthracinus Klug, 1832
Figulus decipiens Albers, 1884
Nigidius bubalus (Swederus, 1787)
Nigidius endroedi Gomes Alves,
1973
Prosopocoilus Westwood, 1845
Prosopocoilus antilopus amicorum
Matsumoto, 2019
Prosopocoilus antilopus beisa
Kriesche, 1919
Prosopocoilus antilopus insulanus
Kriesche, 1919
Prosopocoilus downesii savagei
(Hope, 1835)
Prosopocoilus senegalensis (Klug,
1835)
Family Lycidae Laporte de Castelnau, 1838
Subfamily Lycinae Laporte, 1836
Flagrax Kasantsev, 1992
Flagrax bifoveolatus Pic, 1924
Stadenus Waterhouse, 1879
Stadenus auberti sensifulvus
Fairmaire, 1891
Family Lymexylidae Fleming, 1821
Subfamily Atractocerinae Laporte, 1840
Atractocerus Palisot de Beauvoir, 1801
Atractocerus brevicornis (Linnaeus, 1766)
R
E
Nigidius MacLeay, 1819
R
E
E
E
R
Griffini, 1906
Gomes Alves,
1973
Klug, 1835
Gomes Alves,
1973
Matsumoto,
2019
Griffini, 1906
*
Figulus sublaevis
Figulus sublaevis decipiens
Nigidius auriculatus
Prosopocoelus antilopus
E
Fairmaire, 1891
*
Prosopocoelus antilopus
R
Griffini, 1906
*
Metopodontus downesii
R
Bartolozzi &
Werner, 2004
E
Pic, 1926
Fairmaire, 1891
R
Jordan, 1903
E
*
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
Family Lucanidae Latreille, 1804
Subfamily Lucaninae Latreille, 1804
Figulus MacLeay, 1819
Stadenus semiflavus; Stadenus
auberti semufulvus
(continued)
331
Atractocerus africanus;
Atractocerus frontalis;
Atractocerus brevicornis
africanus
Ophthalmoglipa Franciscolo, 1952
Species
Glipostena nemoralis Franciscolo,
1962
Ophthalmoglipa horaki Ruzzier,
2015
Ophthalmoglipa leblanci Ruzzier,
2015
Family Mycteridae Oken, 1843
Subfamily Hemipeplinae Lacordaire, 1854
Hemipeplus Latreille, 1825
Hemipeplus africanus Grouvelle,
1915
Family Nitidulidae Latreille, 1802
Subfamily Carpophilinae Erichson, 1842
Carpophilus Stephens, 1830
Carpophilus dimidiatus (Fabricius,
1792)
Carpophilus hemipterus (Linnaeus,
1758)
Subfamily Epuraeinae Kirejtshuk, 1986
Epurea Erichson, 1845
Epureae ocularis Fairmaire, 1849
Family Oedemeridae Latreille, 1810
Subfamily Oedemerinae Latreille, 1810
Alloxanthoides Svihla, 1985
Alloxanthoides lateritincta (Pic,
1920)
Monosigynes Vazquez, 2004
Ditylomorphula bicolorites (Pic,
1922)
Monosigynes semipiceus (Karsch,
1881)
ST
R
E
A
Reference
ML
Microland
*
Ruzzier, 2015
*
E
Ruzzier, 2015
R
Microland
I
Luna de
Carvalho, 1984
Luna de
Carvalho, 1984
I
R
Microland
R
E
Serrano
unpublished
data
Pic, 1922
E
Karsch, 1881
Synonyms
*
*
Epureae (Haptoncus) ocularis
Danerces semipicea
G. Nève et al.
Ditylomorphula Svihla, 1985
P
332
Higher taxonomy
Family Mordellidae Latreille, 1802
Subfamily Mordellinae Latreille, 1802
Glipostena Ermisch, 1941
Didymus laevis (Klug, 1835)
E
Pentalobus barbatus (Fabricius,
1801)
Family Ptiliidae Heer, 1843
Subfamily Acrotrichinae Reitter, 1909
Acrotrichis Motschulsky, 1848
R
Gomes Alves,
1965
Jordan, 1903
R
Darby, 2020
R
Darby, 2020
R?
Microland
I
Luna de
Carvalho, 1984
I
Luna de
Carvalho, 1984
R
Paulian, 1941
*
Pselaphus barbatus
*
Odontaeus pallens
Janson, 1907
R
R
Jordan, 1903
(continued)
333
Acrotrichis (Ctenopteryx)
discoloroides Johnson, 1969
Acrotrichis tersa Johnson, 1969
Family Ptilodactylidae Laporte de Castelnau, 1836
Unidentified species
Family Ptinidae Latreille, 1802
Subfamily Anobiinae Fleming, 1821
Stegobium paniceum (Linnaeus,
Stegobium Motschulsky, 1860
1758)
Subfamily Xyletininae Gistel, 1848
Lasioderma serricorne (Fabricius,
Lasioderma Stephens, 1835
1792)
Family Scarabaeidae Latreille, 1802
Subfamily Bolboceratinae Mulsant, 1842
Bolbocaffer Vulcano,Martinez & Pereira Bolbocaffer pallens (Kolbe, 1835)
1969
Subfamily Cetoniinae Leach, 1815
Chlorocala Kirby, 1828
Chlorocala viridicyanea (Palisot de
Beauvois, 1821)
Diplognata Gory & Percheron, 1833
Diplognata (Diplognatha) gagates
Forster, 1771
E
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
Pentalobus Kaup, 1868
12
Family Passalidae Leach, 1815
Subfamily Passalinae Leach, 1815
Didymus Hincks, 1933
Leucocelis Burmeister, 1842
Pachnoda Burmeister, 1842
Phaneresthes Kraatz, 1894
Pseudoheterophana Allard, 1990
Pseudotephraea Kraatz, 1882
Uloptera Burmeister, 1842
Subfamily Dynastinae MacLeay, 1819
Cyphonistes Burmeister, 1847
Oryctes Hellwig, 1798
Species
Dischista rufa (De Geer, 1778)
Grammopyga cincticollis (Hope,
1842)
Grammopyga marginicollis
(Moser, 1904)
Leucocelis feana Janson, 1907
Pachnoda canui Rigout & Allard,
1992
Pachnoda prasina Karsch, 1881
Phaneresthes flavosignata (Moser,
1904)
Pseudoheterophana canui Allard,
1990
Pseudotephraea ancilla ancilla
(Harold, 1879)
Pseudotephraea ancilla canui
Antoine, 1992
Uloptera canui Antoine, 1992
ST
R
R
A
Reference
Jordan, 1903
Janson, 1907
E
Moser, 1904
E
Janson, 1907
Rigout &
Allard, 1992
Karsch, 1881
Moser, 1904
E
E
E
E
ML
Synonyms
Pachnoda rufa; Cetonia rufa
Cetonia prasina
Allard, 1990
E
Harold, 1879
E
Jordan, 1903
E
Antoine, 1992
E
R
E
I
Tephraea ancilla
Karsch, 1881
Vesco et al.,
1999
Fairmaire, 1891
Vargas Ferreira,
1967
G. Nève et al.
Cyphonistes camurus Karsch, 1881
Oryctes (Rykanes) capucinus
Arrow, 1937
Oryctes (Rykanes) latecavatus
Fairmaire, 1891
Oryctes (Rykanoryctes) monoceros
Olivier, 1789
P
334
Higher taxonomy
Dischista Burmeister, 1842
Grammopyga Kolbe, 1895
Subfamily Melolonthinae MacLeay, 1819
Apogonia Kirby, 1819
Apogonia decellei Lacroix, 2008
Apogonia insulana Karsch, 1882
Apogonia tomeensis Lacroix, 2008
Subfamily Orphninae Erichson, 1847
Stenosternus costatus Karsch, 1881
Stenosternus Karsch, 1881
Subfamily Scarabaeinae Latreille, 1802
Onthophagus Latreille, 1802
Onthophagus (Onthophagus)
sellatus Klug, 1845
Onthophagus (Trichonthophagus)
juvencus Klug, 1835
Paraphytus Harold, 1877
Paraphytus africanus Boucomont,
1923
Phalops fimbriatus (Klug, 1835)
Phalops Erichson, 1848
Proagoderus Lansberge, 1883
Proagoderus laticollis Klug, 1835
E
E
R
R
Krell, 1994
E
E
Lacroix, 2008
Karsch, 1882
Lacroix, 2008
E
Karsch, 1881
R
d’Orbigny,
1905
d’Orbigny,
1905
Paulian, 1949
E
R
R
R
R
R
Dechambre,
1983
Dechambre,
1983
Henriques,
1917
R
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
Temnorhynchus Hope, 1837
Rhizoplatys canui Dechambre,
1983
Rhizoplatys mucronatus cedrici
Dechambre, 1983
Temnorhynchus (Temnorhynchus)
coronatus diana (Palisot de
Beauvois, 1805)
Temnorrhynchus (Temnorhynchus)
tridentatus Lansberge, 1886
12
Rhizoplatys Westwood, 1842
*
Temnorhynchus diana
*
*
*
Mecistoceros costatus
*
d’Orbigny,
1913
d’Orbigny,
1913
(continued)
335
Comythovalgus Kolbe, 1884
Cryptodontus Burmeiester, 1847
Family Silvanidae Kirby, 1837
Subfamily Silvaninae Kirby, 1837
Ahasverus Gozis, 1881
Cryptamorpha Wollaston, 1854
Oryzaephilus Ganglbauer, 1899
Family Staphylinidae Lameere, 1900
Subfamily Osoriinae Erichson, 1839
Afrosorius Fagel, 1958
Clastocnemis quadrimaculatus
oremansi Antoine, 2005
Clastocnemis quadrimaculatus
principis Antoine, 2005
Comythovalgus aemulus Kolbe,
1897
Cryptodontus latreilleanus
desaegeri Burgeon, 1946
P
ST
E
E
A
Reference
ML
Antoine, 2005
*
Synonyms
Antoine, 2005
R
Janson, 1907
E
Henriques,
1917
Ahasverus advena (Waltl, 1834)
I
Cryptamorpha sp.
Oryzaephilus mercator (Fauvel,
1889)
Oryzaephilus surinamensis (Linnaeus, 1758)
R?
I
Luna de
Carvalho, 1984
Microland
Luna de
Carvalho, 1984
Luna de
Carvalho, 1984
Afrosorius assiniensis (Fauvel,
1903)
Afrosorius curtipennis Fagel, 1958
Afrosorius strigifrons (Kolbe,
1889)
Afrosorius viettei Fagel, 1958
Nacaeus aethiops (Eppelsheim,
1895)
R
Ferreira, 2014
E
R
Fagel, 1958
Ferreira, 2014
E
R
Fagel, 1958
Fauvel, 1903
I
*
*
G. Nève et al.
Nacaeus Blackwelder, 1942
Species
336
Higher taxonomy
Subfamily Trichiinae Fleming, 1821
Clastocnemis Burmeister & Schaum,
1840
Paederus angusticeps Bernhauer,
1915
Rugilus rubelloides (Fagel, 1951)
Tracypum vietteanum Fagel, 1977
Philonthus longicornis Stephens,
1832
Philonthus peregrinus Fauvel,
1866
Subfamily Tachyporinae MacLeay, 1825
Tachinomorphus Kraatz, 1859
Tachinomorphus africanus
(Eppelsheim, 1895)
Family Tenebrionidae Latreille, 1802
Subfamily Diaperinae Latreille, 1802
Ceropria Laporte & Brullé, 1831
Ceropria anthracina Quedenfeldt,
1885
Ceropria romandi Laporte &
Brullé, 1831
Gnathidium Gebien, 1920
Gnathidium cephalotes Gebien,
1921
Hypophloeus Fabricius, 1790
Hypophloeus insularis Gebien,
1921
Hypophloeus piceus Gebien, 1921
Hypophloeus sternalis Gebien,
1914
Ischnarthron Gebien, 1920
Ischnarthron longipes Gebien,
1921
R
Fagel, 1966
R
E
Fagel, 1953
Fagel, 1977
R
Ferreira, 2014
R
Ferreira, 2014
R
Fauvel, 1903
R
Gebien, 1921
Stilicus rubelloides
R
Gebien, 1921
E
Gebien, 1921
R
Gebien, 1942
Corticeus insularis
E
Gebien, 1921
Gebien, 1914
Corticeus sternalis
E
Gebien, 1921
E
E
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
Rugilus Leach, 1819
Tracypum Fagel, 1977
Subfamily Staphylininae, Latreille, 1802
Philonthus Stephens, 1826
12
Subfamily Paederinae Fleming, 1821
Paederus Fabricius, 1775
337
(continued)
Platydema Laporte de Castelnau &
Brullé, 1831
Stomylus Fåhraeus, 1870
Species
Microcrypticus scriptipennis
(Fairmaire, 1875)
Platydema capucinum Gebien,
1921
Stomylus maculosus (Thomson,
1858)
ST
R
A
E
Reference
Gebien, 1942
Synonyms
Gebien, 1921
R
Gebien, 1942
R
E
Microland
Fairmaire, 1891
*
*
E
Jordan, 1903
*
Prioscelis serrata haesitans
E
Ardoin, 1958
*
Eremobates crux
Eremobates metallicus
E
R
R
R
R
Gebien, 1921
E
E
Gebien, 1942
Ardoin,1958
E
Gebien, 1921
E
Karsch, 1881
E
ML
R
Pselaphidion macularium;
Pselaphidion maculosum;
Platydema maculosum
Ardoin, 1958
Gebien, 1942
*
G. Nève et al.
Subfamily Lagriinae Latreille, 1825 (1820)
Luprops chalceus Gebien, 1921
Luprops Hope, 1833
Physolagria Fairmaire, 1891
Physolagria molleri Fairmaire,
1891
Prioscelis Hope, 1840
Prioscelis haesitans Kolbe, 1903
Subfamily Phrenapatinae Solier, 1834
Afrotagalus Gebien, 1942
Afrotagalus viettei Ardoin, 1958
Subfamily Stenochiinae Kirby, 1837
Alcyonotus Pascoe, 1882
Alcyonotus insularis Ardoin, 1958
Derosphaerus Thomson, 1858
Derosphaerus globicollis Thomson, 1858
Derosphaerus morosus
(Motschulsky, 1872)
Eremobatodes Gebien, 1943
Eremobatodes crux (Gebien, 1921)
Eremobatodes metallicus (Ardoin,
1958)
Menephilus carbonatus Gebien,
Menephilus Mulsant, 1854
1921
Menephilus conquinatus Karsch,
1881
P
338
Higher taxonomy
Microcrypticus Gebien, 1921
Gebien, 1921
E
Gebien, 1921
E
E
Karsch, 1881
Ardoin, 1962
E
Karsch, 1881
E
*
Derosphaerus justi
Derosphaerus marquesii
Gebien, 1921
E
Gebien, 1921
E
Ardoin, 1958
E
*
Robiche, 2000
E
Gebien, 1921
I
Luna de
Carvalho, 1984
Gebien, 1942
R
E
E
E
R
R
*
R
Gebien, 1921
Gebien, 1921
Gebien, 1921
Jordan, 1903
Gebien, 1921
*
*
Toxicum taurus; Cryphaeus aries
(continued)
339
Subfamily Tenebrioninae Latreille, 1802
Alphitobius Stephens, 1829
Alphitobius laevigatus (Fabricius,
1781)
Alphitobius viator Mulsant &
Godart, 1868
Amenophis Thomson, 1858
Amenophis insularis Gebien, 1921
Amenophis minor Gebien, 1921
Amenophis striata Gebien, 1921
Cryphaeus Klug, 1833
Cryphaeus taurus (Fabricius, 1801)
Diaclina Jacquelin du Val, 1861
Diaclina parallela (Thomson,
1858)
E
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
Strongylium Ditmar, 1809
Nesosphaerotus aeneus Gebien,
1921
Nesosphaerotus egena Gebien,
1921
Nesosphaerotus justi Karsch, 1881
Nesosphaerotus kulzeri Ardoin,
1962
Nesosphaerotus marquesi Karsch,
1881
Nesosphaerotus simplicifrons
Gebien, 1921
Nesosphaerotus striatipennis
Gebien, 1921
Nesosphaerotus viettei Ardoin,
1958
Strongylium camiadei Robiche,
2000
Strongylium feai Gebien, 1921
12
Nesosphaerotus Gebien, 1921
Hoplonyx Thomson, 1858
Megacantha Westwood, 1843
Nesopatrum Gebien, 1921
Palorus Mulsant, 1854
Peltoides Laporte de Castelnau, 1832
Tenebrio Linnaeus, 1758
Tribolium Macleay 1825
P
ST
R
A
R
R
E
R
E
R
Synonyms
Gonocephalum granicolle
Opatrum calcaripes
Gebien, 1921
Gebien, 1921
Gebien, 1942
Gebien, 1921
Gebien, 1921
E
Karsch, 1881
Opatrinus josephi
R
R
Gebien, 1921
Gebien, 1921
Platyotus carinicollis
R
Gebien, 1921
R
Gebien, 1921
E
I
R
E
E
R
ML
Karsch, 1881
R
R
Reference
Gebien, 1921
Robiche, 2009
Luna de
Carvalho, 1984
Gebien, 1921
Gebien, 1942
Karsch, 1881
Gebien, 1921
Tenebrioloma semicostata
*
G. Nève et al.
Uloma Dejean, 1821
Species
Gonocephalum angolense
subtilistriatum Kolbe, 1887
Gonocephalum calcaripes (Karsch,
1881)
Gonocephalum feae Gebien, 1921
Gonocephalum prolixum
(Erichson, 1843)
Gonocephalum simplex (Fabricius,
1801)
Hoplonyx insularis Gebien, 1921
Megacantha dentata (Fabricius,
1801)
Nesopatrum josephii (Karsch,
1881)
Palorus carinicollis Gebien, 1921
Palorus subdepressus (Wollaston,
1864)
Peltoides senegalensis Laporte de
Castelnau, 1832
Tenebrio (Afrotenebrio) guineensis
Imhoff, 1843
Tenebrio legalli Robiche, 2009
Tribolium castaneum (Herbst,
1797)
Tribolium semicostata Gebien,
1921
Uloma collaris Gebien, 1921
Uloma costae Karsch, 1881
Uloma laesicollis Thomson, 1858
340
Higher taxonomy
Gonocephalum Solier, 1834
Tenebroides Piller & Mitterpacher, 1783
Family Zopheridae Solier, 1834
Subfamily Colydiinae Billberg, 1820
Bitoma Herbst, 1793
Mecedanum Erichson, 1845
Microprius Fairmaire, 1868
R
Temnocheila patricioi (Karsch,
1881)
Tenebroides maroccanus Reitter,
1884
Tenebroides mauritanicus (Linnaeus, 1758)
Bitoma siccana (Pascoe, 1863)
Mecedanum auberti (Fairmaire,
1882)
Microprius rufulus (Motschulsky,
1863)
Gebien, 1921
Opatrinus atratus; Opatrinus
opacus
E
Karsch, 1881
Trogossita patricioi; Trogosita
patricioi
I
Luna de
Carvalho, 1984
Luna de
Carvalho, 1984
I
R
R
R
Pope, 1961
Serrano,
unpublished
data
Pope, 1961
Bitoma lyctiformis
Microprius confusus
The Beetles (Coleoptera) of Príncipe, São Tomé and Annobón
Family Trogossitidae Latreille, 1802
Subfamily Trogossitinae Latreille, 1802
Temnoscheila Westwood, 1830
Zidalus latipes (Sahlberg, 1823)
12
Zidalus Mulsant & Rey, 1852
341
342
G. Nève et al.
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Chapter 13
Butterflies and Skippers (Lepidoptera:
Papilionoidea) of the Gulf of Guinea
Oceanic Islands
Luís F. Mendes and António Bivar-de-Sousa
Abstract The three Gulf of Guinea oceanic islands, Príncipe, São Tomé, and
Annobón, have always remained isolated from the African continent and correspond
to the westernmost peaks of the Cameroon Volcanic Line, while the island of Bioko,
part of the same ridge, was connected to the mainland during glaciations. Despite the
small area of the oceanic islands, their relief and remoteness have enabled the
evolution of remarkable ecological and biological diversity. Concerning diurnal
Lepidoptera, 91 species and subspecies are known from the oceanic islands:
46 from Príncipe, 64 from São Tomé, and 8 from Annobón; and 35 are endemic:
17 to Príncipe, 23 to São Tomé, and only 5 shared among islands. Further species
have been reported in error, either due to misidentification or to mislabelling. A
revised checklist of the species and subspecies of the Gulf of Guinea oceanic
islands Papilionoidea is presented as is a summary of their taxonomy, distribution,
and ecology.
Keywords Africa · Conservation · Ecology · Endemism · Taxonomy
L. F. Mendes (*)
Departamento de Zoologia e Antropologia (Museu Bocage), Museu Nacional de História
Natural e da Ciência, Universidade de Lisboa, Lisbon, Portugal
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório
Associado, Universidade do Porto, Vairão, Portugal
e-mail: luisfmendes@edu.ulisboa.pt
A. Bivar-de-Sousa
Departamento de Zoologia e Antropologia (Museu Bocage), Museu Nacional de História
Natural e da Ciência, Universidade de Lisboa, Lisbon, Portugal
Sociedade Portuguesa de Entomologia, Lisbon, Portugal
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_13
349
350
L. F. Mendes and A. Bivar-de-Sousa
Introduction
The Gulf of Guinea Oceanic Islands (GGOI), Príncipe, São Tomé, and Annobón
(¼Pagalu), represent the Cameroon Volcanic Line’s westernmost peaks; they have
never been connected to one another nor to the mainland. Bioko (¼Fernando Poo),
on the other hand, is a continental island that was connected to mainland Africa
during glaciations, most recently, ca. 11,000 years (Lambert and Chappel 2001).
Annobón is part of Equatorial Guinea, and with ca. 17 km2, it is located ca. 180 km
SSW from São Tomé and 340 km W from Gabon (Jones and Tye 2006). The
maximum altitude of this small island is ca. 600 m (Quioveo peak) and its biodiversity (Exell 1944, 1956, 1973; Heras et al. 2002), Papilionoidea included, is much
lower than that of the other GGOI. Príncipe is the smaller of the Democratic
Republic of São Tomé e Príncipe main islands. With ca. 140 km2, it is ca. 210 km
SSW off Bioko and 140 km NNE of ST with a maximum altitude ca. 935 m (Pico
Príncipe). It was, however, much larger historically and extended to the SSW (Jones
and Tye 2006), including the plantless Tinhosas Islets. The Tinhosas are currently a
breeding colony of sea birds, a Ramsar site, from which no Papilionoidea are known.
São Tomé is ca. 860 km2, and lies almost 150 km SW of Príncipe, 180 km NNE of
Annobón and ca. 255 NW of Gabon, with a maximum altitude (Pico São Tomé)
ca. 2024 m. the Equator crosses Rolas Islet, which is just South of São Tomé.
The predominant natural ecosystem type of the GGOI was described as rainforest
(Exell 1944, 1973) or tropical moist broadleaf forest (Gascoigne 2004), which is
stratified into lowland (0–800 m), montane (800–1400 m), and mist forest
(1400–2024 m), the last category being absent from Príncipe. In Annobón the
three types appear compressed in its small altitudinal range as in the lower São
Tomé southern peaks (Ogonovszky 2003). Due to rain shadow, NW São Tomé has a
dry forest, which is rich in endemic butterfly species.
In relation to diurnal Lepidoptera, the skippers (Hesperiidae) were formerly
placed in the superfamily Hesperioidea, independent from the butterflies, but
Heikkilä et al. (2012), supported by morphological and genetic data, demonstrated
that they are part of the same evolutionary group, the superfamily Papilionoidea.
Their diversity and endemism in São Tomé and Príncipe has been the focus of
several notable studies (Pyrcz 1992a; Mendes and Bivar-de-Sousa 2012a) and a
further contribution is currently in preparation (Mendes et al. in prep.). Here we
provide an updated checklist of the Papilionoidea of the GGOI and review previously incorrectly cited taxa.
The Papilionoidea of the Gulf of Guinea Oceanic Islands:
Data Sources
The first references to the Papilionoidea of Annobón were given by Aurivillius
(1910), who reported Borbo fatuellus (sub Baoris), and Kheil (1910) who noted
Leptotes pirithous (sub Syntarucus), A. zetes (as monotypic) and Telchinia pharsalus
13
Butterflies and Skippers (Lepidoptera: Papilionoidea) of the Gulf. . .
351
(sub Acraea). Aurivillius (1928) and Bacelar (1948) recorded Euchrysops osiris (sub
Cupido). D’Abrera (1980) described Acraea zetes annobona (type locality), which
also occurs in São Tomé and Príncipe, being endemic to the three islands. Viejo
(1984) added Melanitis leda, Danaus chrysippus, Hypolimnas misippus and
Telchinia pharsalus (sub Acraea) to the list of species of these islands but some of
the samples were reported only from “Spanish Guinea”. Olano and Marcos (1993)
report the species assigned by Viejo (1984) but consider D. chrysippus as restricted
to Rio Muni and Bioko while Euchrysops osiris is assigned to the mainland only.
Acraea zetes annobona is not recognized by Olano and Marcos (1993) despite
Annobón being its type locality. These authors also question the presence in the
islands of Sevenia boisduvalli insularis (today considered a São Tomé endemic) and
of Dixeia piscicollis reported by D’Abrera (1980) from Equatorial Guinea but later
considered as a São Tomé endemic (D’Abrera 1997). These are the only data known
on the Papilionoidea of the most remote and less diverse GGOI. An even lower
diversity is known from the remote Saint Helena that, while not part of the Cameroon
Volcanic Line, lies eastwards of the Mid-Atlantic chain (Ashmole and Ashmole
2000): Lampides boeticus, Danaus chrysippus, Vanessa cardui and Hypolimnas
misippus, all widely ranged migratory species.
The scientific knowledge of butterfly and skipper diversity of the GGOI has
increased intermittently since Cramer (1775–1776). It (almost) stabilized during
the eighteenth century (1850–1870) but suddenly increased from the turn of the
nineteenth until the twentieth century with the contributions of Aurivillius,
Joicey and Talbot, Sharpe and Snellen. After another hiatus, several additional
phases of discovery followed, firstly due to the work of Amélia Bacelar (Bacelar
1948, 1958) in the mid-twentieth century, and then, toward the end of the century
the contributions of Libert (2004, 2011), Pyrcz (1991a–c) and our work in São
Tomé and Príncipe (Mendes et al. 1988, 2018; Mendes and Bivar-de-Sousa 2006,
2012a, b).
Some large collections, which are mostly currently housed in the Museu Nacional
de História Natural e da Ciência (MUHNAC), in Lisbon, Portugal, were studied by
Mendes and Bivar-de-Sousa 2006, 2012a, b; Mendes et al. 2018, but the revised
checklist (Appendix) takes into account bibliographic records that have been
reviewed and confirmed by newly collected data. The bibliographic data considered
for assembling this checklist originated from the following references: Cramer
(1775–76—who reports the first species for São Tomé and for the GGOI: Acraea
medea), Snellen (1873), Sharpe (1893), Holland (1896), Aurivillius (1898, 1910),
Rothschild and Jordan (1900), Eltringham (1912), Le Cerf (1924), Joicey and Talbot
(1926, 1927), Hawker-Smith (1928), Riley (1928), Evans (1937), Bacelar (1948),
Someren (1971a, b, 1972, 1974, 1975), Pinhey (1972), D’Abrera (1980, 1997, 2004,
2009), Plantrou (1983), Hancock (1984), Henning (1988), Pyrcz (1991a, b, c,
1992a, b), Canu (1994), Wojtusiak and Pyrcz (1995, 1997), Pierre et al. (2002),
Hecq (2003a, b), Turlin (2005a, b, 2007a, b, c), Anonymous (2007), Bonfim and
Carvalho (2009), Koçak and Kemal (2009), Williams (2008, 2015), Velzen et al.
352
L. F. Mendes and A. Bivar-de-Sousa
(2009), Libert (2011), Oremans (2012), Pierre and Bernaud (2013, 2014), Collins
and Larsen (2013), Wikipedia (2014), Collins (2015) and Awanao et al. (2018).
Specimens deposited in the Museu Bocage (MB), a precursor institution of
present-day MUHNAC, were also partially studied by the authors. However, all of
MB specimens were destroyed in the fire that engulfed the collections, library, and
associated structures on March 28, 1978. Among the destroyed collections were
Sharpe (1893) São Tomé type specimens, as had been recorded by Fernandes
(1958), the holotype of Pyrrhiades bocagei (sub Rhopalocampta), three specimens
of Leptotes sanctithomae (as Catochrysops sancti-thomae), comprising holotype
and allotype, as well as the holotypes of Acraea niobe, Telchinia insularis (sub
Acraea) and Telchinia newtoni (sub Acraea).
Most of the information concerning newly identified and re-examined specimens
is based on the analysis of specimens from São Tomé and Príncipe collected by the
zoological expeditions held in 1954–1955 by the Centro de Zoologia (CZ) of the
Junta de Investigações do Ultramar and a mission to São Tomé Island in 1984 by
MB and the Faculty of Sciences of the Lisbon University (Mendes et al. 1988).
These studies were followed by Mendes and Bivar-de-Sousa (2006, 2012a, b) and
Mendes et al. (2018) contributions, all based on newly collected specimens between
2004 and 2019. Some of these specimens were collected during a 2015 California
Academy of Sciences funded expedition, to which the senior author was invited by
Dr. Robert (Bob) Drewes to participate. Some other material was studied, namely
that available in the collections of the Centro de Investigação Agronómica e
Tecnológica de São Tomé e Príncipe (CIAT) in Potó, São Tomé Island. This
collection was established by members of the CZ before the country gained independence in 1975. Data available from the private collections of the second
co-author of this study, as well as those of António Figueira (1924–2017; now
housed in the collections of the Museu de História Natural e da Ciência da
Universidade do Porto, Porto, Portugal) and Carlos da Silva were also used. Information from local collaborators, especially those of Rato Cabinda, are also included
in this revised checklist.
Incorrectly Recorded Taxa
Despite most of the known references being scientifically trustworthy, several
reported taxa are based on misidentified or mislabelled specimens of species and
subspecies that are mostly typical from savanna and Sahel-biotopes (see Appendix):
Hesperiidae Sarangesa phidyle, Spialia diomus, S. spio, Gomalia elma, Borbo
gemella and Pelopidas mathias were recorded for the islands but do not occur
there (Appendix). Evans (1937) and Chiba (2009) consider Coeliades hanno as
present in São Tomé, but the only brown Coeliades confirmed in São Tomé and
Príncipe is the morphologically similar C. forestan.
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Butterflies and Skippers (Lepidoptera: Papilionoidea) of the Gulf. . .
353
Papilionidae Papilio dardanus sulfurea is a Bioko endemic whose type locality
was wrongly considered to be Príncipe (Palisot de Beauvois 1805–1821). Its occurrence on Príncipe Island was also recorded by Canu (1994) and by Koçak and Kemal
(2009—sub princeps), but all the recent authors consider it a Bioko endemic.
Graphium angolanus baronis, G. latreillianus theorini and G. ridleyanus, which
are large and unmistakable taxa occurring in continental Africa have also been
recorded from São Tomé based on some specimens in the collections of the Natural
History Museum (NHM) of London (Smith and Vane-Wright 2001); however, the
location of these specimens is likely mislabelled, as no other records of these taxa
exist for the island.
Pieridae Larsen (2005) considers Colotis doubledayi, noted for instance by Ackery
et al. (1995) and D’Abrera (1997) as occurring in São Tomé, as a misidentification.
Berger (1981) is the only record of Belenois gidica for São Tomé. The single
reference of Appias phaola to the island of São Tomé (Bacelar 1948) refers to
three males and one female that were subsequently destroyed during the MB fire.
These likely represented records of A. epaphia aequatorialis, later described from
the island (Mendes and Bivar-de-Sousa 2006). Leptosia medusa, reported also by
Bacelar (1948, four males, one female) from São Tomé corresponds to a
misidentified L. alcesta (Mendes and Bivar-de-Sousa 2012a, b). All the São Tomé
records of species of the genus Mylothris, except those of M. rembina, are putative
misidentifications and were partially rectified: M. asphodelus by Bacelar (1948);
M. bernice by Sharpe (1893); M. nubila by Schultze (1917); M. poppea by Viejo
(1984); M. rhodope and M. spica by Berger (1979); and M. sulphurea by Pyrcz
(1992a, who stresses the muddled knowledge of the genus in São Tomé).
Lycaenidae Hypolycaena philippus, Anthene amarah, Azanus moriqua, Azanus
ubaldus, Leptotes brevidentatus, L. jeannelli, and Zizula hylax were recorded for
the islands but do not occur there (Appendix). Liptena evanescens f. xanthis reported
by Stempffer et al. (1974) from São Tomé either represents a mislabeled specimen or
a locally extirpated population. Libert (2004) reports the presence of Hypomyrina
fournieri either in São Tomé or in Príncipe (material not seen, occurrence not
mapped), but the species is not mentioned as occurring in the GGOI by Ackery
et al. (1995) nor by D’Abrera (2009). Sharpe (1893) reports Rubropelates aruma in
São Tomé, but this record may represent a non-established population or a
misidentified specimen of Deudorix lorisona. In addition, Sharpe (1893) registers
Leptotes pulchra in São Tomé but does not consider the quite common L. pirithous.
Nymphalidae Bicyclus dorothea concolor, B. funebris and B. martius sanaos were
recorded for the islands but do not occur there (Appendix). Furthermore, B. italus
was mapped in São Tomé by Condamin (1973), but all these records may have been
based on a misidentified B. medontias, a similar forest species whose presence on the
island was unknown until recently (Larsen 2005). Precis hierta, Precis orithya,
Salamis anacardii (currently a species of Protogoniomorpha), Byblia ilithyia and
Hamanumida daedalus are certainly not present in São Tomé and Príncipe. Neptis
serena is listed by Koçak and Kemal (2009) for São Tomé and Príncipe, but these
354
L. F. Mendes and A. Bivar-de-Sousa
authors do not report the endemic Neptis larseni from Príncipe; indeed, N. serena is
only assigned to Príncipe when that endemic was described (Wojtusiak and Pyrcz
1997). Pyrcz (1992a) reports an undetermined red Cymothoe that Canu (1994)
assigned to São Tomé, but was unable to find the specimens later; several species
of the C. sangaris group are known from Central and West Africa and thus this
information is insufficient to consider its presence in the GGOI. The same must be
stated about the references of several “acraea” species (currently Acraea and
Telchinia) reported by Bacelar (1958), Mendes and Bivar-de-Sousa (2012a, b),
Pierre and Bernaud (1999, 2009a, b), Pierre et al. (2002), Pyrcz (1992a), Snellen
(1873) and Viejo (1984), namely Acraea pseudegina, Telchinia e. encedon,
T. esebria, T. pentapolis, and T. vesperalis. Telchinia jodutta was reported from
São Tomé and Príncipe by several authors—first reference by Aurivillius (1910)—
though Oremans (2012) describes its insular vicariant, A. severina, with one subspecies in São Tomé and another in Príncipe. Bacelar (1958) refers A. eponina
latifasciata but she did not have access to new specimens, while Pyrcz (1992a)
questioned its presence in São Tomé and Príncipe and Pierre et al. (2002) did not
report the species as occurring in the GGOI despite its huge African range. Bacelar
(1948) reports Acraea monteironis from São Tomé based upon one male whose
identification we could not confirm—if the specimen was in MB it was certainly
destroyed in 1978; this species, described from Angola, was never recorded again
from the island. Viejo (1984), based in Bacelar (1948), was the only subsequent
author who considers Acraea monteironis to occur in São Tomé, without providing
further comments. According to Bacelar (1948), the reference of Aurivillius (1928,
Figs, 57d–e) of an A. esebria form shall represent T. severina instead, a taxon that
has been until recently considered a synonym of T. esebria (Eltringham 1912;
Ackery et al. 1995; Williams 2008; Pierre and Bernaud 2014). This is, however,
certainly not true in the GGOI—it may, indeed, belong to T. s. severina synonymy in
the case of its reference to São Tomé. Reports of Phalanta phalantha aethiopica in
the GGOI must represent the morphologically similar forest dweller P. eurytis,
known from Príncipe, São Tomé, and Rio Muni (Viejo 1984).
Composition, Diversity, and Endemism of the GGOI
Papilionoidea
Isolation, geological age, area, catching-area, relief, climate, and diversity of biotopes are fundamental to the potential biodiversity and endemism of an island
(Whittaker et al. 2017). Among the families of Papilionoidea known in
Sub-Saharan Africa, only Riodinidae has not been recorded in the GGOI. Most of
the subfamilies assigned from the region occur both in Príncipe and in São Tomé (the
scant diversity of Annobón was already discussed). The currently known number of
species (in parentheses) per family and respective subfamily is as follows:
Hesperiidae (nine): Coeliadinae (two), Pyrginae (one), and Hesperiinae (six);
13
Butterflies and Skippers (Lepidoptera: Papilionoidea) of the Gulf. . .
355
Papilionidae (four): Papilioninae (four); Pieridae (12): Coliadinae (five) and Pierinae
(seven); Lycaenidae (21): Miletinae (one), Aphnaeinae (five) and Polyomatinae
(15); and Nymphalidae (45): Libytheinae (one), Danainae (one), Satyrinae (two),
Charaxinae (eight), Nymphalinae (10), Cyrestinae (one), Biblidinae (two),
Limenetidinae (four) and Heliconiinae (16). There are no Papilionoidea genera
that are endemic from the GGOI. The Nymphalidae is the most diverse family
(ca. 45% of the Papilionoidea) and the Heliconiinae (ca. 35%) its most diverse
subfamily.
According to Gascoigne (1995), the Lepidoptera endemicity for São Tomé is
38.3% (47 taxa: 11 endemic species, 7 endemic subspecies) and 21.4% for Príncipe
(42 taxa: six endemic species, three endemic subspecies). These estimates, based on
Pyrcz (1991a, b), did not include the Hesperiidae, lumped the São Tomé and
Príncipe species of the genus Neptis to a single species (N. eltringhami), and
considered Leptotes terrenus and Chilades sanctithomae as independent taxa.
Currently, based on the specimens we have examined and bibliographic references, 91 species and subspecies are considered to occur in the GGOI: 46 are known
for Príncipe, 64 (though three in need of revision) for São Tomé, and eight for
Annobón (Appendix). All the taxa known for Annobón also occur in São Tomé and
Príncipe, with the exception of Telchinia pharsalus, identified as T. p. carmen, but
putatively referring to a still undescribed Annobón subspecies (Kheil 1910; Viejo
1984). The subspecies Acraea zetes annobona is the single taxon that is endemic to
the three islands. The species that occur both in São Tomé and Príncipe are mostly
those with the largest distributions. Regarding endemics (Fig. 13.1), 17 taxa are
endemic for Príncipe (almost 37%), 23 for São Tomé (ca. 36%), and five are endemic
to more than one island. These estimates approach those of Pyrcz (1991a, b),
especially after considering that he did not consider skippers.
Conservation
Modifications of the natural environment associated with human expansion and
climatic change have impacted the diversity of butterflies and skippers around the
globe. Activities with detrimental impacts range from deforestation, fires, charcoal
production, introduction of invasive weeds or of animal pests, use of chemicals,
water, air and soil pollution, expanse of cultivated fields and of monocultures
(agriculture or forestry) and human expansion in its strict sense. The considerable
taxonomic knowledge and data available for lepidopteran distributions and ecological requirements make them important indicators for environmental change and for
monitoring the health of ecosystems (Parmesan 2019).
In the GGOI, population sizes of species with high sensitivity to ecological
changes may be important to monitor, especially under current climate change.
Some of the GGOI species are very common while others seem to be restricted to
356
L. F. Mendes and A. Bivar-de-Sousa
Fig. 13.1 Some endemic Papilionoidea of the Gulf of Guinea oceanic islands. R: recto (dorsal), V:
verso (ventral): (1) Pyrrhiades bocagei, ♂R; (2) Ibid, V. (3.) Papilio nerminae, ♂R; (4) Graphium
leonidas santamarthae, ♂R; (5) Dixeia piscicollis, ♂R; (6) Deudorix (Virachola) odana chalybeate, ♂R; (7) Charaxes antiques, ♂R; (8) Ibid, V; (9) Pseudacraea gamae, ♀R; (10) Acraea zetes
annobona, ♂R; (11) Ibid, V; (12) Acraea medea, ♂R; (13) Ibid, V. Photo credits: (1–3, 5, 10–13)
António Bivar-de-Sousa and Luís Mendes, (4, 6–9) Carlos da Silva. Photos not to scale
13
Butterflies and Skippers (Lepidoptera: Papilionoidea) of the Gulf. . .
357
small areas or associated to specific biotopes (Mendes et al. in prep.). As noted
elsewhere, most of these more rare and poorly distributed taxa are endemics and
strictly associated with natural biotopes, although some exceptions are remarkable:
we frequently found images of the São Tomé endemic Acraea niobe pollinating
cultivated introduced coffee plants Coffea sp. (Rubiaceae) or, as firstly noted Pierre
et al. (2002), feeding on the nectar of the introduced Mexican sunflower, Tithonia
diversifolia (Asteraceae). These observations suggest that some endemic species
may be resilient to some ecological changes.
The observation that some species are known from only a small number of
individuals may be the consequence of two fundamental and unrelated mechanisms.
First, some species are considered rare when they occur in quite localized areas, they
fly during a short period, or they are restricted to particular biotopes, and thus
challenging to locate. However, these species with patchy distributions may be
geographically widespread and common in other parts of their range. Second, insect
abundance is known to fluctuate from year to year according to annual ecological
conditions and in the GGOI some areas are quite complicated to access. Thus,
temporal and geographic biases in survey effort may partly explain why some taxa
appear to be rare. However, some species may be considered threatened because
they are truly rare and at real risk of extirpation or extinction due to environmental
pressures. We note that these concepts apply to both endemic and non-endemic
species.
One good example of a rare endemic species is Dixeia piscicollis, which is
restricted to the São Tomé dry forest and known from a small number of specimens.
However, at the end of the dry season, locally known as gravana, it may be quite
abundant, even becoming the dominant or the only butterfly in the area—although it
is restricted to this area. Some endemic Charaxes restricted to the São Tomé or
Príncipe highland forests also fit this description. Likewise, the insular subspecies of
Graphium leonidas are both rare and limited to precise biotopes and seem to fly
during a short period only.
A certain number of threatened species in São Tomé and Príncipe were reported
by Gascoigne (1995). However, this list included taxa that even if rare, may not be
threatened, as is the case of Pyrrhiades bocagei (sub Coeliades) which is noted as
vulnerable, and despite being present on both islands, is reported only for São Tomé.
Both Graphium leonidas subspecies are listed as endangered; Leptotes terrenus and
Chilades sanctithomae, Pseudacraea gamae are “undetermined,” while Epamera
bellina maris and Charaxes defulvata are said to be extinct, despite Pyrcz (1992a)
recording live specimens of both. The threatened community of Lagoa Azul in São
Tomé is discussed, with special attention on Coeliades bocagei, the “endemic
Charaxes” (species not discriminated), and Neptis eltringhami that occur there.
Dixeia piscicollis was also considered to be threatened though it is common along
the northwestern dry forest.
The statuses of species considered endemic or almost endemic are in dire need of
new data to update assessments, as several of them may be threatened or even
extinct. This is the case for Andronymus thomasi, treated as a subspecies from
358
L. F. Mendes and A. Bivar-de-Sousa
Andronymus neander by Gascoigne (1995) and possibly others. Iolaus bellina maris
and Charaxes defulvata if not extinct, likely occur only in very small numbers.
Potential Future Discoveries and Research
Given the current knowledge of the GGOI Papilionoidea, the intermittent increase
in the number of recognized species over time, and the considerable bias of
knowledge toward São Tomé and Príncipe when compared with Annobón, several
areas of future research are needed. Fieldwork in Annobón is essential, as the
known taxonomic diversity is likely incomplete. São Tomé and Príncipe have been
more extensively surveyed, but large areas of their most pristine forest, where
endemics are expected to have evolved, have been little explored due to the
difficult access, high rainfall, and dense vegetation. As such, new species for the
islands (and even for science) are expected to be found, and populations of some of
the species considered as (almost) extinct may be rediscovered. Information on the
range and abundance of each species is essential to establish their conservation
status. This is especially urgent for the rare island endemics. Although some
information already exists about the activity periods of caterpillars and imagoes,
more data are needed to allow the implementation of effective protection measures.
For instance, the morphology of the caterpillar life stage is unknown for most of
the tropical species, particularly the endemics. Likewise, knowledge of caterpillar
host-plants is also incomplete. In the non-endemic taxa, the caterpillar food-plants
may be different from those of populations in mainland Africa, while for some of
the insular endemics they simply remain unknown. Genetic studies on GGOI
Papilionoidea are virtually inexistent. They are fundamental to taxonomical and
phylogeographic studies and are key to investigating the biogeographic history of
this unique island fauna.
13
Butterflies and Skippers (Lepidoptera: Papilionoidea) of the Gulf. . .
359
Appendix
Commented checklist of Papilionoidea recorded from the Gulf of Guinea oceanic
islands. Names of the 91 species and subspecies considered correctly assigned to
Príncipe (P), São Tomé (ST) and Annobón (A) are numbered. Taxa considered
incorrectly assigned to the GGOI, as justified in the text, are not numbered. K&K
(2009): Koçak and Kemal; M&BS: Mendes and Bivar-de-Sousa. Endemic taxa (E),
if shared by P and ST and/or A, respectively as E-1, E-2 and E-3 according to their
topotypical island. Samples examined by the authors are marked in the SS column
(studied specimens) with a ●; 17 species are known only from reliable bibliographic
references. Preferred habitats (H): A—Humid lowland forest; B—Humid highland
forest; C—Dry forest, forest margins, and somewhat degraded biotopes; D—Several
types of forest; U—Ubiquitous or almost ubiquitous; ?—Doubtful
Families and species/subspecies
Fam. HESPERIIDAE
1. Pyrrhiades bocagei (Sharpe, 1893)
First reference
SS
P
ST
Sharpe (1893)
●
E
D
2. Coeliades forestan (Stoll, 1784)
Sharpe (1893)
●
X
E2
X
Coeliades hanno (Plötz, 1879)
3. Tagiades flesus (Fabricius, 1871)
Riley (1928)
Sharpe (1893)
●
X
X
A,
C
Sarangesa phydile (Walker, 1870)
Spialia diomus (Hopffer, 1855)
Spialia spio (Linnaeus, 1764)
Gomalia elma (Trimen, 1862)
4. Andronymus thomasi Riley, 1928
K&K (2009)
K& K (2009)
K&K (2009)
K&K (2009)
Riley (1928)
●
E
A
5. Artitropa principetome Collins and Larsen
2013
Pelopidas mathias (Fabricius, 1798)
6. Borbo borbonica (Boisduval, 1833)
(Collins and
Larsen 2013)
K&K (2009)
Aurivillius
(1910)
Riley (1928)
Aurivillius
(1910)
K&K (2009)
Sharpe (1893)
E2
E
C
7. Borbo detecta (Trimen, 1893)
8. Borbo f. fatuellus (Hopffer, 1855)
Borbo gemella (Mabille, 1884)
9. Afrogegenes letterstedti (Wallengren, 1857)
Fam. PAPILIONIDAE
10. Papilio nerminae Koçak, 1983
Papilio dardanus sulfurea Palisot de Beauvois
1806
Sharpe (1893)
E1
A
H
C,
D
A
●
X
X
●
●
X
X
X
X
●
X
X
C
E
A,
B
●
X
C
C
Palisot de
Beauvois
(1806)
(continued)
360
Families and species/subspecies
11. Papilio d. demodocus Esper, 1798
Graphium angolanus baronis (Ungemach, 1932)
Graphium latreillianus theorini (Aurivillius,
1831)
12. Graphium leonidas santamarthae Joicey and
Talbot, 1927
13. Graphium leonidas thomasius Le Cerf 1924
Graphium ridleyanus (White, 1843)
Fam. PIERIDAE
14. Catopsilia florella (Faricius, 1775)
15. Eurema b. brigitta (Stoll, 1780)
16. Eurema hecabe solifera (Butler, 1875)
17. Eurema floricola leonis (Butler, 1886)
18. Eurema senegalensis (Boisuval, 1836)
Colotis doubledayi (Hopffer, 1872)
Belenois gidica Godart, 1819
19. Belenois c. creona (Stoll, 1780)
20. Dixeia piscicollis Pinhey, 1972
21. Appias epaphia aequatorialis Mendes &
Bivar-de-Sousa, 2006
22. Appias epaphia piresi Mendes & Bivar-deSousa, 2006
Appias phaola (Doubleday, 1847)
23. Leptosia a. alcesta (Stoll, 1781)
Leptosia medusa (Cramer, 1777)
24. Leptosia n. nupta (Butler, 1873)
Mylothris asphodelus Butler, 1888
Mylothris bernice (Hewitson, 1862)
Mylothris nubila (Möschler, 1884)
Mylothris popea (Cramer, 1777)
25. Mylothris rembina (Plötz, 1880)
Mylothris rhodope (Fabricius, 1775)
Mylothris spica (Möschler, 1884)
Mylothris sulphurea (Aurivillius, 1895)
L. F. Mendes and A. Bivar-de-Sousa
First reference
Snellen (1873)
Smith and
Vane-Wright
(2001)
Smith and
Vane-Wright
(2001)
Joicey and Talbot, (1927)
Le Cerf (1924)
SS
●
P
X
●
E
ST
X
E
●
A
H
U
A,
C
A,
C
Smith and
Vane-Wright
(2001)
Bacelar (1958)
K&K (2009)
Snellen (1882)
Snellen (1882)
Sharpe (1893)
Ackery et al.
(1995)
Berger (1981)
M&BS (2012)
Pinhey (1972)
M&BS (2006)
●
●
●
M&BS (2006)
●
E
C
Bacelar (1948)
Snellen (1873)
Bacelar (1948)
Sharpe (1873)
●
X
A
●
X
X
A,
B
●
X
X
A
Bacelar (1948)
Sharpe (1893)
Schutze (1917)
Viejo (1984)
Schutze (1917)
Berger (1979)
K&K (2009)
K&K (2009)
●
●
●
●
●
X
X
X
X
X
X
U
C
C
D
A
X
E
E
C
C
C
X
X
(continued)
13
Butterflies and Skippers (Lepidoptera: Papilionoidea) of the Gulf. . .
Families and species/subspecies
Fam. LYCAENIDAE
26. Spalgis l. lemolea Druce, 1890
Liptena evanescens xanthis (Holland, 1890)
27. Iolaus (Epamera) bellina maris (Riley, 1928)
Hypomyrina fournieri Gabriel, 1939
Hypolycaena phillippus (Fabricius, 1793)
28. Deudorix (Virachola) l. lorisona (Hewitson,
1862)
29. Deudorix (Virachola) a. antalus (Hopffer,
1855)
30. Deudorix (Virachola) caliginosa Lathy,1903
31. Deudorix (Virachola) odana chalybeata
(Joicey and Talbot, 1926)
Rubropelates a. aruma (Hewitson, 1873)
Anthene amarah (Guérin-Méneville,1849)
32. Anthene l. lunulata (Trimen, 1894)
361
First reference
SS
P
Pyrcz (1992)
●
X
Stempffer
(1974)
Riley (1928)
Libert (2004)
K&K (2009)
Hawker-Smith
(1928)
Pyrcz (1992)
Libert (2004)
Joicey and Talbot (1926)
Sharpe (1893)
K&K (2009)
Viejo (1984)
ST
E
A?
●
X
X?
A
●
X
X
C
●
E
X
E2
C?
A
●
X
X?
X
A,
B
A,
B
C
Pyrcz (1992)
●
X
34. Pseudonacaduba s. sichela (Wallengren,
1857)
35. Lampides boeticus (Linnaeus, 1767)
36. Cacyreus lingeus (Stoll, 1782)
Mendes et al.
(ad.Prep.)
Bacelar (1958)
Joicey and Talbot (1926)
Kheil (1910)
●
X
●
●
X
X
X
X
●
X
X
●
E
Leptotes brevidentatus (Tite, 1958)
Leptotes jeanneli (Stempffer, 1935)
Leptotes pulchra (Murray, 1874)
38. Leptotes pyrczi Libert, 2011
39. Leptotes sanctithomae Sharpe, 1893 (= L.
terrenus (Joicey and Talbot, 1926))
40. Zizeeria knysna (Trimen, 1862)
K&K (2009)
K&K (2009)
Sharpe (1893)
Libert (2011)
Sharpe (1893)
41. Zizina otis antanossa (Mabille, 1877)
Joicey and Talbot (1926)
Pyrcz (1992)
Zizula hylax (Fabricius, 1775)
42. Azanus mirzá (Plötz, 1880)
K&K (2009)
Pyrcz (1992)
Azanus moriqua (Wallengren, 1857)
Azanus ubaldus (Stoll, 1782)
43. Eicochrysops hippocrates (Fabricius, 1793)
44. Euchrysops malathana (Boisduval, 1833)
K&K (2009)
K&K (2009)
Pyrcz (1992)
Aurivillius
(1928)
H
A,
C
33. Anthene prínceps (Butler, 1876)
37. Leptotes p. pirithous (Linnaeus, 1767)
A
E
●
X
X
●
X
X
●
●
●
X
X
X
D
A,
C
C,
D
A
B?
A,
C
A,
C
X
C,
D
X
X
D
C,
D
(continued)
362
Families and species/subspecies
45. Euchrysops cf. osiris (Hopffer, 1855)
L. F. Mendes and A. Bivar-de-Sousa
First reference
Aurivillius
(1928)
K& K (2009)
SS
●
Sharpe (1893)
●
X
X
48. Danaus c. chrysippus (Linnaeus, 1758)
49. Melanitis leda (Linnaeus, 1758)
Snellen (1873)
Sharpe (1893)
●
●
X
X
X
X
Bicyclus dorothea concolor Condamin and Fox,
1964
Bicyclus funebris (Guérin-Méneville, 1844)
Condamin and
Fox (1964)
Condamin
(1973)
Condamin
(1973)
Larsen (2005)
Condamin
(1973)
Aurivillius
(1910)
Joicey and Talbot (1926)
Plantrou (1983)
46. Chilades trochylus (Freyer, 1844)
Fam. NYMPHALIDAE
47. Libythea l. labdaca Westwood, 1851
Bicyclus italus (Hewitson, 1865)
50. Bicyclus medontias (Hewitson, 1873)
Bicyclus martius sanaos (Hewitson, 1866)
51. Bicyclus vulgaris (Butler, 1868)
52. Charaxes defulvata (Joicey and Talbot, 1926)
53. Charaxes c. candiope (Godart, 1824)
54. Charaxes thomasius Staudinger, 1886
62. Precis s. sinuta Plötz, 1880
Staudinger
(1886)
Aurivillius
(1910) as C.
lucretius
Staudinger
(1892)
Joicey and Talbot (1926)
Joicey and Talbot (1927)
Staudinger
(1886)
Pyrcz (1992)
K&K (2009)
K&K (2009)
Aurivillius
(1910)
Sharpe (1893)
63. Hypolimnas a. anthedon (Doubleday, 1845)
Sharpe (1893)
55. Charaxes lemosi (Joicey and Talbot, 1927)
56. Charaxes odysseus Staudinger 1892
57. Charaxes antiquus Joicey and Talbot 1926
58. Charaxes barnsi Joicey and Talbot, 1927
59. Charaxes monteiri Staudinger 1886
60. Vanessa cardui (Linnaeus, 1758)
Precis hierta crebrene (Trimen, 1870)
Precis orythia madagascariensis (Guenée, 1865)
61. Precis pelarga (Fabricius, 1775)
P
X
ST
X?
X
●
X
●
X
X
X
X
H
C,
D
D
A,
C
U
C,
D
B?
C
E
A?
X
A,
C
B
E
●
●
A
X
E
B
E
E
E
A?,
B
B
A
E
B
●
X
X
C
●
X
X
B,
C
C,
D
C,
D
X
●
●
X
X
(continued)
13
Butterflies and Skippers (Lepidoptera: Papilionoidea) of the Gulf. . .
Families and species/subspecies
64. Hypolimnas misippus (Linnaeus, 1764)
65. Hypolimnas m. monteironis (Druce, 1874)
66. Hypolimnas salmacis thomensis Aurivillius,
1910
Protogoniomorpha anacardi (Linnaeus, 1758)
67. Junonia cymodoce lugens (Schultze, 1912)
68. Junonia o. oenone (Linnaeus, 1758)
69. Junonia t. terea (Drury, 1773)
70. Cyrestis c. camillus (Fabricius, 1781)
Byblia ilithyia (Drury, 1773)
71. Sevenia amulia principensis Mendes &
Bivar-de-Sousa, 2018 n.stat.
72. Sevenia boisduvali insularis (Joicey & Talbot
1926)
73. Pseudacraea gamae
Neptis serena Overlaet, 1955
74. Neptis eltringhami Joicey and Talbot 1926
75. Neptis larseni Wojtuziak and Pyrcz, 1997
76. Cymothoe caenis (Drury, 1773)
Cymothoe sp. (“sangaris-group”)
Hamanumida daedalus (Fabricius, 1775)
77. Acraea n. neobule Doubleday, 1847
78. Acraea q. quirina (Fabricius, 1781)
First reference
Snellen (1873)
Pyrcz (1992) as
H. salmacis
Aurivillius
(1910)
K&K (2009)
Bacelar (1958)
Bacelar (1958)
Aurivillius
(1910)
Bacelar (1958)
K&K (2009)
Bacelar
(1958)—no ssp
Sharpe (1893)
Joicey and
Talbo (1926)
K&K (2009)
Joicey and Talbot (1926)
Pyrcz (1991) as
N. eltringhami
van Velzen et
al. (2009)
Pyrcz (1992)—
after Canu
K&K (2009)
K&K (2009)
80. Acraea e. egina (Cramer, 1775)
Aurivillius
(1910)
Snellen
(1873)—no ssp
M&BS (2012)
81. Acraea medea (Craner, 1775)
SS
●
●
363
P
X
X
ST
X
E
●
●
●
X
X
●
X
●
X
●
E
E
A
E
●
A?
E
A,
C
A?
X
X
●
X
X
●
E
E
●
X
Cramer (1775)
●
E
82. Acraea niobe Sharpe, 1893
Sharpe (1893)
●
Acraea pseudegina Westwood, 1852
83. Acraea alcinoe racaji Pyrcz, 1991
Pyrcz (1992)
Snellen (1873)
as A. esebria
Pierre (1985)
Snellen (1873)
84. Telchinia alciope (Hewitson, 1852)
Telchinia esebria (Hewitson, 1861)
A,
B
B
E
●
E
E
X
H
C
A,
B
A,
B
A
C,
D
A,
B
A
X
●
79. Acraea zetes annobona D’Abrera, 1980
A
X
X
C,
D
A
E3
A,
C
A,
B
A,
B
A,
B
A,
B
A
(continued)
364
Families and species/subspecies
Telchinia encedon (Linnaeus, 1758)
85. Telchinia insularis (Sharpe 1893)
Telchinia j. jodutta (Fabricius, 1793)
86. Telchinia lycoa (Godart, 1819)
Telchinia p. pentapolis (Ward, 1871)
87. Telchinia pharsalus carmen (Pyrcz, 1991)
Telchinia serena (Fabricius, 1775)
88. Telchinia severina severina (Ouremans,
2012)
89. Telchinia severina terreirovelhoensis
(Ouremans, 2012)
Telchinia vesperalis (Grose-Smith, 1890)
90. Telchinia newtoni (Sharpe 1893)
Acraea monteironis Butler, 1874
91. Phalanta e. eurytis (Doubleday, 1847)
Phalanta phalantha (Drury, 1773)
L. F. Mendes and A. Bivar-de-Sousa
First reference
K&K (2009)
Sharpe (1893)
Aurivillius
(1910)
Aurivillius
(1910)
Pierre and
Bernaud (1999)
Aurivillius
(1910)—no ssp
Snellen (1873)
as A. manjaca
Berger (1986)
as A. jodutta
Aurivillius
(1910) as A.
jodutta
Pyrcz (1992)
Sharpe (1893)
Bacelar (1958)
Pyrcz (1992)
K&K (2009)
SS
P
A
E
●
●
X
●
E
H
A
A,
C
X?
E
●
●
ST
E
A,
B
A,
B
A,
B
E
●
X
X
A
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Chapter 14
Dragonflies and Damselflies (Odonata)
of Príncipe, São Tomé, and Annobón
Klaas-Douwe B. Dijkstra, Russell B. Tate, and Michel Papazian
Abstract The dragonfly and damselfly (Odonata) fauna of the oceanic islands of the
Gulf of Guinea is impoverished, even compared to other Afrotropical archipelagoes,
with a combined total of 22 species recorded with certainty on São Tomé, Príncipe,
and Annobón. Trithemis nigra Longfield, 1936 from Príncipe is the only known
endemic, although two reported but unidentified species may still prove to be
endemic too. Most recorded species occur widely across and beyond Africa, and
27 equally widespread species are listed as potential additions. Several hypotheses
for the fauna’s impoverishment are briefly discussed.
Keywords Biogeography · Diversity · Gulf of Guinea · Oceanic islands · Odonata
Research History
The Odonata of the Gulf of Guinea have been poorly studied, even if the first records
were provided a century ago (Martin 1908; Campion 1923). The first endemic taxon
was described almost as long ago but remains the only one (Longfield 1936). Pinhey
(1974) was the only specialist ever to visit, being on São Tomé for 2 weeks in April
and May 1971. His review remains the main resource on all the islands’ faunas, only
overlooking the material from Annobón treated by Compte Sart (1962). Just four
species were added to the list for the three islands combined since Pinhey’s visit half
a century ago, all very recently.
K.-D. B. Dijkstra (*)
Naturalis Biodiversity Center, Leiden, The Netherlands
e-mail: kd.dijkstra@naturalis.nl
R. B. Tate
HCV Africa, Johannesburg, South Africa
M. Papazian
OPIE-Provence-Alpes-du-Sud, Muséum d’Histoire naturelle de Marseille, Marseille, France
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_14
371
372
K.-D. B. Dijkstra et al.
Species Diversity
Twenty-two species are known from the islands, of which 19 were recorded from
São Tomé, 9 from Príncipe, and 7 from Annobón (Table 14.1). The specific identity
of two species, however, is uncertain. These and two other species of interest are
discussed below.
Gynacantha sp. — Pinhey (1974) saw a species of this genus or the similar
Heliaeschna on São Tomé on four occasions, but these eluded capture. Two
observers made sightings there since (see Table 14.1), suggesting the taxon is not
rare. Both genera breed in shaded temporary pools. Adults are active at dusk, lurking
in dense vegetation at daytime, making them challenging to find and catch. Pinhey
(1974) remarked that “forest species of these genera on an isolated island might be
expected to be distinctive.” While the Comoros, Seychelles and Mascarene archipelagos indeed have endemic Gynacantha species, these belong to the bispina-group
that is absent on the western side of Africa (Dijkstra 2005). Twelve species occur on
the continent nearest to São Tomé, any of which might be present on the Gulf of
Guinea islands (Dijkstra 2016). Indeed, a female caught there by Gérard Filippi in
March 2022 probably pertains to G. cylindrata Karsch, 1891. That species is
widespread in western and central Africa. Females are hard to separate from those
of G. vesiculata Karsch, 1891 (ranges are similar), so confirmation is desirable.
Orthetrum brachiale (Palisot de Beauvois, 1817) — This species and
O. stemmale (Burmeister, 1839) were confused for 140 years (Pinhey 1979). Both
occur widely on the tropical African mainland, while O. stemmale also extends to the
nearby islands of Madagascar, the Mascarenes, and Seychelles in a variety of
potential but unresolved taxa (see Table 14.2). While the latter’s presence in the
Gulf of Guinea may thus seem likelier, both the material of Pinhey (1974, 1979) and
Papazian et al. (2020) included O. brachiale only. Specimens in the Natural History
Museum (London) and photographic records seen by the first author also agree with
that species. Loureiro and Pontes (2013) reported O. stemmale from Príncipe without
further comment, and Papazian et al. (2022) from São Tomé based on female
specimens not assignable to other Orthetrum species found. Thus, while its presence
seems very likely, confirmation with male specimens is required given the long
history of taxonomic confusion.
Trithemis nigra Longfield, 1936 (Fig. 14.1) — Longfield (1936) described this as
a subspecies of the Denim Dropwing T. donaldsoni (Calvert, 1899) based on two
males, collected on Príncipe on 7 December 1932 and 1 January 1933. Pinhey
(1970) raised the taxon to species level, which by morphology is nearest the
Halfshade Dropwing T. aconita Lieftinck, 1969 and Congo Dropwing
T. congolica Pinhey, 1970 (Damm et al. 2010). Alain Gauthier (pers. comm.)
found T. nigra to be common in 1990. Indeed, it was found at 6 of 15 sites surveyed
on the island’s eastern half in 2011 (Loureiro and Pontes 2013): all streams that were
partly sunny and partly shaded by forest or shrubs. The species was not seen at fully
shaded or seasonal streams, nor at standing or brackish water. While the limited
distribution is below thresholds for Critically Endangered on the IUCN Red List of
English
name
Sahel Wisp
Ceriagrion glabrum
(Burmeister, 1839)
Common
Citril
Ischnura
senegalensis
(Rambur, 1842)
Tropical
Bluetail
Anax ephippiger
(Burmeister, 1839)
Anax imperator
Leach in Brewster,
1815
Gynacantha sp.
Vagrant
Emperor
Blue
Emperor
Chalcostephia
flavifrons Kirby,
1889
Duskhawker
species
Inspector
Príncipe
Series collected 28–29 October 2019
near Santo António (Papazian et al.
2020).
First reported by Martin (1908); confirmed by Loureiro and Pontes (2013),
Papazian et al. (2020) and photographic records.
Surprisingly no records yet.
Surprisingly no records yet.
Surprisingly no records yet.
São Tomé
Both sexes photographed on 3 January
2022 near Neves by Ernst Klimsa. A
female photographed on 23 August
2005 in São Tomé town by Phil
Benstead was probably this species
too.
First reported by Campion (1923);
confirmed by Pinhey (1974).
Annobón
Found at several sites in October 2021
(Papazian et al. 2022) and
photographed on 1 January 2022 near
Neves by Ernst Klimsa.
Not recorded since Pinhey (1974).
First reported by Martin (1908);
confirmed by Compte Sart (1962).
First recorded by Pinhey (1974); confirmed by Papazian and Filippi (2019).
First reported by Martin (1908);
confirmed by Compte Sart (1962).
Seen by Pinhey (1974) in 1971, by
Alain Gauthier in 1991, and by Russell Tate in 2020. See main text on
female caught in March 2022.
Both sexes photographed on 13–
15 January 2022 at Praja Inhame by
Ernst Klimsa.
Dragonflies and Damselflies (Odonata) of Príncipe, São Tomé, and Annobón
Scientific name
Agriocnemis
zerafica Le Roi,
1915
14
Table 14.1 Review of Odonata species recorded from the Gulf of Guinea Islands
(continued)
373
Scientific name
Crocothemis
erythraea (Brullé,
1832)
Crocothemis
sanguinolenta
(Burmeister, 1839)
Diplacodes lefebvrii
(Rambur, 1842)
Orthetrum
africanum (Selys,
1887)
Orthetrum
brachiale (Palisot
de Beauvois, 1817)
English
name
Broad
Scarlet
374
Table 14.1 (continued)
Príncipe
Surprisingly no records yet.
São Tomé
First reported by Longfield (1936);
confirmed by Pinhey (1974) and photographic records.
Not recorded since Pinhey (1974).
Surprisingly no records yet.
First reported by Campion (1923);
confirmed by Pinhey (1974).
First recorded by Pinhey (1974); confirmed by photographic records.
Little Scarlet
Black
Percher
Elongate
Skimmer
Banded
Skimmer
First reported by Longfield (1936);
confirmed by Loureiro and Pontes
(2013) and photographic records.
Pinhey (1974) reported O. brachiale
kalai; confirmed as O. brachiale by
Pinhey (1979), Loureiro and Pontes
(2013), and Papazian et al. (2020).
First reported as O. stemmale capense
by Longfield (1936); confirmed by
Pinhey (1974) and Papazian
et al. (2020).
Julia
Skimmer
Palpopleura lucia
(Drury, 1773)
Lucia
Widow
First reported by Longfield (1936);
confirmed by Pinhey (1974), Loureiro
and Pontes (2013), Papazian et al.
(2020), and photographic records.
Pantala flavescens
(Fabricius, 1798)
Wandering
Glider
First reported by Martin (1908); confirmed by Loureiro and Pontes (2013)
and Papazian et al. (2020).
First reported and illustrated quite
accurately by Compte Sart (1962);
additional record provided by
Pinhey (1974).
Only reported by Martin (1908).
K.-D. B. Dijkstra et al.
Orthetrum julia
Kirby, 1900
First reported by Longfield (1936);
confirmed by Pinhey (1974, 1979),
Papazian et al. (2020), and photographic records.
First reported by Campion (1923) and,
as O. stemmale capense, by Longfield
(1936); confirmed by Pinhey (1974),
Papazian et al. (2020), and photographic records.
First reported by Martin (1908),
Campion (1923) and Longfield
(1936); confirmed by Pinhey (1974),
Papazian et al. (2020), and photographic records.
First reported by Campion (1923);
confirmed by Pinhey (1974) and
Papazian et al. (2020).
Annobón
14
Veiled
Flutterer
Tholymis tillarga
(Fabricius, 1798)
Tramea basilaris
(Palisot de
Beauvois, 1817)
Tramea limbata
(Desjardins, 1835)
Trithemis nigra
Longfield, 1936
Twister
Surprisingly no records yet.
Male photographed on 24 January
2019 near Praia Jalé close to the
island’s southern tip by Anja
Cervencl. Also photographed on
29 December 2021 at Praia Vanha
(Papazian et al. 2022).
Not recorded since Pinhey (1974).
Keyhole
Glider
Surprisingly no records yet.
Not recorded since Pinhey (1974).
Only reported by Martin (1908).
Ferruginous
Glider
Príncipe
Dropwing
Found at two sites in October 2021
(Papazian et al. 2022).
Described by Longfield (1936). Status
studied by Loureiro and
Pontes (2013).
Surprisingly no records yet.
Only reported by Compte
Sart (1962).
Zygonyx sp. near
flavicosta (Sjöstedt,
1900)
Near Ensign
Cascader
Zygonyx torridus
(Kirby, 1889)
Ringed
Cascader
Female reported as
Pseudomacromia sp. by Longfield
(1936) was identified by Pinhey
(1975) as this species.
Female collected on 6 February
2019 at Monte Café (Papazian and
Filippi 2019).
Photographic records were taken from iNaturalist.org and Observation.org, and received directly from Ernst Klimsa
Dragonflies and Damselflies (Odonata) of Príncipe, São Tomé, and Annobón
Rhyothemis notata
(Fabricius, 1787)
375
Table 14.2 Occurrence of Odonata species, that are widespread in western and central Africa, in Atlantic and Indian Ocean islands but that so far have not been
recorded from the Gulf of Guinea islands (Martens et al. 2013; Van Damme et al. 2020; Dijkstra and Cohen 2021)
CV
Com
Mad
*
Mas
•
•
•
*
•
•
•
•
S&A
*
Soc
•
•
•
•
•
•
•
•
•
•
•
•
•
•
•
•
•
*
•
•
•
•
•
•
•
•
*
•
•
•
•
•
•
*
•
•
•
•
•
•
*
•
•
*
•
•
•
Taxa that differ somewhat morphologically on these islands are marked with an asterisk. CV Cape Verde, Com Comoros, Mad Madagascar, Mas Mascarenes,
S&A Seychelles and Aldabra, Soc Socotra
K.-D. B. Dijkstra et al.
English name
Ochre Spreadwing
Pallid Spreadwing
Little Wisp
Blue-green Sprite
Cherry-eye Sprite
Western Orange Emperor
Black Emperor
Common Hooktail
Pygmy Basker
Southern Banded Groundling
Rock Scarlet
Barbet Percher
Bottletail
Epaulet Skimmer
Spectacled Skimmer
Bold Skimmer
Long Skimmer
Banded Duskdarter
Phantom Flutterer
Red-veined Darter
Black-splashed Elf
Violet Dropwing
Red-veined Dropwing
Silhouette Dropwing
Orange-winged Dropwing
Red Basker
Blue Basker
376
Scientific name
Lestes ochraceus Selys, 1862
Lestes pallidus Rambur, 1842
Agriocnemis exilis Selys, 1872
Pseudagrion glaucescens Selys, 1876
Pseudagrion sublacteum (Karsch, 1893)
Anax rutherfordi McLachlan, 1883
Anax tristis Hagen, 1867
Paragomphus genei (Selys, 1841)
Aethriamanta rezia Kirby, 1889
Brachythemis leucosticta (Burmeister, 1839)
Crocothemis divisa Karsch, 1898
Diplacodes luminans (Karsch, 1893)
Olpogastra lugubris (Karsch, 1895)
Orthetrum chrysostigma (Burmeister, 1839)
Orthetrum icteromelas Ris, 1910
Orthetrum stemmale (Burmeister, 1839)
Orthetrum trinacria (Selys, 1841)
Parazyxomma flavicans (Martin, 1908)
Rhyothemis semihyalina (Desjardins, 1835)
Sympetrum fonscolombii (Selys, 1840)
Tetrathemis polleni (Selys, 1869)
Trithemis annulata (Palisot de Beauvois, 1807)
Trithemis arteriosa (Burmeister, 1839)
Trithemis hecate Ris, 1912
Trithemis kirbyi Selys, 1891
Urothemis assignata (Selys, 1872)
Urothemis edwardsii (Selys in Lucas, 1849)
14
Dragonflies and Damselflies (Odonata) of Príncipe, São Tomé, and Annobón
377
Fig. 14.1 Trithemis nigra or Príncipe Dropwing, the only endemic odonate known from the
islands. Photo credits: Nuno de Santos Loureiro
Threatened Species, the survey identified no threats and therefore T. nigra is now
listed as Near Threatened (IUCN 2021).
Zygonyx sp. — Species of this genus favour water with a strong current. Pinhey
(1974) did not see “any Zygonyx near any of the waterfalls and swift-flowing
streams” on São Tomé, although the well-dispersing Z. torridus (Kirby, 1889) was
recently recorded (Papazian and Filippi 2019). Pinhey (1975) examined the
unidentified female reported from Annobón by Longfield (1936), stating that “it
appears to be flavicosta.” The species Z. flavicosta (Sjöstedt, 1900) is widespread in
western and central Africa and cannot be confused with Z. torridus, although other
continental species are similar. The Seychelles, Comoros and Madagascar all have
endemic Zygonyx species; thus, the presence of an endemic species on such a distant
island as Annobón cannot be ruled out.
A Poor Fauna?
Considering how much suitable freshwater is present (Fig. 14.2), the 22 species
known from all islands combined, and 19 from the largest and best-known island of
São Tomé, seem exceptionally few. The Comoros, which geographically and ecologically are perhaps the most comparable island group, harbour 39 species in total,
378
K.-D. B. Dijkstra et al.
Fig. 14.2 Tributary of the Rio Capitango, one of many forested streams on São Tomé. These seem
perfect for endemic odonates, but none are known. Photo credits: Russell B. Tate
with 36 on the oldest and best-studied island of Mayotte. The Mascarenes and
Seychelles (excluding Aldabra) are twice as far from the mainland, but have
29 and 19 confirmed species, respectively, while Mauritius and La Réunion each
harbour 23 species (Dijkstra and Cohen 2021). Sixteen species have been reported
from the Cape Verde islands, the only other major Afrotropical archipelago in the
Atlantic Ocean (Martens et al. 2013). Although that is even fewer than in the Gulf of
Guinea, those islands are also more isolated and substantially drier.
Comparing the species tallies of just a few archipelagos with very different sizes,
histories, habitats, and degrees of isolation is problematic, however. Looking at the
species themselves may therefore be more informative: 16 of the 22 recorded in the
Gulf of Guinea are widespread across Africa, with most species’ ranges including
the other archipelagos mentioned (and parts of Eurasia) as well. Twenty-seven
additional species are found both on the adjacent continent and on these other
islands, but have yet to be found on São Tomé, Príncipe, or Annobón
(Table 14.2): probably at least ten of the more widespread ones are likely present
in the Gulf of Guinea islands, pushing the total species diversity over 30.
Range-restricted species, too, are unexpectedly scarce. Pinhey (1974) noted that
“compared to other orders, particularly Lepidoptera, rich in species or subspecies
only known from these islands, the few endemics are remarkable for their paucity.”
While a quarter of the Comoro, Mascarene, and Seychelles species are confined to
14
Dragonflies and Damselflies (Odonata) of Príncipe, São Tomé, and Annobón
379
their archipelagos (Dijkstra and Cohen 2021), Trithemis nigra from Príncipe is the
only known endemic (Fig. 14.1). São Tomé is six times larger and twice as high but
has no endemic Odonata. Socotra is larger but lies in a very dry corner of Africa
(isolation is similar) and yet has similar numbers: 22 species including a single
endemic (Van Damme et al. 2020). Furthermore, the mainland nearest Socotra has
less than 50 species, whereas the Gulf of Guinea lies at the heart of the Afrotropics’
foremost centre of odonate diversity: well over 200 species are present in the hotspot
centred on the Cameroon highlands (Clausnitzer et al. 2012).
While the islands have been poorly researched, their low species numbers can
probably not be ascribed only to that. The wet climate with often rainy and cloudy
weather may certainly impede the activity of adult odonates and indeed of
odonatologists: Pinhey (1974) found that the hot humidity made it “almost unbearable in April to scramble up the mountain after about 9 a.m.” However, most
widespread species are conspicuous provided it is warm enough. Sampling of five
permanent forest streams in the south of São Tomé by the second author in
September 2020, moreover, produced larvae of Ephemeroptera and Trichoptera,
but no Odonata (Fig. 14.2) suggesting very low densities.
Perhaps the impoverishment on the islands in the Gulf of Guinea can be attributed
to the same factors as the diversity on the continent around it. Odonate diversity and
endemism is greatest at streams and other permanent waters, especially in areas with
forest and varied relief such as in Lower Guinea (Clausnitzer et al. 2012). This is
because species in stable habitats do not have to be good dispersers and can thus
more easily become isolated and highly adapted to their specific environment.
Species in seasonal habitats, by contrast, must be relatively tolerant and dispersive
to survive (Dijkstra et al. 2014).
While very few of over 200 species found across from São Tomé, Príncipe, and
Annobón may be capable of crossing over and colonising the islands, all of the less
than 50 across from Socotra have to be. Orthetrum africanum (Selys, 1887),
Rhyothemis notata (Fabricius, 1787), and Gynacantha cylindrata/vesiculata (see
above) are the only species on São Tomé and Príncipe that are confined to Africa’s
wetter and more forested west and centre, but favour rather open or temporary
habitats and thus occur widely across equatorial Africa. Agriocnemis zerafica Le
Roi, 1915 has a similar but more northerly range, being common at seasonal habitats
across the Sahel but patchy in the rainforest to the south.
The islands’ only endemic fits the same pattern as those three species: the
ancestors of the basitincta-group of species, to which T. nigra belongs, were inferred
to prefer open standing water (Damm et al. 2010). The group first invaded flowing
waters and then those with shade. The continental sister-species of T. nigra take an
intermediate position in this transition, favouring more open and temporary sites in
forests, such as flood pools near rivers. This capacity to penetrate the rainforest
matrix and adapt to peripheral habitats likely allowed for the colonisation of
Príncipe. This dispersal event was estimated to have occurred less than 3 million
years ago (Damm et al. 2010).
Other factors may also have contributed to the poor odonate fauna in the Gulf of
Guinea, such as habitat alteration by humans or volcanism, but these would seem
380
K.-D. B. Dijkstra et al.
unlikely to have impacted these insects specifically to the exclusion of other groups.
The composition of the freshwater communities, however, may also be especially
unsuited to Odonata. The second author noted unusually high densities of crustaceans and Sicydium gobies in his samples, likely caused by the absence of large fish
predators. Although this is highly speculative, their abundance might in turn have led
to rates of predation and/or competition that affect odonate larvae disproportionately.
Conclusions
We consider it unlikely (but not impossible) that prolonged fieldwork by a specialist
may upend the current impression of a poor and unexceptional odonate fauna on São
Tomé, Príncipe, and Annobón. Nonetheless, additional widespread Afrotropical
species are expected, especially on Annobón, while the identities of the Gynacantha
species on São Tomé and Zygonyx on Annobón remain to be clarified. Future work
should focus on larvae, as sampling this life stage is less affected by wet weather, but
also because their ecology might hold the key to the islands’ impoverished fauna.
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Chapter 15
Diversity and Distribution of the Arthropod
Vectors of the Gulf of Guinea Oceanic
Islands
Claire Loiseau, Rafael Gutiérrez-López, Bruno Mathieu, Boris K. Makanga,
Christophe Paupy, Nil Rahola, and Anthony J. Cornel
Abstract The known arthropod vector species on the Gulf of Guinea islands belong
to orders Diptera and Ixodida. Among the Diptera, the family Culicidae (mosquitoes) has the most species, 34 (6 endemic), Ceratopogonidae has 13 (all in the genus
Culicoides), Tabanidae has 6, and Simuliidae has 3 (1 endemic). Ixodida has only
4 species. Most vector species and associated diseases are shared with mainland
Africa. Some of these include (1) the human malaria vector Anopheles coluzzii,
(2) yellow fever and dengue vector Aedes aegypti, and (3) the spotted fever group
rickettsiae and Q fever vector Amblyomma spp. However, there is a considerable
lack of information on the natural cycles of many vector-borne diseases that might
C. Loiseau (*)
CIBIO-InBIO, Research Center in Biodiversity and Genetic Resources, InBIO Associate
Laboratory, Vairão, Portugal
CEFE, Centre d’Écologie Fonctionnelle et Évolutive, Montpellier University, Montpellier,
France
e-mail: claire.loiseau@cibio.up.pt
R. Gutiérrez-López
CIBIO-InBIO, Research Center in Biodiversity and Genetic Resources, InBIO Associate
Laboratory, Vairão, Portugal
B. Mathieu
Université de Strasbourg, Strasbourg, France
B. K. Makanga
Institut de Recherche en Écologie Tropicale, CENAREST, Centre National de la Recherche
Scientifique et Technologique, Libreville, Gabon
C. Paupy · N. Rahola
MIVEGEC, Maladies Infectieuses et Vecteurs: Écologie, Génétique, Évolution et Contrôle,
Montpellier University, Montpellier, France
A. J. Cornel
Mosquito Control and Research Laboratory, Department of Entomology and Nematology,
University of California, Davis, USA
Vector Genetics Laboratory, Department of Pathology, Microbiology and Immunology,
University of California, Davis, USA
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_15
383
384
C. Loiseau et al.
impact local fauna, for which there may be some endemic pathogen lineages.
Increased trade by air and sea should compel authorities to remain vigilant, to
keep unwanted vectors and diseases at bay. Entomological diversity data remains
scarce for Annobón and for the forested interior of the islands, where future sampling
efforts may uncover new endemic species.
Keywords Biting midges · Diptera · Flies · Infectious diseases · Mosquitoes · Ticks
Introduction
The discipline of medical entomology originated in the late nineteenth and early
twentieth centuries (Service 1978), when P. Manson and R. Ross discovered the
obligatory development of specific life stages of the human pathogenic filarial,
Wuchereria bancrofti Cobbold, 1877, and avian malaria Plasmodium parasite in
the mosquito Culex quinquefasciatus Say (Ross 1911). This discipline aims at
studying insects and other arthropods that affect the health of humans, domestic
animals, and wildlife (hereafter called vectors). Vector biology can be subdivided
into medical (emphasis on human), veterinary (domestic animals), and wildlife
disciplines (Edman 2009). However, these are often intertwined, since many vectors
transmit infectious agents that cause similar diseases in both humans and animals
(zoonoses). A large diversity of pathogens is transmitted by hematophagous arthropods (insects or ticks), including filariae (i.e., worms), protozoa (e.g., malaria),
bacteria, and viruses (e.g., dengue, yellow fever, or Zika). Of all the arthropods,
the Order Diptera contains the most species that transmit pathogens to humans and
wildlife, including one of the most studied families, the Culicidae (mosquitoes).
Recent mosquito surveys on Comoros (Mayotte Island: Le Goff et al. 2014),
Seychelles (Le Goff et al. 2012), and Mariana Islands (Guam: Rueda et al. 2011)
reveal high numbers of species but few single-island endemics. By contrast, São
Tomé and Príncipe harbor six endemic mosquito species (Ramos et al. 1994; Ribeiro
et al. 1998; Loiseau et al. 2019) and this high level of mosquito endemism (23%) is
especially unusual considering the proximity of the islands to the mainland. In
comparison, the Galapagos, Hawaii, and Canary archipelagoes do not harbor
endemic mosquito species (Baez 1987; Carles-Tolra 2002; Bataille et al. 2009),
while the Azores and Madeira have only one each (Ribeiro and Ramos 1999). Other
Dipteran families containing disease vector species, such as Simuliidae and
Ceratopogonidae, have been less studied on the Gulf of Guinea oceanic islands,
probably due to their lower diversity and lesser medical importance.
In this chapter, we present an overview of the known biodiversity of arthropod
vectors and their associated diseases on the Gulf of Guinea oceanic islands. We
describe the microhabitats of Culicidae and Simuliidae species and propose future
directions that might help in documenting and describing new vector species from
the archipelago.
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Diversity, Endemism, and Disease Ecology
All vector species on the Gulf of Guinea oceanic islands are Diptera or Ixodida
arthropods.
Class Insecta
Order Diptera
The order Diptera is composed of two suborders, Nematocera and Brachycera (Pape
et al. 2011). More than 150,000 species have been described, including numerous
hematophagous insects able to transmit infectious diseases. Diptera species known
as vectors in the Gulf of Guinea islands belong to five families.
Suborder Nematocera
Family Culicidae
Globally, Culicidae includes 3578 mosquito species and subspecies, in 42 genera
(Walter Reed Biosystematics Unit 2001). Seven hundred and ninety-five species are
known to occur in the Afrotropics (i.e., 22% of the mosquito diversity; Rueda 2008).
Culicidae is one of the most studied Diptera families, both worldwide and in the Gulf
of Guinea oceanic islands. Hence, for this group, we detail relevant expeditions,
from the early twentieth century, which relied mostly on collecting immature stages,
to more recent collections, which used both immature and adult decoy trapping.
Early Expeditions (1932–1964)
Published records dating back from the Percy Sladen and Godman Trust expeditions
in 1932 and 1933 (Edwards 1934) recorded five species on São Tomé (Anopheles
gambiae Giles, 1902, Uranotenia micromelas Edwards 1934, Aedes nigricephalus
Theobald, 1901; Culex fatigans Wiedemann, 1828 and Culex tamsi Edwards, 1934)
and two on Príncipe (Aedes aegypti Linnaeus, 1762 and Eretmapodites chrysogaster
Graham, 1909). Two species described from material collected on this expedition,
U. micromelas and Cx. tamsi, are still considered endemic to São Tomé and
Príncipe. Based on samples collected during expeditions between 1952 and 1955,
15 additional species were reported for São Tomé and Príncipe (Gãndara 1956).
During the program to eradicate tsetse flies on Príncipe (see section on Tabanidae),
nine species of mosquito were found, four of which were new to the islands,
including Aedes (Aedimorphus) larvae that were not identified to species (Pinhão
and Mourão 1961). A few years later, an intensive survey of mosquito larvae at
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14 sites on São Tomé (Mourão 1964) collected five additional species (Uranotaenia
balfouri Theobald, 1904, Aedes metallicus Edwards, 1912, Aedes circumluteolus
Theobald, 1908, Toxorhynchites brevipalpis Theobald, 1901 and Culiseta fraseri
Edwards, 1914).
Further Expeditions in the Second Half of the Twentieth Century
An updated list of Príncipe Island mosquito species, based on specimens collected
during an expedition in 1986, added seven species (Ae. nigricephalus, Culex
antennatus Becker, 1903, C. decens Theobald, 1901, C. nebulosus Theobald,
1901, C. quinquefasciatus Say, 1826, U. micromelas and U. principensis da
Cunha Ramos, 1993) to the seven previously recorded (Ramos et al. 1989). Then,
two new species were described: Toxorhynchites capelai Ribeiro, 1991 (Ribeiro
1993), and Aedes (Aedimorphus) gandarai Ramos, Capela and Ribeiro, 1994
(Ramos et al. 1994). A few years later, the list of mosquito species increased to
14 on Príncipe and 26 on São Tomé (Ribeiro et al. 1998), including 6 São Tomé
endemics, and 1 endemic to both islands (Appendix). The genus Culex is represented
by the most species, 14, followed by Aedes, with 6.
On São Tomé and Príncipe Islands, the only current known vector of human
malaria is Anopheles coluzzii Coetzee and Wilkerson 2013, previously known as An.
gambiae M form. An. coluzzii is abundant in urban and village settings in coastal
areas on both islands. The lower abundance and the possible absence of An. coluzzii
inland and at elevations above 200 m (Pinto et al. 2000a, b), despite an abundance of
semi-permanent pools for immature development, is likely due to much lower
human population densities in these areas. After intensive indoor residual spraying
campaigns, which started in 2005, the overall prevalence of malaria in children
under 9 years old was reduced from 30.5% to 8.3% after the first round, and to 2.1%
after the second (Tseng et al. 2008; Teklehaimanot et al. 2009). Prevalence has
remained low (~1%; Chen et al. 2019), but active surveillance and mosquito control
to prevent malaria outbreaks is ongoing (Lee et al. 2010). The only other Anopheles
species present on São Tomé, but not on Príncipe, is An. coustani Laveran, 1900;
however, its role as a secondary malaria vector is not known.
Lymphatic filariasis, a human parasitic infection, is caused by nematodes
(Wuchereria bancrofti Cobbold, 1887, Brugia malayi Brug, 1927 and B. timori
Partono, 1977), which are transmitted through the bite of infected Ae., Cx., An. and
Mansonia mosquitoes (Chandy et al. 2011). The last report of the presence of
W. bancrofti on São Tomé dates from 1956 and on Príncipe from 1958 (Fraga de
Azevedo et al. 1960). The insecticide spraying that led to the eradication of Glossina
palpalis palpalis Robineau-Desvoidy, 1830 on Príncipe (see below), probably also
impacted mosquito populations, which likely led to eliminating lymphatic filariae on
that island (Fraga de Azevedo et al. 1960). Further surveillance might be needed as
positive serological tests for lymphatic filariasis have been reported on São Tomé in
recent years (Fan et al. 2013; WHO 2019).
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Recent Surveys (Within First Quarter of the Twenty-First Century)
Collections performed by the authors on São Tomé and Príncipe in 2016, 2017, and
2019 added four species to the documented diversity (Ae. albopictus Skuse, 1894,
Ae. tarsalis Edwards, 1927, U. bilineata Theobald, 1909, and U. connali Edwards,
1912). These surveys were primarily focused on collecting mosquito vectors known
to transmit wildlife pathogens, especially to birds. At least eight genera of mosquitoes (Aedes, Aedeomyia, Anopheles, Culex, Coquillettidia, Culiseta, Mansonia, and
Uranotaenia) can transmit avian malaria (Valkiūnas 2004). Avian malaria has had
devastating effects on the endemic bird populations of Hawaii (Fonseca et al. 2000),
demonstrating the pernicious nature of introduced diseases on isolated animal
populations. São Tomé and Príncipe birds are not heavily infected with Plasmodium,
exhibiting an average prevalence of around 12% (Reis et al. 2021); however, the
birds appear to be carrying Plasmodium lineages that originate from the mainland,
particularly in lowland bird populations (Reis et al. 2021). Numerous mosquito
species may be vectors of avian malaria in the Gulf of Guinea oceanic islands, but
their vector competence has not yet been assessed and will be an important future
research direction for monitoring the population health of the endemic avifauna.
The highly anthropophilic Ae. albopictus (invasive tiger mosquito), likely introduced to the Gulf of Guinea during the last 10 years, is now very widespread on both
islands and is of considerable human biting nuisance (Reis et al. 2017; Loiseau et al.
2019). Along with Ae. aegypti, Ae. albopictus is considered an urban cycle vector
(Kamgang et al. 2019b) of Yellow Fever, Dengue, Zika and Chikungunya viruses,
which actively circulate in neighboring African mainland countries (Paupy et al.
2010; Braack et al. 2018; Kamgang et al. 2019a). Periodic outbreaks of Yellow
Fever occur in neighboring mainland countries, namely in Cameroon, Gabon, and
Angola (Chippaux and Chippaux 2018). One study estimated that currently there are
between 51,000 and 380,000 severe cases of yellow fever annually in Africa,
resulting in an estimated 19,000–180,000 deaths (Garske et al. 2014). Dengue
virus strains, in the same Flavivirus genus as Yellow Fever virus (Daep et al.
2014), are now probably one of the most important arboviruses, since globally
they infect over 100 million people annually, resulting in an estimated 500,000
severe Dengue cases (WHO 2014). A serological survey on pregnant women has
actually demonstrated the circulation of this virus on the islands (Yen et al. 2016).
No major outbreak of Dengue has been recorded on the islands until a recent one in
São Tomé in 2022. In addition, nine resident mosquito species found in São Tomé
and Príncipe (Ribeiro et al. 1998) are known as vectors of numerous other arboviruses (e.g., Alphavirus, Flavivirus, or Phlebovirus) in the Afrotropics.
Currently, both Anophelinae and Culicinae subfamilies are present in the Gulf of
Guinea islands, as well as the only Culicidae genus that is endemic to Africa,
Eretmapodites Theobald, 1901. There are 35 resident Culicidae species: 31 on São
Tomé and 15 on Príncipe (Appendix). To our knowledge Ae. indet (Pinhão and
Mourão 1961) has not been collected in the last 70 years, and its current presence on
the islands is questionable. We have not included An. funestus s.l. Giles, 1900, An.
paludis Theobald, 1901, and An. pharoensis Theobald, 1901 (Mesquita 1946, 1952)
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in the current list of species, because malaria control campaigns in the 1980s are
thought to have eradicated them (Pinto et al. 2000a). The only publication on the
mosquitoes of Annobón was about malaria transmission and genetic population
structure of An. coluzzii in Equatorial Guinea (Moreno et al. 2007).
Family Simuliidae
Among the 2200 species of black flies described around the world, 214 are present in
the Afrotropical region (Currie and Adler 2008), including many that transmit
pathogens that affect humans (e.g., filarial disease onchocerciasis; Crosskey 1990),
poultry (Alder and McCreadie 2019), and wild birds (Valkiūnas et al. 2004).
Onchocerciasis (river blindness) is limited to sub-Saharan Africa and is widely
known in southern Cameroon and on Bioko Island, where it is transmitted by species
of the complex Simulium damnosum Theobald, 1903 (Post et al. 2003). Currently,
this vector species does not occur on the Gulf of Guinea oceanic islands (Mustapha
et al. 2004), and no cases of Onchocerciasis have been reported. The avian parasites
Leucocytozoon, closely related to avian malaria, are present, especially in highland
and forest birds of São Tomé and Príncipe (Reis et al. 2021). However, the vector
competence of black fly species for Leucocytozoon spp. remains unknown on the
islands.
Black flies were first documented at one site on São Tomé in 1988 (Grácio 1988).
Extensive sampling of 71 sites on São Tomé reported the presence of two species:
Simulium (Pomeroyellum) alcocki Pomeroy, 1922, and S. (Anasolen) dentulosum
Roubard, 1915, the latter being the most abundant (Grácio 1999). In 1998, the São
Tomé endemic S. (Pomeroyellum) santomi Mustapha, 2004 was added to the list
(Mustapha et al. 2004). On Príncipe, only S. dentulosum is confirmed. No effort has
been made to sample black flies on São Tomé or Príncipe during the last 20 years,
and it has been suggested that they are absent from Annobón (Mustapha et al. 2004).
Family Ceratopogonidae
This family of biting midges includes 6206 species in 112 genera and has a diverse
fossil record (around 300 species; Borkent and Dominiak 2020). Many species of
Ceratopoginidae are important pollinators, and only four genera are known to have
species that feed on blood of vertebrates, including humans (Borkent 2004):
Austroconops Wirth and Lee, 1958, Culicoides Latreille, 1809, Forcipomyia (subgenus Lasiohelea) Meigen, 1818 and Leptoconops Skuse, 1889. Austroconops is the
only genus that is not known to play a role in pathogen transmission, while
Culicoides is the most important in this regard (Borkent 2004). Culicoides includes
1347 described species, and the assessment of this diversity has received much
attention in Africa because of their status as vectors of human filarial nematodes
(Agbolade et al. 2006), and of several viruses responsible for animal diseases, such
as Bluetongue (Mellor 1990) and African Horse Sickness (Mellor et al. 2000; Mellor
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and Hamblin 2004). Culicoides are also known vectors of avian malaria-like parasites of the genera Haemoproteus (Parahaemoproteus) and Leucocytozoon
(Caulleryi) (Valkiūnas 2004). On São Tomé, approximately 20% of the birds are
infected with these parasites, with a higher prevalence in shaded plantations (Reis
et al. 2021). Among the species of Culicoides, several can transmit Haemoproteus,
but vector competence of Culicoides species remains unknown.
The first four species of Culicoides recorded on São Tomé were collected during
the Percy Sladen and Godman Trust expeditions in the 1930s (Edwards 1934), and
identified as C. austeni Carter, Ingram and Macfie, 1920, C. distinctipennis Austen,
1912, C. citroneus Carter, Ingram and Macfie, 1920 and C. grahamii Austen, 1909.
A three-year study of insects in cocoa plantations identified 25 species of
Ceratopogonidae, including only one Culicoides species: C. imicola Kieffer, 1913
(Wirth and Derren 1976). This fifth species recorded on the island is a known
primary vector of Bluetongue and African Horse Sickness viruses, largely distributed in Africa, Asia, and Europe (Guichard et al. 2014). C. distinctipennis, C. milnei
Austen, 1909 and C. imicola were later mentioned as present on São Tomé (Glick
1990), the latter being the sixth Culicoides species recorded on the island. Since the
mid-1970s, there has been no evaluation of the diversity of Culicoides on São Tomé
and Príncipe Islands, and the number of species is thus likely underestimated. There
are 156 species formally described in the Afrotropical region (Labuschagne 2016),
including high diversities on neighboring mainland African countries, such as
Nigeria (Dipeolu 1976) and Cameroon (Callot et al. 1965; Wanji et al. 2019).
Gabon is an exception since only six species have been described so far, probably
due to very few studies carried out in that country (Delécolle et al. 2013; Augot et al.
2017). In 2019, nine species of Culicoides were found in the southeast of São Tomé,
along transects from the center of an oil palm plantation to the native forest. While
morphological and molecular investigations are ongoing, it is likely that seven
species will be added to the records for the island (Appendix). From the four species
first recorded for the island (Edwards 1934), only C. citroneus and C. distinctipennis
were found recently. Surprisingly, no endemic Culicoides species have been found
yet. Considering sampling bias in these islands, it is likely that future studies in
different habitat types, especially deeper in the native forest, or in coffee and cocoa
plantations, will reveal the presence of endemic Culicoides species. Future surveys
will most certainly also increase the number of Culicoides species on Príncipe and
Annobón, as well as clarify their ecology.
Suborder Brachycera
Family Tabanidae
Worldwide, there are currently close to 4400 species and subspecies, and 144 genera
of Tabanidae described (Mullens 2019). Tabanid flies of the genera Tabanus,
Chrysops, and Hybomitra, commonly known as horseflies and deerflies, are of
economic, medical, and veterinary importance (Nevill et al. 1994). However, they
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tend to be less studied than other Dipteran families (Baldacchino et al. 2014).
Tabanid flies serve as biological vectors (pathogens replicate and develop within
the fly), and as mechanical vectors (pathogens are transmitted without amplification
and development within the fly via contaminated blood on mouthparts) of several
wildlife and livestock pathogens, such as Trypanosoma spp. (Nevill et al. 1994),
Babesia spp., and Theileria spp. (Taioe et al. 2017), filarial nematodes, and numerous viruses and bacteria (Baldacchino et al. 2014). In forested Central Africa,
tabanid flies of the genus Chrysops also infect humans with Loa loa Cobbold,
1864, which causes African eye worm (Mullens 2019). This pathogen has not
been reported in São Tomé and Príncipe.
Six species in the genus Tabanus have been recorded on São Tomé and Príncipe:
T. biguttatus Wiedemann, 1830; T. congoiensis Ricardo, 1908; T. obscurefumatus
Surcouf, 1906; T. taeniola, Palisot de Beauvois, 1806; T. principis Bequaert, 1930
(Bequaert 1930) and T. monocallosus (Travassos Santos Dias 1955), the last two
being endemic to the Gulf of Guinea islands. No new tabanid flies have been
recorded on the archipelago in recent years.
Family Glossinidae
Glossinidae includes the single genus Glossina with 23 species, 6 of which are
further divided into 14 subspecies, all but one found in Africa (Krinsky 2019). The
genus is divided into three groups based on their ecological preferences: the savannah flies (subgenus Morsitans), the forest flies (subgenus Fusca), and the riverine
flies (subgenus Palpalis). Species found in sub-Saharan Africa are vectors of the
Trypanosoma parasites that cause sleeping sickness in humans (Welburn et al. 2001)
and trypanosomosis in livestock (Meyer et al. 2016) and can have severe impacts on
domestic cattle production (De Geier et al. 2020).
The first known introduction of the tsetse fly, G. p. palpalis, occurred on Príncipe
Island in 1825 (Fraga de Azevedo et al. 1956). At the end of the nineteenth century
and beginning of the twentieth century, it became a significant health issue for cocoa
plantation workers and local inhabitants, forcing important prophylactic measures
between 1911 and 1914, which included hunting for flies, swamp drainage, clearance of vegetation and slaughter of wild pigs, stray dogs, and civets (Bruto da Costa
1913). The prevalence of Trypanosoma dropped dramatically (Bruto da Costa
1913), and in 1914 the tsetse fly was considered eradicated in Príncipe (Figueiredo
Moura da Silva 2019). In 1956, entomologists rediscovered large numbers of tsetse
fly on Príncipe (Tendeiro 1956) and suggested it had been reintroduced from Bioko
Island. Although no cases of trypanosomiasis were found in humans, animals or in
the tsetse flies, important measures were applied again to eradicate the tsetse flies,
including trapping flies, insecticide spraying, clearing of vegetation, and killing of
wild pigs, monkeys, and dogs (Fraga de Azevedo et al. 1956). Eradication was
effective by July 1958.
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Order Siphonaptera
Two flea species, Ctenocephalides felis Bouché, 1935 (cat flea; Family Pulicidae)
and Tunga penetrans Linnaeus, 1758 (chigoe flea; Family Tungidae), occur in São
Tomé and Príncipe. A high percentage of dogs seem to have cat fleas infected with
Rickettsia felis, an emerging human pathogen often causing febrile illness, while just
over 3% of humans had antibodies against this bacterium (Tsai et al. 2020).
Class Arachnida
Order Ixodida
The Ixodida contains three families: Ixodidae, Argasidae, and Nuttalliellidae
(Nicholson et al. 2019). The Ixodidae or hard-bodied ticks include 15 genera and
707 species, while the Argasidae or soft-bodied ticks contain about 190 species, and
the Nuttalliellidae only one species. Worldwide, they are the most important disease
vectors in the veterinary field and are second only to mosquitoes in public health
importance (Nicholson et al. 2019). Ticks are ectoparasites that blood-feed on
mammals, birds, reptiles, and amphibians, but unlike the short blood-feeding periods
(at most a few minutes) of Diptera, hard-bodied ticks attach and stay on their hosts
for several days. They are implicated in the transmission of numerous infectious
diseases caused by pathogens, such as bacteria (e.g., Rickettsia, Borrelia, Coxiella;
Parola et al. 2013), viruses (e.g., Crimean–Congo hemorrhagic fever virus, Tickborne encephalitis virus; Hoogstraal 1979) and protozoa (e.g., Babesia; Nelder et al.
2016).
Family Ixodidae
Four species of hard-bodied ticks have been recorded through the years from São
Tomé and Príncipe. Amblyomma astrion Dönitz, 1909 and A. splendidum Giebel,
1877, were collected on São Tomé, and A. splendidum on Príncipe (Tendeiro 1957).
Subsequently, Rhipicephalus decolaratus (Koch, 1844) was collected on both
islands (Travassos Santos Dias 1988). In the early 1980s, numerous adult cow and
calf deaths on São Tomé were attributed to neurological complications, likely caused
by heartwater, a tick-borne rickettsial disease of domestic and wild ruminants
transmitted by A. astrion (Uilenberg et al. 1982). In 2016, A. variegatum Fabricius,
1794, was collected from cattle in the Agua Grande district on São Tomé (Hsi et al.
2020). A serological survey demonstrated the presence of Spotted fever group
rickettsiae and Q fever (Coxiella burnetti) antibodies in people, which could explain
continued reports of febrile illness in São Tomé human residents not due to malaria
(Hsi et al. 2020).
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Family Argasidae
To date, Ornithodoros capensis Neumann, 1901 is the only soft tick species reported
for the islands (Travassos 1988). It is an ectoparasite of seabirds in the tropics and
subtropics, and was collected in the nests of Brown Noddy Anous stolidus (Linnaeus, 1758), Black Noddy A. minutus (Boie 1844), and Sooty Tern Onychoprion
fuscatus (Linnaeus, 1766), during an expedition to Tinhosas (small islets south of
Príncipe) in 1970 (Travessos 1988). A recent census of seabird nests on these islets
did not report ectoparasites (Valle et al. 2016; Bollen et al. 2018), but they may not
have explicitly searched for them.
Distribution, Biology, and Habitat Specificity
In this section, we describe the habitat types and preferred environmental conditions
of Culicidae and Simuliidae species, based on the observations of AJC and on the
literature (Mourão 1964; Grácio 1999).
Mosquito Habitat and Distribution on São Tomé and Príncipe
Anthropophilic Mosquitoes
Mosquito species that regularly blood-feed on humans include disease vector
species – Ae. aegypti (Fig. 15.1.1), Ae. albopictus (Fig. 15.1.2), An. coluzzii
(Fig. 15.1.5), Cx. quinquefasciatus, and Ae. circumlutelous – and species not
implicated as disease vectors – Ae. nigricephalus and E. chrysogaster (Fig. 15.1.3).
Immatures of An. coluzzii, vectors of malaria, are found mostly on the coast. They
develop in direct contact with clear or eutrophic groundwater, in swamps, and in
temporary pools, such as in roadside ditches, depressions in pathways, and between
households (Fig. 15.2.1). Blood index values and low sporozoite rates in An. coluzzii
sampled in 1997 and 1998 on São Tomé (Sousa et al. 2001) indicate that they are
meso-endemic, feeding predominantly on dogs, followed by humans, and then pigs.
In recent collections by AJC, An. coluzzii were also attracted to chicken.
Cx. quinquefasciatus (Cx. fatigans in Mourão 1964), a vector of filarial nematodes, is very common in urban areas. It bites humans at night inside homes, and
often rests indoors or underneath houses along with Anopheles mosquitoes. They
represent the majority of mosquitoes in the city of São Tomé (Mourão 1964).
Immatures of Cx. quinquefasciatus are often found in very high numbers in
unmaintained sewage systems and in artificial containers, such as barrels, gutters,
tubs, or vats of water.
Ae. aegypti and Ae. albopictus, vectors of numerous viruses, primarily bite
humans during the day. They have spread worldwide and become cosmopolitan
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Fig. 15.1 Pictures of mosquito species: (1) Aedes albopictus (female); (2) Aedes aegypti (female);
(3) Eretmapodites chrysogaster (female); (4) Toxorhynchites brevipalpis (male); (5) Anopheles
coluzzii (female). Photo credits; Nil Rahola
(Paupy et al. 2009; Brown et al. 2011; Kraemer et al. 2019). Historically, they both
laid eggs in tree cavities (e.g., Erythrina sp., Chlorophora sp.), but now they are
considered container-breeding mosquitoes, as immatures often develop in discarded
plastics, tires, and other rubbish that hold water, and in unused cisterns. Still, both
species lay eggs in the abundant supply of tree cavities, as well as in fallen banana
leaves, in São Tomé and Príncipe. In the past, Ae. aegypti was the most collected
species (Mourão 1964), but its abundance seems to have decreased since Ae.
albopictus became established in São Tomé and Príncipe (Reis et al. 2017), as in
other parts of the world (Bargielowski and Lounibos 2016). The distribution of Ae.
aegypti has now contracted into small enclaves, mostly at higher elevations on São
Tomé, and is rarely collected on Príncipe.
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Fig. 15.2 Examples of microhabitat of Culicidae: (1) Typical roadside ditch located on Príncipe
with large numbers of Anopheles coluzzii larvae. Arrow points to fourth instar larva; (2) Typical
slow-moving river edge on Príncipe supporting large numbers of Uranotaenia micomelas and
Culex decens larvae; (3) Preferred daytime resting location for Cx. cinerellus, Cx. nebulosus and
multiple Uranotaenia species in crab holes in road embankment in Alto Douro, São Tomé. Arrows
point to Culex mosquitoes; (4) Cx. cambournaci larvae in water-filled Heliconia rostrata flower in
Botanical gardens on São Tomé. Arrow points to larvae. Photo credits: Anthony Cornel
Ae. circumluteolus is localized and infrequently captured (human-biting at
Mucumbli, São Tomé), and represents the only typical floodwater Aedes species
on São Tomé, even though immatures have been found in ground pools and in
artificial containers (Mourão 1964). This species is a known vector of significant
arboviruses, such as Rift Valley Fever, Wesselsbron, Bunyamwera, and Pongola
viruses in Africa (Braack et al. 2018).
Finally, E. chrysogaster, another pernicious daytime human blood-feeding mosquito, lays eggs opportunistically in trash, but mostly in natural containers, such as
plant leaf axils, especially in fallen banana and palm leaves, or cocoa and coconut
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shells. This species is present everywhere on the islands but is not known to transmit
diseases in São Tomé and Príncipe.
Opportunistic Mosquitoes
Ae. nigricephalus, an opportunistic blood feeder, bites humans during the day and
does not disperse far from brackish water estuaries and mangroves, where immatures
develop in crab holes. Cx. cinerellus Edwards, 1922 is also specialized to develop in
brackish water crab holes (Hopkins 1952).
Immatures of other abundant mosquito species, which are more likely to feed on
birds, and only seldom feed on humans, such as Cx. decens, Cx. antennatus, and
Lutzia tigripes (de Grandpré & de Charmoy, 1901) also occur in temporary water
bodies. Cx. decens can be abundant on São Tomé (Mourão 1964), and its larvae were
frequently found in artificial containers. On Príncipe, large numbers of larvae were
found along slow-moving rivers (Fig. 15.2.2).
Immatures of other species that seldom bite humans (e.g., Ae. tarsalis,
Ae. gandarai, Culex macfiei Edwards, 1923, Cx. nebulosus) and nectar feeders
(Toxorhynchites capelai and T. brevipalpis; Fig. 15.1.4), develop in tree holes and
less so in banana or plant leaf axils. Rotting coconut fruits serve as significant sites
for the development of Cx. (Culiciomyia) nebulosus, while adults primarily rest in
crab holes (Fig. 15.2.3). Interestingly, immatures of Cx. cambournaci Hamon &
Gandara, 1955 are often found in large numbers in the flowers of Heliconia species,
which have been introduced from the neotropics as ornamentals (Fig. 15.2.4).
The immatures of other species including Cx. annulioris Theobald, 1901,
Cx. invidiosus Theobald, 1901, Cx. thalassius Theobald, 1903, Cx. tamsi, Culiseta
fraseri, L. tigripes, Ur. capelai, Ur. principensis, Ur. balfouri Theobald, 1904,
Ur. bilineata and Ur. connali are typically found in river seepages, and rocky and
thickly vegetated vernal pools. All these opportunistic mosquitoes are potential
vectors of avian Plasmodium.
Black Fly Habitat and Distribution on São Tomé
Immature Simuliidae filter-feed in flowing waterways. Stream size, water velocity,
and seston load are important factors that influence the distribution of black-fly
species (Palmer and Craig 2000; Adler and McCreadie 2019). Interestingly,
S. alcocki and S. dentulosum are not concomitant on São Tomé (Grácio 1999),
S. alcocki is restricted to the northern interior part of the island, while S. dentulosum
was more widespread. Their niches tend to show ecological allopatry with
S. dentulosum found in rivers from sea level to 400 m, while S. alcocki occurs
from 200 to 900 m above sea level. S. alcocki immatures tend to be restricted to the
first 10 cm of the water column, whereas S. dentulosum are found anywhere from
close to the surface to 50 cm below the surface. Finally, S. dentulosum seems to
396
C. Loiseau et al.
prefer streams or rivers with weak water flow (78 cm/s, 87% of oxygen on average),
contrary to S. alcocki which prefers faster water flow (122 cm/s, 98% of oxygen on
average; Grácio 1999). Re-sampling the same sites would be ideal to evaluate if the
habitat and microhabitat specificity of these two species have changed over time. We
suspect S. alcocki as the main vector of Leucocytozoon spp. in birds, since both
vectors and parasites are found in greater abundance at higher elevations.
Directions for Future Disease Insect Vector Research
Sampling Effort in Diverse Habitats and Specific Vector
Families
Among all expeditions and surveys that aimed to collect vectors, we discern two
major sampling paucities. First, the forested interior of São Tomé, in the Obô Natural
Park, and the forested south of Príncipe are poorly studied. The main reason is
probably accessibility, since reaching remote native forest requires long walks and
camping. While mosquitoes have been quite well sampled along the entire coast, and
also in some parts of the interior of the islands, other families such as
Ceratopogonidae or Tabanidae have been sampled in few sites, and do not include
all habitat types found on the islands. Second, Annobón has been poorly sampled for
all groups. Although the island is small (17 km2) and more isolated, we estimate that
some of its arthropod vectors are not yet described. We believe that the Gulf of
Guinea oceanic islands are still full of surprises and that all three islands have the
potential to hold undescribed arthropod vectors.
Surprisingly, there are no records of louse flies (family Hippoboscidae) and sand
flies (family Psychodidae, subfamily Phlebotominae) on the islands. Louse flies, also
known as bird flies, flat flies, or ked flies (Reeves and Lloyd 2019), are vectors of
Haemoproteus parasites in Columbidae birds (Valkiūnas 2004), which have been
detected in the blood of Columba larvata and C. malherbii, both on São Tomé and
Príncipe (Loiseau et al. 2017; Reis et al. 2021). Thus, the presence of louse flies on
São Tomé and Príncipe islands is highly suspected, even though no record has been
published yet. Collection of louse flies can only be done on live birds, or by checking
livestock coats. It is also somewhat surprising that no sand fly species have been
found on any of the islands, although no surveys have specifically searched for them.
Surveys should be done preferentially during the rainy season since these insects are
highly seasonal, with abundance peaks during or right after rain (Munstermann
2019). Leishmania parasites, transmitted by sand flies, are present in Central Africa
(Alvar et al. 2012) but have never been reported on the islands, supporting the
hypothesis that these vectors might be absent.
15
Diversity and Distribution of the Arthropod Vectors of the Gulf of. . .
397
New Complementary Tools to Evaluate Vector Diversity
Skilled entomologists can identify species morphologically, if they have access to
updated descriptions and identification keys (Hajibabaei et al. 2007). Distinguishing
characters, especially subjective ones that are used in identification keys, at the
different stages (i.e., eggs, larvae, and adult specimens) are perceptively difficult
for non-experts, particularly in the tropics where the diversity is often high and many
species are similar. Recent developments in molecular identification techniques,
coupled with reduced sequencing costs can help overcome these identification
difficulties, and even reveal cryptic biodiversity. Identification of species using
metabarcoding approaches on environmental DNA (eDNA) (Boerlijst et al. 2019;
Krol et al. 2019) and on bulk samples (Batovska et al. 2018) is an appealing option,
but it is worth noting that sequences belonging to unknown taxa are still a common
problem in eDNA barcoding. Surveys of mosquito diversity using these techniques
require a sound reference database, which in turn demands a considerable amount of
a priori taxonomic work. This can be achieved by sequencing samples from the field
and from natural history museums that have been identified by experienced
entomologists.
Because dipping methods traditionally used to survey larvae may not always
reflect adult diversity found with traps, determining and comparing species diversity
across different types of samples (water, soil, or bulk samples) using metabarcoding
might be a useful complementary approach. eDNA and bulk sample metabarcoding
also show a high potential to become helpful monitoring tools to evaluate changes in
relative abundance and species diversity in relation to habitat change and to detect
invasive vector species in routine surveys. In addition, novel trap designs as well as
visual and chemical lures to attract insects, including vector species, are always
under development and may also increase surveillance and biodiversity
determinations.
Acknowledgments We sincerely thank Branca Maria do Nascimento Rolão Moriés for searching
for old journals and articles in the historical archive center at the University of Lisbon. We thank
Diego Santiago-Alarcon and Kevin Njabo for their comments and suggestions that enhanced the
clarity of our chapter. This work is funded by National Funds through FCT - Foundation for Science
and Technology under the IF/00744/2014/CP1256/CT0001 Exploratory Research Project (CL) and
the PTDC/BIA-EVL/29390/2017 DEEP Research Project (CL).
Appendix
List of the arthropod vectors of the Gulf of Guinea Oceanic Islands of Príncipe
(P) and São Tomé (ST).
Entomological data are almost non-existent for Annobón. Beside the record of
Anopheles coluzzii on Annobón, and the absence of Simuliidae, we cannot state if
C. Loiseau et al.
398
other vector species are present or absent. Status of each species was defined as
resident (R), endemic (E), introduced (I), or no data (?)
Higher Taxonomy
ORDER DIPTERA
Family Culicidae
Anopheles Meigen,
1818
Subgenus/Group
Species
Anopheles
Cellia
Aedes Meigen, 1818
Aedimorphus
Anopheles coustani Laveran, 1900
Anopheles coluzzii (Anopheles gambiae M
form) Coetzee & Wilkerson, 2013
Aedes nigricephalus Theobald, 1901
Aedes sp. indet
Aedes tarsalis Edwards, 1927
Aedes gandarai Ramos, Capela & Ribeiro,
1994
Aedes circumluteolus Theobald, 1908
Aedes aegypti Linnaeus, 1762
Aedes albopictus Skuse, 1894
Culex annulioris Theobald, 1901
Culex antennatus Becker, 1903
Culex decens Theobald, 1901
Culex invidiosus Theobald, 1901
Culex quinquefasciatus Say, 1826
Culex tamsi Edwards, 1934
Culex thalassius Theobald, 1903
Culex cambournaci Hamon & Gãndara,
1955
Culex cinerellus Edwards, 1922
Culex macfiei Edwards, 1923
Culex nebulosus Theobald, 1901
Culex inconspicuosus Theobald, 1908
Culex rima Theobald, 1901
Culex micolo Ribeiro, Cunha Ramos &
Capela, 1998
Culiseta fraseri Edwards, 1914
Eretmapodites chrysogaster Graham,
1909
Lutzia tigripes De Grandpré & De
Charmoy, 1900
Toxorhynchites capelai Ribeiro, 1993
Toxorhynchites brevipalpis conradti
Gruenberg, 1907
Uranotaenia capelai Ramos, 1993
Uranotaenia micromelas Edwards, 1934
Uranotaenia principensis Ramos, 1993
Uranotaenia balfouri Theobald, 1904
Uranotaenia bilineata Theobald, 1909
Uranotaenia connali Edwards, 1912
Catageomyia
Polyleptiomyia
Neomelaniconion
Stegomyia
Culex Linnaeus
1758
Culex
Culiciomyia
Eumelanomyia
Culiseta Felt, 1904
Eretmapodites
Theobald, 1901
Lutzia Theobald,
1903
Toxorhynchites
Theobald, 1901
Metalutzia
Uranotaenia Lynch
Arribálzaga, 1891
Pseudoficalbia
Theomyia
Afrorhynchus
Uranotaenia
P
ST
R
R
R
R
E
R
R
E
R
I
R
R
R
R
R
I
R
R
R
R
R
E
R
E
R
R
R
R
R
R
E
R
R
R
R
R
E
R
E
E
E
E
R
R
R
(continued)
15
Diversity and Distribution of the Arthropod Vectors of the Gulf of. . .
Higher Taxonomy
Family Simuliidae
Simulium Latreille,
1802
Subgenus/Group
Species
Pomeroyellum
Simulium alcocki Pomeroy, 1922
Simulium santomi Mustapha, 2004
Simulium dentulosum Roubard, 1915
Anasolen
Family Ceratopogonidae
Culicoides Latreille, –
1809
Subgenus
Avaritia
Subgenus
Meijerehelea
Subgenus
Remmia
Group Milnei
Group Neavei
Group
Nigripennis
Family Tabanidae
Tabanus Linnaeus
1758
Group Tabanini
ORDER IXODIDA
Family Ixodidae
Amblyomma Koch,
1844
Family Argasidae
Ornithodoros Koch,
1837
Subgenus
Alectorobius
a Found on Tinhosas Islands
399
P
ST
R
R
E
R
Culicoides citroneus Carter, Ingrain et
Macfie, 1920
Culicoides grahamii Austen, 1909
?
R
?
R
Culicoides imicola Kieffer, 1913
Culicoides trifasciellus Goetghebuer, 1935
Culicoides distinctipennis Austen, 1912
?
?
?
R
R
R
Culicoides enderleini Cornet & Brunhes,
1994
Culicoides austeni Carter, Ingram and
Macfie, 1920
Culicoides hortensis Khamala, 1991
Culicoides krameri Clastrier, 1958
Culicoides milnei Austen, 1909
Culicoides quinquelineatus Goetghebuer,
1934
Culicoides neavei Austen, 1912
Culicoides sp.
?
R
?
R
?
?
?
?
R
R
R
R
?
?
R
R
Tabanus biguttatus Wiedemann, 1830
Tabanus congoiensis Ricardo, 1908
Tabanus obscurefumatus Surcouf, 1906
Tabanus taeniola, Palisot de Beauvois,
1806
Tabanus principis Bequaert, 1930
Tabanus monocallosus Travassos Dias,
1955
R
R
R
R
E
E
Amblyomma astrion Dönitz, 1909
Amblyomma splendidum Giebel, 1877
Amblyomma variegatum Fabricius, 1794
R
Ornithodoros capensis Neumann, 1901
*
R
R
R
400
C. Loiseau et al.
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Chapter 16
Terrestrial Mollusca of the Gulf of Guinea
Oceanic Islands
Martina Panisi, Ricardo F. de Lima, Jezreel do C. Lima,
Yodiney dos Santos, Frazer Sinclair, Leonor Tavares, and David T. Holyoak
Abstract The oceanic islands of the Gulf of Guinea are known for their remarkable
endemic species richness, and the terrestrial Mollusca group is particularly distinctive. This chapter summarizes the exploration and diversity of this group, discussing
biogeography, evolution, ecology, and conservation to identify persisting knowledge gaps. Terrestrial malacological studies in the Gulf of Guinea islands started at
the end of the eighteenth century but have been intermittent. Recent systematic
surveys have continued to find novelties, and the most recent revision lists 96 species,
of which 62 are endemic: Príncipe has 40 terrestrial (60% single-island endemic) and
M. Panisi (*)
Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências,
Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon,
Portugal
R. F. de Lima
Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências,
Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon,
Portugal
Gulf of Guinea Biodiversity Centre, São Tomé, Sao Tome and Principe
J. d. C. Lima
Gulf of Guinea, Biodiversity Centre, Monte Café, Sao Tome and Principe
Y. dos Santos
Fundação Príncipe, Santo António, Sao Tome and Principe
F. Sinclair
Fundação Príncipe, Santo António, Sao Tome and Principe
Fauna & Flora International, Cambridge, UK
L. Tavares
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon,
Portugal
D. T. Holyoak
Quinta da Cachopa, Cabeçudo, Portugal
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_16
407
408
M. Panisi et al.
five seashore species, São Tomé has 52 terrestrial (50% single-island endemic) and
seven seashore species, Annobón has 14 terrestrial species (50% single-island
endemic), 3 species are endemic to Príncipe and São Tomé, and 2 are endemic to
the three islands. The islands were colonized by diverse “clades” arriving from
continental Africa, which is consistent with biogeographical patterns from other
taxonomic groups. However, in line with Mollusca dispersal limitations, inter-island
colonization seems to be less frequent, while there are multiple cases of speciation
within the same island. The land snail assemblage on São Tomé seems to be strongly
structured by land-use type: endemics being associated mostly with forest and
non-endemics to anthropogenically modified environments. Only 13 species have
been recorded across the altitudinal range of São Tomé, suggesting altitude is also
essential to determining species distribution. Habitat loss and introduced species are
important threats, but so far, only the endemic Archachatina bicarinata has been
listed as threatened. Despite recent progress, further studies are still needed to better
understand this unique fauna and inform conservation strategies.
Keywords Africa · Checklist · Conservation · Endemism · Malacofauna ·
Taxonomy
Introduction
This chapter reviews what is known of the terrestrial Mollusca (Gastropoda) of
the three oceanic islands in the Gulf of Guinea, located close to the Equator, off the
Atlantic coast of central Africa: Príncipe, São Tomé (together constituting the
Democratic Republic of São Tomé and Príncipe - STP), and Annobón (part of the
Republic of Equatorial Guinea). Bioko (also part of Equatorial Guinea) is a continental island, and thus it has not been included. The few Mollusca living in
freshwater habitats on STP (Brown 1991; Simões 1992) are not covered, whereas
seashore species are briefly considered. Taxonomy and nomenclature follow a recent
checklist for STP (Holyoak et al. 2020) and a similar revised list for Annobón
(Appendix).
All three islands arose during the Tertiary, forming part of the extensive Cameroon Line of volcanos. The maximum age ranges from approximately 15 Ma on São
Tomé and 6 Ma on Annobón to 31 Ma on Príncipe. The latter is also the only island
without signs of active volcanism in the last 3 Ma (Fitton and Dunlop 1985). They all
retain large proportions of rugged topography, reaching maximum altitudes of
2024 m on São Tomé, 948 m on Príncipe, and 598 m on Annobón. They are formed
mainly of igneous rocks and have relatively small areas of uplifted conglomerates,
sandstones, and shales. The presence of large areas of volcanic bedrock and the
absence of uplifted limestone produced calcium-poor soils that limit the abundance
of land snails. It is also unsurprising that fossil terrestrial Mollusca are unknown,
considering the scarcity of subaerial calcareous sediments.
The islands rise from oceanic depths, and thus, unlike Bioko, they have never
been joined to continental Africa. When ocean levels were lower, during some
16
Terrestrial Mollusca of the Gulf of Guinea Oceanic Islands
409
periods of the Pleistocene, the islands would have had larger land areas than at
present, with maxima estimated as 144 km2 for Annobón (now 17 km2), 1480 km2
for São Tomé (now 857 km2), and 1179 km2 for Príncipe (now 139 km2). Nevertheless, their remoteness from the continent was not significantly reduced (Jones and
Tye 2006; Norder et al. 2018) and colonization by land mollusks clearly involved
long-distance overseas dispersal.
When human colonization began in the late fifteenth century, the islands were
almost entirely covered by tropical rainforest, associated with hot equatorial climates
and rainfall occurring throughout the year in most areas (Loboch 1962; Bredero et al.
1977). The native lowland forests are floristically distinct from montane and mist
forest occurring at higher altitudes (Exell 1944). Much of the lowland forest has been
replaced by cultivation, notably for sugar cane in the sixteenth century and coffee
and cocoa during the nineteenth and early twentieth centuries (Exell 1944). Therefore, it is quite likely that native land mollusk species became extinct and that alien
species arrived before the first thorough scientific assessments of the islands’
malacofauna took place. Moreover, the islands hold a remarkable number of introduced plants (Figueiredo et al. 2011) and mammal species (Dutton 1994), partly due
to being regularly visited by ships involved in the Atlantic triangular trade
(Eyzaguirre 1986).
A few large land-snail shells from the islands reached Europe in the 1700s,
resulting in the naming of Atopocochlis exaratus (Fig. 16.1.6), Columna columna
(Müller 1774), and Archachatina bicarinata (Bruguiére 1792—Fig. 16.1.5). However, the first detailed study of the land Mollusca of the region was made by Rang
(1831), a commander in the French navy who stayed on Príncipe for a month,
allowing him to make careful descriptions of living snails and their habitats, as
well as collecting specimens. Soon afterward, Morelet (e.g., 1848, 1858, 1860, 1868,
1873) named and described specimens brought back to Europe from Príncipe and
São Tomé by voyagers, including Dr. Friedrich Welwitsch. Dr. Dohrn spent
6 months on Príncipe in 1865 with John Keulemans, collecting birds and snails,
which he later described (Dohrn 1866a). Dohrn also named the original material of
(Apothapsia) thomensis (Fig. 16.1.4) from São Tomé (Dohrn 1866b). Dohrn’s slug
specimens were studied by Heynemann (1868). Unfortunately, Dohrn’s main collection was destroyed during the bombing of the Szczecin museum, Poland (Dance
1986).
Greeff (1882) named and described specimens collected during thorough fieldwork on both Príncipe and São Tomé in 1879–1880, including Thyrophorella
thomensis (Fig. 16.1c) and Pyrgina umbilicata as new species in new genera and
(Aporachis) dohrni and (A.) hispida as new species. Nobre (1886, 1891, 1894)
reported on collections made on São Tomé by Adolpho Möller and capitão Castro.
Francisco Newton was employed to collect on all three islands: from November
19, 1892, to early January 1893, he made the first detailed collections on Annobón,
covering birds, mollusks, and more. Girard (1893a, b, 1894, 1895) named and
described his land mollusk collections, including most Annobón endemics. Unfortunately, part of Girard’s work on Annobón remained unpublished, including
Figs. 1–11 (1894) and the newly discovered Dendrolimax newtoni (Ortiz de Zaráte
410
M. Panisi et al.
Fig. 16.1 Photographs of some living terrestrial Mollusca of Príncipe and São Tomé: (1)
Pseudoveronicella thomensis, ca 30 mm, endemic to São Tomé; (2) Pseudoveronicella forcarti,
ca 25 mm, endemic to Príncipe; (3) Thyrophorella thomensis, shell breadth ca 9 mm, endemic to
São Tomé; (4) Apothapsia thomensis, shell breadth ca 12 mm, endemic to São Tomé; (5)
Archachatina bicarinata, shell length ca 155 mm, endemic to Príncipe and São Tomé; (6)
Atopocochlis exaratus, juvenile and adult, shell lengths ca 25 and 45 mm, endemic to São Tomé;
(7) Archachatina marginata, shell length ca 105 mm, introduced on Príncipe and São Tomé; (8)
Limicolaria flammea, shell length ca 22 mm, introduced on São Tomé. Photo credits: (1, 3) David
Holyoak, (2) Frazer Sinclair and Fundação Príncipe, (4–8) Vasco Pissarra and Forest Giants Project.
Not all the species represented in the figure were photographed in their natural habitat
16
Terrestrial Mollusca of the Gulf of Guinea Oceanic Islands
411
and Alvarez 1960) was left as a nomen nudum. Girard’s specimens and probably
many from Nobre were lost in the fire of March 1978, at the National Museum of
Natural History in Lisbon (now integrated in the National Museum of Natural
History and Science—MUHNAC). Crosse (1868, 1888a, b) wrote on the land
mollusk faunas of STP, adding little that was really new, apart from some detailed
descriptions and occasional interpretation of problems.
Germain, based at the Paris Museum, wrote a series of detailed and often wellillustrated papers on the mollusks of west and central Africa, including the Gulf of
Guinea islands. He examined collections by Charles Gravier from São Tomé
(Germain 1908), and by Leonardo Fea, made available by the Genoa Museum
(Príncipe: Germain 1912a, b, 1915; Annobón: Germain 1916). The proportion of
undescribed species he found was low compared to that in earlier accounts.
After a long gap in the publication of new work, Ortiz de Zaráte and Alvarez
(1960) described the results of the Peris-Alvarez Expedition to Annobón, including
several new records and the valid naming of Dendrolimax newtoni. Gascoigne
(1994a, b) lived on São Tomé for many years, publishing several molluscan faunistic
accounts, including new records, and donated specimens he collected to the Natural
History Museum of London (NHMUK).
We began studying the land mollusks of the islands during a visit to São Tomé in
December 2013, which resulted in a review of the taxonomy of Rhysotina (Holyoak
and Holyoak 2016). Subsequent work included the study of Archachatina on São
Tomé (Panisi 2017) and Príncipe (Fundação Príncipe 2019). In November and
December 2018, an expedition team made large selective collections of specimens
and contributed to the publication of an annotated checklist that named 13 hitherto
undescribed species and 6 new genera and gave 11 other new island distributional
records (Holyoak et al. 2020). An expedition team in October and November 2019
studied the distribution and habitat associations of the species occurring on São
Tomé. There is ongoing work on systematics, ecology and conservation of land
mollusks on both islands (Fundação Príncipe 2019; Panisi et al. 2020; Tavares
2021). Since the systematics of land Mollusca has been reviewed in detail very
recently, this chapter will summarize malacological exploration and existing diversity, discussing zoogeography, evolution, ecology, and conservation to identify
some of the persisting knowledge gaps.
Species Diversity
General Patterns
The list of terrestrial mollusks for the oceanic islands of the Gulf of Guinea will
surely change with future research, including new records and a better understanding
of species relationships and endemism. Nevertheless, a fully satisfactory taxonomy
must await improved knowledge of the malacofauna of continental Africa.
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M. Panisi et al.
Table 16.1 Numbers of species of terrestrial mollusks known to occur in the Gulf of Guinea
oceanic islands (Holyoak et al. 2020—Appendix)
Príncipe
São
Tomé
Annobón
Total
Single-island
endemics
24 (60%)
26 (50%)
Shared
endemics
5 (13%)
5 (10%)
Native
9 (22%)
15 (28%)
Introduced
2 (5%)
6 (12%)
Total
terrestrial
40
52
Seashore
5
7
7 (50%)
57 (66%)
2 (14%)
5 (6%)
4 (29%)
18 (20%)
1 (7%)
7 (8%)
14
87
0
9
Percentages were calculated excluding seashore species since these have very distinct ecology and
life-histories
Currently, the malacofauna for the islands includes 9 seashore and 87 strictly land
species (Appendix and Table 16.1).
Seashore species belong to Truncatellidae, Assimineidae, Ellobiidae, and
Onchidiidae, and occur solely on upper levels of marine beaches. Little is known
about this group in the region, but all species are assumed to be native. Only five taxa
have been identified to the species level, and there are no records of seashore species
from Annobón. The number of accepted species in this group will likely change with
further work, especially considering that they have received little sampling effort.
Land species comprise 5 Cyclophoridae or Maizaniidae, 4 Veronicellidae,
31 Achatinidae, 1 Micractaeonidae, 16 Streptaxidae, 1 Punctidae, 1 Charopidae,
1 Succineidae, 2 Cerastidae, 2 Gastrocoptidae, 1 Truncatellinidae, 2 Valloniidae,
1 Agriolimacidae, 2 Euconulidae, 2 Helicarionidae, 14 Urocyclidae, and 1 Helicidae.
All have an external shell, apart from all 4 Veronicellidae, all 3 Dendrolimax
(Urocyclidae) and Deroceras laeve (Agriolimacidae). The islands hold high proportions of endemic taxa: 57 (66%) species are considered single-island endemics,
and 5 (6%) shared endemics (Table 16.1). Endemic species comprise all
5 Cyclophoridae or Maizaniidae, 2 Veronicellidae (Pseudoveronicella thomensis
from São Tomé and P. forcarti from Príncipe—Fig. 16.1.1–2), 23 Achatinidae,
14 Streptaxidae, 2 Gastrocoptidae, 1 Truncatellinidae, 1 Euconulidae, and
12 Urocyclidae. Compared to the African mainland taxa, endemic Achatinidae
include a disproportionately high number of species with sinistral shells, namely
A. bicarinata, all three Columna species and Thyrophorella thomensis.
No family is recognized as endemic to the islands since Thyrophorella was shown
to be a close relative of Pyrgina and placed within Achatinidae, subfamily
Thyrophorellinae (Fontanilla et al. 2017). Rhysotininae is still regarded as an
endemic subfamily, with molecular support (Holyoak and Holyoak 2016). Currently, 14 genera are considered endemic to the islands, holding 24 species (Holyoak
et al. 2020). These include distinctive taxa that are likely to be genuinely endemic,
such as Columna, Thyrophorella, and Rhysotina, and the pairs of genera Bocageia
and Petriola, and Pyrgina and Thomea. Both these pairs are distinctive, but each pair
might be reduced to a single genus. Newly named genera containing only endemic
species (Aporachis, Apothapsia, Principicochlea, Thomithapsia, and
Thomitrochoidea), as well as the endemic Sphinctostrema (Girard 1894), and the
16
Terrestrial Mollusca of the Gulf of Guinea Oceanic Islands
413
São Tomé endemic Thomeomaizania, are less likely to be truly endemic. The same
may be true for near-endemic Atopocochlis, which currently holds only two species:
A. exaratus endemic to São Tomé and A. auripigmentum endemic to Bioko
(Wronski et al. 2014). On the other hand, the Príncipe endemic Cyathopoma
inexspectata might warrant having its own genus (Holyoak et al. 2020).
Land snails and slugs include seven introduced species, five recently reported as
new records for the area (Holyoak et al. 2020). Furthermore, it is unclear if the
widespread Striosubulina striatella, originally described from Príncipe, is native or
introduced on the islands. Other non-endemic species are considered native by
default, but they might have been introduced before the first extensive malacological
assessments of the islands.
Islands Accounts
Príncipe has 5 seashore species and 40 terrestrial species, including 1 Cyclophoridae
or Maizaniidae (recently described), 3 Veronicellidae, 17 Achatinidae,
9 Streptaxidae, 1 Succinidae, 2 Cerastidae, 1 Euconulidae, and 6 Urocyclidae
(Appendix). The island has 24 endemic species, plus 3 shared with São Tomé
(A. bicarinata, Opeas pauper, and Streptostele moreletiana) and 2 shared with
both São Tomé and Annobón (O. dohrni and O. greeffi). Of all endemic species,
8 (1 Cyclophoridae or Maizaniidae, 1 Veronicellidae, 3 Achatinidae, and
3 Urocyclidae) are the sole representatives of their genus on the island. Other genera
are represented by multiple species: Principitrochoidea (Urocyclidae) has 2 islandendemic species, Columna and Subulina (both Achatinidae) have 3, Opeas
(Achatinidae) and Gulella (Streptaxidae) have 4 and Streptostele (Streptaxidae)
has 5. Archachatina marginata (Fig. 16.1.7) and Laevicaulis alte are the only
confirmed introduced species, and their presence was only reported recently
(Holyoak et al. 2020).
São Tomé has 7 seashore species and 52 terrestrial species, comprising
4 Cyclophoridae or Maizaniidae, 3 Veronicellidae, 21 Achatinidae,
1 Micractaeonidae, 2 Streptaxidae, 1 Punctidae, 1 Charopidae, 1 Succineidae,
2 Cerastidae, 1 Gastrocoptidae, 1 Truncatellinidae, 2 Valloniidae, 1 Agriolimacidae,
2 Euconulidae, 2 Helicarionidae, 6 Urocyclidae, and 1 Helicidae (Appendix). The
island has 26 endemic species, plus 5 shared with at least one other nearby oceanic
island. Of all endemic species, 16 are the sole representatives of their genus on the
island (spread across 8 families). Other genera are represented by multiple species:
Thomeaonaizania (Cyclophoridae or Maizaniidae), Aporachis (Achatinidae), and
Apothapsia (Helicarionidae) have 2 island-endemic species, and Petriola, Opeas
(both Achatinidae) and Rhysotina (Urocyclidae) have 3. A. marginata is known to
have been introduced on São Tomé by the mid-twentieth century (Gascoigne
1994a), but it is now widespread (Panisi 2017) and an important source of protein
for people (Carvalho et al. 2015). Recently, 5 other introduced mollusks have been
reported for the island, many of which already seem to be relatively widespread,
others at least locally abundant (Holyoak et al. 2020).
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M. Panisi et al.
Annobón has the least scientifically documented malacofauna of the oceanic Gulf
of Guinea islands, since it is seldom visited by researchers. It is likely that further
visits will substantially increase the species list. Currently, it is known to host
14 terrestrial mollusks, comprising 4 Achatinidae, 6 Streptaxidae, 1 Succineidae,
1 Gastrocoptidae, and 2 Urocyclide (Appendix). The island has 7 endemic species,
plus 2 that are shared with São Tomé and Príncipe. Of all endemic species,
Gastrocopta (Gastrocoptidae) and Dendrolimax (Urocyclidae) are represented by a
single species. By contrast, Opeas (Achatinidae) and Sphinctostrema (Streptaxidae)
are represented by 2, and Gulella (Streptaxidae) by 3. Allopeas gracile is the only
introduced species confirmed on Annobón, despite an unsubstantiated record of a
large species of Achatinidae being used locally for food, which is likely to correspond to the invasive A. marginata (Brendan Sloan, pers. comm.).
An imbalance in the taxonomic composition between the faunas of the different
islands is immediately apparent. São Tomé has very few Streptaxidae (2 species),
and these are uncommon and inconspicuous elements in snail faunas on that island.
By contrast, Príncipe has 9 streptaxid species, and Annobón has 6, and the family is
conspicuous and common in both of those faunas. Since these streptaxids are all
carnivorous, this leads to odd faunal assemblages, at least on Príncipe, where the
commonest snails in ground-litter of native forests at some sites are all predators,
albeit presumably eating mostly non-molluscan invertebrates. The few carnivorous
land snail species on São Tomé might be partly explained by a conspicuous presence
of land flatworms, which presumably originated from a single radiation (Matthias
Neumann, pers. comm.). At least 3 out of the 5 recently described endemic
Othelosoma species were seen feeding on land snails (Neumann 2016), and it is
known that several species remain undescribed (Matthias Neumann, pers. comm.).
Conversely, geoplanids do not seem to occur or are certainly much less conspicuous
on Príncipe (Matthias Neumann, pers. comm.), which might have influenced the
differences in composition of land snail faunas on the two islands. Future studies are
needed to test this hypothesis.
Other taxonomic imbalance results from the presence of Rhysotina and Petriola
(each genus with 3 species) only on São Tomé, whereas Príncipe alone has the genus
Principitrochoidea (3 species). These taxonomic imbalances between islands likely
result in part from in situ speciation in several of the genera as well as differing
outcomes from chance colonization by ancestral species from different families
present on the African mainland. Similar unbalanced patterns occur on other oceanic
archipelagoes. For instance, the Canary Islands have many endemic Enidae, while
the Madeiran Islands have no representatives of the family but instead have endemic
radiations of Clausiliidae (lacking in Canary Islands) and numerous endemic
Ferussaciidae (present only marginally in Canary Islands) (Bank et al. 2002). Chance
events in early colonization and establishment success likewise appear to be the best
explanations for the taxonomic imbalance of the snail faunas of those archipelagos,
rather than any differences in island environments or faunas of their continental
source areas.
16
Terrestrial Mollusca of the Gulf of Guinea Oceanic Islands
415
Biogeographical Considerations
São Tomé is much larger than Príncipe, but is only marginally more species-rich,
both in total numbers of species and endemics. This might be explained by the two
islands having similar sizes during glaciation peaks and Príncipe being much older
(Fernández-Palacios et al. 2016). Considering its small size, Annobón is also
remarkably rich, especially in endemic species, which might be explained by the
combination of old age and larger area during the glaciations.
Many endemic species seem to have resulted from independent colonization
events, based on the observation that there are many genera represented by single
island endemics. Taking into consideration that the distance between islands is
similar to the distance to the continent, most dispersal events likely occurred directly
from the mainland rather than between islands. This pattern of independent colonization is further supported by the distinctiveness of the faunas of each island and by
the small number of “shared endemic” species. On that basis, it has been questioned
if A. bicarinata is truly endemic to both Príncipe and São Tomé, or if it might have
been introduced to one of the islands (Gascoigne 1994b; Panisi et al. 2020),
especially considering that it would have been challenging for such a large snail to
disperse naturally between islands. It has been reported as an important food source
since the end of the nineteenth century (Moller 1894), providing a reason for
intentional introduction on one of the islands, which could be clarified using
molecular techniques (Panisi et al. 2020).
Large endemic land snails are usually absent or rare on oceanic islands. Although
large endemic snails are prominent in the faunas of some of the largest islands such
as Madagascar and Sri Lanka, those are better interpreted biogeographically as
remnants of fragmented continental faunas. Among the few examples on truly
oceanic islands, the large Pseudocampylaea lowii (A. Férussac, 1835) of Porto
Santo (Madeiran Islands) is related to the considerably smaller endemic
P. portosanctana (G.B. Sowerby I, 1824) of the same island, and both can be
regarded as products of the large in situ radiation of smaller Geomitridae since the
late Tertiary on the Madeiran Islands (D. Holyoak, unpublished). The massive
A. bicarinata endemic on the Gulf of Guinea islands, by contrast, is most certainly
derived from large congeneric relatives in continental Africa. Other large
Achatinidae of the islands also have their apparent affinities with relatively largeshelled continental genera of the family. Thus, the overseas dispersal of large-shelled
progenitors to the island species may have been enabled by the location of the Gulf
of Guinea islands within an embayment of the coast of central Africa into which
large rivers flow. Zoogeographers have postulated that “rafts” of floating debris have
occasionally reached the islands, presumably accounting for the endemic frogs and
caecilians on the islands (Measey et al. 2007). This hypothesis could also explain the
colonization of the islands by large-bodied land snails, and presumably also
Pseudoveronicella and Dendrolimax slugs.
Despite frequent colonization being vital to explain the origin of many endemics,
there is strong evidence that others evolved from speciation in situ, namely the
Columna and Streptostele species of Príncipe and the Petriola and Rhysotina of São
416
M. Panisi et al.
Tomé. Molecular studies of better-known taxa, such as birds, amphibians, and
reptiles, have revealed that independent colonization events from the continent
might be the dominant pattern to explain the origin of endemic species in the
archipelago (Ceríaco et al. 2017; Valente et al. 2020). Nevertheless, radiations across
islands also occur (Melo et al. 2011; Bell et al. 2015) and as more molecular studies
become available, our understanding of the dominant patterns may change.
Habitat Associations
Recent surveys carried out on Príncipe and São Tomé have enhanced our understanding of the terrestrial Mollusca and their habitats (Appendix). These surveys
consisted of a series of observations in a range of diverse molluscan habitats
(Fundação Príncipe 2019; Holyoak et al. 2020) and an additional stratified survey
across three different regions and four land-use types on São Tomé (Tavares 2021).
No recent surveys have taken place on Annobón, and the data available on the
terrestrial Mollusca of this island consists of a few records with scant information on
the habitat of each species.
On São Tomé, the presence and abundance of 33 non-seashore species were
analyzed across four land-use categories (Tavares 2021), reflecting a gradient of
increasing forest degradation: native forest, secondary forest, shade plantations, and
non-forested areas. Non-forested areas have lower local species richness (alpha
diversity) than shade plantation and secondary forest, while native forests have
intermediate values. However, due to lower distinctiveness between sites (beta
diversity), shade plantations have the lowest overall species richness (Appendix).
Secondary forest and shade plantation show a higher average abundance than native
forest and non-forested areas. According to the general patterns of richness and
abundance, endemic species tend to be associated with forests, while non-endemics
tend to be associated with degraded areas.
Most species on São Tomé occur in more than one land-use type. Only the
endemic O. pauper, the native Pseudopeas crossei, and the introduced Limicolaria
flammea (Fig. 16.1.8) and L. alte were found exclusively in non-forested areas.
Twenty-one species were found only in forested areas, 18 of which were only in
forests (i.e., not in shade plantantions). Ten of them occur both in secondary or
native forest, half of these being endemic, all achatinids: A. bicarinata, both
Aporachis species, P. umbilicata and Thomea newtoni. Five species were recorded
only in secondary forest: Gastrocopta nobrei, Truncatellina thomensis, Pupisoma
dioscoricola, Afroditropis molleri and Maizania furadana. Two species were
recorded exclusively in native forest, both single-island endemics: Nothapalus
solitarius and Thomeomaizania gascoignei. Thirteen species were recorded in all
the four land-use types, including two introduced species, A. marginata and
Deroceras laeve, and eight endemic species: all three Petriola species, both
Apothapsia species, Dendrolimax greeffi and all three Rhysotina species. Most of
these are widespread and abundant across habitats, as with Apothapsia thomensis,
which is probably the most common land snail in wooded habitats on the island, and
16
Terrestrial Mollusca of the Gulf of Guinea Oceanic Islands
417
the introduced A. marginata, which is widespread across degraded habitats and very
abundant in shade plantations and secondary forest (Panisi 2017).
Concerning altitude, 13 species were recorded across a wide altitudinal range
(Appendix), from lowland (below 800 m a.s.l) to mist forests (above 1400 m a.s.l.,
Exell 1944). Nine species were found exclusively in lowland, 8 exclusively in
montane regions (between 800 and 1400 m a.s.l.), 15 in both lowland and montane
regions, and 3 in montane and mist forests. Introduced species occur mainly at lower
altitudes, while endemic species richness persists across all altitudes. Thirty-seven
species occur in the lowlands, including 5 introduced and 23 endemic (62%
endemic). In montane regions, 39 species were recorded, including 4 introduced
and 25 endemic (64%). Mist forests hold 16 species, the lowest species richness, but
they have only one introduced species, Deroceras laeve, and 13 endemics, the
highest proportion across altitudinal zones (81%).
São Tomé land snails and slugs are associated with a variety of strata (Appendix).
Most species live mainly on or near the ground, namely on leaf-litter, among tree
buttress roots, beneath fallen wood, under rocks, or on shell debris. Live snails often
congregate on anvils of the São Tomé Thrush Turdus olivaceofuscus (Jones and Tye
2006), searching for calcium (Holyoak et al. 2020). Few species are found on leaves,
exceptions include A. thomensis, P. thomensis, and A. exaratus. Some species are
found in waterfall spray-zones, such as the endemic A. hispida, both Pupisoma
species and other small native species.
On Príncipe, recent mollusk sampling has been less extensive and less systematic
than on São Tomé, including ca 30 locations selected ad hoc across a range of habitat
types (Fundação Príncipe 2019; Holyoak et al. 2020). Surveys between 2012 and
2020 have confirmed the continued presence of 30 out of the 40 non-seashore
species known from Príncipe. Additional attention has been given to A. bicarinata,
with over 100 records made between 2018 and 2020, and an ongoing monitoring and
ecological study on both islands (Fauna & Flora International and Fundação Príncipe
2019; Fundação Príncipe 2019; Panisi et al. 2020).
Although the sampling effort is more limited on Príncipe, some patterns of habitat
association appear broadly similar to those described for São Tomé. Sites at the
transition between forested land-use types seem to hold high species richness, and
non-native species seem to prefer disturbed areas, while the endemics prefer forests.
At higher altitudes, species richness is low, but the proportion of endemics is high.
This includes the recently described Principicochlea tenuitesta, which is known only
from the vicinities of the highest point of the island, Pico Príncipe (Fundação
Príncipe 2019; Holyoak et al. 2020).
Most species documented on Príncipe were found within leaf litter on the ground.
Tree canopies were not sampled, although fallen shells have been collected from the
ground. Sieving of leaf litter was only attempted for a small subset of sampling
locations but revealed distinct species and may yield interesting further novelties
(Holyoak et al. 2020). Live specimens, particularly those of Gulella crystallum, are
often apparent in shell debris at Blue-breasted Kingfisher Halcyon malimbica anvils
and empty A. bicarinata shells. Several species were conspicuous on understorey
foliage, especially in some higher altitude sites where the endemic P. forcati and
P. tenuitesta are locally abundant (Appendix).
418
M. Panisi et al.
The low densities of forest-floor snail faunas recorded on both islands, and
especially on Príncipe, deserve future studies but might be linked to calcium
shortages in the topsoil and leaf litter (Juřičková et al. 2008). This would explain
the high concentrations of land snails at the anvil sites of the São Tomé Thrush and
Blue-breasted Kingfisher.
Conservation
Habitat loss and introduced species seem to be key threats to native land snails and
slugs on the oceanic islands of the Gulf of Guinea, as is the case for most animal taxa
on oceanic islands (IUCN 2020), and notably for island snail species (Chiba and
Cowie 2016). Habitat loss on these islands is strongly linked to agricultural expansion and intensification, including horticulture and forest gardens to supply the local
markets, and export cash crops, such as cocoa, oil palm, and coffee. Additional
factors linked to habitat loss include increased use of fire, logging, mining, infrastructure development to support urban and tourism expansion, livestock and
expanding silviculture, with products such as oil palm wine and medicinal plants
(Oyono et al. 2014).
The effect of introduced species on the native malacofauna of these islands is less
well understood, but the introduction of many mammal (Dutton 1994) and plant
species (Figueiredo et al. 2011) might have detrimental impacts on the general
grounds that they affect ecosystem functioning. For instance, feral pigs and cows
feed on understorey plants and revolve the soil, disturbing key forest habitat for
some native land snail and slug species that evolved in the absence of large terrestrial
animals. Introduced species might also have direct effects through predation or
competition (Panisi 2017). Most introduced mollusks seem to avoid forests, where
most native species occur. It is nevertheless hard to assess the effect of introduced
mollusks, since it might be minimal if they have distinct habitats (Tavares 2021—
Appendix), or not so minimal if they are excluding native species from the more
degraded ecosystems. The fast expansion of the introduced A. marginata seems to be
linked to the decline of A. bicarinata, through a process that remains poorly
understood but might involve direct competition and introduced diseases (Panisi
and de Lima 2022). Additionally, A. bicarinata is the only native land snail species
that might be affected by overexploitation, as it is collected for food and traditional
medicine. Despite a steep population decline on both islands (Dallimer and Melo
2010; Panisi 2017), overexploitation continues to be an issue due to the higher
commercial value of each snail individual when compared to the widespread and
abundant A. marginata, but it is currently more recognized by people than the
endemic species (Panisi et al. 2022a).
The malacofauna might also be affected by pollution, given the widespread use of
pesticides to prevent malaria. Agricultural chemicals might also be a problem in São
Tomé, but less so in Príncipe, where the import of agricultural chemicals is limited
(Ministry of Public Works, Infrastructure, Natural Resources and Environment
2019). Finally, climate change is also a potential threat, especially as many of the
16
Terrestrial Mollusca of the Gulf of Guinea Oceanic Islands
419
endemic mollusk species have restricted altitudinal ranges and specific habitat
associations (Holyoak et al. 2020—Appendix).
Considering that at least some of these threats might affect whole populations,
either quickly in the near future or more pervasively in the longer term, many of the
mollusks endemic to Príncipe, São Tomé, and Annobón might go extinct due to
anthropogenic factors, even if specific conservation measures are implemented. This
has been the case in many other oceanic islands across the globe (Chiba and Cowie
2016), and notably in the Pacific (Lydeard et al. 2004). Therefore, it is vital that we
act quickly to protect these species. Protecting the remaining native forest and
additional vital habitats for native fauna is the single most important measure to
secure the future of these species. In this regard, all three islands have significant
proportions of their territory dedicated to biodiversity conservation (UNEP-WCMC
and IUCN 2020), which are predicted to expand soon (BirdLife 2019), even though
enforcement of existing protected areas remains weak (Lima et al. 2017). Additionally, it is also vital to improve our understanding of more pervasive threats, such as
invasive species and climate change, and our knowledge of the ecology of native
mollusk species, which will be key to design species-specific conservation measures.
Despite the remarkable number of endemic species, many remain notoriously
scarce in collections (Holyoak et al. 2020; Tavares 2021), and A.bicarinata is the
only endemic species listed as threatened for the islands (IUCN 2020). It is currently
classified as Vulnerable, although an updated assessment might result in uplisting to
Endangered (Panisi et al. 2022b). T. thomensis, P. umbilicata, and T. newtoni have
also been assessed but were all classified as Data Deficient (IUCN 2020). All these
species were assessed in 1996, and an update is certainly in order, considering that
recent surveys have greatly improved our knowledge on the taxonomy, ecology, and
threats to these species. Even if most species are to remain “Data Deficient,” the
information available to support classification has greatly improved, which might
improve recognition of the importance of the malacofauna of these islands, and help
identify the species that are at greater risk of extinction.
Concluding Remarks
Recent surveys (Holyoak et al. 2020) have added 13 newly described species,
6 microgastropods and 6 introduced species to the STP list of terrestrial mollusks.
They have also enabled confirmation of old records, such as the continued presence
of Gulella joubini on Príncipe, which was hitherto known only from its 1912
holotype. Five of the recently named species are known from unique specimens.
Two undescribed forms that will be new to Príncipe require the collection of
complete adult specimens. Based on these considerations, future research will
undoubtedly yield novelties and should focus on overlooked parts of the indigenous
fauna, namely microgastropods, Annobón, and undersampled regions and habitats,
especially those that are less accessible.
420
M. Panisi et al.
Almost all taxonomy on the land Mollusca of the oceanic islands of the Gulf of
Guinea is based on conventional comparative studies of shell form, sometimes
supplemented by genital anatomy. As a result, problems of species identification
and delimitation have been frequent. Some persist due to insufficient information on
nominal species from the African continent, where mollusk collections are often
even sparser than from these islands. DNA sequence data are often valuable to
elucidate molluscan phylogenies. For instance, genetic data have led to the inclusion
of the formerly recognized family Subulinidae in the broadly defined Achatinidae
(Fontanilla et al. 2017). However, DNA sequencing has not yet been widely used on
species from tropical Africa, where it would surely help clarify the phylogenetic and
biogeographical relationships of this rich and complex malacofauna.
Future research should also focus on the ecology of endemic species, which will
be vital to support conservation initiatives. The ongoing decline and current scarcity
of charismatic big species, such as A. bicarinata on São Tomé and Príncipe and the
genus Columna on Príncipe are starting to be recognized as conservation priorities.
For example, A. bicarinata has been widely used as a flagship for the protection of
the unique malacofauna of São Tomé and Príncipe, and even for the conservation of
their endemic-rich forests (Panisi et al. 2020; Panisi et al. 2022b). Still, information
on many other endemic species remains scant. The unique malacofauna of Príncipe,
São Tomé, and Annobón has been little studied for decades, but we hope that recent
findings will promote a new wave of curiosity about this exceptional diversity and
that it is translated into practical measures for the protection of the endemic species
and their habitats.
Acknowledgments Fieldwork on Príncipe was led by Fundação Príncipe in partnership with the
Regional Government and the Parque Natural do Príncipe. Participants included Ayres Pedronho,
Aramis Andrade, Emanuel Bettencourt, and Davide Dias, through Fundação Príncipe’s project
Understanding the Remarkable Biodiversity of Príncipe Island –funded by the French Facility for
Global Environment with co-funding from Critical Ecosystem Partnership Fund (CEPF-103778),
Flora & Fauna International, and HBD Príncipe. Fiedwork on Sao Tome was supported under the
umbrella of the Forest Giants Project by grants of the Mohamed bin Zayed Species Conservation
Fund (190521916), the National Geographic Society (EC-368E-18) and the Critical Ecosystem
Partnership Fund (109607) to Alisei Onlus NGO, in partnership with STP Direção das Florestas e
da Biodiversidade. Participants included Gabriel Oquiongo from Associação Monte Pico and Vasco
Pissarra from MARE. We also want to thank BirdLife International which provided logistic support
in STP through funding from ECOFAC6 and Rainforest Trust (4875). The Portuguese Government
through the “Fundação para a Ciência e a Tecnologia” (FCT/MCTES) funded MP’s PhD (PD/BD/
140814/2018), and cE3c (UID/BIA/00329/2021). The University of São Tomé and Príncipe was
the host institution for MP in STP. A special thanks to Professor Jorge Palmeirim for supervising
MP and LT. Permits to collect and export specimens were provided by Eng. Arlindo de Carvalho
and Eng. Lourenço de Jesus, former and current Directors of STP Direção Geral do Ambiente.
Finally, we want to acknowledge Dinarte Teixeira and Robert Cameron for their valuable reviews.
16
Terrestrial Mollusca of the Gulf of Guinea Oceanic Islands
421
Appendix
Checklist of terrestrial and seashore Mollusca species recorded from the Gulf of
Guinea oceanic islands
Higher Taxonomy
Species
P
ST
A
IUCN
Altitude
(m)
Family Cyclophoridae J.E. Gray, 1847 or Maizaniidae Tielecke, 1940
molleri (Nobre,
E
NE
860–885
Afroditropis
Bequaert & Clench, 1886)
1936
E
NE
216
Cyathopoma W. &
inexspectata
H. Blanford, 1861
G. Holyoak &
D. Holyoak,
2020
E
NE
240
Maizania
furadana
Bourguignat, 1889
G. Holyoak &
D. Holyoak,
2020
E
NE
1300–1416
gascoignei
Thomeomaizania
Bequaert & Clench, G. Holyoak &
D. Holyoak,
1936
2020
E
NE
96–1415
vandellii (Nobre,
1886)
Family Truncatellidae J.E. Gray, 1840
Truncatella Risso,
clathrus
N
NE
2
1826
R.T. Lowe, 1832
rostrata Gould,
N
NE
1847
Family Assimineidae H. Adams & A. Adams, 1856
Assiminea
sp.
NE
N
N
J. Fleming, 1828
Family Ellobiidae L. Pfeiffer, 1854
Melampus Montflavus (Gmelin,
NE
N
N
fort, 1810
1791)
NE
N
N
pusillus
(Gmelin, 1791)
2
sp.
N
NE
Pedipes
afer (Gmelin,
N
NE
A. Férussac, 1821
1791)
2
sp.
N
NE
Family Onchidiidae Rafinesque, 1815
sp.
N
NE
Onchidella
J.E. Gray, 1850
Family Veronicellidae J.E. Gray, 1840
24–1159
NE
I
I
Laevicaulis
alte
Simroth, 1919
(A. Férussac,
1822)
353–906
Pseudoveronicella
E
NE
forcarti
Germain, 1908
D. Holyoak,
G. Holyoak &
F. Sinclair, 2020
NE
N
N
liberiana
22–1028
(Gould, 1850)
Strata
NF
SF
SP
NN
0
+
0
0
L
1
0
0
0
P, L,
R
0
2
0
0
P, L
2
0
0
0
L, R,
S
1
2
0
1
L, H
0
0
0
+
H
0
0
0
+
H
0
0
0
+
H
0
0
0
+
H
0
0
0
+
H
H
0
0
0
0
0
0
+
+
H
0
0
0
+
H
0
0
0
+
L, S
0
+
0
1
P
2
0
0
0
P, L,
R, S
0
1
4
2
(continued)
422
Higher Taxonomy
M. Panisi et al.
Species
thomensis
(Girard, 1893)
Family Achatinidae Swainson, 1840
bicarinata
Archachatina
(Bruguière,
Albers, 1850
1792)
marginata
(Swainson,
1821)
exaratus
Atopocochlis
(O.F. Müller,
Crosse & Fischer,
1774)
1888
Columna Perry,
columna
1811
(O.F. Müller,
1774)
hainesi
L. Pfeiffer, 1856
leai Tryon, 1866
Lignus J.E. Gray,
alabaster (Rang,
1831)
1834
Limicolaria
flammea
Schumacher, 1817
(O.F. Müller,
1774)
Ischnoglessula
fuscidula
Pilsbry, 1919
(Morelet, 1858)
Striosubulina
striatella (Rang,
1831)
Thiele, 1933
Subulina Beck,
feai Germain,
1837
1912
moreleti Girard,
1893
newtoni Girard,
1893
sp.
Cecilioides
A. Férussac, 1814
Aporachis
dohrni (Greeff,
D. Holyoak, 2020
1882)
hispida (Greeff,
1882)
Bocageia Girard,
lotophaga
1893
(Morelet, 1848)
Nothapalus von
solitarius
Martens, 1897
G. Holyoak &
D. Holyoak,
2020
Petriola Dall, 1905 clavus
(L. Pfeiffer,
1864)
marmorea
(Reeve, 1850)
monticola
(Morelet, 1866)
Pyrgina Greeff,
umbilicata
1882
Greeff, 1882
IUCN
Altitude
(m)
Strata
NF
SF
SP
NN
E
NE
160–1418
P, L,
W
1
3
1
0
E
E
VU
43–1266
L, W,
R
2
1
0
0
I
I
NE
6–1327
L, W,
R, S
3
5
5
3
E
NE
101–928
P
+
1
1
0
E
NE
255–386
1
0
0
0
E
NE
E
E
NE
NE
58
24–386
0
+
0
+
+
+
0
0
I
NE
69–500
L, R,
S
0
0
0
1
N
N
NE
N
N
6–1490
L, W,
R, S
2
5
5
5
P
ST
A
N
NE
P
E
NE
E
NE
194–860
+
+
0
0
E
NE
281–860
+
0
0
0
2
1
0
0
+
1
0
0
+
0
0
0
N
NE
E
NE
959–1490
E
NE
885–1416
E
P, L,
R
R, F
NE
E
NE
1300
E
NE
124–1490
L, W,
R, S
5
4
3
2
E
NE
160–1490
3
4
3
1
E
NE
236–1477
3
3
1
1
E
DD
160–1418
L, W,
R, S
L, R,
S
L, W,
R
3
3
0
0
(continued)
16
Terrestrial Mollusca of the Gulf of Guinea Oceanic Islands
Higher Taxonomy
Species
newtoni Girard,
1893
gracile
(T. Hutton,
1834)
Opeas Albers,
dohrni (Girard,
1850
1893)
greeffi (Girard,
1893)
hannense (Rang,
1831)
pauper (Dohrn,
1866)
subpauper
Germain, 1912
Pseudopeas
crossei (Girard,
S. Putzeys, 1899
1893)
thomensis
Thyrophorella
Greeff, 1882
Girard, 1895
Family Micractaeonidae Schileyko, 1999
Micractaeon
koptawelilense
Verdcourt, 1993
(Germain, 1934)
Family Streptaxidae Gray, 1860
Gulella L. Pfeiffer,
azeitonae
D. Holyoak,
1856
G. Holyoak &
F. Sinclair, 2020
crystallum
(Morelet, 1848)
girardi (Kobelt,
1904)
insularis
(Girard, 1894)
joubini
(Germain, 1912)
nemoralis
(Germain, 1915)
sorghum
(Morelet, 1848)
annobonensis
Sphinctostrema
(Girard, 1894)
Girard, 1894
bocagei (Girard,
1894)
Streptostele Dohrn, abbreviata
1866
D. Holyoak,
G. Holyoak &
F. Sinclair, 2020
fastigiata
(Morelet, 1848)
folini (Morelet,
1858)
truncata
Germain, 1915
Streptostele (?)
feai Germain,
Dohrn, 1866
1912
P
Thomea Girard,
1893
Allopeas H. B.
Baker, 1935
ST
A
E
423
IUCN
Altitude
(m)
Strata
NF
SF
SP
NN
DD
181–1418
L
1
+
0
0
+
0
0
0
I
NE
E
E
E
NE
E
E
E
NE
240
N
NE
12–678
R
0
+
0
1
E
NE
74
R
0
0
0
1
+
0
0
+
E
E
N
NE
N
NE
240–1114
E
DD
323–1490
P, L,
S
3
1
0
1
N
NE
885–1290
L, R,
F
+
2
0
0
E
NE
194
0
+
0
0
E
NE
51–860
+
+
+
0
353–372
+
0
0
0
+
0
0
0
E
NE
E
NE
E
NE
E
E
NE
NE
E
NE
E
NE
E
NE
414
E
NE
24–860
L
2
2
2
0
E
NE
24–194
L
2
2
2
0
N
E
NE
NE
(continued)
424
Higher Taxonomy
M. Panisi et al.
Species
P
moreletiana
E
(Dohrn, 1866)
Tomostele Ancey,
musaecola
1885
(Morelet, 1860)
Family Punctidae Morse, 1864
Punctum Morse,
camerunense de
1864
Winter, 2017
Family Charopidae Hutton, 1884
Trachycystis
iredalei Preston,
Pilsbry, 1893
1912
Family Succineidae Beck, 1837
N
Quickia Odhner,
concisa
(Morelet, 1848)
1950
Family Cerastidae Wenz, 1923
N
burnayi (Dohrn,
Gittenedouardia
1866)
Bank &
Menkhorst, 2008
N
eminula
(Morelet, 1848)
Family Gastrocoptidae Pilsbry, 1918
Gastrocopta Wolannobonensis
laston, 1878
(Girard, 1894)
nobrei (Girard,
1893)
Family Truncatellinidae Steenberg, 1925
Truncatellina
thomensis
R.T. Lowe, 1852
D. Holyoak &
G. Holyoak,
2020
Family Valloniidae Morse, 1864
Pupisoma
dioscoricola
Stoliczka, 1873
(C.B. Adams,
1845)
harpula (Reinhardt, 1886)
Family Agriolimacidae H.Wagner, 1935
Deroceras
laeve
Rafinesque, 1820
(O.F. Müller,
1774)
Family Euconulidae H.B. Baker, 1928
roseus
Afroconulus Van
D. Holyoak &
Mol & van
G. Holyoak,
Bruggen, 1971
2020
Afropunctum
seminium
N
F. Haas, 1934
(Morelet, 1873)
Family Helicarionidae Bourguignat, 1877
moreleti
Apothapsia
(Germain, 1915)
D. Holyoak &
G. Holyoak, 2020
thomensis
(Dohrn, 1866)
Family Urocyclidae Simroth, 1889
greeffi Simroth,
Dendrolimax
1889
Heynemann, 1868
ST
A
IUCN
Altitude
(m)
Strata
NF
SF
SP
NN
R
0
+
0
1
E
NE
I
NE
74–181
N
NE
1254–1292
+
+
0
0
N
NE
1257–1288
+
+
0
0
NE
6–678
P, L
0
+
1
1
N
NE
5–398
P
+
+
1
0
N
NE
24–1477
P, L
1
1
1
1
L, W
0
+
0
0
0
+
0
0
N
N
E
NE
E
NE
6–126
E
NE
1254–1292
N
NE
197–1292
R, F
0
+
0
0
N
NE
885–1292
R, F
+
+
0
0
I
LC
254–1402
P, L,
R, S
1
1
1
2
E
NE
530–1353
P
0
1
0
1
N
NE
236–1400
P, R,
F
2
2
0
0
E
NE
22–1244
P, L
1
1
1
1
E
NE
6–1402
P, L,
W, R
5
5
5
4
E
NE
22–1343
P, L
+
1
1
1
(continued)
16
Terrestrial Mollusca of the Gulf of Guinea Oceanic Islands
Strata
NF
SF
SP
NN
NE
220–498
P
+
0
0
0
L, W,
R, S
L, R
4
3
2
2
1
3
3
2
heynemanni
Heynemann,
1868
newtoni A. Ortiz
de Zaráte &
Alvarez, 1960
hepatizon
(Gould, 1845)
sublaevis
G. Holyoak &
D. Holyoak,
2016
welwitschi
(Morelet, 1866)
dumeticola
(Dohrn, 1866)
E
E?
NE
tenuitesta
D. Holyoak,
G. Holyoak &
F. Sinclair, 2020
aglypta (Dohrn,
Principitrochoidea
1866)
D. Holyoak &
G. Holyoak, 2020
convexa
G. Holyoak,
D. Holyoak &
F. Sinclair, 2020
folini (Morelet,
1848)
Thomithapsia
bomsucessica
G. Holyoak &
D. Holyoak &
D. Holyoak,
G. Holyoak, 2020
2020
trindadensis
Thomitrochoidea
D. Holyoak &
D. Holyoak &
G. Holyoak,
G. Holyoak, 2020
2020
Trochozonites
adansoniae
Pfeffer, 1883
(Morelet, 1848)
Family Helicidae Rafinesque, 1815
Cornu Born, 1778
aspersum
(O.F. Müller,
1774)
E
Africarion
Godwin-Austen,
1883
Principicochlea
D. Holyoak &
G. Holyoak, 2020
A
Altitude
(m)
P
Rhysotina Ancey,
1887
ST
IUCN
Species
Higher Taxonomy
E
425
NE
E
NE
153–1477
E
NE
22–1199
E
NE
54–1323
L, W,
R, S
P
3
3
3
3
NE
860
P
+
0
0
0
E
NE
193–344
L
+
+
0
0
E
NE
24–375
P
+
+
0
+
N
NE
24–216
L
+
+
0
+
E
NE
418–1300
L, W
+
1
0
+
E
NE
22–900
P
+
1
1
0
821–1150
P
0
0
1
2
N
I
NE
LC
Species are listed as endemic (E), presumed autochthonous or native non-endemics (N) or introduced (I) in the island
(s) where they occur: Príncipe (P), São Tome (ST), and Annobón (A). See taxonomic comments in Holyoak et al. (2020).
Global conservation status is reported according to the IUCN Red List of Threatened Species: Not Evaluated (NE), Data
Deficient (DD), Vulnerable (VU), or Least Concern (LC). When available, habitat associations are provided, namely:
altitudinal ranges, strata where live specimens were collected [Live plant (P); Plant litter (L); Dead wood (W); Rocks (R);
Bare soil (S); Seashore (H); Waterfall spray-zone (F)], and relative abundance [Uncertain (+); No records (0); Rare (1);
Not common, but locally abundant (2); Common (3); Abundant (4); Very abundant (5)] for each land-use category
[Native forest (NF); Secondary forest (SF); Shade plantation (SP); Non-forested areas (NN)]
426
M. Panisi et al.
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Open Access This chapter is licensed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits use, sharing,
adaptation, distribution and reproduction in any medium or format, as long as you give appropriate
credit to the original author(s) and the source, provide a link to the Creative Commons license and
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the copyright holder.
Chapter 17
The Fishes of the Gulf of Guinea Oceanic
Islands
Luis M. da Costa, Hugulay Albuquerque Maia, and Armando J. Almeida
Abstract This chapter reviews the current knowledge of the marine (including
deep-sea species) and freshwater fishes of the Gulf of Guinea oceanic islands.
Some biogeographic and conservation considerations are also presented. A total of
1045 species are likely present in the region, including 107 Elasmobranchii (37 confirmed, 65 potential, and 5 erroneous), one confirmed Holocephali, and
937 Actinopteri species (515 confirmed, 385 potential, 32 erroneous, and 5 questionable). Most of the coastal species are shared with the surrounding African
continental shelf, while several species are amphi-Atlantic (present in both sides of
the Atlantic Ocean), and some species have sister-species in the western Atlantic. A
total of 15 species are endemic to the region, and 2 are introduced. Further studies are
still needed to better understand the ichthyofauna of the Gulf of Guinea oceanic
islands and help policymakers better define conservation and protection plans.
Supplementary Information The online version contains supplementary material available at
[https://doi.org/10.1007/978-3-031-06153-0_17].
L. M. da Costa (*)
MARE, Centro de Ciências do Mar e do Ambiente, Faculdade de Ciências, Universidade de
Lisboa, Lisbon, Portugal
Departamento de Zoologia e Antropologia (Museu Bocage), MUHNAC, Museu Nacional de
História Natural e da Ciência, Universidade de Lisboa, Lisbon, Portugal
Royal Museum for Central Africa (RMCA), Vertebrates Section, Ichthyology, Tervuren,
Belgium
H. A. Maia
Departamento de Ciências Naturais, da Vida e do Ambiente, Faculdade de Ciências e
Tecnologias, Universidade de São Tomé e Príncipe, São Tomé, Sao Tome and Principe
A. J. Almeida
MARE, Centro de Ciências do Mar e do Ambiente, Laboratório Marítimo da Guia, Faculdade de
Ciências, Universidade de Lisboa, Cascais, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon,
Portugal
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_17
431
432
L. M. da Costa et al.
Keywords Checklist · Conservation · Eastern Atlantic · Freshwater · Marine ·
Taxonomy
Introduction
The Gulf of Guinea Oceanic Islands (GGOI), Príncipe, São Tomé, and Annobón, are
oceanic islands located in the Tropical Eastern Atlantic. The GGOI are part of the
Cameroon Volcanic Line, an intraplate basalt in the ocean-continent boundary
region, ranging over 1600 km (Burke 2001; Elsheikh et al. 2014; Belay et al.
2019). All three GGOI are ideally located for fish diversity: close enough to the
African continent to host typical shelf region fish species, but also with a narrow
platform separated by seas with over 1500 m depth that provide coastal habitat to
several fishes. In addition, several currents contribute to coastal upwelling (Bakun
1978; Djakouré et al. 2017) and biological productivity (Binet 1997; Ukwe et al.
2006) for highly migratory offshore and deep-sea fish species. The GGOI are at the
crossroads of three major currents: one incoming (from west to east), the Guinea
Current (GC), and two outgoing (from east to west), the South Equatorial Current
(SEC) and the Gabon-Congo Undercurrent (Djakouré et al. 2014). The GC, sourcing
from the combination of the North Equatorial Countercurrent and the Canary
Current, flows east along the western coast of Africa (from Sierra Leone to Nigeria)
with slight seasonal flow variations in direction and velocity, salinity, and
sea-surface temperature (Richardson and Reverdin 1987; Odekunle and Eludoyin
2008; Djakouré et al. 2014, 2017). The northern part of the SEC borders the GC and
flows westward. The Equatorial Undercurrent (EUC) also flows eastward below the
SEC (Djakouré et al. 2014; Herbert et al. 2016; Houndegnonto et al. 2021; see also
Ceríaco et al. 2022a). A Guinea Undercurrent (GUC) is also present, flowing
eastward, in deeper water along the coast. The GGOI are influenced by all these
currents in the “southern alternance region,” dominated by strong seasonal contrasts
and with influxes of equatorial upwelling (Le Lœuff and Cosel 1998). Water salinity,
temperature, and turbidity are also influenced by major freshwater river discharges
(Congo and Niger basins) and resulting plumes (Alory et al. 2021; Houndegnonto
et al. 2021; Ceríaco et al. 2022a). The combination of these characteristics, along
with the upwelling and high biological productivity, contribute to the occurrence of a
spectacular fish diversity.
The marine ichthyofauna of the Gulf of Guinea, including the continental shelf,
continental islands (Bioko), and oceanic islands, presents a remarkable level of
endemism (approximately 20%), but many species are still poorly known and
studied (Jones 1994). The endemism of reef fish species reaches about 65% in
some of these areas, indicating their high degree of isolation (Jones 1994). By
contrast, only three freshwater fish species (all non-indigenous) are recorded for
the islands of Príncipe, São Tomé, and Annobón, all showing tolerance to salinity
and capable of dispersal among the oceanic islands (Jones 1994). The GGOI are part
of the Guinea Current Large Marine Ecosystem (GCLME), extending from Guinea
Bissau to Angola (to the northern seasonal limit of the Benguela Current) and
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433
covering 16 countries’ Exclusive Economic Zones (Ukwe et al. 2006). Because of its
bathymetry, chemistry, hydrography, and trophodynamics, the GCLME is among
the most productive coastal and offshore waters in the world with rich fishery
resources, an important reservoir of marine biological diversity, and excellent
potential for tourism (Ukwe et al. 2003).
Most of the fish species recorded from the GGOI are also present in other parts of
the Gulf of Guinea, with few species endemic to the islands, and several species with
amphi-Atlantic or circum-global distributions. As of 2019, a total of 268 coastal fish
species have been recorded in the GGOI (see “Species Diversity” section) with about
12% of the species (28) reported as endemic to the Gulf of Guinea, and a few of these
only observed in São Tomé and Príncipe, such as Clepticus africanus Heiser, Moura
and Robertson, 2000, and Scorpaena annobonae Eschmeyer, 1969 (Wirtz et al.
2007; Wirtz 2017). This low level of endemism is likely a consequence of the
vagility of marine fishes as zooplankton and the proximity of the islands to the
African continent (Krakstad et al. 2010).
The current chapter presents a brief overview of the marine and freshwater
ecosystems present in the GGOI, the current knowledge of marine and freshwater
fish species, biogeography and evolution, and finally conservation. An updated
taxonomic checklist of marine (coastal, offshore, and deep-water) and freshwater
species is presented, with revised inventories for coastal and reef fish species.
Brief History of Ichthyology Research
In 1871, the Portuguese naturalist Félix António Brito Capello (1828–1879)
published the first list of fishes accessioned at the Lisbon Museum collection. This
list, in three parts, includes specimens from the Portuguese islands of Madeira and
Azores, and from its overseas territories, including São Tomé and Príncipe (Capello
1871a, b, 1872). After his death, António Roberto Pereira Guimarães (?–1889?)
continued Capello’s analysis of the material housed at the Lisbon Museum and
published two additional papers on the topic (Guimarães 1882, 1884). Later, the
Portuguese zoologist Balthazar Osório (1855–1926) presented the first list focusing
on fish species from São Tomé and Príncipe, mostly based on the specimens
collected by the Portuguese naturalists Adolfo Möller (1842–1920) and Francisco
Newton (1864–1909) (Osório 1891, 1892, 1893, 1894, 1895a, 1898, 1906), and
from Annobón (Osório 1895b), with several descriptions of species and original
information. After a gap of about five decades, Frade (1955) and Frade and Correia
da Costa (1956, 1957) reported new records based on pelagic fisheries species (see
also Almeida and Alves 2019). Later, from 1961 to 1987, several international
scientific expeditions provided complementary information (Arnoult et al. 1966;
Bayer et al. 1966; Blanc et al. 1968; Iwamoto 1970; see Afonso et al. 1999 and
Ceríaco et al. 2022b for a detailed bibliography), with rare studies reporting new
records (Thys van den Audenaerde and Tortonese 1974). Only during the late
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twentieth and early twenty-first centuries, several publications focused on São Tomé
or Príncipe and published new species description and records (e.g., Afonso et al.
1999; Wirtz et al. 2007; Rocha et al. 2012; Almeida and Alves 2017, 2019; Iwamoto
and Wirtz 2018). Complementarily, several reports and guides estimating species
occurrence around the Gulf of Guinea Islands were published by FAO and others
(e.g., Allen 1985; Carpenter and De Angelis 2016a–c; Almeida and Biscoito 2019;
Sutton et al. 2020).
Marine and Freshwater Ecosystems
A marine ecosystem can be defined as the geographic area (of any size), comprised
of communities of organisms and their environment, where biological and energy
interactions are greater within than with adjacent ecosystems (Zhao and Costello
2020). This biological system is characterized by two factors: the biotic (e.g., plants,
animals, microbes) and abiotic (e.g., sunlight, oxygen, dissolved nutrients, depth,
temperature). These components influence the dynamics of natural communities at
different spatial scales, from global to local. Marine ecosystems of the GGOI are
underwater equivalent of tropical forests. Both natural systems are complex and
three-dimensional. Furthermore, they have an impressive variety of habitats from the
intertidal zone to the abyssal region (Laborel 1974).
The three oceanic islands (Príncipe, São Tomé, and Annobón) that make up this
system have different geological ages and the steep underwater relief results in a
relatively small, shallow platform (Cowburn 2018; Maia et al. 2018a). The underwater areas of the island seascapes are mainly dominated by volcanic rocky reefs
with limited coral growth (Laborel 1974; Quimbayo et al. 2019). Ecological studies
carried out in recent years have described a variety of marine habitats. For example,
on Príncipe Island, Cowburn (2018) mapped four subtidal habitats and four coastal
habitats along the island. In addition, a recent study investigated the role of four
different reef microhabitats in shaping biological interactions of fishes (Canterle
et al. 2020). Regarding São Tomé Island, the scenario is very similar to that of
Príncipe. Maia et al. (2018a) characterized reef environments on this island based on
the composition of the benthic community and found a diversity of habitats between
the ranges of 10–30 m deep, including a new habitat in the deep reef north of the
island (Morais and Maia 2017).
Major Aquatic Ecosystems in the Gulf of Guinea Oceanic
Islands
Estuaries (Fig. 17.1, 1): An estuary is a coastal zone sheltered from extreme weather
where oceans meet rivers, and nutrients and salts from the ocean mix with those from
the river (Cameron and Pritchard 1963). As a result, estuaries are among the most
17
The Fishes of the Gulf of Guinea Oceanic Islands
435
Fig. 17.1 Gulf of Guinea oceanic island aquatic ecosystems: (1) Estuary; (2) Mangrove forest; (3–
5) Coral reefs; (6) Coral reefs and seagrass; (7) Open and deep-sea ocean; (8) River. Photo credits:
(1, 6–8) Hugulay Albuquerque Maia, (2) Luis MP Ceríaco, (3–5) Luiz Rocha
productive places on Earth and support many life forms. Because they are located
where rivers join the ocean, estuaries have traditionally supported many human
communities and activities like fishing, shipping, and transportation. Some of the
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L. M. da Costa et al.
larger rivers flowing from the islands form brackish lagoons, usually bounded at the
seaward edge by sand banks that only submerge during the highest tides (Cowburn
2018). These lagoons appear to be an important habitat for some resident fish species
(e.g., Periophthalmus barbarus (Linnaeus, 1766)) and a nursery area for reef fish
species (e.g., Lutjanus agennes Bleeker, 1863; Caranx hippos (Linnaeus, 1766)),
crustaceans, molluscs, and other marine life, probably due to the concentration of
nutrients in these areas.
Mangrove Forests (Fig. 17.1, 2): Mangroves are considered blue carbon ecosystems because they are more efficient at absorbing and storing large amounts of
carbon compared to terrestrial ecosystems (Mcleod et al. 2011). Until 2010 this
habitat was mentioned in the literature as present only on the island of São Tomé
(Spalding et al. 2010) but more recently, small extensions on Príncipe Island have
been identified. Haroun et al. (2018) provided updated information about the flora
and fauna, and environmental, conservation and management issues related to
mangroves present along the coasts of these islands.
Coral Reefs (Fig. 17.1, 3–6): Despite crystal-clear waters and optimum temperature for coral development, the GGOI do not present a homogeneous matrix of coral
reefs, but instead exhibit more complex microhabitats spread in their rocky and
biogenic reefs (Maia et al. 2018a). These habitats are composed of some key benthic
organisms, including epilithic algal matrix, calcareous algae, coralline algae (that
form small ~5 cm diameter globular structures over mobile substrates), macroalgae,
hard corals, sponges, zoanthids and gorgonians (Laborel 1974; Maia et al. 2018a).
Rocky reefs and solid shores occur where the volcanic basalt bedrock is exposed
(Cowburn 2018). The seagrass Halodule wrightii Ascherson, 1868 was found along
the coast of São Tomé and Príncipe Islands (Alexandre et al. 2017). No data are
available for Annobón Island.
Open and Deep-Sea Ocean (Fig. 17.1, 7): Open ocean ecosystems vary widely
as the depth of the ocean changes. At the surface of the ocean (the euphotic zone), the
ecosystem receives plenty of light and oxygen and thus is fairly warm and supports
many photosynthetic organisms. Many of the organisms that we associate with
marine ecosystems, such as whales, dolphins, cephalopods, and sharks, live in the
open ocean. As the depth of the ocean increases, it gets darker, colder, and less
oxygen is available. Organisms living in deep-sea ecosystems within the dysphotic
and aphotic zones have unusual adaptations that help them survive in these challenging environments. Some organisms have extremely large mouths that allow
them to catch whatever nutrients fall from shallower ocean depths. Others get their
energy via the chemosynthesis of chemicals from hydrothermal vents. Although the
underwater geomorphology of the GGOI is known, it is thought that they harbor
some of the least known tropical reefs in the world. Underwater forests in
mesophotic reefs are known from the northwest of São Tomé Island (Morais and
Maia 2017) that are dominated by black corals between 30 and 50 m depth.
Streams and Rivers (Fig. 17.1, 8): The hydrographic structure of the GGOI is
radial, from the central mountains to the shore, resulting in numerous streams and
small rivers (up to 27 km length) (e.g., in São Tomé: Ió Grande, Caué, Mussacavu,
Quija, Rio do Ouro, Contador; in Príncipe: Rio Papagaio; in Annobón: A Bobo; see
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The Fishes of the Gulf of Guinea Oceanic Islands
437
Ceríaco et al. 2022a) or crater-lakes (e.g., in São Tomé: Lagoa Amélia; in Annobón:
Lago A Pot). The river network is well distributed around the islands, entering the
sea by creating small estuarine habitats (12 mangroves in São Tomé and 3 in
Príncipe) or small waterfalls or cascades. Several small inland lagoons are also
distributed over the islands. These habitats host the fishes Eleotris vittata Duméril,
1861, Sicydium bustamantei Greeff, 1884, and Aplocheilichthys spilauchen
(Duméril, 1861). Several aquatic invertebrates also inhabit freshwater habitats,
including GGOI endemics such as the snail Neritina manoeli (Dohrn, 1866), or
the crabs Potamonautes principe Cumberlidge, Clark and Baillie, 2002,
Potamonautes saotome Cumberlidge and Daniels, 2018, and Potamonautes
margaritarius (Milne-Edwards, 1869) (Cumberlidge et al. 2002; Allen et al. 2011;
Cumberlidge and Daniels 2018).
Species Diversity
To compile an updated taxonomic checklist of the marine (coastal, offshore, and
deep-water) and freshwater fish species occurring in the GGOI, we reviewed the
bibliography. This included historical and recent inventories and taxonomic studies
(Osório 1891, 1892, 1893, 1894, 1895a, b, 1898, 1906, 1917; Fowler 1936a, b;
Frade 1955; Frade and Correia da Costa 1956, 1957; Arnoult et al. 1966; Bayer et al.
1966; Blanc et al. 1968; Thys van den Audenaerde and Tortonese 1974; Afonso
et al. 1999; Pezold et al. 2006; Fricke 2007; Wirtz et al. 2007; Kovačić and
Schliewen 2008; Schliewen and Kovačić 2008; Rocha et al. 2012; Félix et al.
2016; Reiner and Wirtz 2016; Vasco-Rodrigues et al. 2016; Wirtz and Iwamoto
2016; Almeida and Alves 2017, 2019; Fricke and Wirtz 2017; Tuya et al. 2017;
Wirtz 2017; Iwamoto and Wirtz 2018) as well as general reports and species
revisions on the ichthyofauna of the eastern Atlantic Ocean (Compagno 1984a, b,
2001; Allen 1985; Nakamura 1985; Whitehead 1985; Whitehead et al. 1988;
Carpenter and Allen 1989; Heemstra and Randall 1993; Nakamura and Parin
1993; Nielsen et al. 1999; Krakstad et al. 2010; Ebert 2015; Carpenter and De
Angelis 2016a–c; Last et al. 2016; Vasco-Rodrigues et al. 2018; Parenti and Randall
2020; Sutton et al. 2020). These later sources allowed us to include deep-sea fishes
(mostly Holocephali and Elasmobranchii) and large pelagic species that likely occur
in waters around the GGOI.
In addition, we also compiled a list of species that may occur in the waters of the
GGOI, based on known occurrences in the Gulf of Guinea. Therefore, we searched
for voucher records in databases listing international natural history museum specimens (e.g., FishNet2 2021; Froese and Pauly 2021; GBIF 2021; iDigBio 2021;
OBIS 2021) or other published references. Classification, authority and date follow
Fricke et al. (2021), and family arrangement follows Van der Laan et al. (2014). We
also list several questionable and erroneous records, which were verified by us
against specimens in natural history museum collections or published data. Common
names are mostly those adopted by the Food and Agricultural Organization of the
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United Nations (Carpenter and De Angelis 2016a–c), FishBase (Froese and Pauly
2021) or provided by the original species descriptions.
The compiled full list contains 1045 species (Appendix). Of these, 553 species
are confirmed to occur in the GGOI, including 515 Actinopteri distributed in
39 orders (141 families), 37 Elasmobranchii in six orders (17 families), and one
Holocephali. The 450 potentially occurring species consist of 385 Actinopteri
(30 orders, 109 families) and 65 Elasmobranchii (10 orders, 28 families). Additionally, 32 Actinopteri and five Elasmobranchii previously reported for these islands are
here considered as erroneous and five records of Actinopteri are questionable.
Focusing exclusively on the 553 confirmed species, Elasmobranchii (elasmobranchs: sharks, rays, skates, and wedgefishes) accounts for 6.7% (37 species) of the
diversity, Holocephali (chimaeras) for 0.2% (one species), and Actinopteri
(Actinopterygians: bony or ray-finned fishes) for 93.1% (515 species). A total of
46 orders and 159 families were recorded, with the richest families being Gobiidae
(25 species), Carangidae (23), Serranidae (22), Stomiidae (19), and Myctophidae
(18—Table 17.1).
Elasmobranchii
Among the Elasmobranchii, 37 species of sharks and batoid fishes (wedgefishes and
rays) are confirmed to occur in the GGOI. Sharks, belonging to three orders
(Carcharhiniformes, Lamniformes, Orectolobiformes), account for 45.9% (17 species), while rays, belonging to two orders (Myliobatiformes, Torpediniformes),
account for 51.4% (19 species) of Elasmobranchii diversity. Wedgefishes, order
Rhinopristiformes are represented by a single species (2.7%). The most speciose
orders are Myliobatiformes, with 17 species (46%), followed by Carcharhiniformes
with 12 species (32.4%). A total of 17 families are listed, with Carcharhinidae,
Dasyatidae, and Mobulidae presenting the highest number of species, with 21.6%
(8), 18.9% (7), and 10.8% (4), respectively.
The first record of African wedgefish, Rhynchobatus luebberti Ehrenbaum, 1915,
for São Tomé (Reiner and Wirtz 2016) deserves a special highlight. This species is
Critically Endangered (CR—Kyne and Jabado 2019), and has a limited Eastern
Tropical Atlantic range distribution, from Mauritania to Congo (Carpenter and De
Angelis 2016a). The Scalloped hammerhead shark, Sphyrna lewini (Griffith and
Smith, 1834), and Sand tiger shark, Carcharias taurus Rafinesque, 1810, records
from the GGOI (with the exception of Annobón) are also noteworthy as both species
are also assessed as CR (Rigby et al. 2021). The iconic Whale shark, Rhincodon
typus Smith, 1828, assessed as Endangered (EN—Pierce and Norman 2016), was
observed in 2015 around São Tomé and the Gulf of Guinea (Vasco-Rodrigues et al.
2016). The species presents a circumtropical distribution with high suitability habitat
in the eastern Atlantic (around Gabon, Congo, and Equatorial Guinea) (Sequeira
et al. 2014). Recently, a shark specimen captured by locals had several features
attributable to Tiger shark, Galeocerdo cuvier (Péron and Lesueur, 1822), a Near
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439
Table 17.1 Classification and diversity of the confirmed Gulf of Guinea oceanic islands fish fauna.
Taxonomic arrangement follows Van der Laan et al. (2014)
Class
Elasmobranchii
Holocephali
Actinopteri
Order
Orectolobiformes
Lamniformes
Carcharhiniformes
Torpediniformes
Rhinopristiformes
Myliobatiformes
Chimaeriformes
Elopiformes
Albuliformes
Notacanthiformes
Anguilliformes
Saccopharyngiformes
Clupeiformes
Alepocephaliformes
Siluriformes
Argentiniformes
Stomiiformes
Aulopiformes
Myctophiformes
Lampriformes
Zeiformes
Stylephoriformes
Gadiformes
Polymixiiformes
Beryciformes
Holocentriformes
Ophidiiformes
Scombriformes
Syngnathiformes
Kurtiformes
Gobiiformes
Carangiformes
Cichliformes
Atheriniformes
Cyprinodontiformes
Beloniformes
Mugiliformes
Gobiesociformes
Blenniiformes
Acanthuriformes
Lophiiformes
Tetraodontiformes
Families
2
3
4
1
1
6
1
2
1
1
11
1
2
2
1
4
4
8
1
1
1
1
5
1
3
1
3
8
6
1
3
13
1
1
1
3
1
1
2
7
4
5
Genera
2
3
8
2
1
11
1
2
1
2
34
1
4
3
1
8
25
12
13
1
1
1
8
1
5
3
9
23
10
3
20
36
1
1
1
12
3
2
6
11
7
12
Species
2
3
12
2
1
17
1
3
1
3
43
1
6
3
1
8
41
15
18
1
1
1
11
1
5
3
9
26
11
4
31
62
1
1
1
18
5
2
8
12
10
24
(continued)
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L. M. da Costa et al.
Table 17.1 (continued)
Class
Order
Centrarchiformes
Acropomatiformes
Perciformes *sedis mutabilis*
Perciformes
Families
2
3
12
13
Genera
2
3
39
31
Species
5
4
69
50
Threatened species (NT—Ferreira and Simpfendorfer 2019). Despite the low resolution of the available image (see Fig. 17.2, 1), this is the first observation confirming
the occurrence of this species around São Tomé, but the species had already been
reported from Príncipe (Carpenter and de Angelis 2016a). In a recent study, Bernard
et al. (2021) confirmed that Tiger shark populations from the Atlantic Ocean are
genetically distinct from the Indo-Pacific Ocean populations showing that these
long-distance dispersing populations are not interbreeding.
Holocephali
The sole Holocephali (Chimaeriformes, Rhinochimaeridae), the Sicklefin Chimaera,
Neoharriotta pinnata (Schnakenbeck, 1931), accounts for 0.2% of the confirmed
species in the region and is considered a Near Threatened species. The Sicklefin
Chimaera is known in the eastern Atlantic Ocean off the west African coast from
Western Sahara to Namibia, including the Gulf of Guinea islands. The species is
found at the edge of the shelf in depths ranging from 200 to 600 m (Carpenter and De
Angelis 2016a).
Actinopteri
The Actinopteri is the most diverse fish class, with 515 confirmed species for the
GGOI. A total of 141 families were recorded, with Gobiidae being the richest with
4.8% of the species (25), followed by Carangidae with 4.5% (23), Serranidae with
4.3% (22), Stomiidae with 3.7% (19), Myctophidae with 3.5% (18), Sparidae with
2.9% (15), and Haemulidae, Muraenidae, and Ophichthidae with 2.1% (11) each. All
132 remaining families are represented by fewer than ten species and account for the
remaining 70% of the species. To be as exhaustive as possible, the current checklist
integrates potential deep-sea and large migrant pelagic fish species based on several
guides and reports. Due to the deep water around all three GGOI, several species
(e.g., Opisthoproctus soleatus Vaillant, 1888; Scopelosaurus argenteus (Maul,
1954)) were collected by offshore scientific surveys or accidentally by industrial
fishing vessels. In addition, several deep-sea fish species are already reported in the
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441
Fig. 17.2 Gulf of Guinea oceanic island fishes: (1) Tiger Shark Galeocerdo cuvier (Péron and
Lesueur, 1822); (2) Atlantic Mudskipper Periophthalmus barbarus (Linnaeus, 1766); (3) São Tomé
Clingfish Apletodon wirtzi Fricke, 2007; (4) Island Cowfish (juvenile) Acanthostracion
notacanthus (Bleeker, 1863); (5) Small Goby Bathygobius burtoni (O’Shaughnessy, 1875); (6)
Small Goby Gobius aff. rubropunctatus Delais, 1951; (7) Margintail Paraconger caudilimbatus
(Poey, 1867); (8) African Speckled Scorpionfish Scorpaenodes africanus Pfaff, 1933. Photo
credits: (1) Ivete Carneiro, (2) Luis MP Ceríaco, (3–8) João Luiz Gasparini
literature for the GGOI (e.g., Cyclothone spp., Ichthyococcus ovatus (Cocco, 1838),
Vinciguerria nimbaria (Jordan and Williams, 1895)).
The Actinopteri fishes present a high variety of shapes, distributions, and behaviors. The extraordinary and unusual looking Atlantic mudskipper, P. barbarus,
occurring along the West African coast, from Morocco to Angola and several
offshore islands, is also present in the GGOI (Fig. 17.2, 2). Of special interest are:
the São Tomé clingfish, Apletodon wirtzi Fricke, 2007, endemic to the GGOI and
currently only known from its type locality, Bombom Islet, north of Príncipe Island
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L. M. da Costa et al.
(Fricke 2007; Fig. 17.2, 3); the Island cowfish, Acanthostracion notacanthus
(Bleeker, 1863), which has a restricted distribution around several islands (São
Tomé, Príncipe, Saint Helena, Ascension, and Azores) and two African coastal
locations (Ghana and Angola) (Fig. 17.2, 4); one small goby, Bathygobius burtoni
(O’Shaughnessy, 1875), an Endangered species and Gulf of Guinea endemic (Ghana
to Cameroon, Bioko Island), which is confirmed from São Tomé and Príncipe
islands (Carpenter et al. 2015—Fig. 17.2, 5); another small goby, Gobius aff.
rubropunctatus Delais, 1951, from São Tomé and Príncipe islands that is a putative
undescribed species (Wirtz et al. 2007—Fig. 17.2, 6); the Margintail, Paraconger
caudilimbatus (Poey, 1867), an amphi-Atlantic species, only reported from São
Tomé Island in the eastern Atlantic (Wirtz et al. 2007—Fig. 17.2, 7); and the African
speckled scorpionfish, Scorpaenodes africanus Pfaff, 1933, with a fragmented
distribution including Senegal, São Tomé, and Annobón (Eschmeyer 1969—
Fig. 17.2, 8).
The American whitespotted filefish, Cantherhines macrocerus (Hollard, 1853), a
typical western Atlantic species, also occurs in the eastern Atlantic Ocean. The
species is suspected to have been transported to the Gulf of Guinea by oil platforms
coming from Brazil or the Caribbean (Herrero-Barrencua et al. 2019). Nonetheless,
natural dispersal observed in a western Atlantic congener (Cantherhines pullus
(Ranzani, 1842)) into the Gulf of Guinea (Afonso et al. 1999) suggests a similar
scenario for C. macrocerus is possible (Herrero-Barrencua et al. 2019). Two introduced freshwater species have been reported for the islands: the Mozambique tilapia,
Oreochromis mossambicus (Peters, 1852), in São Tomé (Félix et al. 2016), and the
Banded lampeye, A. spilauchen, in Príncipe (Cravo 2021). Both introduction dates
are not determined, but the Mozambique tilapia is already widespread throughout the
island (Félix et al. 2016).
Compared to the most recent studies regarding the fishes of the GGOI (Wirtz
2017; Iwamoto and Wirtz 2018), the present work includes several unique and
new records: Cichlidae—O. mossambicus, introduced species; Exocoetidae—
Hirundichthys affinis (Günther, 1866), new record for São Tomé; Gempylidae—
Nealotus tripes Johnson, 1865; Monacanthidae—C. macrocerus; Polymixiidae—
Polymixia nobilis Lowe, 1836; Serranidae—Anthias cyprinoides (Katayama &
Amaoka, 1986), Serranus accraensis (Norman, 1931), Serranus drewesi Iwamoto,
2018, Serranus heterurus (Cadenat, 1937); Sparidae—Spicara melanurus (Valenciennes, 1830); and Stomiidae—Bathophilus nigerrimus Giglioli, 1882 (Krakstad
et al. 2010; Félix et al. 2016; Almeida and Alves 2017, 2019; Iwamoto and Wirtz
2018; Vasco-Rodrigues et al. 2018; Herrero-Barrencua et al. 2019; Parenti and
Randall 2020; Cravo 2021). Gobioides cf. africanus (Giltay, 1935), Gobiidae,
reported by Cravo (2021) needs confirmation.
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443
Biogeography and Evolution of Fishes in Gulf of Guinea
Oceanic Islands
Oceanic island ecosystems in the Tropical Eastern Atlantic (TEA) include the Cape
Verde archipelago and the islands of the Gulf of Guinea: Príncipe, São Tomé, and
Annobón (Floeter et al. 2008). Despite its relatively old age, São Tomé has low
marine endemism (e.g., 3% for fishes; Hachich et al. 2015) due to high oceanographic connectivity to the African coast (Wirtz 2003; Floeter et al. 2008). On the
other hand, the regional endemism level of the TEA is high (30%; Floeter et al.
2008), a phenomenon presumably due to the geographic isolation of the TEA from
the other Atlantic reef areas (e.g., ~3500 km from the Brazil and ~8696 km from the
Caribbean; Floeter et al. 2008), as well as a history of recurrent isolation and
connectivity with the Indo-Pacific at an evolutionary timescale (Cowman et al.
2017). Indeed, several species show a trans-Atlantic distribution (amphi-Atlantic)
with most of the species belonging to families of pelagic-spawners with long pelagic
larval durations (e.g., Muraenidae, Serranidae), but also smaller-sized genera (e.g.,
Abudefduf taurus; Müller and Troschel, 1848) and Centropyge aurantonotus Burgess, 1974—Floeter et al. 2008). Entire families are composed of amphi-Atlantic
species (e.g., Diodontidae, Holocentridae, Priacanthidae, Synodontidae). In addition
to the Benguela Current that limits the movements of tropical species from the Indian
Ocean, cold waters from the northeastern Atlantic also limit the geographic range of
tropical species (Floeter et al. 2008; Almada et al. 2013). Thus, the TEA and the
southwestern Indian Ocean only share about 15 species (e.g., Lithognathus
mormyrus (Linnaeus, 1758) and Gnatholepis thompsoni Jordan, 1904) or genera
(e.g., Prionurus and Plectorhynchus—Rocha et al. 2005; Wirtz et al. 2007; Floeter
et al. 2008).
Since the waters of the Gulf of Guinea have received limited scientific attention,
with Annobón the least studied area of the GGOI (Osório 1895b; Blanc et al. 1968),
the marine organisms desperately require further study (Floeter et al. 2008). Recent
works dealing with the biogeography and evolution of some reef fish families
include representatives from this region, as in the case of the genus Clepticus
(Labridae). This recent study revealed that C. africanus, an endemic species from
the Gulf of Guinea, is genetically closer to Clepticus brasiliensis Heiser, Moura and
Robertson, 2000, from the Brazilian coast, than to the Caribbean Clepticus parrae
(Bloch and Schneider, 1801) (Beldade et al. 2009). The biogeographic affinities of
other endemics in the archipelago are largely unknown.
With 268 coastal fish species in the GGOI, the diversity is high when compared to
other Atlantic islands (e.g., 140 coastal fish species from Saint Helena, 170 species
from Azores, or 226 species from Madeira—Table 17.2). This is mostly due to the
location of the GGOI, closer to the African shelf and surrounded by a vortex created
by all the currents crossing the area. However, the total number is low when
compared to the Cape Verde (325 costal fish species) and Canary (330) islands,
probably a sampling artifact due to the dearth of surveys around the GGOI.
444
L. M. da Costa et al.
Table 17.2 Coastal fish species richness, number of endemics and % endemism of Atlantic islands
Islands
Ascension
Cape Verde
Coastal fish species
%
N
Total endemics Endemism
173
11
10.2
325
19
8.4
Saint Helena
Saint Peter and Saint Paul’s
archipelago
Madeira
Canary
Azores
140
117
10
5
12.3
7.7
226
330
170
0
NA
NA
0
NA
NA
São Tomé and Príncipe
268
7
3.0
References
Wirtz et al. (2014)
Wirtz et al. (2013); Freitas
et al. (2018)
Brown et al. (2019)
Vaske et al. (2008)
Wirtz et al. (2008)
Brito et al. (2002)
Santos et al. (1997); Afonso
et al. (2013)
Wirtz et al. (2007); Wirtz
(2017)
Marine fish species are moving, and tropicalization is one of the observed
processes in some eastern Atlantic islands where several TEA species are expanding
their ranges (e.g., Muraena melanotis (Kaup, 1859), Holacanthus africanus
Cadenat, 1951, and Cirrhitus atlanticus Osório, 1893—Brito et al. 2005; Falcón
et al. 2018). We also highlight the occurrence of Epinephelus fasciatus (Forsskål,
1775), an Indo-Pacific species, potentially introduced by ballast water or in association with oil platforms (Brito et al. 2005; Falcón et al. 2018). Rocha et al. (2005)
and confirmed recent connections in several taxa during warm interglacial periods
(Peeters et al. 2004), such as the genus Gnatholepis that invaded the Atlantic from
the Indian Ocean. Currently, the Agulhas Current in extreme conditions can force
any tropical invaders from the Indian Ocean to move to the Atlantic Ocean through
the ‘Agulhas leakage’ that forms water rings at the Agulhas retroflection (Lutjeharms
and Van Ballegooyen 1988; Gordon 2003; Lutjeharms 2006; Beal et al. 2011).
Invading fish species are likely moving with these rings through the Western
Atlantic and South-central Atlantic before ending up in the TEA, rather than moving
north with the Benguela Current, which is probably more lethal to tropical fish
species (Rocha et al. 2005).
Some fish species have highly skewed distributions, with 84 genera occurring in
the eastern Atlantic, but not in the western Atlantic (e.g., Thorogobius,
Wheelerigobius—Floeter et al. 2008; Cowman et al. 2017). Other genera are
amphi-Atlantic, but much more diverse in the eastern Atlantic (e.g., Diplodus,
Scartella—Cowman et al. 2017) or with sister-species in the western Atlantic
(e.g., Hypleurochilus aequipinnis (Günther, 1861)—Wirtz et al. 2007). Finally,
several eastern Atlantic genera occur in the Indo-Pacific, but are not present in the
western Atlantic (e.g., Coris, Lethrinus—Cowman et al. 2017). Cowman et al.
(2017) observed that the Gulf of Guinea fish species assemblages are distinctive
within the east Atlantic cluster (Cape Verde, Gulf of Guinea West, and Sahelian
Upwelling).
17
The Fishes of the Gulf of Guinea Oceanic Islands
445
Conservation
The GGOI, together with Cape Verde, have been considered important global
hotspots for marine conservation (Roberts et al. 2002), with high levels of endemism
(~30%, Floeter et al. 2008). Several factors likely contribute to this designation
including:
1. The geographic location and connectivity with tropical western Atlantic via the
Equatorial Counter Current (Wirtz et al. 2007; Floeter et al. 2008; HerreroBarrencua et al. 2019).
2. The moderate isolation from the Continental slope (Floeter et al. 2008; Hachich
et al. 2015; Cowman et al. 2017; Quimbayo et al. 2019).
3. The Benguela Current working as a shield and limiting Indian Ocean tropical fish
species from moving northward (Floeter et al. 2008).
4. The northeastern Atlantic cold waters limiting the northern range of tropical fish
species (Floeter et al. 2008; Almada et al. 2013).
5. The lowest fish biomass and highest density in reef assemblage (Quimbayo et al.
2019).
With 27 fish species reported, plus two uncertain identifications (Gobioides
cf. africanus and Citharus cf. linguatula (Linnaeus, 1758)—Cravo 2021), mangroves and seagrasses are also essential habitats to the fish diversity by providing
fisheries production (Félix et al. 2016; Alexandre et al. 2017; Cravo 2021).
Globally, mangroves are highly impacted by deforestation for onshore aquaculture (for fish and shellfish production), agriculture, and urban development (FAO
2007; Friess et al. 2019; Goldberg et al. 2020). With at least 35% of world area lost,
mangroves, or inter-tidal forest communities, are one of the major tropical environments threatened by agriculture, overharvesting, changing hydrology, pollution, and
coastal erosion (Valiela et al. 2001). Otero-Ferrer et al. (2020) emphasized that at the
island scale, the protection of fish assemblages needs to consider the interconnected
habitat network by including the seascapes boundaries where fundamental ecological functions might also occur. The GGOI exhibit lower biomass despite higher
primary productivity, an unexpected observation likely caused by intense fishing
activities (Maia et al. 2018a; Quimbayo et al. 2019).
In 2000, Annobón Island and the surrounding waters were designated as a Marine
Nature Reserve at National level, limiting fishing to traditional subsistence practices
and scientific research (UNEP-WCMC and IUCN 2021). In 2006, the São Tomé
Obô and Príncipe Obô Natural Parks were established, covering 262 km2 and 45 km2
in the respectively islands (UNEP-WCMC and IUCN 2021). The natural park in São
Tomé covers three out of 12 mangroves, including Malanza, by far the largest of
such ecosystems in the GGOI (Afonso 2019). The natural park in Príncipe included a
marine portion on the southwestern coast. Since 2012, the Ramsar site of Tinhosas
islets (covering Tinhosa Grande, Tinhosa Pequena and Tinhosinha, south of
Príncipe) and the island of Príncipe are a UNESCO World Biosphere Reserve
(UNEP-WCMC and IUCN 2021).
446
L. M. da Costa et al.
Regarding fishing activities, Equatorial Guinea and São Tomé and Príncipe are
part of the Fishery Committee for the Eastern Central Atlantic (CECAF) with the
purpose of promoting the sustainable utilization of all living marine resources within
the delimited area by proper management and development of the fisheries and
fishing operations. Fisheries catches include small-scale artisanal, subsistence (fishing operations in remote communities with no access to market to supplement family
needs, and portion taken home for consumption from artisanal catch), and foreign
industrial (dominated by fleets from the European Union, Japan, Taiwan, and China)
catches (Belhabib 2015; Maia et al. 2018b). Nevertheless, only limited data from
fisheries surveys are reported (Belhabib 2015). Increasing numbers of fishers,
destructive blast fishing practices, and pollution from industrial fishing vessels
(oil-spills) are the main causes of negative fish catch changes over time (Maia
et al. 2018b). The low biomass of medium and large fish species reflects the longterm fishing pressure on São Tomé Island, as does deeper reef habitats having higher
species richness, abundance, and biomass (Maia et al. 2018a).
Within Elasmobranchii, 27 (73%) out of 37 species are considered threatened
(Vulnerable—VU, Endangered—EN or Critically Endangered—CR) and one species (2.7%) is Data Deficient (DD), following IUCN categories (Appendix). Few
countries impose catch limits and overfishing is a main threat to oceanic sharks, as
are the loss and degradation of habitat and climate change (Pacoureau et al. 2021).
Regarding Actinopteri, 19 (3.7%) out of 515 species are considered threatened
(VU or EN) and 47 species (9.1%) are DD. Fifteen species are reported as endemic
to the GGOI, of which seven are Gobiidae (small species with limited dispersive
abilities) and four are freshwater/brackish species (Appendix). Annobón Island is the
least studied of the GGOI with very few scientific surveys (Osório 1895b; Blanc
et al. 1968). Nevertheless, and as expected, about 75% of its ichthyofauna is shared
with the African coast. From the remaining species, some are endemic to Annobón
Island (S. annobonae), only present around the GGOI (Eleotris annobonensis Blanc,
Cadenat and Stauch, 1968), common to other islands system (Rypticus saponaceus
(Bloch and Schneider, 1801)), or amphi-Atlantic (Uroconger syringinus Ginsburg,
1954). Therefore, the establishment of a network of Marine Protected Area in the
GGOI is fundamental to reduce further negative impacts on the reef by commercial
fisheries and to secure their sustainability.
Concluding Remarks
The present checklist includes coastal, deep-sea, pelagic marine and freshwater fish
species. Nevertheless, further surveys are still needed. These future surveys and
research projects should combine traditional and new approaches (e.g., environmental DNA) to understand and highlight the occurrence of discrete (pelagic) species,
but also to better define the distribution of endemic species around all three GGOI.
Annobón Island should be a region of primary focus because it is the least studied.
Moreover, the creation of one or more Marine Protected Areas in co-management
17
The Fishes of the Gulf of Guinea Oceanic Islands
447
with fisheries will be fundamental to protect the unique GGOI fish biodiversity
hotspot, not only for the endemic species, but also to maintain sustainable fisheries.
Acknowledgments We are very grateful to João Luiz Gasparini who kindly allowed the use of his
photos obtained through National Geographic Society, California Academy of Sciences, Roça Belo
Monte Plantation Hotel and The Rufford Foundation projects. We also thank Luiz Rocha, California Academy of Sciences, for the use of his photos of coral reefs, Luis MP Ceríaco for the use of his
photos of mangroves and Periophthalmus barbarus, and Ivete Carneiro for the use of her photo of
Galeocerdo cuvier. We would like to thank Peter Wirtz and Manuel Biscoito who kindly reviewed
this manuscript and made fruitful contributions.
Appendix
Checklist of marine and freshwater fish species reported from the Gulf of Guinea
Oceanic Islands: Príncipe (P), São Tomé (S), Annobón (A). A complete checklist
including confirmed, potential, erroneous and questionable marine and freshwater
fish species reported from the Gulf of Guinea Oceanic Islands, together with
common names, voucher numbers of museum specimens, and additional notes is
available at [https://doi.org/10.1007/978-3-031-06153-0_17]
X, present; I, introduced; #, museum voucher specimen(s); E, endemic. IUCN
Red List category: not evaluated (NE), data deficient (DD), least concern (LC), near
threatened (NT), vulnerable (VU), endangered (EN), and critically endangered (CR).
Taxa arranged according to Van der Laan et al. (2014). References: (1) Collette and
Nauen (1983); (2) Allen (1985); (3) Nakamura (1985); (4) Whitehead (1985);
(5) Whitehead et al. (1988); (6) Carpenter and Allen (1989); (7) Cohen et al.
(1990); (8) Heemstra and Randall (1993); (9) Nakamura and Parin (1993);
(10) Compagno (1984a); (11) Compagno (1984b); (12) Afonso et al. (1999);
(13) Nielsen et al. (1999); (14) Compagno (2001); (15) Kotlyar (2004); (16) Pezold
et al. (2006); (17) Fricke (2007); (18) Wirtz et al. (2007); (19) Kovačić and
Schliewen (2008); (20) Krakstad et al. (2010); (21) Kotlyar 2011; (22) Schliewen
(2011); (23) Rocha et al. (2012); (24) Ebert (2015); (25) Carpenter and De Angelis
(2016a); (26) Carpenter and De Angelis (2016b); (27) Carpenter and De Angelis
(2016c); (28) Félix et al. (2016); (29) Last et al. (2016); (30) Reiner and Wirtz
(2016); (31) Vasco-Rodrigues et al. (2016); (32) Wirtz and Iwamoto (2016);
(33) Almeida and Alves (2017); (34) Fricke and Wirtz (2017); (35) Tuya et al.
(2017); (36) Wirtz (2017); (37) Yokota and Carvalho (2017); (38) Haroun et al.
(2018); (39) Iwamoto and Wirtz (2018); (40) Vasco-Rodrigues et al. (2018);
(41) Almeida and Biscoito (2019); (42) Almeida and Alves (2019); (43) HerreroBarrencua et al. (2019); (44) Reiner (2019); (45) Parenti and Randall (2020);
(46) Sutton et al. (2020); (47) Cravo (2021)
448
Higher taxonomy
L. M. da Costa et al.
Species
P
S
A
IUCN
Reference
?
X
?
EN
25, 31, 40
?
X
?
VU
10, 12, 18
X
X
?
CR
14
X
X
?
LC
14, 24
X
X
X
EN
14, 25
X
?
?
DD
25
X
X
X
EN
11, 25
X
X
X
VU
25
#
#
X
VU
11, 25
?
X
?
LC
11, 12, 18, 25
?
#
?
VU
11, 25
X
X
?
NT
25
X
?
?
VU
11, 25
X
X
X
X
X
X
NT
VU
11, 12, 18, 25
11, 12, 18, 25
?
X
?
CR
12
X
?
?
VU
11, 25
?
X
?
LC
12, 25, 29
?
X
?
VU
12, 25, 29
?
X
?
CR
30
X
X
X
VU
25, 29
X
X
X
X
?
X
VU
NT
29
25
Class Elasmobranchii
Order Orectolobiformes
Family
Rhincodon typus Smith, 1828
Rhincodontidae
Family
Ginglymostoma cirratum
Ginglymostomatidae (Bonnaterre, 1788)
Order Lamniformes
Family
Carchariidae
Family
Pseudocarchariidae
Family
Lamnidae
Carcharias taurus Rafinesque,
1810
Pseudocarcharias kamoharai
(Matsubara, 1936)
Isurus oxyrinchus Rafinesque,
1810
Order Carcharhiniformes
Family
Scyliorhinus cervigoni Maurin
Scyliorhinidae
and Bonnet, 1970
Family
Paragaleus pectoralis (Garman,
Hemigaleidae
1906)
Family
Carcharhinus brevipinna (Müller
Carcharhinidae
and Henle, 1839)
Carcharhinus falciformis (Bibron
in Müller and Henle, 1839)
Carcharhinus galapagensis
(Snodgrass and Heller, 1905)
Carcharhinus limbatus (Valenciennes in Müller and Henle, 1839)
Galeocerdo cuvier (Péron and
Lesueur, 1822)
Negaprion brevirostris (Poey,
1868)
Prionace glauca (Linnaeus, 1758)
Rhizoprionodon acutus (Rüppell,
1837)
Family
Sphyrna lewini (Griffith and
Sphyrnidae
Smith, 1834)
Sphyrna zygaena (Linnaeus,
1758)
Order Torpediniformes
Family
Tetronarce nobiliana (Bonaparte,
Torpedinidae
1835)
Torpedo torpedo (Linnaeus,
1758)
Order Rhinopristiformes
Rhynchobatus luebberti
Family
Rhinidae
Ehrenbaum, 1915
Order Myliobatiformes
Family
Zanobatus schoenleinii (Müller
Zanobatidae
and Henle, 1841)
Family
Bathytoshia lata (Garman, 1880)
Dasyatidae
Dasyatis marmorata
(Steindachner, 1892)
(continued)
17
The Fishes of the Gulf of Guinea Oceanic Islands
Higher taxonomy
449
Species
P
S
A
IUCN
Dasyatis pastinaca (Linnaeus,
1758)
Fontitrygon margarita (Günther,
1870)
Fontitrygon margaritella
(Compagno and Roberts, 1984)
Pteroplatytrygon violacea (Bonaparte, 1832)
Taeniurops grabatus (Geoffroy
Saint-Hilaire, 1817)
Gymnura altavela (Linnaeus,
1758)
Gymnura sereti Yokota and
Carvalho, 2017
Aetobatus narinari (Euphrasen,
1790)
Aetomylaeus bovinus (Geoffroy
Saint-Hilaire, 1817)
Myliobatis aquila (Linnaeus,
1758)
Mobula birostris (Walbaum,
1792)
Mobula hypostoma (Bancroft,
1831)
Mobula tarapacana (Philippi,
1892)
Mobula thurstoni (Lloyd, 1908)
X
X
?
VU
40
X
X
X
VU
25, 29
X
X
X
NT
25, 29
X
X
X
LC
25, 29
X
X
X
NT
18, 25, 29
X
X
X
EN
25, 29
?
#
?
EN
37
X
X
X
EN
25, 29
X
X
X
CR
25
X
X
X
CR
25, 29
X
X
X
EN
25, 29
X
X
X
EN
25, 29
?
X
?
EN
31, 40
?
X
?
EN
31, 40
X
X
X
NT
25
Family
Megalopidae
Elops lacerta Valenciennes, 1847
Elops senegalensis Regan, 1909
Megalops atlanticus Valenciennes, 1847
X
?
X
X
#
#
X
?
X
LC
DD
VU
26
12, 26, 28
26, 28, 47
Order Albuliformes
Family
Albulidae
Albula goreensis Valenciennes,
1847
?
#
?
NE
18, 42
X
#
X
X
X
X
LC
LC
26
26
X
X
X
LC
26
E
E
E
LC
26
X
X
X
NE
26
Family
Gymnuridae
Family
Aetobatidae
Family
Myliobatidae
Family
Mobulidae
Reference
Class Chondrichthyes | subclass Holocephali
Order Chimaeriformes
Family
Neoharriotta pinnata
Rhinochimaeridae
(Schnakenbeck, 1931)
Class Actinopterygii | subclass Actinopteri
Order Elopiformes
Family Elopidae
Order Notacanthiformes
Family
Aldrovandia oleosa Sulak, 1977
Halosauridae
Halosaurus attenuatus Garman,
1899
Halosaurus ovenii Johnson, 1864
Order Anguilliformes
Family
Panturichthys longus
Heterenchelyidae
(Ehrenbaum, 1915)
Pythonichthys macrurus (Regan,
1912)
(continued)
450
Higher taxonomy
Family
Chlopsidae
Family
Myrocongridae
Family
Muraenidae
Family
Synaphobranchidae
Family
Ophichthidae
Family
Congridae
L. M. da Costa et al.
Species
P
S
A
IUCN
Pythonichthys microphthalmus
(Regan, 1912)
Chlopsis olokun (Robins and
Robins, 1966)
Myroconger compressus Günther,
1870
Anarchias longicauda (Peters,
1877)
Anarchias similis (Lea, 1913)
Channomuraena vittata (Richardson, 1845)
Echidna peli (Kaup, 1856)
Enchelycore nigricans
(Bonnaterre, 1788)
Gymnothorax afer Bloch, 1795
Gymnothorax mareei Poll, 1953
Gymnothorax vicinus (Castelnau,
1855)
Muraena melanotis (Kaup, 1859)
Muraena robusta Osório, 1911
Uropterygius wheeleri Blache,
1967
Histiobranchus bathybius (Günther, 1877)
Brachysomophis atlanticus
Blache and Saldanha, 1972
Callechelys guineensis (Osório,
1893)
Dalophis boulengeri (Blache,
Cadenat and Stauch, 1970)
Dalophis cephalopeltis (Bleeker,
1863)
Echelus myrus (Linnaeus, 1758)
Myrichthys pardalis (Valenciennes, 1839)
Myrophis plumbeus (Cope, 1871)
Ophichthus ophis (Linnaeus,
1758)
Ophichthus rufus (Rafinesque,
1810)
Ophisurus serpens (Linnaeus,
1758)
Pisodonophis semicinctus (Richardson, 1848)
Ariosoma balearicum (Delaroche,
1809)
Bathycongrus bertini (Poll, 1953)
Bathyuroconger vicinus (Vaillant,
1888)
Heteroconger longissimus Günther, 1870
Paraconger caudilimbatus (Poey,
1867)
Paraconger notialis Kanazawa,
1961
X
X
X
NE
Reference
26
X
X
X
LC
26
X
#
?
DD
26, 42
X
X
X
LC
26
?
?
?
X
#
X
LC
LC
26
12, 26, 40
#
?
X
X
#
#
LC
LC
18, 26, 40
12, 26, 40
X
#
X
X
X
X
X
X
#
LC
LC
LC
12, 26
12, 26
26, 40
#
X
X
X
X
X
#
X
X
LC
LC
LC
12, 20, 25, 35, 40
12, 26, 40
26, 31
#
?
?
DD
26
#
?
?
LC
26
?
X
?
LC
26, 30
#
?
?
LC
18, 26
?
#
?
LC
26, 28
?
X
X
#
?
X
LC
LC
20
12, 26, 35, 40
#
?
?
X
?
?
LC
LC
26
20, 26
#
?
?
LC
18
X
X
X
LC
26
?
X
?
LC
X
#
#
LC
26
X
X
X
X
X
X
LC
LC
26
26
X
X
?
LC
18, 35
?
X
?
LC
18
X
X
X
LC
26
(continued)
17
The Fishes of the Gulf of Guinea Oceanic Islands
Higher taxonomy
451
Species
P
S
A
IUCN
Uroconger syringinus Ginsburg,
1954
Xenomystax congroides Smith
and Kanazawa, 1989
Cynoponticus ferox Costa, 1846
X
#
#
LC
26
X
X
X
LC
26
X
X
X
LC
26
Avocettina infans (Günther, 1878)
Nemichthys curvirostris
(Strömman, 1896)
Nemichthys scolopaceus Richardson, 1848
Serrivomer beanii Gill and Ryder,
1883
Hoplunnis punctata Regan, 1915
X
?
#
X
X
?
LC
LC
46
20, 26
?
#
?
LC
26, 46
?
#
?
LC
26, 46
X
#
X
LC
26
X
X
X
LC
26
Order Saccopharyngiformes
Family
Eurypharynx pelecanoides
Eurypharyngidae
Vaillant, 1882
?
#
?
LC
26, 46
Order Clupeiformes
Family
Clupeidae
?
#
?
LC
18, 47
?
?
?
#
#
?
LC
LC
26
12, 20, 42
?
#
?
VU
20, 42
#
X
#
X
?
X
DD
LC
4, 18, 42
5, 26
?
#
?
LC
26, 46
X
#
X
?
X
?
LC
LC
26
46
X
#
X
LC
26
?
#
?
LC
26
?
#
?
LC
26, 46
?
#
?
LC
26, 46
?
#
?
LC
46
?
#
#
LC
26, 46
?
#
?
LC
26, 46
Family
Muraenesocidae
Family
Nemichthyidae
Family
Serrivomeridae
Family
Nettastomatidae
Nettastoma melanura Rafinesque,
1810
Family
Engraulidae
Ethmalosa fimbriata (Bowdich,
1825)
Pellonula vorax Günther, 1868
Sardinella aurita Valenciennes,
1847
Sardinella maderensis (Lowe,
1838)
Sardinella rouxi (Poll, 1953)
Engraulis encrasicolus (Linnaeus, 1758)
Order Alepocephaliformes
Family
Photostylus pycnopterus Beebe,
Alepocephalidae
1933
Family
Holtbyrnia macrops Maul, 1957
Platytroctidae
Searsia koefoedi Parr, 1937
Order Siluriformes
Family Ariidae
Carlarius parkii (Günther, 1864)
Order Argentiniformes
Family
Glossanodon polli Cohen, 1958
Argentinidae
Family
Microstoma microstoma (Risso,
Microstomatidae
1810)
Xenophthalmichthys danae
Regan, 1925
Family
Bathylagichthys greyae (Cohen,
Bathylagidae
1958)
Bathylagoides argyrogaster
(Norman, 1930)
Family
Monacoa grimaldii (Zugmayer,
Opisthoproctidae
1911)
Reference
(continued)
452
Higher taxonomy
Order Stomiiformes
Family
Gonostomatidae
Family
Sternoptychidae
Family
Phosichthyidae
Family
Stomiidae
L. M. da Costa et al.
Species
P
S
A
IUCN
Opisthoproctus soleatus Vaillant,
1888
Winteria telescopa Brauer, 1901
#
#
?
LC
26, 46
?
#
?
LC
26, 46
#
#
?
LC
26, 46
?
#
#
LC
26
?
#
#
LC
26
?
?
#
#
#
#
LC
LC
26, 46
26
?
?
#
#
?
?
LC
LC
26
26, 46
#
?
?
DD
26, 46
#
#
?
LC
26, 46
#
#
#
LC
26, 46
?
#
#
LC
26, 46
?
#
?
LC
46
?
#
?
LC
26, 46
#
#
?
LC
46
?
#
#
#
?
#
LC
LC
26, 46
26, 46
?
#
?
LC
26, 46
?
#
#
LC
26, 46
#
?
?
LC
26, 46
?
?
#
?
#
#
LC
LC
26, 46
26
#
#
#
LC
26, 46
#
?
?
LC
26, 46
?
#
?
LC
26, 46
?
#
?
LC
26, 46
?
#
?
LC
26
?
#
?
LC
26, 46
Bonapartia pedaliota Goode and
Bean, 1896
Cyclothone acclinidens Garman,
1899
Cyclothone braueri Jespersen and
Tåning, 1926
Cyclothone livida Brauer, 1902
Cyclothone microdon (Günther,
1878)
Diplophos taenia Günther, 1873
Gonostoma atlanticum Norman,
1930
Manducus maderensis (Johnson,
1890)
Sigmops elongatus (Günther,
1878)
Argyropelecus affinis Garman,
1899
Argyropelecus gigas Norman,
1930
Argyropelecus olfersii (Cuvier,
1829)
Argyropelecus sladeni Regan,
1908
Maurolicus muelleri (Gmelin,
1789)
Polyipnus polli Schultz, 1961
Sternoptyx diaphana Hermann,
1781
Sternoptyx pseudobscura Baird,
1971
Valenciennellus tripunctulatus
(Esmark, 1871)
Ichthyococcus ovatus (Cocco,
1838)
Pollichthys mauli (Poll, 1953)
Vinciguerria attenuata (Cocco,
1838)
Vinciguerria nimbaria (Jordan
and Williams, 1895)
Aristostomias grimaldii
Zugmayer, 1913
Aristostomias xenostoma Regan
and Trewavas, 1930
Astronesthes caulophorus Regan
and Trewavas, 1929
Astronesthes niger Richardson,
1845
Astronesthes richardsoni (Poey,
1852)
Reference
(continued)
17
The Fishes of the Gulf of Guinea Oceanic Islands
Higher taxonomy
Order Aulopiformes
Family
Aulopidae
Family
Ipnopidae
Family
Scopelarchidae
Family
Notosudidae
Family
Synodontidae
Family
Paralepididae
453
Species
P
S
A
IUCN
Borostomias elucens (Brauer,
1906)
Chauliodus sloani Bloch and
Schneider, 1801
Eustomias melanonema Regan
and Trewavas, 1930
Eustomias monoclonoides Clarke,
1999
Eustomias monoclonus Regan and
Trewavas, 1930
Leptostomias gracilis Regan and
Trewavas, 1930
Malacosteus niger Ayres, 1848
Neonesthes capensis (Gilchrist
and von Bonde, 1924)
Pachystomias microdon (Günther, 1878)
Photostomias atrox (Alcock,
1890)
Photostomias guernei Collett,
1889
Stomias affinis Günther, 1887
Stomias boa (Risso, 1810)
Stomias longibarbatus (Brauer,
1902)
?
#
?
LC
Reference
26, 46
#
#
#
LC
26, 46
?
#
?
LC
26, 46
?
#
?
LC
26, 46
?
?
#
LC
26
#
?
?
LC
46
?
?
#
#
?
?
LC
LC
26, 46
26, 46
?
#
?
LC
26, 46
?
#
?
LC
26, 46
?
#
#
LC
26, 46
?
?
?
#
#
#
?
?
?
LC
LC
LC
26, 46
26
26, 46
Aulopus cadenati Poll, 1953
X
X
X
LC
26
Bathypterois phenax Parr, 1928
#
?
?
LC
26
Scopelarchoides danae Johnson,
1974
Scopelarchus analis (Brauer,
1902)
Scopelarchus michaelsarsi
Koefoed, 1955
Scopelosaurus argenteus (Maul,
1954)
Scopelosaurus lepidus (Krefft and
Maul, 1955)
Scopelosaurus smithii Bean, 1925
Saurida brasiliensis Norman,
1935
Saurida parri Norman, 1935
Synodus intermedius (Spix and
Agassiz, 1829)
Synodus synodus (Linnaeus,
1758)
Trachinocephalus myops (Forster,
1801)
Lestrolepis intermedia (Poey,
1868)
Paralepis elongata (Brauer, 1906)
#
#
?
LC
26, 46
?
#
?
LC
26, 46
?
#
?
LC
26, 46
#
?
?
LC
26, 46
?
#
?
LC
26, 46
#
#
Err
?
LC
LC
26, 46
?
#
Err
?
LC
LC
20
12, 18
#
#
?
LC
12, 26, 40, 42
#
#
X
LC
12, 20, 26
#
#
?
LC
26, 46
?
#
?
LC
26, 46
(continued)
454
L. M. da Costa et al.
Higher taxonomy
Species
P
S
A
IUCN
Family
Evermannellidae
Family
Omosudidae
Odontostomops normalops (Parr,
1928)
Omosudis lowii Günther, 1887
?
#
?
LC
26, 46
?
#
?
LC
26, 46
#
#
#
LC
26, 46
?
#
?
LC
26, 46
?
#
?
LC
?
#
?
LC
?
#
#
LC
26, 46
?
?
?
#
#
#
?
?
?
LC
LC
LC
26
26, 46
26, 46
?
#
#
LC
26, 46
?
#
?
LC
26
?
#
?
LC
26, 46
?
#
?
LC
26, 46
?
#
?
LC
26
?
#
?
LC
26, 46
?
#
?
LC
26, 46
?
?
#
#
#
?
LC
LC
26, 46
26, 46
?
#
#
LC
26, 46
Order Lampriformes
Family
Eumecichthys fiski (Günther,
Lophotidae
1890)
?
#
?
LC
20, 26, 46
Order Polymixiiformes
Family
Polymixia nobilis Lowe, 1836
Polymixiidae
?
#
?
LC
33, 42
#
?
?
DD
20
#
#
?
LC
26, 46
Order Myctophiformes
Family
Benthosema suborbitale (Gilbert,
Myctophidae
1913)
Bolinichthys photothorax (Parr,
1928)
Centrobranchus nigroocellatus
(Günther, 1873)
Ceratoscopelus warmingii
(Lütken, 1892)
Dasyscopelus asper (Richardson,
1845)
Diaphus holti Tåning, 1918
Diaphus luetkeni (Brauer, 1904)
Diaphus vanhoeffeni (Brauer,
1906)
Diogenichthys atlanticus (Tåning,
1928)
Hygophum macrochir (Günther,
1864)
Hygophum reinhardtii (Lütken,
1892)
Lampanyctus alatus Goode and
Bean, 1896
Lampanyctus isaacsi Wisner,
1974
Lepidophanes guentheri (Goode
and Bean, 1896)
Lobianchia dofleini (Zugmayer,
1911)
Myctophum affine (Lütken, 1892)
Myctophum nitidulum Garman,
1899
Notolychnus valdiviae (Brauer,
1904)
Order Zeiformes
Family Zeidae
Zeus faber Linnaeus, 1758
Order Stylephoriformes
Family
Stylephorus chordatus Shaw,
Stylephoridae
1791
Reference
(continued)
17
The Fishes of the Gulf of Guinea Oceanic Islands
Higher taxonomy
Order Gadiformes
Family
Bregmacerotidae
Family
Melanonidae
Family Moridae
Family
Bathygadidae
Family
Macrouridae
Order Beryciformes
Family
Berycidae
Family
Melamphaidae
Family
Cetomimidae
455
Species
P
S
A
IUCN
Bregmaceros atlanticus Goode
and Bean, 1886
Melanonus zugmayeri Norman,
1930
Gadella imberbis (Vaillant, 1888)
Laemonema laureysi Poll, 1953
Physiculus cyanostrophus Anderson and Tweddle, 2002
Physiculus huloti Poll, 1953
Bathygadus macrops Goode and
Bean, 1885
Bathygadus melanobranchus
Vaillant, 1888
Coelorinchus geronimo Marshall
and Iwamoto, 1973
Malacocephalus laevis (Lowe,
1843)
Malacocephalus occidentalis
Goode and Bean, 1885
?
#
?
LC
26, 46
?
#
#
LC
26, 46
X
X
?
#
X
#
X
X
?
LC
LC
LC
20, 26
7, 26
20
?
X
#
X
?
X
LC
LC
26
7, 26
X
X
X
LC
7, 26
X
X
X
LC
26
X
X
X
LC
7, 26
X
X
X
LC
7, 26
Beryx decadactylus Cuvier, 1829
?
X
?
LC
31, 40
Melamphaes eulepis Ebeling,
1962
Poromitra megalops (Lütken,
1878)
Scopelogadus mizolepis (Günther,
1878)
Cetostoma regani Zugmayer,
1914
?
#
?
LC
15, 46
?
X
?
DD
15, 26
?
#
?
LC
15, 26, 46
?
#
?
DD
#
#
#
LC
12, 26, 35, 40, 42
#
X
#
#
#
#
LC
LC
12, 26, 35, 40, 42
12, 35, 40
#
?
?
LC
26
#
X
?
X
?
X
LC
LC
13, 26
13, 20, 26
?
#
?
DD
?
?
#
LC
13, 26
#
?
?
#
#
#
?
?
?
LC
LC
LC
20, 26
26
13, 18, 26
Order Holocentriformes
Family
Holocentrus adscensionis
Holocentridae
(Osbeck, 1765)
Myripristis jacobus Cuvier, 1829
Sargocentron hastatum (Cuvier,
1829)
Order Ophidiiformes
Family
Acanthonus armatus Günther,
Ophidiidae
1878
Bassozetus normalis Gill, 1883
Brotula barbata (Bloch and
Schneider, 1801)
Ophidion saldanhai Matallanas
and Brito, 1999
Spectrunculus grandis (Günther,
1877)
Family
Carapus acus (Brünnich, 1768)
Carapidae
Echiodon dentatus (Cuvier, 1829)
Family
Grammonus longhursti (Cohen,
Bythitidae
1964)
Reference
(continued)
456
Higher taxonomy
L. M. da Costa et al.
Species
P
S
A
IUCN
Parabrotula plagiophthalma
Zugmayer, 1911
?
#
?
LC
27
#
#
?
LC
20, 27, 46
#
#
X
?
?
?
LC
LC
27
20
X
X
X
VU
27, 40
?
?
?
#
#
#
?
?
?
LC
LC
LC
27, 46
27
27, 46
?
X
?
LC
1, 12, 27, 40
?
#
#
#
?
X
LC
LC
1, 12, 27, 40
1, 12, 20, 40
?
X
?
LC
1, 12, 27, 35, 40
X
?
X
#
#
#
X
?
X
LC
LC
LC
1, 27
42
1, 12, 27, 42
?
X
?
NT
1, 12, 27
?
#
X
?
?
?
VU
LC
1, 12, 27, 40, 46
46
?
#
?
DD
27, 46
#
?
?
DD
27, 46
#
#
#
LC
46
?
#
?
LC
27, 46
#
#
#
?
#
#
#
?
?
LC
LC
LC
9, 27
9, 27, 42, 46
9, 20, 27, 46
X
#
#
LC
9, 20, 27, 46
X
X
X
LC
9, 27
#
#
X
LC
12, 20, 25, 40
?
X
?
LC
12, 27, 35, 40
X
#
#
VU
12, 20, 27, 35, 40, 42
X
#
X
LC
18, 27
Order Scombriformes
Family
Cubiceps pauciradiatus Günther,
Nomeidae
1872
Nomeus gronovii (Gmelin, 1789)
Family
Ariomma bondi Fowler, 1930
Ariommatidae
Family
Pomatomus saltatrix (Linnaeus,
Pomatomidae
1766)
Family
Chiasmodon niger Johnson, 1864
Chiasmodontidae
Kali kerberti (Weber, 1913)
Pseudoscopelus altipinnis Parr,
1933
Family
Acanthocybium solandri (Cuvier,
Scombridae
1832)
Auxis thazard (Lacépède, 1800)
Euthynnus alletteratus
(Rafinesque, 1810)
Katsuwonus pelamis (Linnaeus,
1758)
Sarda sarda (Bloch, 1793)
Scomber colias Gmelin, 1789
Scomberomorus tritor (Cuvier,
1832)
Thunnus albacares (Bonnaterre,
1788)
Thunnus obesus (Lowe, 1839)
Family
Paracaristius aquilus Stevenson
Caristiidae
and Kenaley, 2011
Paracaristius nudarcus Stevenson and Kenaley, 2011
Platyberyx andriashevi (Kukuev,
Parin and Trunov, 2012)
Platyberyx opalescens Zugmayer,
1911
Family
Taractichthys longipinnis (Lowe,
Bramidae
1843)
Family
Gempylus serpens Cuvier, 1829
Gempylidae
Nealotus tripes Johnson, 1865
Nesiarchus nasutus Johnson,
1862
Promethichthys prometheus
(Cuvier, 1832)
Ruvettus pretiosus Cocco, 1833
Order Syngnathiformes
Family
Dactylopterus volitans (Linnaeus,
Dactylopteridae
1758)
Family Mullidae Mulloidichthys martinicus
(Cuvier, 1829)
Pseudupeneus prayensis (Cuvier,
1829)
Family
Callionymus bairdi Jordan, 1888
Callionymidae
Reference
(continued)
17
The Fishes of the Gulf of Guinea Oceanic Islands
Higher taxonomy
Family
Aulostomidae
Family
Fistulariidae
Family
Syngnathidae
Order Kurtiformes
Family
Apogonidae
Order Gobiiformes
Family
Eleotridae
Family
Gobiidae
457
Species
P
S
A
IUCN
Synchiropus phaeton (Günther,
1861)
Aulostomus strigosus Wheeler,
1955
Fistularia petimba Lacépède,
1803
Fistularia tabacaria Linnaeus,
1758
Enneacampus kaupi (Bleeker,
1863)
Hippocampus algiricus Kaup,
1856
Microphis aculeatus (Kaup, 1856)
X
X
X
LC
27
X
#
X
LC
12, 20, 25, 40
#
#
X
LC
20
X
#
X
LC
12, 26, 40
?
X
?
LC
36
#
#
?
VU
18, 40
#
#
?
DD
18, 28, 47
Apogon imberbis (Linnaeus,
1758)
Apogon pseudomaculatus
Longley, 1932
Paroncheilus affinis (Poey, 1875)
Phaeoptyx pigmentaria (Poey,
1860)
#
#
#
LC
12, 18, 27, 35, 40
?
#
?
LC
18, 35, 40
X
X
#
X
X
#
LC
LC
18, 27, 35
18, 27, 40
X
#
X
LC
22, 27, 28
X
X
X
LC
E#
E#
E#
DD
?
?
#
NE
#
?
#
E#
X
E
LC
VU
27
22, 28
X
#
X
LC
22, 27, 28, 42
#
#
?
EN
12, 22, 27, 28, 40
X
X
#
LC
22, 27
#
#
#
LC
22, 27
X
#
#
VU
18, 22, 27
X
X
X
LC
22, 27, 30
E
E#
?
VU
18, 22, 27
?
#
?
LC
12, 40
X
X
X
LC
22, 27
X
X
X
X
X
X
LC
LC
22, 27
22, 27
Bostrychus africanus
(Steindachner, 1879)
Dormitator lebretonis
(Steindachner, 1870)
Eleotris annobonensis Blanc,
Cadenat and Stauch, 1968
Eleotris feai Thys van den
Audenaerde and Tortonese, 1974
Eleotris vittata Duméril, 1861
Awaous bustamantei (Greeff,
1882)
Awaous lateristriga (Duméril,
1861)
Bathygobius burtoni
(O’Shaughnessy, 1875)
Bathygobius casamancus
(Rochebrune, 1880)
Bathygobius soporator (Valenciennes, 1837)
Corcyrogobius lubbocki Miller,
1988
Ctenogobius lepturus (Pfaff,
1933)
Didogobius amicuscaridis
Schliewen and Kovačić, 2008
Gnatholepis thompsoni Jordan,
1904
Gobioides africanus (Giltay,
1935)
Gobioides sagitta (Günther, 1862)
Gobionellus occidentalis
(Boulenger, 1909)
Reference
18, 27, 28
(continued)
458
L. M. da Costa et al.
Higher taxonomy
Species
P
S
A
IUCN
#
#
?
LC
18, 22
X
X
X
LC
22, 27
X
#
#
LC
18
?
E#
?
VU
18, 19, 22, 27, 40
#
#
#
LC
18
#
#
X
LC
18, 22, 27
X
#
X
LC
22, 27, 28, 47
E#
E#
E#
LC
16, 18, 22, 27
E#
E#
E#
DD
16, 18, 22, 27
?
E#
?
NE
X
#
#
LC
18, 22, 27, 40
E#
E#
?
LC
12, 18, 22, 40
?
X
?
LC
22
Family
Oxudercidae
Gobius aff. rubropunctatus
Delais, 1951
Gobius senegambiensis
Metzelaar, 1919
Gorogobius nigricinctus (Delais,
1951)
Gorogobius stevcici Kovačić and
Schliewen, 2008
Nematogobius brachynemus
Pfaff, 1933
Nematogobius maindroni
(Sauvage, 1880)
Porogobius schlegelii (Günther,
1861)
Sicydium brevifile Ogilvie-Grant,
1884
Sicydium bustamantei Greeff,
1884
Thorogobius laureatus Sauberer,
Iwamoto and Ahnelt, 2018
Wheelerigobius maltzani
(Steindachner, 1881)
Wheelerigobius wirtzi Miller,
1988
Yongeichthys thomasi
(Boulenger, 1916)
Periophthalmus barbarus (Linnaeus, 1766)
#
#
X
LC
27, 28, 47
X
X
X
X
X
X
LC
LC
27
12, 27, 35, 40
X
#
X
LC
18, 20, 27
X
#
X
LC
12, 20, 27, 42
#
#
#
NT
12, 20, 27, 28, 42
X
X
X
VU
27
X
X
X
LC
27
X
?
?
DD
20
?
#
?
LC
20
X
X
X
LC
20, 27
X
#
X
LC
20, 27
?
?
?
?
?
#
#
X
#
#
?
#
?
#
?
DD
LC
LC
DD
12, 20, 27, 42
12, 27, 40
20, 27
44
Order Carangiformes
Family
Sphyraena afra Peters, 1844
Sphyraenidae
Sphyraena barracuda (Edwards,
1771)
Sphyraena guachancho Cuvier,
1829
Sphyraena sphyraena (Linnaeus,
1758)
Family
Galeoides decadactylus (Bloch,
Polynemidae
1795)
Pentanemus quinquarius (Linnaeus, 1758)
Polydactylus quadrifilis (Cuvier,
1829)
Family
Psettodes belcheri Bennett, 1831
Psettodidae
Family
Citharus linguatula (Linnaeus,
Citharidae
1758)
Family
Syacium guineense (Bleeker,
Cyclopsettidae
1862)
Family
Arnoglossus imperialis
Bothidae
(Rafinesque, 1810)
Arnoglossus sp. Bleeker, 1862
Bothus guibei Stauch, 1966
Bothus lunatus (Linnaeus, 1758)
Bothus podas (Delaroche, 1809)
Chascanopsetta lugubris Alcock,
1894
Reference
(continued)
17
The Fishes of the Gulf of Guinea Oceanic Islands
Higher taxonomy
Family
Paralichthyidae
Family Soleidae
Family
Cynoglossidae
Family
Istiophoridae
Family
Carangidae
459
Species
P
S
A
IUCN
Monolene microstoma Cadenat,
1937
Citharichthys stampflii
(Steindachner, 1894)
Dagetichthys lusitanicus (de Brito
Capello, 1868)
Dicologlossa cuneata (Moreau,
1881)
Heteromycteris proboscideus
(Chabanaud, 1925)
Microchirus boscanion
(Chabanaud, 1926)
Microchirus frechkopi
Chabanaud, 1952
Microchirus hexophthalmus
(Bennett, 1831)
Microchirus wittei Chabanaud,
1950
Pegusa lascaris (Risso, 1810)
Pegusa triophthalma (Bleeker,
1863)
Cynoglossus browni Chabanaud,
1949
Cynoglossus cadenati
Chabanaud, 1947
Cynoglossus canariensis
Steindachner, 1882
Cynoglossus monodi Chabanaud,
1949
Cynoglossus senegalensis (Kaup,
1858)
Istiophorus albicans (Latreille,
1804)
Istiophorus platypterus (Shaw,
1792)
Makaira nigricans Lacépède,
1802
Alectis alexandrina (Geoffroy
Saint-Hilaire, 1817)
Alectis ciliaris (Bloch, 1787)
Caranx bartholomaei Cuvier,
1833
Caranx crysos (Mitchill, 1815)
Caranx fischeri Smith-Vaniz and
Carpenter, 2007
Caranx hippos (Linnaeus, 1766)
Caranx latus Agassiz, 1831
Caranx lugubris Poey, 1860
Caranx rhonchus Geoffroy SaintHilaire, 1817
Chloroscombrus chrysurus (Linnaeus, 1766)
Decapterus macarellus (Cuvier,
1833)
Decapterus punctatus (Cuvier,
1829)
X
X
X
LC
Reference
27
?
#
?
LC
44
X
X
X
DD
27
?
#
?
LC
18
X
#
X
DD
27
X
X
X
DD
27
?
#
?
DD
20
?
#
?
LC
20
X
#
X
LC
27
X
X
#
X
X
X
LC
DD
27
27
?
#
?
DD
44
#
?
?
DD
?
#
?
NT
44
?
#
?
NT
18
?
#
?
NT
12
?
X
?
NE
3, 12, 40
?
#
?
LC
27
?
X
?
VU
3, 31, 40
X
X
X
LC
1, 27, 35
X
X
X
X
X
?
LC
LC
27
18, 20, 40
X
X
#
#
#
X
LC
LC
12, 20, 40, 42
18
X
#
X
?
#
#
X
X
X
X
?
?
LC
LC
LC
LC
12, 18, 35, 40
18, 27, 40
18, 27, 40
X
#
X
LC
27
X
#
X
LC
12, 20, 27, 42
X
#
X
LC
12, 20, 27, 40
(continued)
460
Higher taxonomy
L. M. da Costa et al.
Species
P
S
A
IUCN
Elagatis bipinnulata (Quoy and
Gaimard, 1825)
Hemicaranx bicolor (Günther,
1860)
Lichia amia (Linnaeus, 1758)
Pseudocaranx dentex (Bloch and
Schneider, 1801)
Selar crumenophthalmus (Bloch,
1793)
Selene dorsalis (Gill, 1863)
Seriola carpenteri Mather, 1971
Seriola rivoliana Valenciennes,
1833
Trachinotus goreensis Cuvier,
1832
Trachinotus ovatus (Linnaeus,
1758)
Uraspis secunda (Poey, 1860)
Echeneis naucrates Linnaeus,
1758
Remora brachyptera (Lowe,
1839)
Remora remora (Linnaeus, 1758)
Coryphaena equiselis Linnaeus,
1758
Coryphaena hippurus Linnaeus,
1758
X
#
X
LC
12, 27, 35, 40, 42
X
X
X
LC
27
X
X
X
X
X
X
LC
LC
27
27
X
#
#
LC
12, 20, 42
X
X
X
#
X
X
X
X
?
LC
LC
LC
12, 20, 27, 42
20, 27
18, 20, 27, 40
?
X
?
LC
X
#
#
LC
12, 27, 35, 42
X
X
X
X
X
?
LC
LC
12, 20, 27
27, 40
#
X
?
LC
12, 27
?
?
#
X
?
?
LC
LC
27
12, 27
?
#
?
LC
31, 40
?
I
?
LC
28
Order Atheriniformes
Family
Atherina lopeziana Rossignol and
Atherinidae
Blache, 1961
X
X
X
DD
26
Order Cyprinodontiformes
Family
Aplocheilichthys spilauchen
Procatopodidae
(Duméril, 1861)
I
?
?
LC
47
Order Beloniformes
Family
Belonidae
X
X
X
LC
12, 26
X
X
X
LC
26
X
X
X
LC
12, 18
X
X
X
LC
26
X
#
X
LC
12, 42
#
#
X
LC
12, 26
Family
Echeneidae
Family
Coryphaenidae
Order Cichliformes
Family
Cichlidae
Oreochromis mossambicus
(Peters, 1852)
Ablennes hians (Valenciennes,
1846)
Platybelone argalus (Lesueur,
1821)
Platybelone argalus
annobonensis Collette and Parin,
1970
Strongylura senegalensis (Valenciennes, 1846)
Tylosurus acus rafale Collette and
Parin, 1970
Tylosurus crocodilus (Péron and
Lesueur, 1821)
Reference
(continued)
17
The Fishes of the Gulf of Guinea Oceanic Islands
461
Higher taxonomy
Species
P
S
A
IUCN
Family
Hemiramphidae
Hemiramphus balao Lesueur,
1821
Hemiramphus brasiliensis (Linnaeus, 1758)
Hyporhamphus picarti (Valenciennes, 1847)
Cheilopogon cyanopterus (Valenciennes, 1847)
Cheilopogon melanurus (Valenciennes, 1847)
Cheilopogon milleri (Gibbs and
Staiger, 1970)
Cheilopogon pinnatibarbatus
(Bennett, 1831)
Exocoetus obtusirostris Günther,
1866
Exocoetus volitans Linnaeus,
1758
Fodiator acutus (Valenciennes,
1847)
Hirundichthys affinis (Günther,
1866)
Prognichthys gibbifrons (Valenciennes, 1847)
X
#
#
LC
12, 26, 42
X
X
X
LC
26
X
X
X
LC
26
X
#
#
LC
20, 26
?
X
?
LC
12
#
X
X
LC
26
X
X
X
LC
?
#
?
LC
#
X
?
LC
?
X
?
LC
X
#
#
LC
X
#
X
LC
?
X
?
DD
?
X
?
NE
30
X
#
?
X
#
#
X
?
?
LC
LC
DD
26
18, 42, 47
18, 26, 28, 47
E#
?
E#
E#
?
?
LC
NE
17, 18, 27, 40
34
#
#
#
LC
12, 27
?
X
#
LC
12, 27
?
X
#
LC
12, 40
?
?
X
LC
27
#
#
?
LC
18
?
#
?
LC
12, 40
#
#
#
LC
12, 40
?
#
#
LC
12
Family
Exocoetidae
Order Mugiliformes
Family
Mugilidae
Chelon dumerili (Steindachner,
1870)
Chelon richardsonii (Smith,
1846)
Mugil cephalus Linnaeus, 1758
Mugil curema Valenciennes, 1836
Parachelon grandisquamis
(Valenciennes, 1836)
Order Gobiesociformes
Family
Apletodon wirtzi Fricke, 2007
Gobiesocidae
Lecanogaster gorgoniphila Fricke
and Wirtz, 2017
Order Bleniiformes
Family
Labrisomidae
Family
Blenniidae
Labrisomus nuchipinnis (Quoy
and Gaimard, 1824)
Entomacrodus cadenati Springer,
1967
Hypleurochilus aequipinnis
(Günther, 1861)
Hypleurochilus langi (Fowler,
1923)
Hypleurochilus
pseudoaequipinnis Bath, 1994
Microlipophrys velifer (Norman,
1935)
Ophioblennius atlanticus (Valenciennes, 1836)
Scartella cristata (Linnaeus,
1758)
Reference
20, 26
(continued)
462
Higher taxonomy
L. M. da Costa et al.
Species
Order Acanthuriformes
Family
Lobotes surinamensis (Bloch,
Lobotidae
1790)
Family
Centropyge aurantonotus BurPomacanthidae
gess, 1974
Holacanthus africanus Cadenat,
1951
Family
Drepane africana Osório, 1892
Drepaneidae
Family
Chaetodon hoefleri Steindachner,
Chaetodontidae
1881
Chaetodon robustus Günther,
1860
Prognathodes marcellae (Poll,
1950)
Family
Chaetodipterus lippei
Ephippidae
Steindachner, 1895
Ephippus goreensis Cuvier, 1831
Family
Acanthurus monroviae
Acanthuridae
Steindachner, 1876
Prionurus biafraensis (Blache
and Rossignol, 1962)
Family
Antigonia capros Lowe, 1843
Antigoniidae
Order Lophiiformes
Family
Antennariidae
Family
Oneirodidae
Family
Ceratiidae
Family
Linophrynidae
Antennarius multiocellatus
(Valenciennes, 1837)
Antennarius pardalis (Valenciennes, 1837)
Antennarius striatus (Shaw, 1794)
Histrio histrio (Linnaeus, 1758)
Lophodolos acanthognathus
Regan, 1925
Oneirodes anisacanthus (Regan,
1925)
Oneirodes carlsbergi (Regan and
Trewavas, 1932)
Ceratias uranoscopus Murray,
1877
Cryptopsaras couesii Gill, 1883
Linophryne arborifera Regan,
1925
Order Tetraodontiformes
Chilomycterus mauretanicus
Family
Diodontidae
(Le Danois, 1954)
Chilomycterus reticulatus (Linnaeus, 1758)
Diodon holocanthus Linnaeus,
1758
Diodon hystrix Linnaeus, 1758
P
S
A
IUCN
Reference
?
#
?
LC
12, 27
?
#
?
LC
18, 40
#
X
?
LC
12, 27, 40
X
X
?
LC
12, 18, 20, 27, 42
?
#
#
LC
20, 27
?
#
?
LC
12, 18, 40, 42
?
#
?
LC
18, 20, 27, 40
?
X
?
LC
30
?
X
X
X
?
#
LC
LC
12, 20, 27, 40
12, 18, 20, 27, 35
E
E#
E
LC
12, 18, 27, 35
?
#
?
LC
27
?
#
?
LC
18
#
#
?
LC
18, 20, 26
?
?
?
#
#
#
?
?
?
LC
LC
LC
26
26
26
?
#
?
DD
26
?
#
?
LC
26
?
#
?
LC
26, 46
?
?
#
#
?
?
LC
LC
20
26
#
X
X
LC
20, 27
?
X
#
LC
12, 40
#
X
#
LC
12, 20
?
X
?
LC
12
(continued)
17
The Fishes of the Gulf of Guinea Oceanic Islands
Higher taxonomy
Species
Family
Tetraodontidae
Canthigaster rostrata (Bloch,
1786)
Canthigaster supramacula Moura
and Castro, 2002
Lagocephalus laevigatus (Linnaeus, 1766)
Lagocephalus lagocephalus (Linnaeus, 1758)
Sphoeroides marmoratus (Lowe,
1838)
Sphoeroides pachygaster (Müller
and Troschel, 1848)
Acanthostracion guineense
(Bleeker, 1865)
Acanthostracion notacanthus
(Bleeker, 1863)
Aluterus heudelotii Hollard, 1855
Aluterus monoceros (Linnaeus,
1758)
Aluterus schoepfii (Walbaum,
1792)
Aluterus scriptus (Osbeck, 1765)
Cantherhines macrocerus
(Hollard, 1853)
Cantherhines pullus (Ranzani,
1842)
Stephanolepis hispida (Linnaeus,
1766)
Balistes capriscus Gmelin, 1789
Balistes punctatus Gmelin, 1789
Balistes vetula Linnaeus, 1758
Canthidermis maculata (Bloch,
1786)
Canthidermis sufflamen (Mitchill,
1815)
Melichthys niger (Bloch, 1786)
Family
Ostraciidae
Family
Monacanthidae
Family
Balistidae
Order Centrarchiformes
Family
Kyphosus bigibbus Lacépède,
Kyphosidae
1801
Kyphosus incisor (Cuvier, 1831)
Kyphosus sectatrix (Linnaeus,
1758)
Kyphosus vaigiensis (Quoy and
Gaimard, 1825)
Family
Cirrhitus atlanticus Osório, 1893
Cirrhitidae
Order Acropomatiformes
Family
Synagrops bellus (Goode and
Synagropidae
Bean, 1896)
Family
Epigonus constanciae (Giglioli,
Epigonidae
1880)
Epigonus denticulatus Dieuzeide,
1950
Family
Howella sherborni (Norman,
Howellidae
1930)
463
P
S
#
Err
#
#
X
A
IUCN
Reference
LC
20
?
LC
18, 35, 40
#
X
LC
12, 20, 27
X
X
#
LC
20, 27
X
X
X
LC
12, 27, 35, 40
#
X
X
LC
20, 27
X
X
X
LC
20, 27
#
X
?
DD
1, 39
#
X
X
X
?
X
LC
LC
30
20
X
X
X
LC
27
X
X
#
?
X
?
LC
LC
12, 27, 35, 40
43
X
X
#
LC
12, 27, 35, 40
#
X
#
LC
#
#
X
X
#
#
X
#
#
X
X
X
VU
VU
NT
LC
12, 20, 27, 35, 40
12, 20, 27, 35, 40
27
27
X
X
?
LC
12, 35, 40
X
X
X
LC
27, 35, 40
X
X
X
LC
27
X
?
#
#
X
?
NE
LC
12, 28
42
X
X
X
LC
#
#
X
LC
12, 27, 35, 40
?
#
?
LC
20
?
#
?
LC
18
?
#
?
LC
#
#
?
NE
46
(continued)
464
Higher taxonomy
L. M. da Costa et al.
Species
Order Perciformes *sedis mutabilis*
Family
Alphestes afer (Bloch, 1793)
Serranidae
Anthias anthias (Linnaeus, 1758)
Anthias cyprinoides (Katayama
and Amaoka, 1986)
Cephalopholis nigri (Günther,
1859)
Cephalopholis taeniops (Valenciennes, 1828)
Epinephelus adscensionis
(Osbeck, 1765)
Epinephelus aeneus (Geoffroy
Saint-Hilaire, 1817)
Epinephelus costae
(Steindachner, 1878)
Epinephelus goreensis (Valenciennes, 1830)
Epinephelus marginatus (Lowe,
1834)
Hyporthodus haifensis
(Ben-Tuvia, 1953)
Liopropoma emanueli Wirtz and
Schliewen, 2012
Liopropoma n.sp.
Paranthias furcifer (Valenciennes, 1828)
Pseudogramma guineensis (Norman, 1935)
Rypticus saponaceus (Bloch and
Schneider, 1801)
Rypticus subbifrenatus Gill, 1861
Serranus accraensis (Norman,
1931)
Serranus cabrilla (Linnaeus,
1758)
Serranus drewesi Iwamoto, 2018
Serranus heterurus (Cadenat,
1937)
Serranus pulcher Wirtz and
Iwamoto, 2016
Family
Heteropriacanthus cruentatus
Priacanthidae
(Lacépède, 1801)
Priacanthus arenatus Cuvier,
1829
Branchiostegus semifasciatus
(Norman, 1931)
Family
Erythrocles monodi Poll and
Emmelichthyidae
Cadenat, 1954
Family
Apsilus fuscus Valenciennes,
1830
Lutjanidae
Lutjanus agennes Bleeker, 1863
Lutjanus dentatus (Duméril,
1861)
Lutjanus endecacanthus Bleeker,
1863
P
S
A
IUCN
Reference
?
#
?
X
#
?
?
X
X
LC
LC
DD
18, 27, 36, 40, 45
12, 20
45
#
#
?
LC
8, 12, 27, 35, 40, 42
#
#
#
LC
8, 12, 27, 35, 40, 42, 45
#
#
#
LC
12, 40, 42, 45
X
X
X
NT
12, 20, 27, 35
X
X
X
DD
27
X
#
X
NT
12, 20, 27, 40
?
#
?
VU
27, 42
X
X
X
LC
27
?
X
?
NE
31, 40
X
#
X
#
?
#
LC
18
8, 12, 20, 27, 40, 42
X
#
#
LC
18, 27, 45
X
#
#
LC
12, 18, 20, 27, 35, 40, 42
#
X
X
#
#
?
LC
LC
18, 27, 45
20, 39, 45
#
#
?
LC
27, 39, 42
?
?
E#
#
?
#
DD
LC
39, 45
39, 45
E#
E#
?
LC
18, 32, 40, 45
X
X
#
LC
12, 35, 40
#
#
X
LC
20
?
X
?
LC
12
?
#
?
LC
12, 42
X
#
X
LC
2, 12, 20, 27, 40
X
#
#
#
X
X
DD
DD
27, 28, 40, 47
2, 27, 40, 42
#
#
X
DD
2, 18, 27, 28, 42
(continued)
17
The Fishes of the Gulf of Guinea Oceanic Islands
Higher taxonomy
Family
Gerreidae
Family
Haemulidae
Family
Sparidae
465
Species
P
S
A
IUCN
Lutjanus fulgens (Valenciennes,
1830)
Lutjanus goreensis (Valenciennes, 1830)
Lutjanus griseus (Linnaeus, 1758)
Eucinostomus melanopterus
(Bleeker, 1863)
Gerres nigri Günther, 1859
Brachydeuterus auritus (Valenciennes, 1832)
Parakuhlia macrophthalmus
(Osório, 1893)
Parapristipoma humile
(Bowdich, 1825)
Parapristipoma octolineatum
(Valenciennes, 1833)
Plectorhinchus macrolepis
(Boulenger, 1899)
Plectorhinchus mediterraneus
(Guichenot, 1850)
Pomadasys incisus (Bowdich,
1825)
Pomadasys jubelini (Cuvier,
1830)
Pomadasys perotaei (Cuvier,
1830)
Pomadasys rogerii (Cuvier, 1830)
Pomadasys suillus (Valenciennes,
1833)
Boops boops (Linnaeus, 1758)
Dentex canariensis Steindachner,
1881
Dentex congoensis Poll, 1954
Dentex gibbosus (Rafinesque,
1810)
Dentex macrophthalmus (Bloch,
1791)
Lithognathus mormyrus (Linnaeus, 1758)
Oblada melanura (Linnaeus,
1758)
Pagellus bellottii Steindachner,
1882
Pagrus africanus Akazaki, 1962
Pagrus auriga Valenciennes,
1843
Pagrus caeruleostictus (Valenciennes, 1830)
Pagrus pagrus (Linnaeus, 1758)
Spicara alta (Osório, 1917)
Spicara melanurus (Valenciennes, 1830)
Spicara nigricauda (Norman,
1931)
X
#
X
LC
Reference
2, 12, 20, 27, 40, 42
#
#
X
DD
12, 20, 27, 28, 40, 47
?
X
?
#
#
#
LC
LC
12, 27, 28, 42, 47
X
X
X
#
X
X
LC
NT
27
18, 20, 27
X
#
X
DD
12, 27, 40
X
X
X
LC
27
X
X
X
LC
27
X
#
X
LC
27, 28
X
X
X
LC
27
X
#
#
LC
20, 27, 40, 42
X
#
X
LC
28
?
X
#
LC
X
#
#
X
X
?
LC
NE
12, 20
X
#
Err
X
LC
LC
12, 20, 27, 35, 40, 42
20
#
X
#
X
X
X
LC
LC
12, 20, 27, 42
27
X
X
X
LC
27
X
X
X
LC
27
X
X
X
LC
27, 35
X
#
X
LC
12, 20, 27, 42
X
X
X
X
X
X
LC
LC
27
27
X
#
X
LC
12, 20, 27, 42
?
X
X
X
X
X
?
X
X
LC
LC
LC
27
27, 40
X
#
?
LC
12
(continued)
466
L. M. da Costa et al.
Higher taxonomy
Family
Lethrinidae
Family
Sciaenidae
Family
Monodactylidae
Family
Cepolidae
Order Perciformes
Family
Pomacentridae
Family
Labridae
Family Scaridae
Species
P
S
A
IUCN
Spondyliosoma cantharus (Linnaeus, 1758)
Lethrinus atlanticus Valenciennes, 1830
Pseudotolithus senegalensis
(Valenciennes, 1833)
Pseudotolithus senegallus
(Cuvier, 1830)
Umbrina canariensis Valenciennes, 1843
Umbrina cirrosa (Linnaeus,
1758)
Monodactylus sebae (Cuvier,
1829)
Cepola pauciradiata Cadenat,
1950
X
X
X
LC
Reference
27
#
#
#
LC
6, 12, 20, 27, 40, 42
?
#
?
EN
18, 20
?
#
?
VU
18, 42
?
X
#
LC
20
?
X
?
VU
18
X
#
X
LC
18, 27, 28
X
#
X
DD
27
Abudefduf hoefleri (Steindachner,
1881)
Abudefduf saxatilis (Linnaeus,
1758)
Abudefduf taurus (Müller and
Troschel, 1848)
Azurina multilineata (Guichenot,
1853)
Chromis cadenati Whitley, 1951
Chromis limbata (Valenciennes,
1833)
Microspathodon frontatus Emery,
1970
Stegastes imbricatus Jenyns, 1840
Acantholabrus palloni (Risso,
1810)
Bodianus pulchellus (Poey, 1860)
Bodianus speciosus (Bowdich,
1825)
Clepticus africanus Heiser,
Moura and Robertson, 2000
Coris atlantica Günther, 1862
Doratonotus megalepis Günther,
1862
Thalassoma newtoni (Osório,
1891)
Xyrichtys novacula (Linnaeus,
1758)
Xyrichtys sanctaehelenae (Günther, 1868)
Nicholsina collettei Schultz, 1968
Nicholsina usta (Valenciennes,
1840)
Scarus hoefleri (Steindachner,
1881)
Sparisoma choati Rocha, Brito
and Robertson, 2012
X
#
?
DD
27, 35, 40, 42
X
#
X
LC
12, 27, 35, 40, 42
?
#
#
LC
18
#
X
?
LC
12, 27, 35, 40
?
?
X
X
?
?
LC
LC
31, 40
31, 40
X
#
#
LC
12, 27, 35, 40, 42
#
X
#
X
#
X
LC
LC
12
18, 27
?
X
#
X
?
X
LC
DD
12, 18, 40, 42
12, 20
?
E#
?
DD
18, 35
X
X
X
X
?
?
LC
LC
12, 35, 40
27
X
#
?
LC
18, 27
#
#
X
LC
12, 20, 27, 35, 40
?
#
?
LC
18
X
?
X
#
X
?
LC
LC
18, 27
18
#
#
X
LC
12, 27, 35, 40
X
#
X
NE
18, 23, 27, 35
(continued)
17
The Fishes of the Gulf of Guinea Oceanic Islands
467
Higher taxonomy
Species
P
S
A
IUCN
Family
Ammodytidae
Family
Trachinidae
Gymnammodytes capensis (Barnard, 1927)
Trachinus armatus Bleeker, 1861
Trachinus lineolatus Fischer,
1885
Trachinus radiatus Cuvier, 1829
Uranoscopus albesca Regan,
1915
Uranoscopus cadenati Poll, 1959
Uranoscopus polli Cadenat, 1951
Bembrops greyae Poll, 1959
?
X
?
LC
X
?
#
X
?
?
LC
LC
20
26
X
X
?
X
?
X
LC
LC
20
27
X
#
?
X
X
#
X
X
?
LC
LC
LC
27
12, 20, 27
27, 44
Helicolenus dactylopterus (Delaroche, 1809)
Ectreposebastes imus Garman,
1899
Setarches guentheri Johnson,
1862
Pontinus accraensis Norman,
1935
Pontinus kuhlii (Bowdich, 1825)
Scorpaena angolensis Norman,
1935
Scorpaena annobonae
Eschmeyer, 1969
Scorpaena elongata Cadenat,
1943
Scorpaena laevis Troschel, 1866
Scorpaena normani Cadenat,
1943
Scorpaena stephanica Cadenat,
1943
Scorpaenodes africanus Pfaff,
1933
Chelidonichthys gabonensis (Poll
and Roux, 1955)
Chelidonichthys lastoviza
(Bonnaterre, 1788)
Lepidotrigla cadmani Regan,
1915
Lepidotrigla carolae Richards,
1968
Peristedion cataphractum (Linnaeus, 1758)
Solitas gruveli (Pellegrin, 1905)
X
X
X
LC
26
X
X
#
LC
26
X
X
X
LC
26
X
#
X
LC
18, 26
?
X
#
X
?
X
DD
LC
12, 26
26
?
?
#
DD
X
X
X
LC
26
X
X
#
X
#
X
LC
LC
12, 20, 26
26
X
X
X
LC
26
?
#
#
DD
18, 26
?
#
?
LC
20
X
?
?
LC
20
#
#
X
LC
26
X
#
X
LC
20, 26
X
X
X
LC
26
X
#
X
LC
20, 26
Family
Uranoscopidae
Family
Bembropidae
Family
Sebastidae
Family
Setarchidae
Family
Scorpaenidae
Family
Triglidae
Family
Peristediidae
Family
Platycephalidae
Reference
468
L. M. da Costa et al.
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Chapter 18
The Amphibians of the Gulf of Guinea
Oceanic Islands
Rayna C. Bell, Luis M. P. Ceríaco, Lauren A. Scheinberg,
and Robert C. Drewes
Abstract This chapter reviews the diversity, evolutionary relationships, ecology,
and conservation of the Gulf of Guinea oceanic islands’ endemic caecilian and
anuran fauna. A total of nine amphibian species (representing five families) are
known from São Tomé and Príncipe islands, all of which are endemic. No amphibians have been reported from Annobón. Taxonomic research on this group of
animals began in the second half of the nineteenth century with subsequent refinement following the advent of molecular techniques. The presence of several amphibians from distinct evolutionary lineages is unexpected for oceanic islands and has
motivated several biogeographic studies to reconstruct the evolutionary histories of
these enigmatic species. Yet, the continental source for many of the islands’
amphibians remains unknown. The amphibians of São Tomé and Príncipe also
exhibit intriguing phenotypic diversity for addressing long-standing hypotheses in
evolutionary biology, including body size evolution and gigantism on islands,
intraspecific variation and interspecific divergence in coloration, and reproductive
and dietary niche partitioning. Recent studies have confirmed the presence of the
fungal pathogen Batrachochytrium dendrobatidis in amphibian communities on
both São Tomé and Príncipe, but it is unclear whether this pathogen is negatively
impacting local populations. Most of the Gulf of Guinea oceanic island endemic
amphibians are incredibly abundant and widespread, occurring in primary forest,
secondary forest, and agricultural habitats across the islands. Three anuran species
R. C. Bell (*) · L. A. Scheinberg · R. C. Drewes
Department of Herpetology, Institute for Biodiversity Science and Sustainability, California
Academy of Sciences, San Francisco, CA, USA
e-mail: rbell@calacademy.org
L. M. P. Ceríaco
Museu de História Natural e da Ciência da Universidade do Porto, Porto, Portugal
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório
Associado, Universidade do Porto, Vairão, Portugal
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO, Vairão, Portugal
Departamento de Zoologia e Antropologia (Museu Bocage), Museu Nacional de História
Natural e da Ciência, Universidade de Lisboa, Lisbon, Portugal
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_18
479
480
R. C. Bell et al.
(Hyperolius thomensis, Leptopelis palmatus, Ptychadena newtoni) have more limited distributions and/or more specialized ecologies; consequently, additional landuse change poses a threat to the long-term persistence of these taxa.
Keywords Anura · Gymnophiona · Hybridization · Endemism · Taxonomy ·
Conservation
Introduction
Island faunas have inspired evolutionary biologists for centuries, and the enigmatic
history of insular amphibians is particularly captivating. Amphibians are considered
poor dispersers across saltwater barriers and are thus naturally absent from most
oceanic islands (Darwin 1859; Vitt and Caldwell 2014). Yet overseas dispersal and
in situ diversification have contributed to the accumulation of a surprisingly diverse
amphibian fauna in the Gulf of Guinea oceanic islands, which are located
250–300 km from the western coast of Central Africa. The presence of a combined
nine amphibian species on São Tomé and Príncipe islands, all of which are endemic,
presents an intriguing biogeographic anomaly within which to explore the potential
pathways and timing of overseas dispersal events. In addition, some lineages have
further diversified within and between islands in the archipelago, presenting the
opportunity to investigate the tempo and mechanisms underlying in situ diversification. This chapter presents an updated taxonomic overview of the amphibians on São
Tomé and Príncipe islands (no amphibians occur on Annobón), highlighting the
biogeographic patterns, organismal biology, and conservation threats for each species. The amphibian fauna of Bioko Island, a land-bridge island that is part of
the Gulf of Guinea archipelago, is entirely distinct from that of the oceanic islands
in the archipelago (see Sánchez-Vialas et al. 2020). We also provide a brief history of
the research on amphibians in the archipelago and highlight important avenues for
future work.
History of Amphibian Research
The history of amphibian research in the Gulf of Guinea oceanic islands is closely
linked to the history of reptile research, as most authors have worked with both
groups. Ceríaco et al. (2022) provide a comprehensive summary of the herpetological surveys and studies carried out on the islands. Hence, we focus on the primarily
amphibian-focused studies and refer to Ceríaco et al. (2022) for more general
studies.
The first herpetological studies in the Gulf of Guinea oceanic islands were based
on opportunistic collections by European medical staff and colonial officers who
visited or worked in the region. The first published record of an amphibian from São
Tomé dates to 1868, when the German zoologist Wilhelm C. H. Peters (1815–1883)
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described the Príncipe Giant Tree Frog Hylambates (currently Leptopelis) palmatus
based on three female specimens (holotype ZMB 6067) collected by German
explorer Heinrich Wolfgang Ludwig Dhorn (1838–1913) on Príncipe (Peters
1868). In 1870, Peters described the Príncipe Puddle Frog Arthroleptis dispar
(later transferred to Phrynobatrachus by Laurent 1941) based on a single specimen
from Príncipe (holotype ZMB 6133; Peters 1870), also collected by Dhorn. In 1873,
the Portuguese zoologist José Vicente Barboza du Bocage (1823–1907), director of
the National Museum of Lisbon (also known as Museu Bocage, now Museu
Nacional de História Natural e da Ciência, Lisbon, Portugal; MUHNAC), described
the São Tomé caecilian Siphonops (currently Schistometopum) thomense based on
two preserved specimens donated to the museum by Pedro Carlos de Aguiar
Craveiro Lopes (1834–?), Portuguese governor of São Tomé and Príncipe at the
time (Bocage 1873). In 1874, Peters described Siphonops brevirostris based on a
single specimen with imprecise locality information (“Westküste Afrikas [Guinea]”)
that he acquired from an animal dealer (Peters 1874). The type locality for
S. brevirostris has since been restricted to Ilhéu das Rolas (Gorham 1962), but the
justification for this restriction is doubtful (Nussbaum and Pfrender 1998). This
specimen is extant at the Museum für Naturkunde (Berlin, Germany; ZMB) and
Nussbaum and Pfrender (1998) indicate the holotype is ZMB 4911 rather than ZMB
4711 as reported in the description. In his major revision of caecilians, Peters
subsequently placed both S. thomense and S. brevirostris in the primarily neotropical
genus Dermophis based on a combination of shared morphological features (Peters
1879). Upon examining specimens of S. thomense, Peters later determined that his
S. brevirostris was the same as Bocage’s S. thomense (Peters 1880), and this
synonymy continues to be recognized by most authors. Finally, Parker (1941) placed
the species in the genus Schistometopum where it remains today.
The German zoologist Richard Greeff (1829–1892) explored São Tomé and Ilhéu
das Rolas (a small islet ~2 km off the southern tip of São Tomé) from 1879 to 1880
and provided one of the first reports of its herpetofauna (Greeff 1884a). Greeff was
particularly interested in São Tomé caecilians and published a brief study on their
biology (Greeff 1884b). Greeff’s specimens are still extant in the collections of the
Museum für Naturkunde (Berlin, Germany; ZMB), Zoologische Staatssammlung
München (München, Germany; ZSM), and Zoologisches Museum Hamburg (Hamburg, Germany; ZMH).
In 1885, the Botanical Gardens of the University of Coimbra sent their chief
gardener Adolfo Frederico Möller (1842–1920) to São Tomé to explore and collect
natural history specimens for the Botanical Gardens and the university museum.
Most of the zoological specimens collected by Möller were sent to the University of
Coimbra (now part of the Museu da Ciência da Universidade de Coimbra; Coimbra,
Portugal; MCUC) and Vieira (1886) published a brief inventory of these specimens.
Almost all of this material was examined and identified by José Vicente Barbosa du
Bocage and is still extant in the collections of MCUC (Themido 1941; LMPC pers.
obs.). Some amphibian and reptile specimens, however, were likely sent by Möller
to the Russian zoologist Jacques von Bedriaga (1854–1906) who was a scholar at the
University of Coimbra. Bedriaga published a thorough revision of the amphibians
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and reptiles of São Tomé (Bedriaga 1892), where he described Moller’s Reed Frog,
Rappia (currently Hyperolius) molleri, endemic to São Tomé (Bedriaga 1892).
There are no further records of the specimens sent by Möller to Bedriaga, and they
are presumably lost; however, one syntype of H. molleri is extant at the Natural
History Museum (London, UK; NHMUK).
Also in 1885, Francisco Xavier Oakley de Aguiar Newton (1864–1909) was
hired by the Museu Bocage to conduct zoological surveys in the Gulf of Guinea.
From 1885 to 1895, Newton explored all the Gulf of Guinea islands, as well as
Benin, and his specimens were ultimately deposited in the Museu Bocage. The
amphibians were studied by Barbosa du Bocage and based on this collection, he
described the São Tomé Giant Reed frog Hyperolius thomensis and Newton’s
Grassland frog Rana (currently Ptychadena) newtoni, both from São Tomé (Bocage
1886). Unfortunately, the entirety of Newton’s collections was lost in the fire that
destroyed the Museu Bocage in 1978.
The Italian explorer Leonardo Fea (1852–1903) explored the four principal
islands of the Gulf of Guinea from 1901 to 1902 under the sponsorship of the
Museo Civico di Storia Naturale of Genoa (currently known as Museo Civico di
Storia Naturale “Giacomo Doria;” Genoa, Italy; MSNG). Fea’s collections were
initially studied by George Albert Boulenger (1858–1937; Boulenger 1906) and are
still extant in the MSNG with a small subset in the Natural History Museum of
London (NHMUK). Based on material Fea collected on Príncipe, Boulenger (1906)
described Phrynobatrachus feae, which was later placed in synonymy with P. dispar
by Schätti and Loumont (1992).
During the 1950s and 1960s, the Portuguese Zoology Center of the Overseas
Research Committee (Centro de Zoologia da Junta de Investigações do Ultramar;
Lisbon, Portugal; CZL) conducted zoological surveys on São Tomé and Príncipe.
Several herpetological specimens were collected by different researchers associated
with the colonial enterprise over the course of multiple scientific surveys. The
material collected during these surveys was studied by the Portuguese herpetologist
Sara Maria Bárbara Marques Manaças (1896–?), resulting in two publications
(Manaças 1958, 1973). Most of the specimens were housed in the collections of
the Instituto de Investigação Científica Tropical (Lisbon, Portugal; IICT), but in
2016 they were incorporated into the MUHNAC collections.
Throughout the 1960s and 1970s, several authors used existing specimens in
various collections for taxonomic revisions of different genera. For instance, the
Swiss herpetologist Jean-Luc Perret (b. 1925) reviewed the taxonomic position and
status of São Tomé and Príncipe anurans (Perret 1962, 1966, 1973, 1976, 1988).
Perret placed both reed frog species in a new genus Nesionixalus based on several
shared morphological features (Perret 1976); however, subsequent morphological
and genetic analyses have found strong support for both species belonging to the
genus Hyperolius (Drewes 1984; Drewes and Wilkinson 2004; Portik et al. 2019).
The North American herpetologist Edward Harrison Taylor (1889–1978) described
Schistometopum ephele based on material collected from São Tomé by the Leonardo
Fea Expedition and deposited in the MSNG (MSNG 8773; Taylor 1965).
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483
Following the independence of São Tomé and Príncipe from Portugal in 1975,
several teams undertook expeditions to the islands to document biodiversity. In 1984
a team from the zoology and anthropology department of the Faculty of Sciences of
the University of Lisbon and the Museu Bocage, Lisbon, Portugal, led by Luis
Mendes (b. 1946), conducted a 1-month zoological expedition to São Tomé
(Mendes et al. 1988). Although the expedition did not have a dedicated herpetologist, some amphibian specimens were collected, and these are extant in MUHNAC
collections.
Ronald Nussbaum (b. 1942) from the University of Michigan and Michael
Pfrender (b. 1960) visited the islands of São Tomé and Príncipe in 1988 and placed
S. ephele in synonymy with S. thomense (Nussbaum and Pfrender 1998). The
specimens they collected are in the University of Michigan Museum of Zoology
(Ann Arbor, United States of America; UMMZ). From 1989 to 1991, expeditions to
São Tomé and Príncipe led by Catherine Loumont (b. 1942), Tillman Nill (dates
unknown) Jakob Fahr (dates unknown) and Jan Haft (b. 1967), resulted in reviews of
the herpetofauna of these islands, including important natural history data on
amphibians (Loumont 1992; Schätti and Loumont 1992; Fahr 1993; Haft and
Franzen 1996). Some of these specimens are housed in the ZMB and the collections
of the Musée d’Histoire Naturelle de la Ville de Genéve, Switzerland (MHNG).
The beginning of the twenty-first century marked a new period for the study of the
amphibians of the Gulf of Guinea oceanic islands. Robert C. Drewes (b. 1942),
herpetology curator of the California Academy of Sciences (San Francisco, United
States of America; CAS), and his team have made 12 expeditions to the islands since
2001. The amphibian collections resulting from these expeditions are deposited at
CAS and are currently the largest in the world (Table 18.1). Drewes and his
colleagues have published several studies, including the description of the São
Tomé Puddle Frog, Phrynobatrachus leveleve (Uyeda et al. 2007), taxonomic
reviews and updates (Drewes and Stoelting 2004; Drewes and Wilkinson 2004),
biogeographic history (Measey et al. 2007), and population genetics (Stoelting et al.
2014). During this same period, John Measey (b. 1968) and colleagues conducted
evolutionary, ecological, and biomechanics studies of the São Tomé caecilian,
making important contributions to our understanding of these secretive animals
(Delêtre and Measey 2004; Measey and Herrel 2006; Measey and Van Dongen
2006; Wollenberg and Measey 2009; Herrel and Measey 2010, 2012). More
recently, Rayna C. Bell (b. 1985), herpetology curator of the CAS, has contributed
studies on the biogeographic and evolutionary history of Hyperolius (Bell et al.
2015a, b, 2017), hybridization of H. molleri and H. thomensis on São Tomé (Bell
et al. 2015b; Bell and Irian 2019), the description of H. drewesi, endemic to Príncipe,
and the evolutionary history of the São Tomé caecilians (O’Connell et al. 2021). As
the type material of H. thomensis was lost in the 1978 fire at the Museu Bocage in
Lisbon, Portugal (Drewes and Wilkinson 2004), and the original type localities of
H. thomensis and H. molleri were vague and may have included individuals with
hybrid ancestry, Bell (2016) designated neotypes for both H. thomensis and
H. molleri. Bell participated in several expeditions led by Drewes, and most of the
specimens are at CAS with a smaller subset at the Smithsonian Institution’s National
R. C. Bell et al.
484
Table 18.1 Natural history institutions housing type specimens and significant collections of
amphibians from the Gulf of Guinea oceanic islands. Total number of specimen records includes
tadpole lots and clutches of eggs. Acronyms follow Sabaj (2020)
Collection
CAS—California Academy of Sciences, San Francisco,
California, USA
UMMZ—University of Michigan Museum of Zoology,
Ann Arbor, Michigan, USA
MHNG—Muséum d’Histoire Naturelle de la Ville de
Genève, Geneva, Switzerland
MSNG—Museo Civico di Storia Naturale “Giacomo
Doria,” Genova, Italy
MUHNAC/IICT—Museu Nacional de História Natural
e da Ciência/Instituto de Investigação Científica Tropical, Lisbon, Portugal
NHMUK—Natural History Museum, London, UK
USNM—National Museum of Natural History,
Smithsonian Institution, Washington, District of
Columbia, USA
NMP-P6V—National Museum in Prague, Prague,
Czech Republic
ZMB—Museum für Naturkunde, Berlin, Germany
FMNH—Field Museum of Natural History, Chicago,
Illinois, USA
ZSM—Zoologische Staatssammlung München,
München
MCUC—Museu da Ciência da Universidade de Coimbra, Coimbra, Portugal
ZMH—Zoologisches Museum Hamburg, Hamburg,
Germany
São
Tomé
793
Príncipe
320
Type
specimens
4
Total
1113
757
16
–
773
583
39
–
622
68
55
22
123
68
43
–
111
60
29
13
35
–
75
64
19
–
–
19
17
14
3
–
–
20
14
8
–
–
8
7
–
–
7
4
–
–
4
2
3
Museum of Natural History (Washington DC, United States of America; USNM).
Since 2013, a team from MUHNAC led by Luis M. P. Ceríaco (b. 1987) completed
four herpetological surveys in São Tomé and Príncipe. A few amphibian specimens
were collected and are now housed in MUHNAC.
Diversity and Endemism
Although the islands of São Tomé and Príncipe have never been physically
connected to the African continent, they host a remarkable nine endemic species
of amphibians, each of which is restricted to just one of the islands (Table 18.2,
Fig. 18.1). We provide a brief summary of the taxonomic status of each species, its
biogeographic history (when known), and notes on distribution, ecology, and
behavior.
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Table 18.2 List of amphibians from Príncipe and São Tomé islands (no amphibians are known
from Annobón)
Higher taxonomy
Order Gymnophiona
Family Dermophiidae
Schistometopum Parker
1941
Order Anura
Family Arthroleptidae
Leptopelis Günther
1859 “1858”
Family Hyperoliidae
Hyperolius Rapp, 1842
Species/subspecies
P
Schistometopum thomense (Bocage 1873)
Schistometopum ephele (Taylor 1965)
Leptopelis palmatus (Peters 1868)
E
Hyperolius drewesi Bell 2016
Hyperolius molleri (Bedriaga 1892)
Hyperolius thomensis Bocage 1886
E
Family Phrynobatrachidae
Phrynobatrachus
Phrynobatrachus dispar (Peters, 1870)
Günther, 1862
Phrynobatrachus leveleve Uyeda, Drewes &
Zimkus 2007
Family Ptychadenidae
Ptychadena Boulenger
Ptychadena newtoni (Bocage 1886)
1917
ST
IUCN
E
E
LC
EN
E
E
LC
EN
E
LC
LC
E
EN
E
E, endemic. IUCN Red List Categories (IUCN 2021): LC, least concern; VU, vulnerable; EN,
Endangered
Gymnophiona
Caecilian diversity in the Gulf of Guinea oceanic islands includes two endemic
species (family Dermophiidae) that are distributed across São Tomé Island, even
though caecilians were reported from Príncipe Island in error (Taylor 1968). The
presence of these enigmatic and secretive amphibians on an oceanic island is
especially captivating given their presumed low vagility and dispersal potential
(Taylor 1968). Caecilians are not the only fossorial vertebrates that have reached
the archipelago, however, as there are also several endemic fossorial squamates on
both São Tomé and Príncipe (Ceríaco et al. 2022). This high level of endemic
diversity among vertebrates with low dispersal potential provides strong support
for the overseas rafting hypothesis proposed by Measey et al. (2007) and described
in further detail in Melo et al. (2022).
Family Dermophiidae
The São Tomé caecilian S. thomense was initially described by Bocage (1873), and
though he did not observe the species in life, he noted the two preserved specimens
were uniform light yellow and olive in coloration, respectively. Unfortunately, a fire
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Fig. 18.1 Gulf of Guinea oceanic island amphibians: (1) São Tomé caecilians, Schistometopum
thomense (top) and Schistometopum ephele (bottom), from São Tomé Island; (2) Príncipe Giant
Tree Frog, Leptopelis palmatus, from Príncipe Island; (3) Drewes’ Reed Frog, Hyperolius drewesi,
from Príncipe Island; (4) Moller’s Reed Frog, Hyperolius molleri, from São Tomé Island; (5) São
Tomé Giant Reed Frog, Hyperolius thomensis, from São Tomé Island; (6) Leveleve Puddle Frog,
Phrynobatrachus leveleve, from São Tomé Island; (7) Príncipe Puddle Frog, Phrynobatrachus
dispar, from Príncipe Island; (8) Newton’s Grass Frog, Ptychadena newtoni, from São Tomé Island.
Photo credits: Andrew Stanbridge
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487
at the Lisbon Museum in 1978 destroyed this material and reports of a possible
extant syntype at the Berlin Museum (ZMB 8738) are doubtful because the size of
the specimen does not match Bocage’s description (Nussbaum and Pfrender 1998).
Several decades later, Taylor described S. ephele and recognized S. ephele as distinct
from S. thomense based on its smaller, pointier head and prominent brown flecking
pattern (Taylor 1965). The provenance of this material is reported as “Agua Izé,
400–700 m, Ilha São Thomé,” a locality that is likely between Agua Izé (a coastal
community on the eastern side of the island) and the community of Java that is
directly inland of Agua Izé at ~600 m elevation (pers comm G. Doria, MSNG). In the
description, Taylor also noted that two other individuals under this number were
uniform yellow (unflecked) and thus referred to S. thomense. Nussbaum and
Pfrender (1998) quantified coloration, morphometric, and meristic variation of
Schistometopum specimens collected from ten sites across São Tomé (including
Ilhéu das Rolas). Although they found strong separation in a multivariate comparison of northern and southern populations, Nussbaum and Pfrender (1998)
interpreted this variation as a phenotypic cline in a widespread species, placing
S. ephele in synonymy with S. thomense. Stoelting et al. (2014) revisited this
hypothesis with mtDNA (16s and ND4) sequence data and sampling from more
than 20 sites across the island. These authors found deep genetic divergence between
lineages that they proposed may correspond to S. thomense and S. ephele; however,
the distributions of these mtDNA lineages overlapped in the center of the island.
Consequently, Stoelting et al. (2014) proposed that the lineages diverged in allopatry
but refrained from making taxonomic recommendations solely based on these
maternally inherited loci. A more recent study examining genome-wide variation
found strong support for distinct lineages corresponding to S. thomense and
S. ephele, and inferred a history of divergence in allopatry with a narrow hybrid
zone where the ranges presently overlap in the center of São Tomé Island (O’Connell
et al. 2021). Based on this evolutionary history, and the revised interpretation of the
apparent phenotypic cline in the Nussbaum and Pfrender (1998) study, O’Connell
et al. (2021) removed S. ephele from synonymy with S. thomense.
The only other species in the genus Schistometopum is the East African
S. gregorii, which presents an intriguing biogeographic scenario for the island
endemic species (Wilkinson et al. 2003; San Mauro et al. 2014). Depending on the
method and/or mutation rate used, estimates for divergence between S. thomense and
S. gregorii based on mtDNA loci range from 0.6 to 3.2 Myr (Loader et al. 2007),
indicating that dispersal to São Tomé occurred relatively recently in the islands’
13 Myr history. Using genome-wide markers, divergence between S. thomense and
S. ephele on São Tomé was estimated at 281–326 kya with secondary contact
between the lineages occurring ~100 kya (O’Connell et al. 2021), highlighting that
São Tomé is accumulating endemic diversity via both overseas dispersal and in situ
diversification even in the more recent period of its long geologic history. On São
Tomé, caecilians occur in a wide variety of habitats ranging from sea level to over
1400 m elevation, including agricultural fields, modified landscapes, and the ~2 km2
islet Ilhéu das Rolas (Bocage 1886; Loumont 1992; Fahr 1993; Haft and Franzen
1996; Nussbaum and Pfrender 1998; Drewes and Stoelting 2004; Measey and Van
488
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Dongen 2006; Stoelting et al. 2014). Due to this broad distribution and high
abundance (estimated density 0.3 per m2; Measey 2006), caecilians are well
known to São Toméans, who refer to them as “Cobra-bobô” (i.e., yellow snake).
At collection sites with harder, mineral soils, animals may be found under leaf
litter or rotten logs, whereas at sites with softer soils, including agricultural fields,
animals are found within the soil (Haft 1992; Haft and Franzen 1996; Delêtre and
Measey 2004). Likewise, in drier habitats, caecilians occur deeper in the soil
(Nussbaum and Pfrender 1998) whereas, after heavy rains and in the evening, they
can be observed moving aboveground (Fahr 1993; Haft and Franzen 1996). Correspondingly, laboratory studies quantifying the behavior and biomechanics of
burrowing in São Tomé caecilians indicated that they did not construct tunnels in
soils with high compaction and that even intermediate levels of soil compaction can
deter or prevent burrowing (Ducey et al. 1993). In addition, in laboratory settings,
caecilians opted to use existing tunnels rather than construct new ones (Ducey et al.
1993). These behaviors are consistent with the more terminal mouth position of São
Tomé caecilians relative to the subterminal (countersunk lower jaw) mouths of
caecilians that are dedicated burrowers (Sherratt et al. 2014). Like all caecilians,
São Tomé caecilians show skin-vertebral independence and use internal and wholebody concertina locomotion while burrowing or moving through narrow tunnels
(Herrel and Measey 2010). When moving across high friction substrates (i.e., a moist
towel) São Tomé caecilians switch to lateral undulating locomotion (Herrel and
Measey 2010). An extensive survey of caecilian body size variation across São
Tomé found that individuals at higher elevation sites (where soil temperatures are
cooler) were longer and heavier than individuals at lower elevations (Measey and
Van Dongen 2006). This trend has been noted in many endothermic vertebrates with
the explanation that larger body sizes result in lower heat loss via larger surface-areato-volume ratios (Bergmann 1847); however, the potential mechanisms to explain
this pattern in an ectotherm are less clear.
São Tomé caecilians are sexually dimorphic in head size (but not in body size),
which could indicate ecological divergence between the sexes (e.g., differences in
diet; Nussbaum and Pfrender 1998) or antagonistic behaviors among males (Delêtre
and Measey 2004). Delêtre and Measey (2004) tested this first hypothesis with a diet
study of males, females, and juveniles from both natural forest and agricultural sites.
Earthworms (including epigeic [surface-active] and endogeic [deeper soil-dwelling]
species) accounted for over 98% of identified prey items, with the remaining
contents comprising centipedes, ants, mites, and unidentified larvae (Delêtre and
Measey 2004). Counter to expectations, the authors did not find significant differences in prey mass or prey size between the sexes (though prey size did correlate
with gape diameter among females), suggesting that larger head size in males is not
related to capturing larger prey. A subsequent study of caecilian diets reexamined the
Delêtre and Measey (2004) earthworm morphospecies dataset and found that adults
fed on both epigeic and endogeic earthworms in equal proportions, whereas juveniles appeared to only feed on endogeic species (Jones et al. 2006). Future research
investigating the extent of dietary specialization in São Tomé caecilians (across
habitats and throughout the year) as well as potential ontogenetic shifts in diet will
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489
provide important insight into the role caecilians play in mediating population
dynamics of soil ecosystem engineers (earthworms, termites and ants) and soil
ecology more broadly (Lavelle et al. 1997; Jones et al. 2006).
Observations in captivity suggest that São Tomé caecilians are predominantly
nocturnal, sit-and-wait predators, extending their heads beyond their burrows and
waiting for prey to come within reach (Haft and Franzen 1996; Hofer 1998). To our
knowledge, predation behaviors in field settings have not yet been documented in the
scientific literature; however, in laboratory settings São Tomé caecilians feeding on
earthworms exerted strong bite forces and used long-axis body rotations to subdue
and shred their prey (Measey and Herrel 2006; Herrel and Measey 2012). Laboratory
measurements of resting metabolism and aerobic capacity of São Tomé caecilians
indicated they have very low resting metabolic rates with a high capacity for aerobic
metabolism that is consistent with a largely sedentary, sit-and-wait predatory lifestyle (Smits and Flanagin 1994). The same study also revealed surprisingly high
cutaneous gas exchange in caecilians despite their thickened skin, suggesting that
cutaneous respiration is likely sufficient to support resting metabolic rates (Smits and
Flanagin 1994).
Based on the current understanding of reproductive biology in caecilians, all
species have internal fertilization via an intromittent organ formed by an eversible
portion of the male’s cloaca (the phallodaeum) that may vary in shape and ornamentation among species (Gower and Wilkinson 2002). The phallodaeum of São
Tomé caecilians is quite similar to that of S. gregorii from Tanzania, but Tanzanian
and Kenyan S. gregorii differ from one another, and these populations have previously been hypothesized to be distinct species (Taylor 1968; Gower and Wilkinson
2002). A better understanding of intraspecific and interspecific variation in
phallodaeum morphology would provide deeper insights as to the potential significance of this trait in reproductive isolation. Several authors have noted bite marks on
the heads of male and female São Tomé caecilians from both field-caught and
laboratory individuals (e.g., Nussbaum and Pfrender 1998; Teodecki et al. 1998).
Biting among conspecific males in territorial disputes and males biting females
during copulation have been proposed as alternative hypotheses for larger head
size in males (Delêtre and Measey 2004). The role of biting in communication
and/or sexual selection in São Tomé caecilians would be a compelling future avenue
of behavioral research in these curious organisms.
Viviparity has evolved independently in several lineages of caecilians, including
the family Dermophiidae, which are all viviparous (Gower et al. 2008; San Mauro
et al. 2014). Observations of São Tomé caecilians in captivity suggest clutch sizes
typically range from 2 to 7 young that are fully formed at birth with no signs of gill
scars (Nussbaum and Pfrender 1998). The energetic demands of reproduction are
likely high as young caecilians are born at up to 50% the length of their mothers
(Wake 1977; Nussbaum and Pfrender 1998), and females reproduce biennially
(Teodecki et al. 1998). In addition, developing fetuses have specialized dentition
with which to scrape the epithelium of the oviduct and stimulate the secretion of
nutrient-rich “uterine milk” from their mothers during gestation (Parker 1956; Parker
and Dunn 1964; Wake 1977). Captive-born young reached adult size after 2 years
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(Haft and Franzen 1996), and the adult coloration and pattern were present at birth
(Nussbaum and Pfrender 1998). It is tempting to consider that the prominent yellow
coloration of São Tomé caecilians may be aposematic, and a study of yellow
coloration across all caecilians indicates that this conspicuous coloration has evolved
multiple times in species that are surface-active (Wollenberg and Measey 2009).
Anecdotal evidence suggests São Tomé caecilians are distasteful (Hofer 1998;
Teodecki et al. 1998); however, their chemical defenses have not yet been characterized. Likewise, the dominant predators of São Tomé caecilians are also unknown;
consequently, much additional foundational research is needed to understand
whether this yellow coloration is cryptic or aposematic. While a role in intraspecific
communication and/or sexual selection is also a possible explanation for this bright
coloration, São Tomé caecilians likely have poor eyesight (Mohun et al. 2010) and
like all caecilians are considered to rely primarily on olfactory cues to sense their
environments (Himstedt and Simon 1995).
Anura
Anuran diversity in the Gulf of Guinea oceanic islands includes seven endemic
species from four families: Arthroleptidae, Hyperoliidae, Phrynobatrachidae, and
Ptychadenidae (Table 18.2).
Family Arthroleptidae
The Príncipe Giant Tree Frog Leptopelis palmatus has historically been confused
with another large-bodied species from continental Africa, L. rufus, with several
authors placing L. rufus in synonymy with L. palmatus (Anderson 1909; Parker
1936; Witte 1941; Perret 1962). Throughout this period of nearly a century of
taxonomic confusion, L. palmatus was reported from Cameroon, Equatorial Guinea
(including Bioko Island), Gabon, and Nigeria (Boulenger 1882; Mocquard 1902;
Boulenger 1906; Nieden 1910; Ahl 1931; Schiøtz 1963; Mertens 1965). Perret
(1973) resurrected L. rufus after comparing a large series of males and females
with the sole female holotype of L. palmatus available for study and clarified that
L. palmatus was an insular species. Upon this close examination, Perret (1973)
confirmed that the two species differed in tympanum size and several additional
morphological features, concluding that the two species may not even be closely
related. Male specimens were finally collected and formally described following an
expedition to the islands in 2002 (Drewes and Stoelting 2004). Loumont (1992)
characterized the karyotype of this species, reporting 24 chromosomes.
The phylogenetic relationships within the African genus Leptopelis are poorly
understood, and consequently, the biogeographic history of L. palmatus remains
unclear. Previous studies have hypothesized that L. palmatus is closely related to a
group of large-bodied species in West and Central Africa (L. macrotis, L. millsoni,
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and L. rufus) based on a combination of mtDNA and morphological data (Idris
2004). A more recent mtDNA phylogeny with expanded taxonomic sampling does
not support this relationship (Jaynes et al. 2021), and a more robust phylogenetic
inference is sorely needed. The distribution of L. palmatus ranges from sea level to
over 600 m elevation on Príncipe, primarily in forested habitats (Loumont 1992;
Drewes and Stoelting 2004). Males and females can be observed at night perched
one meter or higher off the ground on branches or leaves, especially near small
flowing streams (Loumont 1992; Drewes and Stoelting 2004; RCB and LAS pers.
obs). By contrast, large females have been encountered on or near the ground both in
the evening and during the day (Drewes and Stoelting 2004; RCB and LAS pers
obs). Although males lack vocal sacs (Drewes and Stoelting 2004), they produce
advertisement calls at breeding sites (characterized in Jaynes et al. 2021). Both male
and female dorsal coloration is variable, ranging from dark green/black with or
without small white spots to bright green and even bright yellow (Manaças 1958;
Loumont 1992; Drewes and Stoelting 2004; Jaynes et al. 2021). It does not appear
that this variation is sexually dimorphic or related to ontogeny, as has been described
in many species of the African genus Hyperolius (Schiøtz 1967; Portik et al. 2019).
Manaças (1958) reported Orthoptera (crickets), Blattodea (cockroaches and termites), and Coleoptera (beetles) in the stomach contents of specimens they
examined.
Sexual size dimorphism is quite pronounced in L. palmatus, with male snout–
vent length less than half that of females (Drewes and Stoelting 2004). In addition,
the largest measured female was 110 mm snout–vent length (Loumont 1992), which
remains the largest reported size of any female specimen in the entire genus
Leptopelis by more than 20 mm (Channing and Rödel 2019). Despite these large
adult body sizes, post-metamorphic individuals are quite small (10–11 mm; Drewes
and Stoelting 2004). This combination of extreme sexual size dimorphism and
exceptionally large body size in females may indicate selection for increased fecundity (e.g., Darwin 1874). Unfortunately, the reproductive biology of L. palmatus is
entirely unknown. Other species in the genus Leptopelis bury their eggs in humid
soil from which larvae hatch and complete their development within streams or
ponds (Portik and Blackburn 2016). One species, L. brevirostris, is thought to
reproduce by direct development because females produce large eggs that are buried
far from water (Perret 1966; Amiet and Schiøtz 1974; Schiøtz 1999). Documenting
this important aspect of its biology will be critical to understanding the habitats
L. palmatus relies upon throughout its lifecycle.
Family Hyperoliidae
Three species of reed frogs in the genus Hyperolius are endemic to the islands of São
Tomé and Príncipe: the São Tomé Giant Reed Frog Hyperolius thomensis and
Moller’s Reed Frog H. molleri (both endemic to São Tomé), and H. drewesi
(endemic to Príncipe). Prior to the recognition of H. drewesi as a distinct species,
H. molleri was reported from both São Tomé and Príncipe islands (Loumont 1992;
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Fahr 1993; Drewes and Wilkinson 2004). Loumont (1992) characterized the karyotypes of H. thomensis and H. molleri (sensu stricto), reporting 24 chromosomes.
Phylogenetic analyses indicate that the three island species form a monophyletic
group and are part of the H. cinnamomeoventris species complex (Drewes and
Wilkinson 2004; Schick et al. 2010; Bell et al. 2015a, 2017; Portik et al. 2019).
Within the H. cinnamomeoventris species complex, the island endemics are most
closely related to H. olivaceus, a species distributed throughout the Lower Guinean
forests of Gabon and the Republic of Congo (Bell et al. 2017). The distribution of
H. olivaceus encompasses the Ogooué River and the mouth of the Congo River,
suggesting that either river drainage could have served as a source for a vegetation
raft that ferried reed frogs to the archipelago. Divergence time estimates indicate the
island endemics and H. olivaceus shared a most recent common ancestor in the LateMiocene to Pliocene (Bell et al. 2015a, 2017; Portik et al. 2019). The island
endemics, however, shared a most recent common ancestor within the last
1.7–0.5 Ma, with divergence between H. molleri and H. drewesi estimated at
1.1 Ma to 270 ka (Bell et al. 2015a). As with the São Tomé caecilians, the timing
of colonization and in situ diversification of the reed frogs are quite recent in the
islands’ long geological histories. The pattern of divergence among the three species
is consistent with a single dispersal event to the islands and suggests that reed frogs
first colonized São Tomé Island, diversified in situ, and then dispersed to Príncipe
Island (Bell et al. 2015a, b). The pattern of lower genetic diversity in H. drewesi
relative to H. molleri is also consistent with this colonization history (Bell et al.
2015b). Although it appears that dispersal between São Tomé and Príncipe occurred
at some point in the past, analyses of mtDNA and genome-wide variation indicated
that gene flow between the islands is not ongoing (Bell et al. 2015b).
H. thomensis inhabits closed-canopy, primary forest habitats from 300 to 1300 m
elevation, which are primarily on the wetter southern half of São Tomé (Loumont
1992; Drewes and Stoelting 2004; Gilbert and Bell 2018; Bell and Irian 2019). By
contrast, H. molleri occurs in a wide range of habitats across the island from sea level
to ~1400 m elevation, including swampy areas in the drier habitats on the northern
side of São Tomé, agricultural areas, secondary and primary forests (Loumont 1992;
Fahr 1993; Bell et al. 2015b; Gilbert and Bell 2018; Bell and Irian 2019). H. drewesi
is ecologically similar to H. molleri, occurring in a wide range of habitats across
Príncipe Island from sea level to ~600 m elevation (Loumont 1992; Drewes and
Stoelting 2004; Bell 2016). Observations in the field and in captivity suggest that all
three species are primarily nocturnal (Fahr 1993); however, like most anurans, these
species are primarily observed during their reproductive periods, and thus less is
known about their activities during other times of day or throughout the rest of
the year.
The forest specialist H. thomensis differs from the other two species in its
reproductive biology. First, males of H. thomensis produce advertisement calls
from high up in the canopy (from 1 to >5 m), whereas males of H. molleri and
H. drewesi call from perches 30–200 cm above ground on leaves and thin branches
overhanging slow-moving streams and pools of standing water (Fahr 1993; Gilbert
and Bell 2018). Furthermore, the abundance of individuals at breeding sites varies
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between species, with only a single to several H. thomensis calling at a given site
versus upwards of 50 individuals of H. molleri congregating along a 15 m long
stretch of stream (Fahr 1993; Gilbert and Bell 2018). These differences in calling site
and breeding aggregation size may be associated with the specialized microhabitats
H. thomensis select to deposit their eggs. While H. molleri and H. drewesi deposit
their egg masses on leaves overhanging water (Fahr 1993; Drewes and Stoelting
2004; Bell 2016), which is the typical reproductive mode for Hyperolius (Portik and
Blackburn 2016), H. thomensis deposit their eggs on the walls of water-filled cavities
in trees, rotting logs, and bamboo (Drewes and Stoelting 2004; Gilbert and Bell
2018). These specialized breeding microhabitats are the only standing water available for anuran reproduction in some landscapes and may provide shelter to vulnerable eggs and larvae from potential predators (Drewes and Stoelting 2004; Lehtinen
et al. 2004); however, they also present some unique challenges (lower dissolved
oxygen, lower nutrient availability; Guimarães-Souza et al. 2006; Ferreira et al.
2019). Large egg size (2–2.5 mm; Perret 1976) and small clutch size in H. thomensis
(20–40; Drewes and Stoelting 2004) relative to most species of Hyperolius (Channing and Rödel 2019) may be adaptations to the specialized reproduction in this
species.
All three Hyperolius endemic to São Tomé and Príncipe are sexually dimorphic
in size, with females displaying larger body sizes than males (Bell 2016; Bell and
Irian 2019). The forest specialist H. thomensis is also substantially larger than
H. molleri, H. drewesi, and H. olivaceus and is among the largest of the ~150
described species in the genus (Portik et al. 2020). The selective mechanisms
underlying body size evolution in Hyperolius and in anurans more broadly are still
poorly understood (Womack and Bell 2020); consequently, investigating ecological
differences among these closely related species may provide some important
insights. For instance, although both H. thomensis and H. molleri are insectivorous
(Perret 1976), they may consume different sizes or types of prey, as demonstrated in
other sympatric reed frog species that differ in body size (Luiselli et al. 2004). Males
of all three species possess dorsal epidermal asperities (fine projections from the
skin; Perret 1988), which are pigmented in H. thomensis and H. molleri but not in
H. drewesi (Bell 2016). The potential functions of these sexually dimorphic features,
which are also present in several continental species of Hyperolius, are poorly
understood. Although the island reed frogs do not exhibit sexual dichromatism, as
exhibited by a large proportion of the genus Hyperolius (Portik et al. 2019),
H. molleri and H. drewesi exhibit differences in juvenile and adult coloration
(Schiøtz 1967) with metamorphic and juvenile individuals of both species displaying
light brown coloration with thin, white dorsolateral lines (Loumont 1992; Fahr 1993;
Bell 2016). In addition, H. thomensis exhibit bright orange and black ventral
coloration that is often associated with aposematism and chemical defense in
amphibians (e.g., Kang et al. 2017), but this hypothesis has not yet been tested in
H. thomensis. A handful of colorful Hyperolius from Cameroon was screened for
defensive alkaloids, and none were found (Portik et al. 2015). Similar to L. palmatus,
H. thomensis also exhibit extensive variation in dorsal coloration ranging from dark
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R. C. Bell et al.
or bright green to turquoise to golden with dark spots, whereas both H. molleri and
H. drewesi are consistently bright green (RCB and LAS pers. obs).
Despite differences in body size, coloration, and breeding biology, H. thomensis
and H. molleri hybridize where their ranges are sympatric (Bell et al. 2015b). Males
of the two species produce advertisement calls that differ in dominant frequency, and
these differences are strongly correlated with body size (Gilbert and Bell 2018).
Correspondingly, hybrid males are intermediate in body size and produce advertisement calls with intermediate peak frequencies (Gilbert and Bell 2018). Variation in
both size and ventral coloration among hybrid frogs overlaps with that of H. molleri
(Bell and Irian 2019); consequently, hybrids cannot reliably be identified without
genetic analysis. Several sites with high proportions of hybrid individuals are at the
boundary of primary forest and agricultural development, where breeding frogs
congregate around artificial bodies of water (e.g., cisterns; Bell and Irian 2019).
Hybrids can also be found at the crater lake Lagoa Amélia, which is within 1 km of
the forest edge (Bell and Irian 2019). Although adult H. thomensis can be found in
anthropogenically modified habitats and reproduce at these sites (Strauss et al.
2018), these environments may be population sinks if larvae and juveniles experience lower survival than in forested sites. In addition, the geographic extent of
hybridization between H. thomensis and H. molleri across the island is unknown as
are the potential consequences of hybridization, both of which warrant further
attention.
Family Phrynobatrachidae
Two species of puddle frogs in the genus Phrynobatrachus are endemic to São Tomé
and Príncipe: P. dispar on Príncipe and P. leveleve on São Tomé and Ilhéu das
Rolas. Prior to the recognition of P. dispar and P. leveleve as a distinct species,
P. dispar was reported from both Príncipe and São Tomé (including Ilhéu das Rolas;
Boulenger 1906; Loumont 1992; Fahr 1993; Drewes and Stoelting 2004). Loumont
(1992) characterized the karyotypes of Phrynobatrachus on both São Tomé and
Príncipe, reporting 16 chromosomes.
Unlike the island endemic reed frogs, phylogenetic analyses of the genus
Phrynobatrachus indicate that divergence between P. dispar on Príncipe and
P. leveleve on São Tomé is not recent (Uyeda et al. 2007; Zimkus et al. 2010).
Genetic divergence at mtDNA (cytochrome b) between the two is ~19% (Uyeda
et al. 2007), and the island endemics form a monophyletic group with
P. mababiensis (Zimkus et al. 2010), a southern African species that ranges from
Angola to Tanzania and Mozambique (Channing and Rödel 2019). This pattern
suggests that Phrynobatrachus may have colonized the archipelago twice, though
estimates of continental species diversity and phylogenetic relationships in this
genus are still in a state of flux. Genetic diversity within species on each island
(based on mtDNA) is quite low, further supporting the existence of only a single
species on each island and Schätti and Loumont’s (1992) proposed synonymy of
Boulenger’s P. feae (Uyeda et al. 2007).
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Puddle frogs are abundant and widespread on both islands (and on Ilhéu das
Rolas), occurring from sea level to ~1400 m on São Tomé and from sea level to
~950 m on Príncipe in primary forest, secondary forest, agricultural fields and
residential areas (Loumont 1992; Fahr 1993; Drewes and Stoelting 2004; Uyeda
et al. 2007). They can be found perched low to the ground in grasses or shrubs, in
crevices, and on the ground, especially near small bodies of water (Loumont 1992;
Fahr 1993). Like many species of Phrynobatrachus, P. dispar and P. leveleve are
active during the day and at night but are most often encountered at twilight (Fahr
1993). Both species use a wide range of water bodies for reproduction, including
small temporary puddles at higher elevations (Fahr 1993), which P. leveleve sometimes share with Ptychadena newtoni (Drewes and Stoelting 2004). On Príncipe,
P. dispar shares breeding sites with H. drewesi and heterospecific amplexus between
the species has been observed (Bell and Scheinberg 2016). Relatively small clutch
size (15–30 eggs) and rapid larval development (14–20 days) suggest the puddle
frogs’ reproductive biology is well suited for breeding in ephemeral puddles, which
may enable P. dispar and P. leveleve to occupy higher elevations than the other
island endemic anurans (Fahr 1993). Male advertisement calls have been described,
however, these studies were conducted prior to two species being recognized, and
the calls likely correspond only to P. leveleve (Loumont 1992; Fahr 1993). Likewise,
Fahr (1993) reports that adults in captivity live up to 2 years, but it is not clear
whether these observations correspond to P. dispar or to P. leveleve or both.
Like many frogs, P. dispar and P. leveleve exhibit sexual size dimorphism with
females being slightly larger than males (Uyeda et al. 2007). These diminutive frogs
fall within the typical size range of Phrynobatrachus on the continent (Channing and
Rödel 2019); however, similar to the São Tomé caecilians, patterns of intraspecific
body size variation on each island are consistent with Bergmann’s Rule with larger
individuals occupying higher elevations (Uyeda et al. 2007). Males of both species
have dorsal epidermal asperities, and these are also present in females of P. dispar
but apparently absent in female P. leveleve (Uyeda et al. 2007). Both species are also
highly variable in coloration but are generally of various shades and patterns of
brown (Uyeda et al. 2007).
Family Ptychadenidae
Newton’s Grassland Frog P. newtoni is endemic to São Tomé, but like many of the
Gulf of Guinea amphibians, this species has a convoluted taxonomic history. First,
P. newtoni was placed in synonymy of P. oxyrhynchus by Andersson (1937), and
then in synonymy of P. mascareniensis by Guibé and Lamotte (1957). Perret (1976)
removed P. newtoni from synonymy with P. mascareniensis and noted that although
the species resembled P. oxyrhynchus, it was likely unique given the high level of
endemism on the Gulf of Guinea islands. A phylogenetic study of mitochondrial
DNA indicated that P. newtoni was indeed unique and that it was part of the
P. mascareniensis species complex (Measey et al. 2007). Loumont (1992) characterized the karyotype of P. newtoni, reporting 24 chromosomes.
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R. C. Bell et al.
The P. mascareniensis complex consists of a dozen named and candidate taxa
with a distribution that covers much of continental Africa, Madagascar, the Seychelles, and the Mascarenes (Zimkus et al. 2017). Within the P. mascareniensis
species complex, P. newtoni appears to be most closely related to the Nile Grass
frog, P. nilotica, which occurs along the Nile Basin and into eastern Africa (Zimkus
et al. 2017). This relationship is somewhat surprising considering that lineages
within the P. mascareniensis complex occur throughout West and Central Africa,
and are much more proximate to the Gulf of Guinea. Previous authors have
interpreted this pattern as evidence for rafting along the Congo River drainage as a
dispersal route to the islands (Measey et al. 2007). Divergence time estimates
suggest P. newtoni and P. nilotica shared a most recent common ancestor in the
Mid- to Late-Miocene (Zimkus et al. 2017); however, a more robust phylogeny of
the P. mascareniensis species complex will provide a better understanding of the
evolutionary history of P. newtoni.
On São Tomé, P. newtoni occurs in lower elevation habitats (sea level to ~600 m)
including plains, agricultural fields, and around human-built structures (Loumont
1992; Fahr 1993; Drewes and Stoelting 2004). Most of the remaining habitat at these
lower elevations is heavily impacted by human activities, and thus while P. newtoni
appears to be somewhat resilient to these landscape changes, there is some concern
that very little of its original habitat remains (Fahr 1993; Drewes and Stoelting
2004). Not much is known of the biology of P. newtoni. Throughout its distribution,
P. newtoni occurs with both H. molleri and P. leveleve, and the three species may use
the same temporary water bodies for reproduction (Fahr 1993; Drewes and Stoelting
2004). As with most anurans, this species is sexually size-dimorphic and is the
largest species in the genus Ptychadena with females reaching up to 76 mm snout–
vent length (Loumont 1992; Channing and Rödel 2019). Its advertisement call is
described (Loumont 1992; Fahr 1993) and it is mostly a nocturnal species but can be
found during the day if it is raining (Fahr 1993). Like most Ptychadena, P. newtoni is
primarily a ground-dwelling species and is a very accomplished jumper (Fahr 1993).
As documented in P. mascareniensis on Madagascar (Tolojanahary et al. 2011), the
diet of P. newtoni likely consists primarily of arthropods.
Conservation
Most of the Gulf of Guinea oceanic island endemic amphibians are incredibly
abundant and widespread, occurring in primary forest, secondary forest, and agricultural habitats across the islands (e.g., S. ephele, S. thomense, H. molleri,
H. drewesi, P. dispar, P. leveleve). By contrast, H. thomensis, L. palmatus and
P. newtoni appear to have more specialized habitat requirements, and these habitats
are under considerable anthropogenic pressure. Consequently, these species are
considered Endangered according to the most recent IUCN assessments
(Table 18.2; IUCN 2021). In the case of H. thomensis and L. palmatus, these species
appear to prefer closed-canopy forest habitats and have more specialized
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497
reproduction; thus, they may be more susceptible to deforestation. For H. thomensis
in particular, deforestation may directly limit the availability of suitable breeding
sites as cavities that collect water typically occur in large mature trees. Furthermore,
if deforestation is associated with hybridization between H. thomensis and H. molleri
(as suggested in Bell and Irian 2019), the rarer H. thomensis may be at risk of
extinction by hybridization (Rhymer and Simberloff 1996). In the case of
P. newtoni, although this species occurs around the São Tomé capital and other
heavily modified landscapes (e.g., the Agripalma oil palm plantation), very little of
its original habitat remains unchanged and the impacts of land use on recruitment
and adult survival are unknown. Although the São Tomé caecilian also appears quite
resilient to land-use change, reports that it may be extirpated from the heavily
developed Ilhéu das Rolas are concerning (Loumont 1992).
The amphibian chytrid fungal pathogen, Batrachochytrium dendrobatidis (Bd), is
implicated in the declines and extinctions of amphibians across the globe (Scheele
et al. 2019). Although the pathogen has been documented in many species across the
Afrotropics, our understanding of how this pathogen impacts Afrotropical anuran
diversity lags far behind that of other regions (Zimkus et al. 2020). Surveys of
freshly sampled and historical specimens confirmed that the pathogen is present on
both São Tomé and Príncipe (Hydeman et al. 2013, 2017). The earliest infections
date from the oldest specimens screened to date (2001), indicating that the pathogen
has been present on the islands for at least 20 years (Hydeman et al. 2017). All of the
endemic species have tested positive for Bd (including the caecilians), and genomic
sequencing of the positive samples indicates that the more virulent Bd-GPL strain
occurs on the islands (Byrne et al. 2019). No symptomatic individuals have been
reported; however, we recommend careful monitoring of this emergent pathogen.
Future Research
The biogeographic history of the amphibian fauna of the Gulf of Guinea oceanic
islands is emerging as our understanding of evolutionary relationships within African genera continues to improve. Robust phylogenies of Leptopelis and
Phrynobatrachus, and better resolution within the Ptychadena mascareniensis species complex, will fill important gaps in our understanding of how and when
representatives of these genera reached the islands. The ecology and behavior of
all the island species are incompletely understood, including basic aspects of reproductive biology (e.g., L. palmatus) and dependence on particular habitats (e.g.,
P. newtoni, H. thomensis), which are likely important considerations for effective
conservation management. Like most vertebrates, São Tomé and Príncipe’s amphibians also serve as hosts for many parasites, including the fungal pathogen Bd and a
recently described nematode (Meteterakis saotomensis; Junker et al. 2015), but the
diversity of this microfauna and potential impacts on the amphibian hosts are poorly
known. For instance, a recent study identified cryptic infection of P. leveleve
(misidentified as P. dispar in the study) tadpoles by Perkinsea protists (Chambouvet
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R. C. Bell et al.
et al. 2015) that have caused mass mortality events in the United States (Davis et al.
2007). Further studies investigating the prevalence of this parasite in the tadpoles of
the other endemics and whether it is associated with tadpole mortality are sorely
needed. Beyond these more practical avenues for future research, the amphibians of
São Tomé and Príncipe also exhibit intriguing phenotypic diversity for addressing
long-standing hypotheses in evolutionary biology, including body size evolution and
gigantism on islands (e.g., H. thomensis, L. palmatus, P. newtoni), intraspecific
variation and interspecific divergence in coloration, and reproductive and dietary
niche partitioning.
Acknowledgments We thank Eng. Arlindo de Ceita Carvalho, Director General of the Ministry of
Environment, Daniel Pontes, Director of the Príncipe Obo National Park, and the former President
of Príncipe Autonomous Region, Dr. José Cassandra, for permission to collect and export specimens for study. We were assisted in the field by Pedro Ceríaco, Ostelino da Conceição Rocha, Ana
Carolina Sousa, Pedro Dias, Lauren Esposito, Maria Jerónimo, Mariana Pimentel Marques, Brian
Simison, Felipe Spina, and Andrew Stanbridge. Expeditions to São Tomé and Príncipe by RCD,
LAS and RCB were supported by donations from many generous friends and colleagues to the
California Academy of Sciences Gulf of Guinea Fund. We are grateful to the curators and collection
managers Giuliano Doria, Andreas Schmitz, Frank Tillack, Jakob Hallermann, and Patrick Campbell of the Museo Civico di Storia Naturale “Giacomo Doria” (Genoa, Italy), the Musée d’Histoire
Naturelle de la Ville de Genéve (Genéve, Switzerland), the Museum für Naturkunde (Berlin,
Germany) Zoologisches Museum (Hamburg, Germany), and the Natural History Museum
(London, UK), respectively, for allowing access and providing information about the collections
in their care. We thank David Blackburn, John Boyette, Vaclav Gvozdík, Kevin Mulder, Kyle
O’Connell, Ivan Prates, Rachel Quock, Ryan Schott and Mike Yuan for discussion and feedback to
improve this manuscript.
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Chapter 19
The Terrestrial Reptiles of the Gulf
of Guinea Oceanic Islands
Luis M. P. Ceríaco, Mariana P. Marques, Rayna C. Bell,
and Aaron M. Bauer
Abstract This chapter reviews current knowledge on the diversity of terrestrial
reptiles in the Gulf of Guinea oceanic islands and provides a brief history of research
on this group of animals. A total of 29 species of terrestrial reptiles (representing
14 genera and seven families) are resident on the Gulf of Guinea oceanic islands, of
which 22 species are endemic. Taxonomic work on these animals began in the
second half of the nineteenth century, with more recent updates following the advent
of molecular techniques and more comprehensive sampling. Although nearly complete, the taxonomic inventory of the Gulf of Guinea oceanic island terrestrial
L. M. P. Ceríaco (*)
Museu de História Natural e da Ciência da Universidade do Porto, Porto, Portugal
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório
Associado, Universidade do Porto, Vairão, Portugal
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO, Vairão, Portugal
Departamento de Zoologia e Antropologia (Museu Bocage), Museu Nacional de História
Natural e da Ciência, Universidade de Lisboa, Lisbon, Portugal
e-mail: lmceriaco@mhnc.up.pt
M. P. Marques
Departamento de Zoologia e Antropologia (Museu Bocage), Museu Nacional de História
Natural e da Ciência, Universidade de Lisboa, Lisbon, Portugal
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório
Associado, Universidade do Porto, Vairão, Portugal
Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Porto, Portugal
Present Address: BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO,
Vairão, Portugal
R. C. Bell
Department of Herpetology, Institute for Biodiversity Science and Sustainability, California
Academy of Sciences, San Francisco, CA, USA
A. M. Bauer
Department of Biology and Center for Biodiversity and Ecosystem Stewardship, Villanova
University, Villanova, PA, USA
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_19
505
506
L. M. P. Ceríaco et al.
reptiles is still ongoing, and further studies on the natural history, ecology, and
conservation of these animals are urgently needed.
Keywords Conservation · Endemism · Herpetofauna · Introduced species ·
Taxonomy
Introduction
Across the world, islands harbor a rich diversity of reptile species, many of them
endemic. In contrast to other groups of non-volant terrestrial vertebrates such as
small mammals and amphibians, reptiles are successful dispersers across marine
barriers due to their ecology and physiology, which enable them to endure longdistance rafting events (Vitt and Caldwell 2004). Some island reptiles, such as the
Galapagos tortoises and marine iguanas, rank amongst the most iconic species in the
world. These species are especially famous for providing Charles Darwin
(1809–1882) with the inspiration for his theory of evolution by natural selection.
Island reptiles have since become important models for the study of evolution and
adaptation in insular environments. For instance, the anoles (Squamata:
Dactyloidea) of the West Indies and lacertids (Squamata: Lacertidae) of the Mediterranean islands are now classic systems for evolutionary and ecological studies
(e.g., Corti et al. 2006; Losos 2009). In the eastern Atlantic, reptiles of the Madeira,
Cabo Verde and the Gulf of Guinea oceanic archipelagos have been the subject of
phylogenetic and biogeographic studies (e.g., Jesus et al. 2003, 2005a–c, 2006,
2007, 2009; Vasconcelos et al. 2010), recent descriptions of cryptic diversity (e.g.,
Miller et al. 2012; Ceríaco 2015; Ceríaco et al. 2016, 2017, 2021a; Soares et al.
2018), as well as ecological studies (e.g., Lopes et al. 2019).
With approximately 30 species and exceptional endemism, the Gulf of Guinea
archipelago is a hotspot for reptile diversity, especially when considering the small
land area of the islands. Here we present an updated taxonomic overview of the
terrestrial reptiles of these islands and surrounding islets, highlighting diversity,
endemism, biogeographic patterns and conservation. Marine turtles are the only
non-terrestrial reptiles occurring in these islands and are covered in Ferreira-Airaud
et al. (2022). We also provide a brief history of the research on reptiles in the
archipelago and highlight important avenues for future work.
History of Reptile Research
The first record of a reptile from the Gulf of Guinea oceanic islands was the description
of Mocoa (currently Panaspis) africana by Gray (1845). There are no data regarding
the collector or precise locality of collection, but the type locality has since been
restricted to Príncipe Island (Soares et al. 2018). Some decades later, the curator of the
Zoological Museum of Berlin, Wilhelm Peters (1815–1883), described Typhlops
(Ophthamidion) [currently Afrotyphlops] elegans based on specimens collected by
19
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507
the German explorer Heinrich Wolfgang Ludwig Dhorn (1838–1913) on Príncipe
(Peters 1868). Subsequently, the German zoologist Richard Greeff (1829–1892)
explored São Tomé and Rolas islet from 1879 to 1880 and provided one of the first
reports of their herpetofauna (Greeff 1884). Based on specimens collected by Greeff,
two species of reptile were described: Scalabotes (now Lygodactylus) thomensis by
Peters (1881) and Hemidactylus greeffii by Bocage (1886a). Some of Greeff’s specimens are still extant in the collections of the Museum für Naturkunde Berlin (ZMB)
and Zoologisches Museum Hamburg (ZMH).
Following Greeff’s surveys, two Portuguese museums funded expeditions to the
Gulf of Guinea oceanic islands. In 1885, the Botanical Gardens of the University of
Coimbra sent their chief gardener Adolfo Frederico Möller (1842–1920) to São
Tomé to explore and collect natural history specimens for the Botanical Gardens and
the university museum. Most of the zoological specimens collected by Möller were
sent to the Zoological Museum of the University of Coimbra (ZMUC, now part of
the Museu da Ciência da Universidade de Coimbra—MCUC), and a brief inventory
of these specimens was published by Vieira (1886). Almost all of this material was
examined and identified by the Portuguese zoologist José Vicente Barbosa du
Bocage (1823–1907) and is still extant in the collections of MCUC (Themido
1941; LMPC pers. obs.). Some amphibian and reptile specimens, however, were
likely sent by Möller to the Russian zoologist Jacques von Bedriaga (1854–1906)
who was a correspondent scholar with the University of Coimbra. Bedriaga
published a thorough revision of the amphibians and reptiles of São Tomé and
described a new subspecies of gecko, Hemidactylus mabouia var. molleri (currently
a synonym of H. longicephalus, see below), in honor of Adolfo Möller and provided
a detailed description of a specimen of Dendroaspis jamesonii from the island
(Bedriaga 1892, 1893a–c). Bedriaga’s publications triggered criticism from Bocage
(1892a–c, 1893), who cast doubts on the identity of Hemidactylus mabouia var.
molleri (Bocage 1892a) and the Dendroaspis (Bocage 1892c). These disagreements
have since been addressed in Ceríaco and Marques (2012) and Ceríaco et al. (2018).
There are no further records of the specimens sent by Möller to Bedriaga and they are
presumably lost.
Also in 1885, Francisco Xavier Oakley de Aguiar Newton (1864–1909), commonly known as Francisco Newton, was hired by the National Museum of Lisbon to
conduct zoological surveys in the Gulf of Guinea. From 1885 to 1895, Newton
explored all the Gulf of Guinea islands, as well as Benin, and his specimens were
ultimately deposited in the Zoological Section of the National Museum of Lisbon.
This material was studied by Barbosa du Bocage, director of the museum, and Júlio
Guilherme Bethencourt Ferreira (1866–1948), Bocage’s pupil. Based on Newton’s
collections Bocage described four species of reptile from the Gulf of Guinea oceanic
islands: Feylinia polylepis, Mabuia [¼ currently Trachylepis] ozorii, Typhlops [¼
currently Letheobia] newtoni, and Philothamnus girardi. Also based on these
collections, Bocage provided important revisionary works on the fauna of these
islands (Bocage 1886a–c, 1873, 1887, 1890, 1892a–c, 1893, 1895, 1903, 1905), and
Ferreira (1897) described Hemidactylus newtoni from Annobón. The entirety of
Newton’s collections was unfortunately lost in the fire that destroyed the Museu
Bocage, Lisbon, in 1978.
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L. M. P. Ceríaco et al.
Following Newton’s steps, the Italian explorer Leonardo Fea (1852–1903)
explored the four principal islands of the Gulf of Guinea from 1901 to 1902 under
the sponsorship of the Museo Civico di Storia Naturale of Genoa, Italy (currently
known as Museo Civico di Storia Naturale “Giacomo Doria;” MSNG). Fea’s
collections, which are still extant in the MSNG with a small subset in the Natural
History Museum of London (BMNH), were initially studied by George Albert
Boulenger (1858–1937). Based on these collections, Boulenger (1906) described
four new taxa: Hemidactylus aporus from Annobón, Typhlops [currently Letheobia]
feae from São Tomé, Boodon [¼Boaedon] bedriagae, from both São Tomé and
Príncipe, and Gastropyxis [currently Hapsidophrys] principis from Príncipe. Some
of these specimens were revisited by Lilia Capocaccia in a revision of certain snake
genera (Capocaccia 1961a) and the type catalog of the MSNG (Capocaccia 1961b).
A small collection of reptiles from São Tomé and Príncipe, collected by Henri
Navel (1878–1963) in 1920, was subsequently studied by the French herpetologist
Fernand Angel (1881–1950), who described Typhlops naveli (currently considered
as a junior synonym of Letheobia newtoni; fide Roux-Estève 1974) from Príncipe
(Angel 1920). An additional contribution to the knowledge of São Tomé snakes was
provided by the curator of the American Museum of Natural History, Charles
M. Bogert (1908–1992), who used specimens collected by the Portuguese explorer
José G. Correia (1881–1954) to review the identity of the São Tomé Jitas (Boaedon;
Bogert 1940).
During the 1950s and 1960s the Portuguese Centro de Zoologia da Junta de
Investigações do Ultramar (CZL) conducted zoological surveys on São Tomé and
Príncipe. The first mission, conducted by the Portuguese zoologist Fernando Frade
Viegas da Costa (1898–1983; commonly referred to simply as Fernando Frade),
lasted from September 10 to December 26, 1954. Between 1966 and 1967, several
herpetological specimens were collected by different researchers associated with the
colonial enterprise over the course of multiple scientific surveys. The material
collected during these surveys was studied by the Portuguese herpetologist Sara
Maria Bárbara Marques Manaças (1896–death date unknown), resulting in two
publications (Manaças 1958, 1973). Most of the specimens were housed in the
collections of the Instituto de Investigação Científica Tropical (IICT), in Lisbon,
Portugal, but in 2016 they were incorporated into the collections of the Museu
Nacional de História Natural e da Ciência (MUHNAC), of the University of Lisbon,
Lisbon, Portugal. A total of 157 reptile specimens from these expeditions are still
extant in these collections (Ceríaco and Marques 2018; Ceríaco et al. 2021b).
Throughout the 1960s and 1970s, several authors used existing specimens in
various collections for taxonomic revisions of different genera, resulting in important contributions to the knowledge of the Gulf of Guinea oceanic islands taxa. For
instance, the French herpetologist Georges Pasteur (1930–2015) used specimens of
the Fea collections in the BMNH to revise the Lygodactylus of these islands (Pasteur
1962), leading to the description of two subspecies of L. thomensis: L. thomensis
delicatus from Príncipe, and L. thomensis wermuthi from Annobón. The Swiss
herpetologist Jean-Luc Perret (1925–) used specimens from the CZL and Fea
collections in the BMNH for his major revision of the genus Panaspis (Perret
1972). Subsequently, the Romanian herpetologist Ion Eduard Fuhn (1916–1987)
19
The Terrestrial Reptiles of the Gulf of Guinea Oceanic Islands
509
used specimens from Fea collections housed in the BMNH to describe Panaspis
annobonensis from Annobón and review the Panaspis of São Tomé and Príncipe, at
the time both considered P. africana (Fuhn 1972).
Following the independence of Equatorial Guinea (from Spain in 1968) and São
Tomé and Príncipe (from Portugal in 1975), several teams undertook expeditions to
the islands to further expand knowledge on their herpetological diversity. In 1984 a
team from the zoology and anthropology department of the Faculty of Sciences of
the University of Lisbon and the Museu Nacional de História Natural (Museu
Bocage), Lisbon, led by Luis Mendes (1946–), conducted a 1 month (June 13 to
July 7) zoological expedition to São Tomé (Mendes et al. 1988). Although the
expedition did not have a dedicated herpetologist, some reptile specimens were
collected, and these are still extant in MUHNAC collections (Ceríaco and Marques
2019).
Ronald Nussbaum (1942–) from the University of Michigan and Michael
Prfender (1960–) visited the islands of São Tomé and Príncipe in June and July of
1988. While mainly focused on the study of amphibians, especially the São Tomé
endemic caecilian Schistometopum thomense (Bocage, 1873), Nussbaum and
Pfrender also collected several reptile specimens, of which 333 are still in the
collections of the University of Michigan Museum of Zoology (UMMZ; see University of Michigan Museum of Zoology 2020). These specimens have not been
included in any publication or study, although they represent the third largest reptile
collection from São Tomé and Príncipe in any museum and are an important source
of data on the geographical distributions of many species. From 1989 to 1991
expeditions to São Tomé and Príncipe led by Catherine Loumont (1942–), Tillman
Nill (date of birth unknown), Jakob Fahr (1966–) and Jan Haft (1967–), resulted in
reviews of the herpetofauna of these islands (Schätti and Loumont 1992; Nill 1993;
Haft 1993). Some of these specimens are housed in the ZMB and the collections of
the Muséum d’Histoire Naturelle de la Ville de Genève, Geneva, Switzerland
(Andreas Schmitz pers. comm.)
A major contribution to our understanding of the herpetofauna of the three
oceanic islands of the Gulf of Guinea was provided by José Jesus (1967–) from
the University of Madeira, Funchal, Portugal, who dedicated part of his Ph.D. thesis
to study the phylogeny and phylogeography of the islands’ reptiles, providing
molecular data for many of the taxa. Jesus and his team visited Príncipe, São
Tomé and Annobón in the summer of 2002, and based on the specimens and tissues
collected, provided the first molecular phylogenetic and phylogeographic context for
the species of the genus Trachylepis (Jesus et al. 2005a, b), Hemidactylus (Jesus
et al. 2005c), Lygodactylus (Jesus et al. 2006), Panaspis (Jesus et al. 2007) and
Philothamnus (Jesus et al. 2009) occurring in these islands. Jesus et al. (2003) also
provided an updated checklist of the reptiles of Annobón, in which they noted the
first records of Tropical House Gecko, Hemidactylus mabouia, and the invasive
Flowerpot snake, Indotyphlops braminus on the island. The specimens collected by
Jesus and his team were primarily deposited in the collections of the University of
Madeira, with smaller subsets in MUHNAC and the California Academy of Sciences
(CAS), San Francisco.
510
L. M. P. Ceríaco et al.
Table 19.1 Main natural history institutions housing reptile specimens from the Gulf of Guinea
oceanic islands. Acronyms follow Sabaj (2020)
Collection
CAS: California Academy of Sciences, San
Francisco, United States of America
MUHNAC/IICT: Museu Nacional de
História Natural e da Ciência/Instituto de
Investigação Científica Tropical, Lisbon,
Portugal
UMMZ: University of Michigan Museum
of Zoology, Ann Arbor, United States of
America
MHNG: Muséum d’Histoire naturelle de la
Ville de Genève, Geneva, Switzerland
MSNG: Museo Civico di Storia Naturale
‘Giacomo Doria’, Genova, Italy
MHNCUP: Museu de História Natural e da
Ciência da Universidade do Porto, Porto,
Portugal
MNHN: Muséum National d’Histoire
Naturelle, Paris, France
NHM: Natural History Museum, London,
United Kingdom
ZMH: Zoologisches Museum Hamburg,
Hamburg, Germany
SNM: Natural History Museum of Denmark, Copenhagen, Denmark
MCZ: Museum of Comparative Zoology,
Harvard University, Cambridge, United
States of America
a
São
Tomé
228
Príncipe
219
Annobón
8
Type
specimens
24
Total
455
108
239
14
26
361
122
210
–
–
332
136
–
–
7
136
43
49
9
5
101
22
18
–
13
5
2
6
7
3
15a
8
1
1
1
10
10
–
–
–
10
1
4
1
–
6
–
40
–
18
Probably more
At about the same time, in 2001, the CAS led by herpetology curator Robert
“Bob” C. Drewes (1942–), began what would become known as the CAS Gulf of
Guinea Expeditions. This project, which has made a total of 12 expeditions to the
islands as of 2020, is still ongoing and has been one of the most comprehensive
efforts to study the biodiversity of São Tomé and Príncipe islands since Francisco
Newton’s expedition in the nineteenth century. Due to Drewes’ herpetological
background, the project has always had a strong emphasis on the study of the
amphibians and reptiles of these islands (see Bell et al. 2022). The reptile collections
resulting from these expeditions are currently the largest in the world (Table 19.1),
with a total of 449 specimens (Scheinberg and Fong 2019). One important taxonomic contribution from these expeditions was the description of the Príncipe
Gecko, Hemidactylus principensis Miller, Sellas and Drewes, 2012, the first
endemic reptile described from the Gulf of Guinea oceanic islands since 1972
(Miller et al. 2012).
19
The Terrestrial Reptiles of the Gulf of Guinea Oceanic Islands
511
Finally, since 2013, a team from MUHNAC led by Luis M. P. Ceríaco (1987–)
started herpetological surveys in São Tomé and Príncipe. A total of four expeditions
(two in 2013, one in 2015, one in 2016) to Príncipe and São Tomé islands, as well as
to Tinhosa Grande islet, were conducted by the team, which resulted in the collection
of 155 reptile specimens, currently housed in MUHNAC collections (Ceríaco and
Marques 2019). Combined with the specimens collected by Mendes et al. (1988) and
those originally from IICT (Ceríaco and Marques 2018), MUHNAC collections hold
a total of 354 specimens of São Tomé and Príncipe reptiles and are the second largest
in the world. Building on the knowledge amassed through newly collected specimens, the available Portuguese and North American collections, as well as the
molecular baseline provided by the Jesus et al. studies, Ceríaco and team have
contributed to the taxonomic revision of most of the reptile groups occurring on
the islands. This led to the description of: three species of skinks of the genus
Trachylepis (Ceríaco 2015; Ceríaco et al. 2016)—Trachyelpis adamastor Ceríaco,
2015, Trachylepis thomensis Ceríaco, Marques and Bauer, 2016, and Trachylepis
principensis Ceríaco, Marques and Bauer, 2016, endemic to Tinhosa Grande islet,
São Tomé, and Príncipe, respectively; a new species of Cobra (Ceríaco et al.
2017)—Naja (Boulengerina) peroescobari Ceríaco, Marques, Schmitz and Bauer,
2017; a new species of the genus Panaspis, endemic to São Tomé (Soares et al.
2018)—Panaspis thomensis Ceríaco, Soares, Marques et al., 2018; and a new
species of lamprophid snake of the genus Boaedon (Ceríaco et al. 2021a)—Boaedon
mendesi Ceríaco, Arellano, Jadin et al., 2021. In 2018 Ceríaco’s team moved to the
Museu de História Natural e da Ciência of the University of Porto (MHNCUP) and
new field work has been carried out since then.
Diversity and Endemism
At present, a total of 29 reptile species have been reported as resident from the
oceanic islands of the Gulf of Guinea (Table 19.2). Of these, 22 are endemic to one
or two islands, three are presumed invasive/introduced species, and one corresponds
to questionable records of a putative species of mamba. An additional species is
considered vagrant to São Tomé. We discuss the taxonomic status and biology of
each species in more detail below.
Crocodilians
There are currently no established crocodilian populations inhabiting the Gulf of
Guinea oceanic islands. Historical records dating back to the first decades of
Portuguese presence suggest that a species of Crocodylus occurred on São Tomé.
A report from the Portuguese navigator Gonçalo Pires (birth and death dates
unknown), transcribed by Valentim Fernandes (ca. 1450–1519) and subsequently
512
L. M. P. Ceríaco et al.
Table 19.2 List of terrestrial reptiles from Príncipe (P), São Tomé (ST) and Annobón (A) islands
Higher taxonomy
Order Crocodylia
Family Crocodylidae
Crocodylus Laurenti,
1768
Order Testudines
Family Pelomedusidae
Pelusios Wagler, 1830
Order Squamata
Family Gekkonidae
Hemidactylus Goldfuss,
1820
Lygodactylus Gray, 1864
Family Scincidae
Feylinia Gray, 1845
Panaspis Cope, 1868
Trachylepys Fitzinger,
1843
Family Typhlopidae
Afrotyphlops Broadley
and Wallach, 2009
Letheobia Cope, 1869
Indotyphlops Hedges,
Marion, Lipp, Marin and Vidal,
2014
Family Lamprophiidae
Boaedon Duméril, Bibron
and Duméril, 1854
Species/subspecies
P
Crocodylus niloticus Laurenti, 1768
Pelusios castaneus (Schweigger,
1812)
Hemidactylus aporus Boulenger, 1906
Hemidactylus greeffii Bocage, 1886
Hemidactylus mabouia (Moreau de
Jonnés, 1818)
Hemidactylus longicephalus Bocage,
1873
Hemidactylus principensis Miller,
Sellas and Drewes, 2012
Hemidactylus newtoni Ferreira, 1897
Lygodactylus delicatus Pasteur, 1962
Lygodactylus thomensis (Peters, 1881)
Lygodactylus wermuthi Pasteur, 1962
A
IUCN
V
X
X
I
E
I
I
I
LC
E?
I
NT
E
E
E
E
E
E
Afrotyphlops elegans (Peters, 1868)
E
Letheobia newtoni (Bocage, 1890)
Letheobia feae (Boulenger, 1906)
Indotyphlops braminus (Daudin,
1803)
E
E
DD
LC
LC
LC
LC
LC
LC
E
E
DD
LCa
LC
LC
E
LC
E
X
E
LC
E
E
I
E
E
DD
NT
LC
LC
E
Feylinia polylepis Bocage, 1887
Panaspis africana (Gray, 1845)
Panaspis thomensis Ceríaco et al.
2016
Panaspis annobonensis (Fuhn, 1972)
Trachylepis adamastor Ceríaco, 2015
Trachylepis affinis (Gray, 1838)
Trachylepis thomensis Ceríaco,
Marques and Bauer, 2016
Trachylepis ozorii (Bocage, 1893)
Boaedon bedriagae Boulenger, 1906
Boaedon mendesi Ceríaco et al. 2021
ST
DD
DD
LC
LC
NE
(continued)
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The Terrestrial Reptiles of the Gulf of Guinea Oceanic Islands
513
Table 19.2 (continued)
Higher taxonomy
Family Colubridae
Philothamnus Smith,
1847
Hapsidophrys Fischer,
1856
Family Elapidae
Naja Laurenti, 1768
Dendroaspis Schlegel,
1848
Species/subspecies
Philothamnus thomensis Bocage,
1882
Philothamnus girardi Bocage, 1893
Hapsidophrys principis (Boulenger,
1906)
Naja (Boulengerina) peroescobari
Ceríaco, Marques, Schmitz and Bauer,
2017
Dendroaspis cf. jamesoni (Trail,
1843)
P
ST
A
E
LC
E
E
IUCN
LC
LC
E
EN
?
LC
Status in each island: E, endemic; I, introduced; V, vagrant; X, resident; ?, uncertain. IUCN Red List
Categories: DD, data deficient; LC, least concern; NE, not evaluated; NT, near threatened; EN,
endangered
a
As T. principensis
published by several authors (Henriques 1917; Baião 1940; Ceríaco et al. 2018)
mentions the following:
There were many lizards of about twelve cubits [approximately 540 cm], but now there are
few. They eat men and women, cows and bulls and all types of animals. These lizards don’t
exit the water, as their tails stay always inside freshwater, and any animal that he captures he
takes into the water and in the water he kills it, and it rears up on his tail achieving the size of
a man. The current captain, Fernã do Mello, has a very big and fearful lizard contained in a
pond, and above this pond he mounted a scaffold to allow its observation. This lizard used to
move from the river to the pond several times a month. And he caused a lot of damage to the
men and animals, and 1 day, a small and despicable man who observed the lizard for some
time, once he found it in the pond and with his hoe he cut the lizard’s limbs and closed the
pond so he couldn’t ever escape and went to tell this to the captain.
[LMP Ceríaco’s translation from the archaic Portuguese original]
In a subsequent passage of the text, the authors refer to the “very big lizards, that
now fear the men.” [author’s translation from the archaic Portuguese original]. Due
to the perceived danger that the São Tomé crocodiles posed to the Portuguese
settlers, it is fair to assume that the population was completely extirpated. As no
archeological remains of these animals are known, the taxonomic identity of this
historical São Tomé crocodilian cannot be determined but is likely that they were
either an insular population of Crocodylus niloticus Laurenti, 1768, or C. suchus
Geoffroy Saint-Hilaire, 1807.
However, the presence of crocodiles in the islands may be more common than the
available data suggest. In early April 2021, a live crocodile appeared on Roça
Colónia Açoreana beach, in the southeastern part of São Tomé Island (Fig. 19.1,
1). Other records of a large lizard seen in the Angra Toldo region, and said to be a
crocodile, had previously surfaced on social media, but these records have never
been confirmed. The animal from Colónia Açoreana was a female Crocodylus
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L. M. P. Ceríaco et al.
Fig. 19.1 Crocodile from Colónia Açoreana beach, São Tomé Island: (1) Live photo of the animal
on 4 April 2021; (2) Skin of the specimen in the biology laboratory of the Portuguese School of São
Tomé; (3, 4) Specimen after being shot. Photo credits: (1) Maria Branco, (2) Luis M. P. Ceríaco,
(3, 4) Unknown
19
The Terrestrial Reptiles of the Gulf of Guinea Oceanic Islands
515
niloticus, of approximately two meters total length, which was observed and
photographed for several weeks on the beach. Due to the safety concerns it
presented, the animal was killed by the authorities at the end of the month
(Fig. 19.1, 3–4). The specimen’s head and skin were prepared by two of the authors
(LMPC and MPM) and deposited in the biology laboratory of the Portuguese School
of São Tomé and Príncipe (Fig. 19.1, 2). Molecular studies are underway to identify
the source population of the animal in continental Africa. At about the same time of
the appearance of the crocodile in Colónia Açoreana, two Angolan fishermen in a
castaway boat that had drifted from the Angolan coast near the mouth of Congo
River were rescued near São Tomé by the local authorities. The Gulf of Guinea sea
currents and the considerable flow of the Congo River at that time due to heavy rains
on the continent may help to explain both of these arrivals.
Terrapins
Family Pelomedusidae
Only one species of terrapin occurs in the Gulf of Guinea oceanic islands, the West
Africa mud turtle, Pelusios castaneus (Schweigger, 1812) (Fig. 19.2, 1). The species
has mostly been recorded from São Tomé, where it is locally known as “Bencú” and
is used by Santomeans in the local gastronomy. Recent sightings in Príncipe suggest
that the species also occurs on the island, but currently, there are still no available
specimens in public collections to permit a clearer and detailed assessment of its
taxonomic status. The species has a considerable distribution through West and
Central Africa, extending from Senegal to northern Angola (Bour et al. 2016;
Rhodin et al. 2017). Fritz et al. (2010) presented evidence from three mitochondrial
and three nuclear loci that the population from São Tomé is closely related to
populations from Ivory Coast and represents a recent colonization. A subsequent
study by Kindler et al. (2016) using the same loci but with additional geographic
sampling uncovered several geographically distinct clades across the distribution of
P. castaneus, with the São Tomé population nested within a West African clade
along with specimens from Ivory Coast and Nigeria. Despite not being a common
species, P. castaneus has been reported from the island since the 1880s (Greeff
1884; Bocage 1886a, 1889) and was more recently found in Oque d’el Rei, Água
Grande District (February 2013, specimens deposited in the collections of
MUHNAC). Data on the distribution, abundance, ecology, and natural history of
this species in São Tomé are still very limited, although it is expected that the species
inhabits rivers, streams and temporary water bodies as it does throughout its range in
continental Africa (Bour et al. 2016). As the phylogenetic studies indicate, a possible
human-mediated introduction of P. castaneus to São Tomé cannot be rejected, but
further research is needed to clarify the evolutionary history of this population.
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L. M. P. Ceríaco et al.
Fig. 19.2 Gulf of Guinea oceanic island reptiles: (1) West African mud turtle, Pelusios castaneus,
from São Tomé Island; (2) Príncipe Gecko, Hemidactylus principensis, from Príncipe Island; (3)
Manyscale Feylinia, Feylinia polylepis, from Príncipe Island; (4) Adamastor Skink, Trachylepis
thomensis, from São Tomé Island; (5) Elegant Worm Snake, locally known as Cobra-bobô,
Afrotyphlops elegans, from Príncipe Island; (6) Mendes’ House Snake, locally known as Jita,
Boaedon mendesi, from Príncipe Island; (7) Príncipe Emerald Snake, locally known as Suá-suá,
Hapsidophrys principis, from Príncipe Island; (8) São Tomé Cobra, locally known as Cobra-preta,
Naja peroescobari, from São Tomé Island. Photo credits: (1–8) Luis M. P. Ceríaco
19
The Terrestrial Reptiles of the Gulf of Guinea Oceanic Islands
517
Squamata
Squamate diversity in the Gulf of Guinea oceanic islands includes 28 species from
two families of lizards—Gekkonidae, Scincidae—and four families of snakes—
Typholpidae, Lamprophiidae, Colubridae and Elapidae. All species are endemic to
the islands, except for one native skink (family Scincidae), two introduced geckos
(family Gekkonidae), one introduced snake (family Typholopidae), and one gecko
(family Gekkonidae) and one snake (family Elapidae) that are based on doubtful or
problematic records that require further investigation.
Family Gekkonidae
The geckos of the Gulf of Guinea oceanic islands belong to two different genera: the
Dwarf Geckos of the genus Lygodactylus Gray, 1864, and the Tropical House
Geckos of the genus Hemidactylus Goldfuss, 1820. Each island is represented by
its own endemic form of Lygodactylus: the Príncipe Dwarf Gecko, L. delicatus
Pasteur, 1962, the São Tomé Dwarf Gecko, L. thomensis (Peters, 1881), and the
Annobón Dwarf Gecko, L. wermuthi Pasteur, 1962. Following the initial description
of L. thomensis by Peters (1881), several authors considered the populations on all
three islands as conspecific (e.g., Bocage 1886a, 1892b, 1893, 1903, 1905;
Boulenger 1885, 1906; Sternfeld 1917; Loveridge 1947). Pasteur (1962) reviewed
the group and described delicatus and wermuthi as subspecies of thomensis based on
morphological and coloration differences. With the exception of Manaças (1958),
subsequent authors followed the Pasteur (1962) taxonomy (Schätti and Loumont
1992; Haft 1993). Jesus et al. (2006) were the first to provide molecular data for these
island taxa and found the level of divergence in 12S and 16S mitochondrial genes
was within the level of divergence observed between other species within the genus.
With this combination of phenotypic and genetic distinctiveness, and their allopatric
distributions, Ceríaco et al. (2018) considered each island population as a valid
species. Data on the distribution, abundance, ecology, and natural history of the three
species are limited. Lygodactylus thomensis and L. delicatus are commonly observed
in human settlements, especially on walls, fences and other structures (Manaças
1958, LMPC pers. obs.); however, Jesus et al. (2003) noted that L. wermuthi has
only been found in forested areas. Manaças (1958) recorded specimens of flies
(Diptera) in the stomach contents of L. delicatus.
The taxonomy of the genus Hemidactylus is considerably more complex. A total
of six species are currently recorded for the islands. Four of these are endemic to the
islands: the Príncipe Gecko, Hemidactylus principensis Miller, Sellas and Drewes,
2012, endemic to Príncipe and Tinhosa Grande islet (Fig. 19.2, 2); Greeff’s Gecko,
H. greeffii Bocage, 1866, endemic to São Tomé and Rolas islet; Newton’s Gecko,
H. newtoni Ferreira, 1897, endemic to Annobón; and the Annobón Gecko, H. aporus
Boulenger, 1906. The remaining two species are most likely human introductions—
the Long-Headed Tropical Gecko, H. longicephalus, Bocage, 1873, occurring on
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São Tomé and Príncipe, the Tropical House Gecko, H. mabouia (Moreau de Jonnès,
1818), occurring on all three islands and Rolas.
Príncipe and São Tomé islands, as well as the surrounding islets of Tinhosa
Grande and Rolas, respectively, host an endemic lineage of the genus Hemidactylus
comprising H. principensis and H. greeffii (Bauer et al. 2010; Miller et al. 2012;
Ceríaco et al. 2020a). These two species exhibit a clear synapomorphic character that
differentiates them from all other African species of Hemidactylus: the absence of
the terminal phalanx and claw of the first digit (thumb) of the manus (Bocage 1886a,
1905; Boulenger 1906; Loveridge 1947; Haft 1993; Miller et al. 2012). Both species
are members of the African-Atlantic clade, a group mainly comprising Angolan and
Western African species that are closely related to Brazilian species such as
H. brasilianus Amaral, 1935 (Ceríaco et al. 2020a). While H. greeffii was described
in the 1880s by Bocage (1886a), H. principensis was only recently described by
Miller et al. (2012) on the basis of genetic divergence and several morphological
differences, including iris coloration and body size. The unidentified Hemidactylus
from Tinhosa Grande reported by Ceríaco (2015) was shown, through the use of
molecular data, to be conspecific with H. principensis from Príncipe Island (Ceríaco
et al. 2020b). The known distribution of both species is very limited (Greeff 1884;
Bocage 1886a, 1905; Boulenger 1906; Manaças 1958; Schätti and Loumont 1992;
Haft 1993; Miller et al. 2012). Both species appear to be less abundant in more
developed areas and preferring less disturbed habitats (LMPC pers. obs.); however,
they are able to colonize and thrive in both forested and more xeric areas, as in the
case of the Tinhosa Grande islet population.
The Annobón endemics, H. newtoni and H. aporus, have a more convoluted
taxonomic history. H. newtoni was described by Ferreira (1897) based on a series of
seven specimens collected by Francisco Newton in 1893: one adult male, five adult
females and one juvenile. These same specimens were previously examined by
Bocage (1893), who tentatively identified them as H. mabouia, noting, however,
that they differed from H. mabouia in being “smaller and having relatively larger and
closer dorsal tubercles.” Ferreira (1897) considered the dorsal patterns of transverse
“W” shaped markings extending from the neck to the insertion of the tail, the number
and disposition of the dorsal tubercles, and the “very long and flattened digits, with
strong claws and enlarged proximally, with larger and more numerous number of
subdigital lamellae [7–8 in the first finger, 11–12 in the fourth toe]” as diagnostic
characters for H. newtoni. Bocage (1903) provided a French translation of the
original Ferreira (1897) description in Portuguese. Surprisingly, neither Ferreira
(1897) nor Bocage (1903) provided data on the number of preanal or femoral
pores of the male specimen. Loveridge (1947) interpreted this omission as a complete lack of preanal or femoral pores in the male syntype, which would thus
resemble the other putative endemic species, H. aporus (see below). Loveridge
noted that “if correctly counted, the greater number of subdigital scansors of
H. newtoni, approaching those of H. echinus O’Shaughnessy, 1875, afford good
grounds for separation.” The type series of H. newtoni was lost in the fire that
destroyed the collections of Museu Bocage (Lisbon) in 1978. Jesus collected new
material in the early 2000s and provided the first molecular data for H. newtoni
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(Jesus et al. 2005c), noting that it was sister to “an individual from an undescribed
form from São Tomé,” recently identified as H. longicephalus by LMPC (pers. obs.).
Further studies are needed to better understand the phylogenetic placement of
H. newtoni among its African congeners and begin to understand its evolutionary
history, as well as its natural history, distribution and ecology.
The second Annobón endemic, H. aporus, was described by Boulenger (1906)
based on several specimens, including males and females, collected by Fea.
According to the author, the species is very similar to H. bocagii
[¼H. longicephalus], but differs by having the dorsal tubercles “larger, closer
together, forming 16–20 more regular longitudinal series” and lacking precloacal
or femoral pores in males (present in H. longicephalus; see Ceríaco et al. 2020a, b).
The species differs from H. newtoni in the number of subdigital lamellae (“5
lamellae under the inner digit, 7 under the third and fourth” in H. aporus fide
Boulenger (1906) versus “7–8 in the first finger, 11–12 in the fourth toe” in
H. newtoni fide Ferreira (1897)). Loveridge (1947) considered the species valid,
noting that the absence of pores in the males distinguishes aporus from all other
West African species with the exception of sympatric H. newtoni [if this is indeed
true], from which it differs in “possessing fewer subdigital scansors, 7 (instead of
11–12) under the fourth toe, and 16–20 (instead of irregularly disposed) dorsal
tubercles.” The species has not been collected since its original description over a
century ago, and our current knowledge is limited to the very brief, original
description (Meiri et al. 2017). The type series is still extant in the Museo Civico
di Storia Naturale “Giacomo Doria,” Genoa, Italy (Giulliano Doria pers. comm.).
While the available evidence supports the identity of H. newtoni as a valid species,
the status of H. aporus requires further research.
The presence of Hemidactylus longicephalus, a coastal species endemic to
western Angola and southwestern Democratic Republic of the Congo, was first
noted in São Tomé when Bedriaga (1892) misidentified the specimens at his disposal
as a new subspecies of H. mabouia, which he named as H. mabouia var. molleri. The
convoluted history of this putative taxon was briefly discussed by Ceríaco and
Marques (2012) and Ceríaco et al. (2018). Ceríaco et al. (2020a) definitively
synonymized molleri with longicephalus, a hypothesis already put forward by
Loveridge (1947). In addition to the records from São Tomé provided by Bedriaga
(1892), Bocage (1903; as H. bocagii, a junior synonym of longicephalus) and
Manaças (1958) provided records from Príncipe, and Carranza and Arnold (2006)
and Ceríaco et al. (2020a) provided additional records of the species for São Tomé.
Jesus et al. (2005c) noted the presence of a putative new species of Hemidactylus
from São Tomé, which was later confirmed to be conspecific with longicephalus
(LMPC pers. obs.) Both morphological and molecular data provided by Ceríaco
et al. (2020a), unambiguously identify the São Tomé and Príncipe populations as
conspecific with the Angolan form. Consequently, the authors concluded that the
species naturally colonized the islands relatively recently or were introduced to the
islands through human activities, as São Tomé, Príncipe and Angola were Portuguese colonies, and the islands were an important stopover for ships departing from
Angola to the Americas and Europe (Ceríaco et al. 2020a). Due to the limited
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number of collected specimens, not much is known about the ecology and distribution of this species on the islands, but in Angola, it tends to be found in coastal
lowland areas or in human settlements (Ceríaco et al. 2020a).
Finally, H. mabouia is one of the most widespread and ubiquitous species of
gecko in the world, native to Central and Western Africa but introduced to North,
Central and South America, as well as the Caribbean (Kraus 2009; Agarwal et al.
2021). There are historical and modern records of this species on the three islands
(e.g., Greeff 1884; Bocage 1886c, 1889, 1892a, 1905; Vieira 1886; Bedriaga 1892;
Boulenger 1906; Manaças 1958, 1973; Schätti and Loumont 1992; Haft 1993; Hofer
2002; Jesus et al. 2003, 2005c; Miller et al. 2012; Ceríaco et al. 2018, 2020a). Jesus
et al. (2005c) and Ceríaco et al. (2020a) provided molecular evidence indicating that
the Gulf of Guinea oceanic islands populations are almost indistinguishable from the
continental populations of the species, suggesting a recent arrival/introduction to the
archipelago. The species is very common in human settlements and is often observed
on houses and other buildings at night.
Family Scincidae
The skinks occurring on the Gulf of Guinea oceanic islands belong to three different
genera: the feylinias of the genus Feylinia Gray, 1845, leaf-litter skinks (also known
as snake-eyed skinks) of the genus Panaspis Cope, 1868, and the common skinks of
the genus Trachylepis Fitzinger, 1843. The fossorial and limbless Many-scaled
Feylinia, Feylinia polylepis Bocage, 1887 is endemic to Príncipe (Fig. 19.2, 3).
Described by Bocage (1887) as a subspecies of Feylinia currori Gray, 1845, the
species has been recorded on the island by several authors (Bocage 1903; Boulenger
1906; Angel 1920; Manaças 1958, 1973; Brygoo and Roux-Estève 1983; Hofer
2002; Ceríaco et al. 2018; Soares et al. 2018). Due to its secretive lifestyle, this
species is still poorly known in terms of its ecology, natural history, and phylogenetic position, although, as noted by Brygoo and Roux-Estève (1983), its taxonomic
validity is unquestionable. The species is morphologically most similar to Feylinia
currori, but the lack of molecular data for most of the representatives of the genus
limits any attempt to understand its phylogenetic placement. The feylinia is very
common and is found under leaf-litter, logs, or rocks.
The taxonomic history of leaf-litter skinks, genus Panaspis, of the Gulf of Guinea
oceanic islands is quite complex. All authors who have dealt with this species during
the nineteenth and the first half of the twentieth century considered that populations
on the three islands were conspecific (e.g., Greeff 1884; Bocage 1886a, 1889, 1903,
1905; Bedriaga 1892; Boulenger 1906; Manaças 1958), bearing the specific epithet
africana (or aftricanum, depending on the genus they were placed in by the different
authors—see Soares et al. 2018). The species was originally described as Mocoa
africana by Gray (1845). Although Gray (1845) did not provide a precise type
locality, the type specimen is unambiguously identifiable as originating from
Príncipe (Soares et al. 2018). Subsequently, Fuhn (1972) revised the Gulf of Guinea
Panaspis, leading to the description of the Annobón population as P. africana
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annobonensis. Perret (1973) considered annobonensis as a full species, a decision
that would later be supported using molecular data (three mitochondrial and one
nuclear locus) by Jesus et al. (2007) and Medina et al. (2016). A more recent
taxonomic revision by Soares et al. (2018) led to the description of a third species—Panaspis thomensis Ceríaco, Soares, Marques et al., 2018, endemic to São
Tomé. The three species form a clade within the genus Panaspis along with
P. cabindae (Bocage, 1866) from Angola (Medina et al. 2016; Soares et al. 2018).
Panaspis africana, P. annobonensis, and P. thomensis are some of the most conspicuous reptiles on their respective islands. They are typically encountered in
forested areas in leaf-litter, and even in gardens in more urban areas (Jesus et al.
2003; Soares et al. 2018).
Similar to the Leaf-litter skinks, the common skinks of the genus Trachylepis are
also among the most conspicuous lizards on these islands. Four species occur in the
Gulf of Guinea oceanic islands: Trachylepis adamastor Ceríaco, 2015, endemic to
Príncipe and Tinhosa Grande islet; T. thomensis Ceríaco, Marques and Bauer, 2016,
endemic to São Tomé and surrounding islets (Fig. 19.2, 4); T. ozorii (Bocage, 1893),
endemic to Annobón; and T. affinis (Gray, 1838) on Príncipe. Originally described in
the late nineteenth century by Bocage (1893), the taxonomy and nomenclatural
history of T. ozorii have always been stable (see Ceríaco et al. 2016). Based on
mitochondrial sequence data, Jesus et al. (2005a) concluded that T. ozorii was not
closely related to any of the Gulf of Guinea oceanic island Trachylepis. This result
was confirmed by Ceríaco et al. (2016) and Weinell et al. (2019), the latter demonstrating that T. ozorii is sister to the Western African species Trachylepis polytropis
(Boulenger, 1903) and represents a distinct dispersal event to the archipelago. Jesus
et al. (2003) noted that the species was widespread across the island, but was not
usually found in wet or shaded areas.
The taxonomy of T. adamastor and T. thomensis is somewhat more muddled than
that of the Annobón congener. For a long time, both the Príncipe and São Tomé
populations were considered conspecific to the T. maculilabris (Gray, 1845) species
complex (see Ceríaco et al. 2016), a widespread species in West and Central Africa,
long known to harbor cryptic diversity (Mausfeld-Lafdhiya et al. 2004). Jesus et al.
(2005a) were the first to show, based on molecular data (three mitochondrial loci),
that the populations from Príncipe and São Tomé were not conspecific. As a first step
to clarify the taxonomy of the group, Ceríaco (2015) described T. adamastor from
Tinhosa Grand islet. The available specimens had been preserved in formalin, and
therefore, no molecular data were available for comparison with the other island
populations. Consequently, the species was described solely based on its striking
size and coloration differences relative to the other island’s specimens. Ceríaco et al.
(2016) later described two additional species based on a combination of morphological and genetic data: T. principensis from Príncipe and T. thomensis from São
Tomé. In a species-level phylogeny of the genus, Weinell et al. (2019) confirmed the
distinctiveness of the Príncipe and São Tomé populations and noted that the species
were not each other’s closest relatives—the Príncipe lineage (incorrectly labeled by
Weinell et al. (2019) as T. thomensis) is sister to T. maculilabris, while the São Tomé
population (incorrectly labeled by Weinell et al. (2019) as T. principensis) is sister to
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the Indian Ocean endemic Trachylepis comorensis (Peters, 1854), which occurs in
Comoros, Madagascar and coastal Mozambique. Both Ceríaco et al. (2016) and
Weinell et al. (2019) lacked molecular data for T. adamastor and were unable to
assess its taxonomic position in the context of a molecular phylogeny. Ceríaco et al.
(2020b) provided the first molecular data for T. adamastor, showing that it is
actually conspecific to T. principensis, rendering T. principensis as a junior synonym
of T. adamastor. Trachylepis thomensis is commonly found in forested areas and in
human settlements, showing an almost exclusively terrestrial lifestyle. By contrast,
T. adamastor is more abundant in less populated areas, ranging from forested
habitats to the open, rocky habitats of the Tinhosa Grande islet. Trachylepis
adamastor is commonly found basking on trees (Ceríaco et al. 2016). More recently
the population size and diet of the Tinhosa Grande population of T. adamastor was
reviewed by Sousa et al. (2022).
The presence of T. affinis, a complex of species occurring from Senegal to
Angola, on São Tomé and Príncipe has been interpreted differently by several
authors. In particular, Fischer (1886) described Euprepes cupreus from São Tomé,
and this taxon is currently considered a junior synonym of T. affinis (Ceríaco et al.
2016, 2018). To date, Fischer’s (1886) record remains the only available record of
this species on São Tomé. By contrast, several authors reported the species from
Príncipe under a variety of names—Mabuya raddoni (Angel 1920; Manaças 1958,
Hofer 2002), Mabuya blanlingii [sic] (Manaças 1958) and Mabuya/Trachylepis
affinis (Hallermann 1998; Jesus et al. 2005a; Ceríaco et al. 2016, 2018). These are
all currently synonyms of T. affinis, according to Ceríaco et al. (2016), based on the
molecular similarity between Principe and other continental populations. The species likely represents a recent arrival to the island, and further data are needed to
assess if a São Tomé population is extant. In Príncipe, the species is mostly found in
the vicinity of human settlements, especially around Santo António city.
Family Typhlopidae
Considering the diminutive size and isolation of the Gulf of Guinea oceanic islands,
the diversity of typhlopid snakes is remarkable. At least four species from three
different genera—Afrotyphlops Broadley and Wallach, 2009, Letheobia Cope, 1868,
and Indotyphlops Hedges, Marion, Lipp, Marin and Vidal, 2014—occur on the
islands. The genus Afrotyphlops is represented by the Príncipe endemic Afrotyphlops
elegans (Peters, 1868), locally known as “Cobra-bobô” (Fig. 19.2, 5), which is the
same name used on São Tomé to refer to the endemic caecilians of the genus
Schistometopum Parker, 1941 (Bell et al. 2022). Not much is known about the
ecology of this fossorial species, however, in multi-locus and morphological phylogenetic analyses of typhlopid snakes, Kornilios et al. (2013) and Hedges et al. (2014)
showed that it is closely related to the Central African Afrotyphlops angolensis
(Bocage, 1866).
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Two species of Letheobia are currently recognized and both occur on Príncipe
and São Tomé: Letheobia newtoni (Bocage, 1890) and Letheobia feae (Boulenger,
1906). Both species were originally described from São Tomé (Bocage 1890;
Boulenger 1906), and recent molecular data indicate the species are distinct and
form a monophyletic group with Letheobia simoni (Boettger, 1879) and L. episcopus
(Frazen and Wallach, 2002), from Israel and Turkey, respectively (Kornilios et al.
2013; Hedges et al. 2014). This intriguing biogeographic pattern may be an artifact
of our current poor knowledge of the taxonomic diversity and distribution of the
species of genus Letheobia. Two other forms were described from Príncipe:
Boulenger (1906) described Typhlops [¼Letheobia] principis and Angel (1920)
described Typhlops [¼Letheobia] naveli. Both of these species were later synonymized with L. feae and L. newtoni, respectively, by Roux-Estève (1974). No
molecular data exist for the Príncipe populations, and thus their taxonomic relationships with the São Tomé forms have not been fully ascertained. Given the patterns of
speciation in the archipelago and the morphological conservatism of these snakes,
the possibility that the Príncipe forms represent valid species should be investigated.
Due to their mostly fossorial lifestyles, almost nothing is known about the ecology
and distribution of either species.
Finally, Jesus et al. (2003) reported the presence of Indotyphlops
(as Ramphotyphlops) braminus (Daudin, 1802) on Annobón. These small, fossorial
snakes are an invasive species originally from Southern Asia and have been introduced to islands across the globe (Wallach 2009).
Family Lamprophiidae
Two species of lamprophid snakes occur in the Gulf of Guinea oceanic islands:
Boaedon bedriagae Boulenger, 1906, endemic to São Tomé, and B. mendesi,
endemic to Príncipe (Fig. 19.2, 6). The two taxa were considered conspecific by
most authors over the last century but were recently split into distinct species by
Ceríaco et al. (2021a). The species are sister taxa and are closely related to the
southern African B. capensis Duméril, Bibron & Duméril, 1854 species complex,
contrary to the historical assignment to either the Boaedon lineatus Duméril, Bibron
& Duméril, 1854 or Boaedon fuliginosus (Boie, 1827) species complexes from
Western and Central Africa (Ceríaco et al. 2021a). Locally known as “Jita,” these
species rank amongst the most well-known species on the islands, where the locals
recognize them as harmless. Both species are quite common and are often found in
both pristine habitats and agricultural areas (Ceríaco et al. 2021a). Both species can
be observed perched in trees or in vegetation and are often observed at reed frog
(Hyperolius spp.) breeding sites, suggesting anurans may be an important part of
their diet (RCB, LMPC pers. obs.).
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Family Colubridae
The colubrids of the Gulf of Guinea oceanic islands belong to two different genera:
the arboreal emerald snakes, genus Hapsidophrys Fischer, 1856, represented by the
Príncipe endemic Hapsidophrys principis (Boulenger, 1906), locally known as Suá-suá (Fig. 19.2, 7), and the arboreal green snakes of the genus Philothamnus (Smith,
1847), represented by the São Tomé endemic, Philothamnus thomensis Bocage,
1882, also locally known as Suá-suá, and the Annobón endemic Philothamnus
girardi Bocage, 1893.
The Príncipe Suá-suá, H. principis was described in the early twentieth century
by Boulenger (1906), although older records exist from the late nineteenth century,
as Gastropyxis (¼ Hapsidophrys) smaragdina (Bocage 1887, 1903). The species is
relatively poorly studied, but Jesus et al. (2009) provided a phylogeny based on two
mtDNA loci supporting H. principis as a distinct evolutionary lineage sister to
H. smaragdina from Gabon. Hapsidophrys principis is an arboreal species, mostly
found in forested areas (LMPC pers. obs.).
Regarding the two species of Philothamnus, recent molecular revisions by
Engelbrecht et al. (2019) provided some insights regarding their taxonomic validity
and placement within the genus. With a molecular dataset of three mtDNA and two
nuDNA loci, Engelbrecht et al. (2019) found that the island species form a strongly
supported clade with West-Central African congener P. dorsalis (Bocage, 1866).
Species delimitation analyses with this same dataset found moderate support for
P. thomensis as a distinct evolutionary lineage but no support for P. girardi as a
distinct lineage (Engelbrecht et al. 2019). Given the geographic isolation of
P. girardi on Annobón, morphological differences noted by Bocage (1893), and
the relatively modest molecular dataset and geographic sampling in Engelbrecht
et al. (2019), we conservatively maintain P. girardi as a valid species. Philothamnus
thomensis is considered a forest specialist but can also be found in shade-plantation
habitats and gardens (RCB, pers. obs.), while Jesus et al. (2003) noted that P. girardi
is widespread on Annobón, mainly in large open spaces with shrubs and grasses,
outside of the main village.
Family Elapidae
Only one species of elapid snake is confirmed for the Gulf of Guinea oceanic islands:
the São Tomé endemic Naja (Boulengerina) peroescobari Ceríaco, Marques,
Schmitz and Bauer, 2017, locally known as “Cobra-preta” (Fig. 19.2, 8). It is the
only venomous species of snake in the Gulf of Guinea oceanic islands, and human
fatalities can occur even if rare (Ceríaco et al. 2017). As a large and conspicuous
snake, it was one of the first reported species of reptiles for São Tomé. The species
was historically identified as Naja melanoleuca Matschie, 1893, a widely distributed
Central African species (Ceríaco et al. 2016). Until recently, it was assumed that
Portuguese settlers introduced Cobra-preta to control rodent pests that afflicted
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agricultural crops. However, historical, morphological and molecular evidence reject
this hypothesis (Ceríaco et al. 2017; Wüster et al. 2018) and instead indicate that the
Cobra-preta is distinct from N. melanoleuca and is endemic to São Tomé. The
Cobra-preta is classified as Endangered by the International Union for the Conservation of Nature (IUCN 2021), and is the only threatened terrestrial reptile from the
Gulf of Guinea oceanic islands. The Cobra-preta is mostly seen in forested and shady
habitats across the southern half of the island and is apparently absent in the
northeast regions. It is commonly seen basking on roads during the day (Ceríaco
et al. 2017). The invasive Least weasel, Mustela nivalis Linnaeus, 1766, and Black
rat, Rattus rattus Linnaeus, 1758, have been reported as prey items of the species
(Ceríaco et al. 2017).
There are unconfirmed records of a second species of elapid snake on São Tomé:
a green Mamba of the genus Dendroaspis. The evidence regarding the presence of
this snake on São Tomé was summarized in Ceríaco et al. (2018). Three experienced
herpetologists reported a species of mamba from the island: Dendroaspis jamesoni
by Jan (1857, 1858, 1859, 1863), Jan and Sordelli (1870) and Fischer (1856, 1885)
and Dendroaspis angusticeps by Bedriaga (1893a). Fischer (1856) even provided a
drawing of the specimen from “Insel St. Thomé (West-Africa)” (Fig. 19.3). Unfortunately, none of the specimens examined by the three different authors is still
extant. The specimen examined by Jan (1857, 1858, 1859, 1863) was destroyed
during the Allied bombing of Milan, Italy, during the World War II. Fischer’s (1885)
specimen likely suffered the same fate when the ZMH collections were damaged
during WWII. The specimens sent by Adolfo Möller to Bedriaga and used by the
latter to describe his specimen of Dendroaspis angusticeps (Bedriaga 1893a) are also
currently unaccounted for. Lacking the original specimens and without any recent
record of the species, there are significant doubts regarding these accounts, and
several authors have recognized this mystery (Schätti and Loumont 1992; Nill 1993;
Ceríaco et al. 2018). Either the historical records are simply cases of mistaken
identity and/or poor locality data, or there is an elusive species of green Mamba
on São Tomé that has evaded researchers for more than a century.
Conservation
Although no studies have yet been conducted to specifically assess the threats faced
by the reptiles of the Gulf of Guinea oceanic islands, it is likely that these are similar
to the threats faced by their continental African counterparts. Habitat degradation
and destruction caused by land-use change, climate change, non-native species, and
direct persecution (especially in the case of snakes) can have seriously detrimental
effects on local populations of reptiles. Given their abundance and mostly generalist
ecology, as well protected habitats in the Obô Natural Parks on São Tomé and
Príncipe, most species of reptiles from the Gulf of Guinea oceanic islands are not
currently considered threatened (IUCN 2021; Table 19.2). The endemic geckos
H. greeffii and H. principensis, however, are considered Near Threatened, and
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Fig. 19.3 Fischer’s (1856)
plate of “Dendroaspis
Jamesonii Schlegel” from
“Insel St. Thomé (WestAfrica)”
their apparently low abundance and the potential for competition with introduced
congeners H. mabouia and H. longicephalus may have negative impacts on their
populations. Many species, including Hemidactylus aporus, H. newtoni, Panaspis
annobonensis, Letheobia newtoni and L. feae are classified as Data Deficient due to
insufficient population and distribution data and lingering taxonomic uncertainty.
Currently, only Naja (Boulengerina) peroescobari is considered threatened, as
Endangered. This classification is due to its endemic status and threats associated
with both direct persecution and indirect death by car traffic. More detailed studies
are needed to uncover potential risks caused by land-use change, one of the main and
more prevalent threats to reptiles of the Gulf of Guinea oceanic islands, as well as
local strategies to mitigate persecution, especially in the case of the Cobra-preta.
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In recent years several reports on social media have depicted non-native species
occurring on São Tomé Island. For instance, a dead specimen of an adult Orton’s
Boa Constrictor (Boa constrictor ortonii Cope, 1877), a subspecies endemic to Peru,
South America, was found in the vicinity of São Tomé airport in August 2018. These
animals are not easily transported by accident, and its presence on the island is likely
due to intentional importation. Boas are listed by the Convention on International
Trade in Endangered Species of Wild Fauna and Flora (CITES), and thus importation to the country should be registered. Consulting the CITES Trade Database
(UNEP–WCMC and CITES 2021), there are no records of any live specimen of
reptile being legally imported to the country since 1975. Thus, illegal trade may be
operational in the country, which could constitute a major threat to the native
biodiversity. In March 2020, an adult female of agama, Agama sp. was found
basking on the walls of a building in downtown Santo António city, Príncipe. The
specimen was collected and euthanized and deposited at the facilities of Príncipe
Trust Foundation in Santo António (Frazer Sinclair, pers. comm.). The specimen
was collected at a construction site with raw materials imported from the African
mainland, suggesting this individual was a stowaway. To our knowledge, no other
specimens have been observed on the island. Some species of the genus Agama are
usually human commensals and have already been introduced to the Cape Verde
islands (Vasconcelos et al. 2014). Research is underway to identify the source
population of this sole agama female specimen.
Future Research
Despite over a century of research, the taxonomy and diversity of terrestrial reptiles
from the Gulf of Guinea oceanic islands are still incompletely documented. Taxonomic revisionary studies are sorely needed for some groups (as noted above), and
the presence of the São Tomé Green Mamba remains an intriguing mystery. In
addition, the biogeographic history of most lineages is poorly understood in part
because the taxonomy of continental species is still in flux. Other than some
anecdotal data presented in taxonomic reviews (e.g., Ceríaco et al. 2016, 2017),
there are few studies focused on the ecology, natural history, and conservation of
species. Furthermore, in contrast to the comprehensive assessments that have been
conducted for other groups, notably birds (Melo et al. 2022), no studies exist on the
impacts of invasive species or land use for terrestrial reptiles (Soares et al. 2022).
Another important topic that needs further attention is the venom composition,
medical significance and social impact of N. peroescobari snakebite. Finally,
Pacheco et al. (2020) report considerable Haemocystidium parasite diversity in
reptiles, and although this study did not include samples from any Gulf of Guinea
oceanic islands taxa, the topic presents an exciting opportunity to investigate
parasite-host interactions in an insular community.
528
L. M. P. Ceríaco et al.
Acknowledgments We thank Eng. Arlindo de Ceita Carvalho and Eng. Lourenço Monteiro de
Jesus, respectively former and current Directors General of the Ministry of Environment, Daniel
Pontes, Director of the Príncipe Obô Natural Park, and the former President of Príncipe Autonomous Region, Dr. José Cassandra, for permission to collect and export specimens for study. An
important acknowledgment to the Portuguese School of São Tomé, namely to its director Manuela
Costeira and professors Carlos Gomes, António Almeida, Pedro Lorena and Sandra Ferreira, for
their support in the study of the crocodile carcass. We were assisted in the field by Ostelino da
Conceição Rocha, Pedro Ceríaco, Ana Carolina Sousa, Pedro Dias, Robert C. Drewes, Lauren
Esposito, Maria Jerónimo, Lauren Scheinberg, Felipe Spina, and Andrew Stanbridge. We also
thank Rachel Crosby, former director of Príncipe Trust for support during our field trips to Tinhosa
Grande Islet. We are grateful to the curators and collection managers Giuliano Doria, Andreas
Schmitz, Frank Tillack, Jakob Hallermann, and Lauren Scheinberg of the Museo Civico di Storia
Naturale “Giacomo Doria” (Genoa, Italy), the Musée d’Histoire Naturelle de la Ville de Genéve
(Geneva, Switzerland), the Museum für Naturkunde (Berlin, Germany) and Zoologisches Museum
(Hamburg, Germany), and the California Academy of Sciences (San Francisco, USA), respectively,
for allowing access and providing information about the collections in their care. We thank Maria
Branco for use of her photos of and Crocodylus niloticus. During the course of this work, Mariana
P. Marques was funded by Fundação para a Ciência e Tecnologia (SFRH/BD/129924/2017) and is
now funded by NORTE-01-0246-FEDER-000063, supported by Norte Portugal Regional Operational Programme (NORTE2020), under the PORTUGAL 2020 Partnership Agreement, through
the European Regional Development Fund (ERDF). Jean-François Trape and Andreas Schmitz are
thanked for their comments and insights on previous versions of this manuscript.
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Chapter 20
The Sea Turtles of São Tomé and Príncipe:
Diversity, Distribution, and Conservation
Status
Betania Ferreira-Airaud, Vanessa Schmitt, Sara Vieira,
Manuel Jorge de Carvalho do Rio, Elisio Neto, and Jaconias Pereira
Abstract The unique islands of São Tomé and Príncipe harbor five of the seven
existent sea turtle species, and offer optimal conditions for these threatened species
both on the beaches and on the foraging sites at sea. These populations might have
been exploited since the sixteenth century and are still being harvested. In the past
decade, our knowledge of these populations has greatly improved, highlighting their
regional and global importance. Several conservation initiatives have also prioritized
their protection. This chapter reviews our knowledge on the diversity, distribution,
and conservation status of sea turtles in São Tomé and Príncipe, providing a brief
history of conservation actions from the past 20 years and presenting ongoing
research and conservation initiatives.
Keywords Caretta caretta · Chelonia mydas · Conservation · Dermochelys
coriacea · Eretmochelys imbricata · Lepidochelys olivacea
Introduction
Sea turtles have been traveling the oceans for millions of years and with an incredible
resilience have survived to the present day. This is probably why they are much
appreciated and arouse so much interest in the general public and scientists, alike.
Turtles belong to the most ancient line of living reptiles, first appearing more than
B. Ferreira-Airaud (*)
Associação Programa Tatô, Barão de São João, Portugal
e-mail: betaniaferreira@programatato.pt
V. Schmitt · J. Pereira
Fundação Príncipe, Santo António, Sao Tome and Principe
S. Vieira
Associação Programa Tatô, São Tomé, Sao Tome and Principe
M. J. d. C. d. Rio · E. Neto
ONG MARAPA, São Tomé, Sao Tome and Principe
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_20
535
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200 million years ago, in the late Triassic. But it was probably around some
110 million years ago, in the Jurassic, during the reign of dinosaurs, that turtles
entered the sea and shared the ocean with several other air-breathing reptiles, such as
ichthyosaurus and plesiosaurus. While the end of the Cretaceous was the scene of the
mass extinction of large reptiles that dominated the earth, sea turtle lineages persisted
until the present day (Lutz and Musick 1997; Motani 2009).
These large marine reptiles are well adapted to life in the ocean, performing vast
migrations between foraging and nesting areas that can be thousands of kilometers
apart, and inhabiting a variety of neritic and pelagic habitats of tropical and subtropical waters globally (Carr 1982). The oceanic islands of the Gulf of Guinea,
particularly São Tomé and Príncipe, harbor important breeding and foraging grounds
for sea turtles. Sea turtle nesting grounds on Annobón, the smallest island in the Gulf
of Guinea, are limited with only a few suitable beaches available, although important
foraging grounds might exist (Castroviejo et al. 1994; Fretey 2001).
It was only in the 1990s that the presence of five sea turtle species in São Tomé
and Príncipe was confirmed (Fig. 20.1): the Green Turtle Chelonia mydas (Linnaeus,
1758), the Olive Ridley Turtle Lepidochelys olivacea (Eschscholtz, 1829), the
Hawksbill Turtle Eretmochelys imbricata (Linnaeus, 1766), the Leatherback Turtle
Dermochelys coriacea (Vandelli, 1761), and the Loggerhead Turtle Caretta caretta
(Linnaeus, 1758). Research in the past decade has greatly improved our knowledge
of these populations, highlighting their regional and global importance. Simultaneously, there have also been significant efforts towards their protection. Since data
regarding sea turtles in Annobón is scarce and that there are no conservation
initiatives targeting these species on that island, this chapter will focus on Príncipe
and São Tomé.
History of Sea Turtle Conservation in São Tomé and Príncipe
The first references to sea turtles in São Tomé and Príncipe date back to 1883. At this
time, sea turtles were described as being common and were exploited by local
communities, with carapaces used in the manufacture of jewelry and other ornamental items (Greeff 1884; Bocage 1903). The first sea turtle surveys of the Atlantic
coast of Africa started as early as 1957 (Carr 2002), but it was only between 1985
and 1994 that the first attempts were made to describe the status of sea turtles in São
Tomé and Príncipe (Stuart and Adams 1990; Schneider 1992; Atkinson et al. 1994;
Castroviejo et al. 1994; Graff 1996).
Between 1994 and 1996, a more comprehensive survey was initiated on São
Tomé Island thanks to a collaboration between ECOFAC (European Commission
Program for the Conservation and Sustainable Use of Forest Ecosystems in Central
Africa) and the U. S. Peace Corps. This survey confirmed the sea turtle species
occurring in São Tomé and Príncipe, identified the main nesting beaches, assessed
the impact of harvesting by the local communities (Graff 1996) and resulted in the
baseline information being used to implement a monitoring and protection program
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537
Fig. 20.1 Sea turtles of the Gulf of Guinea islands: (1) Female Green Turtle Chelonia mydas; (2)
Green Turtle hatchlings; (3) Female Leatherback Turtle Dermochelys coriacea; (4) Leatherback
Turtle hatchlings; (5) Female Olive Ridley Turtle Lepidochelys olivacea; (6) Juvenile Hawksbill
Turtle Eretmochelys imbricata; (7) Male Loggerhead Turtle Caretta caretta; (8) Mating Green
Turtles. Photo credits: (1) Maria Branco | Programa Tatô, (2, 4, 7) Ana Besugo, (3) Ivana Tacikova,
(5) Joana Meneses, (6) Victor Jimenez | Programa Tatô, (8) Lara Baptista | Fundação Príncipe
538
B. Ferreira-Airaud et al.
on the main nesting beaches (Graff 1996; Rosseel 1997). This project gave rise to
Programa Tatô (Tatô refers to the Olive Ridley Turtle in the local language) in 1998.
Led by ECOFAC until 2001, it included the monitoring of the main nesting beaches,
training of local community members as beach rangers and the construction of
hatcheries (Dontaine and Neves 1999; Fretey and Dontaine 2001; Formia et al.
2003). In 2002, MARAPA (Mar, Ambiente e Pesca Artesanal), a national NGO
created in 1999, took responsibility for Programa Tatô’s conservation activities. This
program survived until 2008 under the jurisdiction of the Central Africa Protected
Areas Network (RAPAC) in partnership with the regional network PROTOMAC
(Protection Tortues Marines Afrique Centrale), when it suddenly collapsed. Since
then, several groups have kept sea turtle conservation efforts going on both islands.
In Príncipe, the Center for the Biodiversity Conservation of Príncipe Island
(CBioP), an international research center under the responsibility of the University
of Algarve’s CCMar—Ocean Sciences Center in Portugal and the Regional Government of Príncipe, started Programa Sada (Sada refers to the Hawksbill Turtle in
the local language) in 2009. The program aims to ensure sea turtle protection and
conservation actions in partnership with the regional government and local communities of Príncipe, and focuses on the populations of the Critically Endangered
Hawksbill Turtle. In 2010, the Government of the Autonomous Region of Príncipe
approved the creation of the Sea Turtle Commission (Comissão Tartaruga Marinha)
by the Natural Park of Príncipe, with the main goal of promoting and reinforcing sea
turtle protection and their sustainable use on Príncipe.
In 2012, the Natural Park of Príncipe joined efforts with Here Be Dragons
Príncipe (HBD, a tourism investment company established in 2010 for the sustainable development of Príncipe Island) and the Association for the Research, Protection, and Conservation of Sea Turtles in Lusophone Countries (ATM, a Portuguese
NGO) to develop a comprehensive sea turtle monitoring and protection program on
Príncipe Island. After two extremely successful seasons in Príncipe, ATM in 2014
combined efforts with the NGO MARAPA on São Tomé and their partnership
reinitiated Programa Tatô. This resulted in the growth of Programa Tatô’s team. In
2018, Programa Tatô was no longer just a MARAPA project. The coordination team,
with the support and encouragement of its technical and financial partners, decided
to give more autonomy and sustainability to this program and created an International NGO, Association Programa Tatô—the original name, which was well known
to all local communities, national authorities, civil society as well as international
partners, was preserved.
Meanwhile, on Príncipe, with the transition of ATM to São Tomé Island in 2014,
Protetuga Project was created and managed by Fundação Príncipe (FP), a national
NGO, established to support environmental and social actions by the HBD group
with funding from the South African private-investor and businessman Mark
Shuttleworth. At the end of 2016, due to budget cuts from the main donor, FP
started to work with its regional, national, and international partners to become
independent. Today, FP is independent and has a strategic plan focused on the
conservation of biodiversity and the social and economic development of the
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539
communities on the island, with more than 15 different donors and projects directed
at marine and terrestrial conservation.
Regarding Annobón, although classified as a Nature Reserve since 2000, there is
no information or knowledge of any sea turtle conservation efforts on the island.
Species and Status
The modern marine turtles are placed in two families and are the only living
members of what had been a large and diverse fauna: the family Dermochelyidae,
which consists of a single species, the Leatherback Turtle, and the family
Cheloniidae, which comprises six species of hard-shelled sea turtles: the Loggerhead
Turtle, the Green Turtle, the Hawksbill Turtle, the Olive Ridley Turtle, the Kemp’s
Ridley Turtle Lepidochelys kempii Garman 1880, and the Flatback Turtle Natator
depressus (Garman, 1880).
Five of the seven modern species are found in São Tomé and Príncipe, all of
which are listed as threatened (IUCN 2021): the Olive Ridley, the Leatherback and
the Loggerhead Turtles as Vulnerable, the Green Turtle as Endangered), and the
Hawksbill Turtle as Critically Endangered. All of these five species nest on the
beaches of the islands, except for the Loggerhead, which is occasionally found at sea
(unpublished data). The Green Turtle is the most common sea turtle in the archipelago, nesting on virtually all sandy beaches of both islands (unpublished data). This
nesting population exhibits relatively high levels of genetic diversity and distinctiveness, representing an important genetic pool in the region (Hancock 2019). The
Olive Ridley Turtle is the second most numerous species on São Tomé, while only
sporadic nesting occurs on Príncipe (unpublished data). These islands harbor one of
the last remaining Hawksbill Turtle nesting aggregations in the region, which have a
unique genetic haplotype and low genetic variability (Monzón-Argüello et al. 2011)
and are one of the 11 most threatened sea turtle populations in the world (Wallace
et al. 2011), emphasizing the high degree of isolation and vulnerability of this
population. The Leatherback Turtle is the least abundant nesting species in the
archipelago (unpublished data).
Distribution and Habitat
São Tomé and Príncipe are unique islands with clear warm oceanic waters
surrounded by shallow rocky reefs sparsely colonized by hard and soft corals, vast
beds of rhodoliths, and great diversity of macroalgae and seagrass meadows, which
are more common in São Tomé. Coastlines change from an extensive shallow shelf
and low wave exposure in the northern coasts to short and deeper shores more
exposed to waves in the southern coasts of both islands. Freshwater enters the sea
from small streams and rivers, forming small estuarine habitats in a few areas with
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mangroves bordering some of the river mouths (Bollen 2017; Cowburn 2018;
Airaud et al. 2020; Ferreira-Airaud et al. 2021).
São Tomé has a diversity of beaches ranging from golden yellow sand to dark
gray sandy or rocky stretches and varying between 0.17 and 2.11 km in length.
Coastal vegetation is shaped by a wide range of precipitation and relatively homogeneous temperature (daily average of 27 C): coastal meadows and a savanna-type
ecosystem can be found on the northern coast, where rainfall is less than 700 mm a
year, while in the south yearly rainfalls over 7000 mm feed luscious rainforests
(Ceríaco et al. 2022; Dauby et al. 2022). Mangroves can be found on sheltered coasts
along this gradient. Príncipe displays a luxurious green wilderness with a magnificent topography of volcanic landscapes. The forest is omnipresent and, in most
places, falls directly into the ocean from high cliffs with several narrow beaches up
to 1.4 km in length ranging from white, golden to black sand or rocky stretches.
This exceptional environment offers optimal conditions for colonization by sea
turtles, both on the nesting beaches and on foraging sites at sea.
Nesting Beaches
Sea turtle nesting occurs on almost all the sandy beaches of both islands that offer
suitable conditions for nesting, even though distribution and density vary between
species. The nesting season on both islands coincides with the rainy season, which
runs from October to May, providing suitable conditions for nesting and incubation.
In São Tomé, nesting occurs on the northern, eastern, and southern coasts
(Fig. 20.2). The northern and eastern coastal areas host large human settlements,
whereas the southern (particularly southwestern) beaches are relatively remote. The
lack, or very low prevalence, of nesting on the western coast of São Tomé is likely
due to the rocky beaches characterizing this stretch of coast.
In Príncipe, nesting occurs mainly on the northern and southeastern beaches
(Fig. 20.3). Most of the southern beaches are particularly remote with almost no
human settlements.
In Annobón, nesting is limited due to the availability of only a few suitable
beaches (Castroviejo et al. 1994), this oceanic island.
Green Turtle The Green Turtle is the most common species in the archipelago. Its
nesting has been confirmed on virtually all sandy beaches of both islands, ranging
from 49 to 1177 nests per year on São Tomé and from 287 to 2050 nests per year on
Príncipe (from data collected by our team between 2014 and 2020). Data collected
since 2014 confirm what was observed during the initial surveys in the 1990s,
namely that Green turtles on São Tomé nest mainly in the south, with Praia Jalé
being the preferred beach (70% of the total nesting by the species), followed by Praia
Grande, both in the region of Porto Alegre, in the Caué district (Fig. 20.2a). This area
is characterized by high rainfall, dense tree cover, beaches with steeper slopes and
high wave exposure. On Príncipe, green turtles nest mainly in Praia Grande do Norte
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Fig. 20.2 Distribution of the average number of nests per species in São Tomé, from 2017 to 2020:
(a) Green Turtle Chelonia mydas; (b) Olive Ridley Turtle Lepidochelys olivacea; (c) Hawksbill
Turtle Eretmochelys imbricata; and (d) Leatherback Turtle Dermochelys coriacea
Fig. 20.3 Distribution of the average number of nests per species in Príncipe, from 2017 to 2020:
(a) Green Turtle Chelonia mydas; (b) Hawksbill Turtle Eretmochelys imbricata; and (c) Leatherback Turtle Dermochelys coriacea
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B. Ferreira-Airaud et al.
in the northern part of the island and in Praia Infante in the south (Fig. 20.3a). Green
turtle nesting occurs year-round (except June), with a nesting peak in December and
January.
Olive Ridley Turtle Major nesting grounds of Olive Ridley Turtles in West Africa
are in Angola and Gabon (Metcalfe et al. 2015; Morais and Tiwari 2022). Nevertheless, this is the second most numerous species on São Tomé, ranging from 326 to
683 nests per year between 2014 and 2020 (unpublished data). On Príncipe only two
nesting observations were recorded on Praia Macaco in 2012, and on Praia Grande
do Norte in 2018. This species nests year-round (except June), with a nesting peak in
November and December. Olive Ridley Turtles seem to prefer the northern area of
São Tomé from Praia Juventude to Praia das Conchas, adjacent to the fishing
communities of Micoló, Fernão Dias, and Morro Peixe, where 90% of the nesting
occurs (Fig. 20.2b). This area is characterized by lower rainfall, gentle sloping
beaches, an extensive shallow shelf and low wave exposure shores. The northern
part of São Tomé is also notable for the presence of seagrass meadows, an ecologically valuable marine habitat and feeding grounds for the Green Turtle.
Hawksbill Turtle The Hawksbill Turtle is the most threatened turtle species on São
Tomé and Príncipe and, nowadays, its distribution is less extensive due to the
indiscriminate harvesting for its meat and shell (Fretey et al. 2000). Nevertheless,
the number of nests appears to be increasing slightly, ranging from 13 to 246 nests
per year on São Tomé and from 43 to 118 nests per year on Príncipe (unpublished
data collected between 2014 and 2020). Most of its nesting (60%) on São Tomé
occurs on Rolas Islet, south of São Tomé, highlighting the importance of this islet as
a priority site for the conservation of this Critically Endangered species (Fig. 20.2c).
On Príncipe, the preferred beaches are Praia Infante in the south and Praia Grande do
Norte in the north (Fig. 20.3b). Hawksbill nesting occurs from August to April with a
nesting peak in December and January. Like Green Turtles, Hawksbill Turtles seem
to prefer beaches characterized by dense tree cover, steeper slopes, high wave
exposure and high rainfall.
Leatherback Turtle One of the major nesting grounds for Leatherback Turtles is in
Gabon, approximately 300 km from São Tomé and Príncipe, with as many as
36,185–126,480 nests, and 5865–20,499 breeding females per year (Witt et al.
2009). In São Tomé and Príncipe, it is the least abundant nesting species with
15–155 nests per year in São Tomé and 3–44 nests per year in Príncipe, (unpublished
data collected between 2014 and 2020). Nesting occurs from September to March
with a nesting peak in December. Although this species has a more heterogeneous
distribution, there is a certain preference for the southeastern beaches on São Tomé
(Fig. 20.2d) and the northern and eastern beaches on Príncipe (Fig. 20.3c).
Loggerhead Turtle Extensive surveys in the eastern Atlantic suggest that the only
significant nesting aggregation is in Cabo Verde (Fretey 2001; Ehrhart et al. 2003;
Marco et al. 2012). Historically, in São Tomé and Príncipe there have been only a
couple of observations of Loggerhead Turtle nesting on São Tomé, but there is no
evidence that this species has ever nested frequently on the islands (Fretey 2001).
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Since 2014, only one nesting event (82 cm CCL—curved carapace length) has been
registered on São Tomé, in January 2017 at Praia Inhame in the south of the island
(Porto Alegre region; our data). In addition to these isolated events, Loggerhead
Turtles are occasionally observed at sea (our data).
Foraging Grounds
After hatchlings emerge from the nest and make it safely to the sea, they swim in a
frenzy to reach the open ocean. The “lost years” characterize this lesser-known
period when young sea turtles stay away from coastal areas until they become
juveniles. Foraging habitats vary among species (Musick and Limpus 1997). All
species occurring in São Tomé and Príncipe are found foraging year-round in coastal
waters.
Green Turtle Local fishermen have indicated several foraging or aggregation sites
of Green Turtles around both Príncipe and São Tomé, which have been confirmed
through in-water surveys developed by the sea turtle conservation programs (our
data). Both islands host two distinct immature groups of foraging green turtles: small
immature, likely to have recruited recently from the oceanic to the neritic zone, and
larger immatures that explore the local resources for extended periods.
On São Tomé, Green Turtle immatures hand-captured at sea since 2014 during
Programa Tatô in-water surveys ranged from 34 to 45 cm CCL (Curve Carapace
Length; Hancock et al. 2018), which is consistent with historical records from the
1990s of small immatures ranging from 33 to 45 cm CCL (Fretey and Dontaine
2001). This is within the expected size range at recruitment for post-pelagic turtles of
this species (Musick and Limpus 1997) but slightly smaller than other locations in
the Atlantic (Reisser et al. 2013) and Pacific (Arthur et al. 2008).
Small immature Green Turtles are more commonly found in a foraging ground
identified in the south of São Tomé; it is possible that the rocky substrate of southern
São Tomé is well suited for omnivores because it is rich in macroalgae and benthic
invertebrates and provides more resting or hiding sites for the smallest individuals
than the exposed seagrass beds located in the north foraging ground. Large immatures range from 45 to 75 cm CCL, since the minimum size observed in nesting
females on São Tomé ranges between 72 and 75 cm CCL. These large immatures are
more often found feeding upon green algae and seagrasses in the northern foraging
ground, where there are large seagrass meadows.
On Príncipe, the recruitment size for small immatures is lower than on São Tomé,
with the smallest individual observed having 28 cm CCL; large immatures on
Príncipe have a maximum CCL over 70 cm. Individuals are observed, mainly in
rocky reefs covered with macroalgae all around Príncipe, but to date the main green
turtle foraging grounds on Príncipe have not been identified. Analysis of stomach
contents of stranded immature green turtles revealed that these animals feed on
several algae species present on rocky reefs around the island. Transmitters with
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cameras placed on adult females nesting in Praia Grande do Norte, north of Príncipe,
in 2018, confirmed that these females feed on algae during the inter-nesting period in
the bays near the nesting beach.
These foraging sites clearly indicate that these islands are important recruitment
and development habitats for immature Green Turtles in the region, and that after
reaching maturity, adults move to other foraging sites in the region. Ongoing satellite
telemetry studies will refine our understanding of adult foraging grounds and
migration routes.
Olive Ridley Turtle Globally, Olive Ridley Turtles may use a wide range of
foraging habitats, primarily neritic in relatively shallow benthic waters or sometimes
in major estuaries as recorded in Australia (Whiting et al. 2007), Oman (Rees et al.
2012), French Guiana (Plot et al. 2015), and Brazil (Santos et al. 2019). They are also
known to feed in oceanic deep waters, as seen in Costa Rica (Plotkin 2010), India
(Ram et al. 2009), Gabon and Angola (Maxwell et al. 2011).
The foraging behavior of Olive Ridley Turtles in São Tomé and Príncipe is
largely unknown, with only a few observations in the past few years during
in-water surveys. However, recent incidental fishery bycatch records, beach
strandings, and fishermen testimonials revealed that the coastal waters of both
islands may host important foraging areas for both adults and immatures throughout
the year. Small immatures were observed on a few occasions at both islands. The
smallest were registered in 2014 on São Tomé with a CCL of 20 cm, and in 2015 on
Príncipe with a CCL of 18.8 cm; others individuals within the same size range have
been observed since then. According to a local fisherman, they can be seen feeding
on eggs of flying fish (Exocoetus spp.) that breed on the southwest coast of São
Tomé from June to August.
Hawksbill Turtle As with Green Turtles, shallow waters of both islands host yearround Hawksbill Turtle foraging aggregations of small and large immatures, and of
mature males and females in rocky reef and coralline algae (rhodolith) habitats. On
São Tomé, the main foraging grounds are in the south, at Rolas Islet, and on the
northwest coast, adjacent to Neves and Santa Catarina. On Príncipe, most of the
rocky reefs are used by the species, where it can find a variety of suitable food items,
such as rhodoliths and macroalgae, hard and soft corals and other invertebrates.
While immature Hawksbill Turtles found in shallow waters are assumed to be
residents for certain periods, ongoing satellite telemetry studies on nesting females
have revealed that most of the adults migate from nesting to foraging grounds,
adults may.
On São Tomé, the smallest Hawksbill Turtle hand-captured at sea was 30 cm
CCL, while the minimum size observed for nesting females was 55 cm CCL on São
Tomé.
On Príncipe, the smallest immature had 26.5 cm CCL (Ferreira et al. 2018).
Leatherback Turtle Leatherbacks are the most pelagic sea turtle species, spending
much of their life in the open sea, but foraging over continental shelves where
environmental conditions favor the presence of gelatinous zooplankton, their favorite prey (Dodge et al. 2014).
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In São Tomé and Príncipe there are no recent records of Leatherbacks foraging in
the coastal waters, besides sightings and bycatch by local fishermen during the
nesting season. Older records mention three immatures in Príncipe, ranging from
17 to 21 cm CCL, and a of 14 cm CCL one on São Tomé (Fretey et al. 1999).
However, since there are no recent records of small immatures, these are thought to
be occasional, even though there has been no concerted effort to record immatures of
this species.
Loggerhead Turtle In São Tomé and Príncipe, sporadic observations at sea of
adult loggerheads have been recorded over the years during in-water surveys
(Ferreira et al. 2015), from local fishermen and in incidental fishery bycatch reports.
The most recent record was in 2020, when one was captured with two adult Olive
Ridley Turtles, in a bottom gill net around the coast of Príncipe.
Main Threats for the Survival of Sea Turtles
Sea turtles were once very abundant, but today all seven sea turtle species are
threatened at a global scale (IUCN 2021). Unquestionably, human interference
throughout the past centuries is the cause of their decline (Lutcavage et al. 1997).
Today most of the threats affecting sea turtles in the oceanic islands of the Gulf of
Guinea are not exclusive to this part of the world, although cumulative impacts make
their conservation particularly challenging.
Historical records reveal that sea turtles were once abundant in São Tomé and
Príncipe (Matos 1916) and might have been heavily exploited for their meat and
shells since the sixteenth century, when São Tomé and Príncipe were first inhabited
(Greeff 1884; Parsons 1962; Parsons 1972). The Portuguese transported hundreds of
sea turtles on caravels to feed their crews (Fretey et al. 2000; Loureiro and Torrão
2008) and carapaces and scales were delivered to royal and noble families that
collected tortoiseshell jewelry and art objects (Orey 1995). Parsons (1962) indicated
that a tortoiseshell industry existed on the islands and supported a domestic trade.
Later on, there was also a trading network with Angola, where tortoiseshell products
were made into souvenirs (Brongersma 1982; Stuart and Adams 1990; Carr and Carr
1991). The Convention on International Trade in Endangered Species (CITES) came
into effect in 1975, to protect plant and animal species from unsustainable levels of
international commercial trade, but it was only ratified by São Tomé and Príncipe in
2001 (de Lima et al. 2022). Angola ratified CITES only in 2013, and local artisans of
São Tomé and Príncipe report that the occasional clandestine trading of turtle shells
still persists.
In the 1990s, 43 artisans working with turtle scutes, known as “tartarugueiros,”
were identified (35 in São Tomé and 8 in Príncipe), and an inventory of the scutes
and manufactured objects that they possessed weighed 225 kg and 45 kg, respectively, for an estimated value of around 30,000 Euros (Fretey et al. 2000). In 2002/
2003, with funds from European Union, all stocks of scutes and manufactured
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objects were bought from the artisans and donated to the National Museum of São
Tomé and Príncipe, and recently destroyed. Until this period, the use of the Hawksbill Turtle shell for the manufacture of handicrafts and jewelry was the greatest
driver of the indiscriminate harvest and decline of this species. Today it is still
common to find turtle jewelry being sold in some shops in São Tomé, mostly to
uninformed tourists.
In the 1990s, almost every sea turtle found at the beach or sea was killed for its
meat or shell (Fretey 1998), and despite many conservation efforts over the past few
decades, turtles are still killed for their meat and eggs in São Tomé and Príncipe. At
sea, adult sea turtles were indiscriminately captured using hooks, harpoons, and
gillnets set in front of the main nesting beaches (Castroviejo et al. 1994). Fresh or
salted turtle meat was until very recently part of certain traditional menus in São
Tomé and Príncipe, and the shell was very often used in the preparation of these
dishes as well as for traditional medicinal or as an aphrodisiac (Fretey 1998).
However, the use of these animals in traditional ceremonies is not as common as
in other West African countries (Barbosa and Regalla 2016). Up until 2016, it was
still possible to buy sea turtle meat in the local markets. The most expensive was
Green Turtle meat, which sold for 50–100 dobras (2–4 euros) for approximately
300 g, while the least expensive was the Olive Ridley, which sold for around
300 dobras (12 euros) per turtle. Although these practices have decreased drastically
in both islands, they still represent a threat to sea turtles in some communities.
Finally, a variety of domestic animals and natural predators, including crabs, rats,
dogs, and pigs, also depredate sea turtle eggs and hatchlings. Approximately 60% of
the sea turtle nests in São Tomé must be transferred to protected hatcheries to prevent
nest predation.
In addition to direct exploitation, sea turtles are affected by several indirect threats
in São Tomé and Príncipe. Commercial fisheries (many from east Asian countries)
operating in the Gulf of Guinea are thought to incidentally capture many sea turtles,
mainly Olive Ridley and Leatherback Turtles (Huang 2015). Small-scale fishing
activity in both São Tomé and Príncipe represents a major source of income for
coastal communities who have few economic resources and opportunities, and the
unintentional take in a major threat to sea turtles, particularly longline (vertical and
horizontal), demersal gillnet, surface driftnet and purse seine (pers. obs.). However,
little is known about the impacts of these artisanal fisheries on sea turtles and other
marine resources in São Tomé and Príncipe. The Gulf of Guinea is also the focus of
extensive and rapidly increasing oil exploitation activities. Vast oil reserves have
been discovered in the last decade, in areas that host important sea turtle habitats.
Drilling activities by large international oil corporations, associated with pollution
and habitat destruction, are threats that have been increasing and are expected to
continue increasing in the region, soon expanding to São Tomé and Príncipe
(de Lima et al. 2022).
With a human population estimated to have just surpassed the 200,000 mark, and
to be growing at 1.5% each year (Central Intelligence Agency 2021), construction
around São Tomé is increasing fast, namely for the tourism sector. The increase in
tourism will bring, along with its benefits, some environmental challenges, such as
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547
the increase in disturbance of nesting beaches, the need of sand for construction, and
the increase in artificial lights by the coast. Despite a national ban of sand mining
activities on beaches since 1999 (Decreto-Lei n 35/99) and recently updated (Law
n. 9/2020, from 22 of September), sand continues to be extracted, namely from sea
turtle nesting beaches, where the effects of sand removal is accelerating erosion,
causing the disappearance of several nesting beaches, and exacerbating the consequences of sea level rise due to climate change.
Around urban areas on both islands, most sewage is discharged untreated into the
sea. The most extreme national example may be seen in São Tomé city, where the
Água Grande river regularly pumps a combination of untreated sewage and petrochemical waste (from the city’s electric generators) directly into the sea at Ana
Chaves Bay. In Príncipe, dead stranded turtles found on the beach have been
analyzed by Fundação Príncipe to understand whether there is a relationship with
the increased presence of waste in the sea and these events. Preliminary analyses
show that young and adult turtles (mostly Green Turtles) feed on various solid
residues, mostly plastic. In addition to the increasingly presence of this type of
waste in the intestinal tract of these animals, it is common to see immature Green
Turtles with fibropapillomatosis, a disease that results in the production of tumors,
both external and internal, which are benign but may obstruct crucial functions, such
as swimming, feeding, sight, and buoyancy, and may lead to death (Herbst 1994). A
strong link between this disease and the environmental health of the coastal habitats
is already known (Santos et al. 2010; Santos et al. 2011). The first records of this
disease in turtles in Príncipe date from 2009 (Loureiro and Matos 2009). Turtles are
also particularly vulnerable to a variety of environmental conditions, such as higher
water temperature, pollutants, and marine biotoxins, all of which can weaken their
immune functions, making them more susceptible to a wide range of pathogens. Sea
turtles are often considered sentinels of ecosystem health and in fact, it has been
suggested that fibropapillomatosis could serve as an effective tool to monitor
ecosystem health in near-shore marine habitats (Aguirre and Lutz 2004).
Conservation
Since the initiation of conservation activities in the country in 1998, one of the first
strategies was to work with the government to implement a National Law to protect
these threatened species in São Tomé and Príncipe. In 2001, the first draft of the
decree was proposed to the national government, but it was only in 2014 that the
national law protecting sea turtles and criminalizing the consumptive use of sea
turtles and their by-products was adopted in São Tomé and Príncipe (Decreto-Lei n
8/2014). Remarkably, 5 years before the national law was officialized, the regional
government of Príncipe, which has administrative autonomy, implemented a law to
protect sea turtles on the island (Decreto-Lei n 03/2009), which may have encouraged the national government to take action. However, as in many developing
nations around the world, enforcement of environmental laws is still challenging,
548
B. Ferreira-Airaud et al.
since relevant institutions often lack the technical capability and means to effectively
implement the legislation. Since the adoption of the sea turtle national law in 2014,
there have been virtually no penalties or sanctions against sea turtle hunters or
traders in São Tomé. As for Príncipe, only two cases were penalized with the
payment of a fine and some other cases were included in the social assistance
program. In this social assistance program, violators of the sea turtle protection
law are required to perform social services for the regional government and for the
Fundação Príncipe sea turtle conservation program, including a mandatory participation in awareness-raising activities in their own community. This initiative has
been an opportunity to involve and promote a change in the mentality of those who
violate the law protecting sea turtles.
Before the creation of these domestic laws, São Tomé and Príncipe ratified
several international conventions that support in-situ conservation actions (de Lima
et al. 2022). The Convention on Biological Diversity (CBD) was ratified in 1999,
followed by the Convention on the Conservation of Migratory Species of Wild
Animals and CITES in 2001, and by the Abidjan Convention (United Nations
Environment Program) in 2002. Although these laws were approved and several
conventions were ratified, legal protection of sea turtles does not automatically
translate into realistic changes felt on a daily basis. In fact, one of the biggest
challenges to sea turtle conservation in developing countries, such as São Tomé
and Príncipe, is changing the habits of coastal communities for whom sea turtles are
an important source of subsistence and income and are essential for survival. So, as
with many other conservation programs worldwide (e.g., Marcovaldi et al. 2005), a
consistent and long-lasting conservation program that integrates and generates direct
and indirect socio-economic benefits for local communities is essential to prevent
sea turtle extinction.
Today, Programa Tatô in São Tomé, and Fundação Príncipe in Príncipe are the
key drivers of sea turtle conservation and research in the country. Both conservation
programs are based on the key principle that the participation and engagement of
local communities are essential for a successful conservation program. On São
Tomé, more than 80 people are involved in the conservation activities of Programa
Tatô (90% of whom are nationals) and include members from the local communities,
young professionals, and 51 rangers responsible for monitoring and protecting
foraging grounds and 77 out of the 107 breeding beaches. On Príncipe, Fundação
Príncipe, has a team of around 62 people (91% of whom are nationals) developing
marine and terrestrial conservation projects, including 32 rangers, who monitor and
protect foraging grounds and 36 out of the 50 beaches.
On São Tomé, Programa Tatô initiated a conversion process in 2016, to identify
and develop alternative livelihoods for the women who were trading sea turtle
products at the main national market, giving rise to a productive group of
17 women willing to transition towards a new livelihood, independent of the sale
of sea turtle meat and eggs. Currently, these women produce handicrafts, including
school uniforms, reusable masks, and menstrual pads. The program includes continuous follow-up, ensuring the consolidation of this group and their economic
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549
sustainability, thus promoting a long-term behavioral change and the recovery of sea
turtle populations in São Tomé and Príncipe (Vieira et al. 2017).
We note, however, that the monitoring of beaches and foraging grounds and the
direct involvement of a small percentage of the country’s inhabitants is not enough to
improve the conservation status of sea turtles. Besides direct employment by creating new jobs for research, internships, ecotourism guides and production of handicrafts, both organizations also develop active and innovative environmental
education and public awareness campaigns. In São Tomé, these campaigns were
developed after a study to estimate the prevalence of consumption, preference, and
availability of sea turtle meat and eggs, and make use of trusted influencers and
communication channels. This study helped develop a structured and rigorous
approach using behavioral insights to guide behavior change efforts (Veríssimo
et al. 2020; Thomas-Walters et al. 2020). Communication, education, and awareness
proved to be fundamental strategies not only because they create a better relationship
and trust between conservation organizations and communities, but also because
they contribute to the development of environmental awareness about the ecological
and socio-economic value of sea turtles and about the benefits of their conservation.
Awareness efforts involve a variety of initiatives, including educational school
programs, sports activities, theater, radio and TV programs and soap operas, beach
and ocean clean-ups, and fishing sector awareness activities, among others.
Considering the challenges that sea turtle conservation faces nowadays, both
Programa Tatô and Fundação Príncipe have adopted an integrated approach,
which is essential to improve the protection and sustainable management of key
sea turtle habitats, while developing a community-based marine conservation program that combines research, ecological monitoring, protection of critical sites,
environmental education, advocacy, community-based ecotourism, reconversion of
former poachers and traders, and development of alternative livelihoods. Thus, these
programs have been addressing the diverse and complex challenges of sea turtle
conservation, increasing our knowledge of all the sea turtle species that occur on and
around both islands, and improving the relationship between sea turtles and diverse
stakeholders from small-scale fishing communities to national politicians. Although
human threats are still a reality, levels of sea turtle harvest have decreased considerably, and the number of sea turtles recorded on the nesting beaches appears to be
increasing (Thomas-Walters et al. 2020). Today sea turtle conservation in São Tomé
and Príncipe has an increasing and wider public appreciation, support, and understanding, which provide an opportunity for local stewardship, changing attitudes
towards sea turtles and other living marine resources, and preparing future generation to be more aware of environmental topics.
Although research is underway on both islands to better understand the reproductive ecology, spatial and temporal movements, the foraging grounds, and the
impacts of anthropogenic threats, it is essential to increase our scientific knowledge
for adequate and effective sea turtle conservation guidance, so that critical habitats
may be protected using evidence-based conservation priorities and strategies. Major
challenges for the future include obtaining resources to maintain the levels of
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B. Ferreira-Airaud et al.
operation developed to date, to continue to support and improve the self-sufficiency
of former sea turtle hunters and traders, and to promote greater self-sufficiency of
both conservation programs. Nevertheless, the commitment of Programa Tatô and
Fundação Príncipe will remain focused on the coastal communities, who are the true
motivation for and the main component of any marine conservation program.
Acknowledgments A special thanks to Manjula Tiwari, Frederic Airaud, Estrela Matilde and the
editors for their reviews and comments, and to Jacques Fretey for all the historical information that
was essential for this chapter. We would like to thank all the people involved in sea turtle research
and conservation over the past two decades. We are grateful to the work, dedication, and collaboration of all the sectors of society: fishermen and women traders and their families and communities, national authorities, young professionals, technical staff of Marapa, Programa Tatô and
Fundação Príncipe, researchers, and all the national and international partner organizations and
funders committed and dedicated to sea turtle conservation. We would also like to thank the
indispensable support of the National and Príncipe Regional Governments. We are also grateful
for the hard work of all Programa Tatô and Fundação Príncipe staff and for the crucial support of
local coastal communities involved in the activities of both conservation programs.
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Open Access This chapter is licensed under the terms of the Creative Commons Attribution 4.0
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Chapter 21
The Avifauna of the Gulf of Guinea Oceanic
Islands
Martim Melo, Peter J. Jones, and Ricardo F. de Lima
Abstract Although birds have always been one of the best-known taxa on the Gulf
of Guinea oceanic islands, our understanding of their ecology and evolution has
increased substantially in the last two decades. Intensive field-based surveys have
allowed the first detailed island-wide distribution maps for most species and a much
better grasp of habitat associations, highlighting the importance of native forests for
many of the endemic birds. Molecular data have provided important insights into
evolutionary history, leading to an extensive revision of the taxonomy of the islands’
endemic avifauna. Most speciation events are much more recent than the age of the
islands, indicating a high species turn-over that is likely explained by the islands’
history of intense volcanic activity and their moderate distances to the mainland.
These islands have the highest accumulation of endemic bird species for small
oceanic islands: at least 29 endemic species occur in three islands with a total area
of just over 1000 km2. This may be explained by their particular geographic location:
offshore from a species-rich continent at distances that allowed the colonization and
evolution in isolation of many distinct lineages. All these contributions are now
M. Melo (*)
Museu de História Natural e da Ciência da Universidade do Porto, Porto, Portugal
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório
Associado, Universidade do Porto, Vairão, Portugal
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO, Vairão, Portugal
FitzPatrick Institute of African Ornithology, University of Cape Town, Cape Town,
South Africa
P. J. Jones
Chirnside, Scotland
R. F. de Lima
Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências,
Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon,
Portugal
Gulf of Guinea Biodiversity Centre, São Tomé, Sao Tome and Principe
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_21
555
556
M. Melo et al.
being used to ensure bird conservation, through updated species conservation status
and species action plans for the most threatened species, and also to promote the
conservation of the native forests on which most of the endemic birds depend.
Keywords Biodiversity · Birds · Conservation · Endemism · Radiation · Speciation
Birds are one of the animal groups with which people are most familiar. This is
especially true in the oceanic islands of the Gulf of Guinea where the avifauna has a
prominent position in popular culture. The islands’ birds have also been a preferential target of scientific investigation since the colonial period, in part due to the
exceptionally high number of endemic species. This richness has played an important role in bringing global attention to the unique biota of these islands. The state of
ornithological knowledge on these islands was summarized at the start of the present
century (Jones and Tye 2006), but since then a wealth of new information has been
gathered by an increasing number of studies. Here we provide an updated overview
of the diversity, ecology, and evolution of this remarkable avifauna.
We follow the taxonomy and nomenclature of Clements et al. (2021), which is
identical to the most recent checklist of the birds of the region (de Lima and Melo
2021). Taxonomic authorities are presented in the checklist (Appendix).
History of Ornithological Research
The avifauna of the Gulf of Guinea islands was little known before the nineteenth
century. These relatively isolated oceanic islands were logistically difficult to access,
with rugged, inhospitable interiors, so that progress was slow and sporadic, with
decades-long gaps between collections. By the end of the nineteenth century, the
avifauna was well documented, although important collections made at various
times in the twentieth century further contributed to recognizing the importance of
the islands’ unusually high endemism. Throughout this period, it became clear that
several endemic taxa were extremely rare and their forest habitats vulnerable to
development, prompting conservation concerns in recent decades. Easier access to
the islands and better logistical support have made it possible to run longer-term
research and conservation projects, and the advent of modern molecular phylogenetics has enabled significant insights into the evolutionary history of the endemic
bird community.
Apart from a few specimens collected earlier, the avifauna remained little known
until the 1840s, when the islands were used as a base for the British Expedition to the
River Niger. Expedition members collected several new species on São Tomé and
Annobón but visited Príncipe only briefly and did not collect any birds there (Allen
and Thomson 1848). Considerable confusion surrounded the provenance and identity of these specimens, however, due in part to the repeated loading and unloading
21
The Avifauna of the Gulf of Guinea Oceanic Islands
557
of cargoes between ships and between islands. Other misidentifications resulted
simply because African bird taxonomy was then in its infancy.
The most important early collections on Príncipe and São Tomé were made
between 1847 and 1850 for the museums of Hamburg and Bremen by Carl Weiss,
most of whose specimens were described in Hamburg by Gustav Hartlaub (1850,
1857), but confusion surrounded many Príncipe specimens that were wrongly
ascribed to the African continent. These confusions were eventually resolved with
the help of Heinrich Dohrn and John Gerrard Keulemans, whose collections on
Príncipe between April and September 1865 were complemented by the field notes
of Keulemans that proved to be a valuable source of information (Dohrn 1866;
Keulemans 1866).
In 1885, Adolpho Frederico Moller obtained some birds from São Tomé while
collecting plants for the Coimbra Botanic Gardens (Vieira 1887). Between 1885 and
1895, Francisco Newton assembled a comprehensive collection from all three
islands for the Lisbon Museum, which were described in a long series of papers
by José du Bocage (Bocage 1867, 1879, 1887a, b, 1888a–c, 1889a–c, 1891,
1893a, b, 1903, 1904). Newton was also a keen observer whose descriptions of
behavior and ecology were partially published by Bocage as ancillary information.
However, the original letters that Newton wrote to Bocage to accompany his
specimens and almost all the specimens themselves were destroyed in the disastrous
1978 fire in the Museu Bocage in Lisbon. By the end of the nineteenth century, most
landbird species had been described but an important collection was made for the
museum at Genoa by Leonardo Fea between 1899 and 1901 (Salvadori 1903a–c).
Two significant collections were made in the early decades of the twentieth
century. Boyd Alexander visited the main islands in 1909 collecting for the British
Museum (Bannerman 1914, 1915a, b) and José Correia and his wife Virginia
collected on Príncipe and São Tomé for the American Museum of Natural History
in 1928–29 (Correia 1928–29; Amadon 1953). Both Alexander and the Correias
kept extensive field notes on the distribution and status of the endemic bird species
they collected at a time when agricultural exploitation of the islands was at its peak
and some species had evidently become very rare. Correia’s valuable and entertaining diary (1928–29) remains unpublished, but his collection allowed Amadon (1953)
to produce an important synthesis on the avian zoogeography of the Gulf of Guinea
islands.
The next ornithological survey of Príncipe and São Tomé took place in 1949,
when an Oxford University team published the first detailed field notes for most of
the endemic birds (Snow 1950). Annobón has always been difficult to access
because of its remoteness, so there was an even longer gap between Alexander’s
1909 expedition and subsequent visits by Aurélio Basilio in 1955 (Basilio 1957) and
Hilary Fry in 1959 (Fry 1961).
A Portuguese scientific mission to Príncipe and São Tomé in 1954 collected birds
and assessed the status of those that might require protection under colonial law
(Frade 1958, 1959; Frade and Santos 1977). René de Naurois visited the islands
several times in 1963 and 1970–73, publishing extensively on the ecology and
systematics of most indigenous species, including all the endemic birds (Naurois
558
M. Melo et al.
1972a, b, 1973a, b, 1975a, b, 1979, 1980, 1981, 1982, 1983a, b, 1984a–d, 1985,
1987a–c, 1988a–c; Naurois and Castro Antunes 1973; Naurois and Wolters 1975).
He also wrote the first book to deal exclusively with the birds of all three oceanic
Gulf of Guinea islands (Naurois 1994).
In June 1983, ornithologists from the Dresden Museum visited São Tomé (Günther and Feiler 1985) and again in March-April 1991, the second time as part of a
multi-disciplinary expedition (Nadler 1993). Annobón belatedly received further
attention with visits by Mike Harrison (1990) and Jaime Pérez del Val (2001). In
1996–97 an expedition by the University of the Azores conducted the first detailed
study dedicated to seabirds (Monteiro et al. 1997).
The Red Data Book for African birds considered seven endemic bird species of
these islands to be threatened (Collar and Stuart 1985), highlighting the fact that four
single-island endemics on São Tomé had not been seen for over 50 years and were
possibly extinct. This publication prompted conservation initiatives by the International Union for Conservation of Nature (IUCN—Jones and Tye 1988; Burlison and
Jones 1988) and by the European Union. The latter acted mostly through ECOFAC,
a program sponsored by the European Union promoting the conservation and
sustainable use of forest ecosystems in Central Africa (Anon. 1994) that published
the first field guide to the birds of São Tomé and Príncipe (Christy and Clarke 1998).
Increased attention led to the rediscovery of all four “missing” bird species: São
Tomé Short-tail Motacilla bocagii in 1987 (Eccles 1988), Sao Tome Ibis Bostrychia
bocagei, Newton’s Fiscal Lanius newtoni in 1990 (Atkinson et al. 1994), and São
Tomé Grosbeak Crithagra concolor in 1991, more than a century after it had last
been seen (Sergeant et al. 1992). On Príncipe, the rare endemic Príncipe Thrush
Turdus xanthorhynchus was rediscovered in 1996, after more than 50 years (Christy
and Gascoigne 1996).
The number of ornithological studies has greatly increased since the turn of the
twenty-first century, leading to numerous taxonomic changes and a much better
understanding of this unique avifauna (Jones and Tye 2006; Melo 2007; de Lima and
Melo 2021). However, there is still much to be discovered as exemplified by the
existence of the Príncipe Scops-Owl, which was only confirmed in 2016, 90 years
after Correia collected information from local people on its putative occurrence
(Verbelen et al. 2016).
Species Diversity and Distribution
General Patterns
According to the latest assessment (de Lima and Melo 2021), the avifauna of the
oceanic islands of the Gulf of Guinea comprises 146 confirmed species (Appendix).
These include 66 resident species, which contain a remarkably high number of
endemics: 29 (44%) species and 16 (24%) subspecies (Table 21.1). Seventeen
species (26%) are possibly non-native, six are breeding migrant species (all of
21
The Avifauna of the Gulf of Guinea Oceanic Islands
559
Table 21.1 Numbers of bird species known from the Gulf of Guinea oceanic islands (de Lima and
Melo 2021: Appendix). Percentages of endemics and possibly non-native species were calculated
for the number of residents. One endemic species, the Príncipe Seedeater Crithagra rufobrunnea,
has three endemic subspecies, which were not added to the tally of endemic subspecies
Island
Príncipe
São
Tomé
Annobón
TOTAL
Residents
Singleisland
Total endemics
32
8 (25%)
50
17 (34%)
Shared
endemics
3 (9%)
3 (6%)
Endemic
subspecies
9 (28%)
7 (14%)
Possibly
non-native
5 (16%)
17 (34%)
Non-resident
NonBreeding breeding
seabirds
migrants
5
3
3
4
11
66
1 (9%)
3 (5%)
3 (27%)
16 (24%)
3 (27%)
17 (26%)
4
6
1 (9%)
26 (39%)
1
4
which are seabirds), four are regular non-breeding migrants, and 62 are vagrants.
Eight species are of uncertain status, including five that may breed in the archipelago
and three that have been recorded on the islands in the past. Additionally, the
occurrence of 51 species remains unconfirmed, being based solely on
uncorroborated observations (de Lima and Melo 2021).
The most outstanding feature of the resident bird assemblage is the high level of
endemism (Fig. 21.1). Almost all endemic species are single-island endemics, except
for the Sao Tome Pigeon Columba malherbii, which occurs on all three islands, and
the Sao Tome Spinetail Zoonavena thomensis and Príncipe Seedeater Crithagra
rufobrunnea, both of which occur on Príncipe and São Tomé (Table 21.2). Endemic
subspecies are also mostly restricted to a single island with two exceptions. The
Little Swift Apus affinis bannermani occurs on Príncipe and São Tomé and is also
considered the taxon present on the neighboring land-bridge island Bioko. Likewise,
the African Emerald Cuckoo Chrysococcyx cupreus insularum is considered the
taxon present on all three oceanic islands in the archipelago (Table 21.3, Box 21.1).
Another defining feature is the unusually high phylogenetic diversity of these
oceanic islands, with resident birds representing 28 families (Appendix).
Non-endemic native resident species include a large proportion of aquatic species, including three Ardeidae, one Phalacrocoracidae, and one Rallidae. They also
include single representatives of Accipitridae, Psittacidae, Sturnidae, Nectariniidae,
and Estrildidae. Possibly non-native species include five Ploceidae, three
Phasianidae, three Estrildidae, two Columbidae, and single representatives of
Apodidae, Psittacidae, Viduidae, and Fringillidae.
Breeding migrants include six seabird species: four Laridae, one Phaethontidae,
and one Sulidae. Apart from the White-tailed Tropicbird Phaethon lepturus, which
can breed in tree cavities and cliffs on the main islands, these species breed on bare
offshore islets, such as Boné de Jóquei, Tinhosas (both near Príncipe), Sete Pedras,
Rolas (both near São Tomé) and Tortuga (near Annobón). There are surprisingly few
regular non-breeding migrants: three coastal waders (Scolopacidae) and the Barn
Swallow Hirundo rustica (Hirundinidae). This contrasts with the large number of
occasional migrants, comprising 62 species belonging to 27 families (Appendix),
560
M. Melo et al.
Fig. 21.1 Some of the endemic birds of the oceanic islands of the Gulf of Guinea, including four
Critically Endangered species (1–4), an undescribed species that was only confirmed for the first
time in 2016 (8), two giants (3, 7) and a dwarf (1), and two phenotypically “aberrant” species (5, 6):
(1) São Tomé Ibis Bostrychia bocagei; (2) Newton’s Fiscal Lanius newtoni; (3) São Tomé
Grosbeak Crithagra concolor; (4) Príncipe Thrush Turdus xanthorhynchus; (5) Dohrn’s ThrushBabbler Sylvia dohrni; (6) São Tomé Short-tail Motacilla bocagii; (7) São Tomé Sunbird Dreptes
thomensis; (8) Príncipe Scops-Owl Otus sp. nov. Photo credits: (1, 2, 4, 5) Lars Petersson, (3, 8)
Martim Melo, (6, 7) Paul van Giersbergen
21
The Avifauna of the Gulf of Guinea Oceanic Islands
561
Table 21.2 Endemic bird species of the Gulf of Guinea oceanic islands: Príncipe (P), São Tomé
(ST), and Annobón (A), with their respective IUCN Red List category (IUCN 2021). Taxonomy
and nomenclature follow Clements et al. (2021)
Species
Order Columbiformes
Family Columbidae
Columba thomensis
Columba malherbii
Treron sanctithomae
Order Caprimulgiformes
Family Apodidae
Zoonavena thomensis
Order Pelecaniformes
Family Threskiornithidae
Bostrychia bocagei
Order Strigiformes
Family Strigidae
Otus sp. nov.
Otus hartlaubi
Order Passeriformes
Family Oriolidae
Oriolus crassirostris
Family Monarchidae
Terpsiphone atrochalybeia
Family Laniidae
Lanius newtoni
Family Cisticolidae
Prinia molleri
Family Sylviidae
Sylvia dohrni
Family Zosteropidae
Zosterops ficedulinus
Zosterops griseovirescens
Zosterops feae
Zosterops lugubris
Zosterops leucophaeus
Family Sturnidae
Lamprotornis ornatus
Family Turdidae
Turdus xanthorhynchus
Turdus olivaceofuscus
Family Nectariniidae
Anabathmis hartlaubii
Anabathmis newtonii
Dreptes thomensis
Common name
P
ST
A
IUCN
Maroon Pigeon
São Tomé Pigeon
São Tomé Green-Pigeon
•
•
•
•
•
EN
NT
EN
São Tomé Spinetail
•
•
LC
•
CR
•
NEa
VU
São Tomé Oriole
•
VU
São Tomé Paradise-Flycatcher
•
LC
Newton’s Fiscal
•
CR
São Tomé Prinia
•
LC
São Tomé Ibis
Príncipe Scops-Owl
São Tomé Scops-Owl
•
Dohrn’s Thrush-Babbler
•
LC
Príncipe White-eye
Annobón White-eye
São Tomé White-eye
Black-capped Speirops
Príncipe Speirops
•
•
EN
VU
NT
LC
LC
Príncipe Starling
•
LC
Príncipe Thrush
São Tomé Thrush
•
Príncipe Sunbird
Newton’s Sunbird
São Tomé Sunbird
•
•
•
•
•
CR
LC
•
•
LC
LC
VU
(continued)
562
M. Melo et al.
Table 21.2 (continued)
Species
Family Ploceidae
Ploceus princeps
Ploceus grandis
Ploceus sanctithomae
Familiy Motacillidae
Motacilla bocagii
Familiy Fringillidae
Crithagra rufobrunneab
Crithagra concolor
Common name
P
Príncipe Golden-Weaver
Giant Weaver
São Tomé Weaver
•
São Tomé Short-tail
Príncipe Seedeater
São Tomé Grosbeak
•
ST
A
IUCN
•
•
NT
VU
VU
•
VU
•
•
LC
CR
IUCN Red List categories: LC, least concern; NT, near threatened; VU, vulnerable; EN, endangered; CR, critically endangered; NE, not evaluated
a
Recently discovered and still being described. Field data suggest it might classify as CR (Freitas
2019)
b
Crithagra rufobrunnea is represented by three endemic subspecies (Table 21.3)
mostly shorebirds and passerines, whose number will continue to grow as currently
uncorroborated records are confirmed. These patterns reinforce the hypothesis that
migrants, whether Afrotropical or Palearctic, do not regularly cross the open sea of
the Gulf of Guinea (Jones and Tye 2006).
Island Accounts
Príncipe has 88 confirmed species (Table 21.1, Appendix), including 32 resident
species, of which 8 are single-island endemics and 3 are shared endemics with the
neighboring islands (Tables 21.1 and 21.2). Príncipe also holds 9 (28%) endemic
subspecies from species occurring on the mainland, together with two endemic
subspecies of the endemic Príncipe Seedeater (Table 21.2). Five species (16%) are
possibly non-native: two Columbidae, two Estrildidae, and one Apodidae. Príncipe,
and especially its surrounding islets, holds breeding colonies of all seabird species
that reproduce in the oceanic islands of the Gulf of Guinea, except Bridled Tern
Onychoprion anaethetus. Tinhosas islets are remarkable for their seabird colonies,
which hold around 200,000 breeding pairs of Sooty Tern O. fuscatus, accounting for
1% of the global population of this species and meeting the criteria for Important
Bird Area (Valle et al. 2016). Both Tinhosas and Boné de Jóquei also hold important
but declining breeding colonies of Brown Booby Sula leucogaster.
São Tomé has 96 confirmed species (Table 21.1, Appendix), including 50 resident
species, of which 17 (34%) are single-island endemics and 3 (6%) are endemics
shared with the nearby islands (Tables 21.1 and 21.2). This island also holds seven
(14%) endemic subspecies of species that occur in continental Africa, together with
one endemic subspecies of the endemic Príncipe Seedeater (Tables 21.1 and 21.3).
Seventeen species (34%) are possibly non-native: five Ploceidae, three Estrildidae,
21
The Avifauna of the Gulf of Guinea Oceanic Islands
563
Table 21.3 Endemic bird subspecies of the Gulf of Guinea oceanic islands: Príncipe (P), São Tomé
(ST), and Annobón (A). Taxonomy and nomenclature follow Clements et al. (2021); taxonomic
authorities given in Appendix. Notes link to taxonomic comments in Box 21.1
Species
Order Galliformes
Family Phasianidae
Coturnix delegorguei histrionica
Order Columbiformes
Family Columbidae
Columba larvata principalis
Columba larvata simplex
Treron calvus virescens
Order Cuculiformes
Family Cuculidae
Chrysococcyx cupreus insularum
Order Caprimulgiformes
Family Apodidae
Apus affinis bannermani
Order Pelecaniformes
Family Threskiornithidae
Bostrychia olivacea rothschildi
Order Strigiformes
Family Tytonidae
Tyto alba thomensis
Family Strigidae
Otus senegalensis feae
Order Coraciiformes
Family Alcedinidae
Corythornis cristatus thomensis
Corythornis cristatus nais
Halcyon malimbica dryas
Order Psittaciiformes
Family Psittacidae
Psittacus erithacus princeps
Order Passeriformes
Family Dicruridae
Dicrurus modestus modestus
Family Monarchidae
Terpsiphone rufiventer smithii
Family Sturnidae
Onychognathus fulgidus fulgidus
Familiy Fringillidaea
Crithagra rufobrunnea
rufobrunnea
Common name
P
Harlequin Quail
Lemon Dove
ST
A
•
1
•
2
2
3
•
African Green-Pigeon
•
Emerald Cuckoo
•
•
Little Swift
•
•
Olive Ibis
•
Barn Owl
•
4
5
6
7
•
African Scops-Owl
•
Malachite Kingfisher
Notes
8
Blue-breasted Kingfisher
•
•
9
9
10
Gray Parrot
•
11
Velvet-mantled Drongo
•
12
•
Black-headed ParadiseFlycatcher
•
Chestnut-winged Starling
Príncipe Seedeater
•
13
14
•
(continued)
564
M. Melo et al.
Table 21.3 (continued)
Species
Crithagra rufobrunnea thomensis
Crithagra rufobrunnea fradei
a
Common name
P
ST
•
A
Notes
•b
Crithagra rufobrunnea is an endemic species of Príncipe and São Tomé
Endemic to the 3 ha islet of Boné de Jóquei, c. 3 km off Príncipe
b
two Phasianidae, two Columbidae, two Psittacidae, and single representatives of
Apodidae, Viduidae, and Fringillidae. São Tomé and its surrounding islets, notably
Sete Pedras and Rolas, hold breeding colonies of three seabird species: Brown
Noddy Anous stolidus, White-tailed Tropicbird, and Brown Booby.
Annobón has 30 confirmed species (Table 21.1, Appendix), including 11 resident
species, of which one is a single-island endemic and one is an endemic shared with
São Tomé and Príncipe (Tables 21.1 and 21.2). It has three endemic subspecies, two
of which are treated as full species by some authors (Table 21.3, Box 21.1), three
native non-endemic species (Cuculidae, Rallidae, and Ardeidae), and three possibly
non-native species (two phasianids and one estrildid). Seabird colonies include
Brown Noddy, Black Noddy Anous minutus, Bridled Tern, and White-tailed
Tropicbird.
Box 21.1: Comments on Taxonomic Uncertainties
The numbers link to the species in Table 21.3. Taxonomic authorities given in
Appendix
1. Coturnix delegorguei histrionica. Endemic subspecies from São Tomé
whose validity should be re-appraised combining multiple lines of evidence, including molecular data.
2. The systematic position of the Lemon Dove has never been satisfactorily
resolved. Currently treated as Columba larvata, it was, for a long time,
placed in its own genus, Aploplelia. Its current placement within Columba
remains uncertain (Pereira 2013): it groups together with the Bronzenaped Pigeon superspecies (C. malherbii, C. delegorguei,
C. iriditorques) within a larger clade encompassing the Old-World
Columba and most Streptopelia species, but the exact affinities with
these two genera remain unresolved. The plumage of Columba larvata
provides little phylogenetic information as it varies widely, both between
and within populations, and it may also change with age (Amadon 1953;
Serle 1959). As such, it is imperative to conduct a full taxonomic revision
supported by extensive molecular sampling (Baptista et al. 2020), where
many of the current arrangements are unlikely to prevail. The subspecies
from São Tomé have been treated by some authorities as a distinct species,
but evidence supporting it is anecdotal (Baptista et al. 2020). Molecular
(continued)
21
The Avifauna of the Gulf of Guinea Oceanic Islands
565
Box 21.1 (continued)
evidence for the São Tomé and Príncipe populations detected large differentiation in mitochondrial haplotypes, suggesting at least two colonization events from the mainland (Pereira and Melo, unpublished results).
The same data also showed that these populations are closely related to
those from southern Cameroon but very distinct from those from Malawi
(up to 3.2 my divergence), suggesting that there may be multiple distinct
species on the mainland. No molecular data are available for the Annobón
population, which is currently placed under C. l. inornata, occurring from
Sierra Leone to Gabon.
3. Treron calvus has 15 recognized subspecies, many of which might not be
valid (Hoyo et al. 2020). Molecular data placed the endemic Príncipe
subspecies, T. c. virescens, together with birds from Bioko, currently
treated as an endemic subspecies, T. c. poensis, and revealed two cases
(in 14) of mitochondrial introgression from T. sanctithomae, endemic
from São Tomé, into the Príncipe population (Pereira 2013).
4. Chrysococcyx cupreus insularum. Endemic subspecies of the three Gulf
of Guinea oceanic islands, although most authorities treat or recommend
treating C. cupreus as a monotypic species (HBW and BirdLife International 2020; Clements et al. 2021; Gill et al. 2021).
5. Apus affinis bannermani is a subspecies considered to be restricted to the
Gulf of Guinea islands of Príncipe, São Tomé, and Bioko (Clements et al.
2021; Gill et al. 2021)—so not strictly speaking an endemic of the oceanic
islands. The validity of this subspecies should be re-appraised as it has
been considered indistinguishable from the neighboring mainland population (Amadon 1953).
6. Bostrychia olivacea rothschildi. Molecular studies on museum specimens
are required to determine if this extinct endemic subspecies from Príncipe
is valid, and whether it was more closely related to the São Tomé
B. bocagei or to the mainland species B. olivacea.
7. Tyto alba thomensis. Recent molecular evidence suggested that this phenotypically distinct taxon, restricted to São Tomé, may constitute a separate species (Uva et al. 2018; Alves 2019).
8. Otus senegalensis feae. A recent assessment, using multiple lines of
evidence but no molecular data, considered the scops-owl from Annobón
as a valid endemic species, Otus feae (Collar and Boesman 2020). Both
molecular data and phenotypic data (Freitas 2019) place it well within the
intra-specific variation of Otus senegalensis, which indicates a recent
colonization. The Annobón population is now very likely isolated from
O. senegalensis, which is absent from the neighboring mainland. A deep
phylogeographic study of O. senegalensis sensu lato is needed to understand its evolutionary history and clarify the taxonomic status of the
(continued)
566
M. Melo et al.
Box 21.1 (continued)
Annobón population. In any case, several authorities already recognize it
as a valid endemic species (e.g., HBW and BirdLife International 2020;
Gill et al. 2021).
9. Corythornis cristatus thomensis and Corythornis cristatus nais are
endemic subspecies from São Tomé and from Príncipe, respectively.
Genetically they fall well within the nominate subspecies: mitochondrial
divergences from samples from Malawi were only 0.3% for C. c.
thomensis and 0.9% for C. c. nais, and divergence between the two
island lineages is 0.8% (Melo and Fuchs 2008). The two subspecies
have phenotypic differences: C. c. nais being intermediate between
C. cristatus and C. leucogaster, while C. c. thomensis has darker plumage
than mainland birds, especially the juveniles (Christy and Clarke 1998). It
is possible that these populations represent recent and distinct colonization
events that are now evolving in isolation. They are treated as separate
endemic species by BirdLife International (HBW and BirdLife International 2020).
10. Halcyon malimbica dryas. Endemic subspecies from Príncipe, whose
likely validity should nevertheless be confirmed using multiple lines of
evidence, including molecular data.
11. Psittacus erithacus princeps. Mitochondrial data inferred a relatively
simple, albeit curious, history for the gray parrots from Príncipe (Melo
and O’Ryan 2007), which created the only real taxonomic conundrum for
the avifauna of the Gulf of Guinea oceanic islands. This population is the
result of two colonization events: one that occurred up to 1.4 mya and a
contemporary one. The first colonization came from the mainland stock
that evolved into P. timneh, whereas the recent colonization came from
P. erithacus. We cannot exclude that the latter was an accidental introduction linked to the Portuguese trade of this species from Angola to
Europe, which used to be done by boats that made a stopover in Príncipe
(Melo and O’Ryan 2007). Most of the Príncipe birds (75%) have the
Príncipe mitochondrial lineage, even though morphologically they are
closer to P. erithacus. We still do not know the overall impact on the
genome of the mixing of the two lineages. The International Ornithological Council opted to use the genetic evidence to treat the Príncipe
population as a subspecies of P. timneh (Gill et al. 2021), while other
authorities have kept the original treatment (HBW and BirdLife International 2020; Clements et al. 2021). We consider this to be an open issue
that can only be sorted out with an extensive genetic investigation.
12. Dicrurus modestus modestus. The drongo present on Príncipe has been
treated for a long time as an endemic species, although its taxonomic
status was always considered unclear (Jones and Tye 2006). A recent
(continued)
21
The Avifauna of the Gulf of Guinea Oceanic Islands
567
Box 21.1 (continued)
molecular study on the D. adsimilis complex returned a new taxonomic
arrangement for the group, in which the Príncipe population is conspecific
with the populations occurring in the forests of the Lower Congo Forest
Block, despite clear differences in bill and tail size (Fuchs et al. 2018).
13. Terpsiphone rufiventer smithii. The population of T. rufiventer from
Annobón was, until recently, often treated as a separate species, and still
is by some authors (Gill et al. 2021). As it is unlikely that there is regular
gene flow with the neighboring mainland populations, this population is
likely on an independent evolutionary trajectory.
14. Onychognathus fulgidus fulgidus. The nominate subspecies of this large
forest starling was described from São Tomé, to which it is endemic. The
birds on São Tomé are larger, more robust, and more vocal than those
occurring on the African mainland (Amadon 1953; Christy and Clarke
1998), warranting molecular research to determine if it may constitute a
distinct species.
Habitat Associations
The aquatic avifauna of the islands is species-poor but occupies a wide variety of
ecological niches (Lima et al. 2021). Regularly breeding seabirds include two
noddies, two terns, one tropicbird, and one booby, all of which breed in different
sets of offshore islets (Monteiro et al. 1997; Jones and Tye 2006—Appendix), where
they have distinct nesting microhabitats (Leventis and Olmos 2009; Valle et al.
2016; Bollen et al. 2018). The White-tailed Tropicbird also breeds on cliffs and trees
on the main islands, and a putatively distinct form of the Band-rumped Storm-Petrel
Hydrobates castro is thought to breed within burrows on the ground in São Tomé’s
native forests (Flood et al. 2019). The resident Black Kite Milvus migrans parasitus
is also commonly found foraging at sea. Other resident aquatic bird species include
predominantly coastal species that also occur along larger rivers, such as Western
Reef-Heron Egretta gularis and Long-tailed Cormorant Microcarbo africanus.
Predominantly freshwater species also occur along the coast and in brackish waters,
such as Common Moorhen Gallinula chloropus and Striated Heron Butorides
striata. The islands receive remarkably few non-breeding aquatic species as regular
visitors, most of which occur on the coast or along the lower reaches of rivers and
streams. The lagoons on the northern coast of São Tomé and the bay of Santo
António on Príncipe are the main localities where vagrant aquatic birds have been
recorded (Jones and Tye 2006; de Lima et al. 2021).
Until the 1990s, assessments of the distributions and habitat associations of the
terrestrial birds of the oceanic islands of the Gulf of Guinea were mostly based on
non-systematic observations (Jones and Tye 2006) and focused on understanding the
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M. Melo et al.
links between endemic species and land-use types to evaluate conservation status
(Jones and Tye 1988; Atkinson et al. 1991; Peet and Atkinson 1994). Knowledge
greatly improved following systematic surveys on both Príncipe (Baillie 2001;
Dallimer and King 2008; Dallimer et al. 2012; Fundação Príncipe 2019) and São
Tomé (Dallimer et al. 2009; de Lima et al. 2013, 2014; Soares 2017; Soares et al.
2020). These studies have shown that native species, including endemics, dominate
the avifauna across the islands, while non-natives tend to be restricted to degraded
environments, such as plantations and notably, to non-forested areas. A few of the
endemics are more sensitive to anthropogenic influence and are currently restricted
to the best-preserved forests. The Giant Weaver Ploceus grandis on São Tomé and
the Príncipe Golden-Weaver P. princeps seem to be the only endemic species that
are clearly more abundant outside forests, even though the Sao Tome Pigeon, the
Sao Tome White-eye Zosterops feae and a few of the endemic subspecies are also
frequently encountered outside native forest. As in other tropical forests (e.g.,
Newbold et al. 2013), species sensitive to forest degradation tend to be larger, and
insectivorous or frugivorous, while non-natives are mostly small and granivorous.
Other environmental factors are often correlated with land use, making it hard to
disentangle their effect on bird assemblages but, overall, the highest proportions of
endemics are found in remote steep areas at higher altitudes and with higher rainfall.
Annobón is seldom visited by ornithologists, and thus the ecology of its avifauna
remains the most incompletely documented (Sloan 2017).
Several studies have focused on the habitat associations of the islands’ Critically
Endangered species: Sao Tome Ibis (Margarido 2015; de Lima et al. 2017), Newton’s Fiscal (Maia and Alberto 2009; Lewis et al. 2018), Príncipe Thrush (Dallimer
et al. 2010; Rebelo 2021), and Sao Tome Grosbeak (Solé et al. 2012), as well as the
Príncipe Scops-Owl, which has also been proposed to qualify as Critically Endangered (Freitas 2019). Other studies have addressed the habitat associations of the
Gray Parrot Psittacus erithacus on Príncipe (Valle et al. 2017), the Annobón
population of the African Scops-Owl Otus senegalensis feae (Rodriguez-Prieto
et al. 2014), the distinctive São Tomé subspecies of Barn Owl Tyto alba thomensis
(Alves 2019), and the endemic pigeons of São Tomé (Carvalho et al. 2014). In
addition to providing an understanding of distribution and ecology, these studies
have also helped in estimating population sizes (i.e., Azevedo 2015) and informing
conservation strategies (BirdLife International 2014a, b; Fundação Príncipe et al.
2021).
The Endemic Birds
How Many Endemics?
Endemism in the oceanic islands of the Gulf of Guinea is restricted to resident
landbirds (Jones and Tye 2006; de Lima and Melo 2021), although the still
undescribed local population of the Band-rumped Storm-Petrel may represent an
21
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exception (Flood et al. 2019). Out of the 66 resident landbird species of the three
islands, 17 are possibly non-native (de Lima and Melo 2021), and of the remaining
49 confirmed extant natives, 90% are endemic at the species or subspecies level
(Tables 21.2, 21.3, and 21.4, Appendix). The exact number of endemic species
varies according to different authorities (Hoyo 2020), with the most recent assessments recognizing 32 (HBW and BirdLife International 2021), 31 (Gill et al. 2021),
and 29 species (Clements et al. 2021; de Lima and Melo 2021). These discrepancies
Table 21.4 Divergence time estimates, in million years (Ma), between endemic birds of the
oceanic islands of the Gulf of Guinea and their closest mainland relative(s); square brackets indicate
clades. These estimates are illustrative only as they were derived from different markers and used
different rates and estimation methods. When available, 95% confidence intervals are shown. Note
that the ages of the oldest known sub-aerial rocks are 31 Ma for Príncipe, 15 Ma for São Tomé and
6 Ma for Annobón (Ceríaco et al. 2022)
Island taxa
Columba thomensis
Columba malherbii
Treron sanctithomae
Tyto alba thomensis
Otus sp. nov
Otus hartlaubi
Oriolus crassirostris
Terpsiphone
atrochalybeia
Lanius newtoni
Sylvia dohrni
Zosterops ficedulinus
Zosterops
griseovirescens
Zosterops feae
Zosterops lugubris
Zosterops leucophaeus
Turdus xanthorhynchus
Turdus olivaceofuscus
Ploceus sanctithomae
Ploceus grandis
Motacilla bocagii
Crithagra rufobrunnea
Mainland sister taxa
Columba arquatrix
[Columba iriditorques |
C. delegorguei]
Treron calvus
all other taxa under Tyto alba
[Otus hartlaubi |
O. senegalensis]
Otus senegalensis
Oriolus brachyrhynchus
laetiora
Terpsiphone corvina or
T. mutata comorensis
Lanius mackinnoni
[Sylvia abyssinica | S. atriceps
| S. galinieri | S. nigricapillus]
Large clade including mainland taxa and the Indian Ocean
maderaspatanus clade
Turdus pelios
[Ploceus bicolor – Anaplectes
(¼ Ploceus) rubriceps]
Ploceus weynsi
[Motacilla clara | M. capensis]
Crithagra striolata and other
African taxa
Divergence
time (Ma)
1.5 (1.0–2.1)
1.3 (0.6–2.1)
2.0 (1.9–2.6)
c. 1.8
0.9 (0.7–1.1)
Reference
Pereira (2013)
Pereira (2013)
c. 1.7b
Pereira (2013)
Uva et al. (2018)
Melo et al.
(unpublished data)
Melo et al.
(unpublished data)
Jønsson et al. (2019)
c. 1.4c
Bristol et al. (2013)
2.1 (0.9–3.7)
c. 8.1d
Fuchs et al. (2011)
Cai et al. (2019)
0.9 (0.7–1.1)
Melo and O’Ryan
(2007)
c. 4e
c. 5f
c. 1.2–1.4g
Batista et al. (2020)
Melo et al. (2010)
De Silva et al. (2019)
c. 1.6–1.8h
3.3 (2.2–4.6)
1.7
(1.0–2.3)i
De Silva et al. (2019)
Alström et al. (2015)
Melo et al. (2017)
0.8 (0.6–1.0)
(continued)
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M. Melo et al.
Table 21.4 (continued)
Island taxa
Crithagra concolor
Mainland sister taxa
[C. citrinelloides |
C. mozambica | C. leucopygia]
Divergence
time (Ma)
0.6
(0.4–0.8)j
Reference
Melo et al. (2017)
a
Genetic divergence from other O. brachyrhynchus taxa, and sister species relationship with
O. crassirostris, may warrant treatment as separate species O. laetior (Jønsson et al. 2019)
b
Divergence time estimate read from chronogram (Supplementary Fig. S4: Jønsson et al. 2019)
c
Divergence time estimate read from chronogram (Fig. 3: Bristol et al. 2013)
d
Divergence time estimate read from chronogram (Fig. 3a: Cai et al. 2019)
e
Divergence time estimated from large scale genomic data and fossil calibrations
f
Divergence time estimated from cytochrome b data using Weir and Schluter’s (2008) rate.
Estimates from ND2 and ND3 using Lerner’s et al. (2011) rates returned estimates of c. 2 mya
(not shown)
g
Divergence time estimated from uncorrected pairwise distances estimated from partial COI
sequences (298 and 100 bp) from De Silva et al. (2019) using Weir and Schluter’s (2008) rate
h
Divergence time estimated from uncorrected pairwise distances estimated from partial sequences
of ND2 (543 bp) and COI (298 bp) from De Silva et al. (2019) using Weir and Schluter’s (2008) rate
i
Divergence time estimated from cytochrome b data using Weir and Schluter’s (2008) rate
j
Divergence time estimated from mitochondrial (ND2, ND3) and nuclear (GAPDH, MYO2, ODC)
DNA using Lerner’s et al. (2011) rates. These very recent estimates may be driven by the behavior
of the ND2 in recent times (i.e., closer to the tips of the trees)
are restricted to recent speciation events, in which some authors treat sister taxa as
species, while others treat them as subspecies (Box 21.1). Such divergent taxonomic
treatments are to be expected considering that speciation is a continuous process, and
authorities agree that there is a total of 45 distinct evolutionary lineages (endemic
species and subspecies, including the Príncipe Scops-Owl). Here we follow a
conservative approach, where recent divergence events are treated as subspecies
until further evidence emerges, resulting in a total of 29 endemic species (Tables 21.1
and 21.2) and 16 endemic subspecies (Tables 21.1 and 21.3). Additionally, the
endemic Príncipe Seedeater has diverged into three single-island endemic subspecies: the nominate restricted to Príncipe, another to Boné de Jóquei (islet c. 3 km
offshore from Príncipe), and the third to São Tomé (Table 21.3), a taxonomic
arrangement supported by molecular data (Melo 2007).
Bird Endemism of the Gulf of Guinea Oceanic Islands
in Perspective
Although confined to a land area of just over 1000 km2, the 29 endemic species of
Príncipe, São Tomé, and Annobón represent 60% of the endemic bird species of the
vast Guinean Forests of West Africa biodiversity hotspot (area: 621,705 km2; IUCN
2015). It is not surprising for oceanic islands to be centers of endemism, but it is still
instructive to compare the bird endemism levels of the Gulf of Guinea islands with
those found elsewhere. The Galapagos have 22 endemic landbirds in 13 islands
21
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571
Fig. 21.2 The number of endemic bird species in the oceanic islands of the Gulf of Guinea has no
equivalent worldwide. Left—number of endemic bird species in relation to island area for all the
small oceanic islands of the world that have at least one endemic species; data from Coyne and Price
(2000). Right—adaptation of Figure 1 from Mayr’s (1965) global analysis of species turnover on
islands (percentage of bird endemism in relation to island area), where three island categories were
defined: A—solitary, well-isolated islands; B—single islands near continents or large archipelagos;
C—islands in the Gulf of Guinea. In both cases, the Gulf of Guinea islands follow a distinct
trajectory, characterized by a much higher number of endemics than expected from their area alone
totaling some 8000 km2, whereas the six largest Hawaiian Islands have 30 extant
endemic species and 19 documented extinct endemics in over 16,000 km2
(Stattersfield et al. 1998). The high level of bird endemism within the relatively
restricted area of the Gulf of Guinea oceanic islands has no parallel, with the islands
following a very distinct trajectory to the global pattern (Mayr 1965; Fig. 21.2). In a
survey of the 45 small islands (<10,000 km2) that have at least one endemic species,
the mean number of endemic species is 2 and the mode is a single species (Coyne
and Price 2000). By comparison, São Tomé, 857 km2, has 17 single-island endemic
species and Príncipe, 139 km2, has eight, plus three additional shared endemic
species. A recent worldwide analysis of bird communities on oceanic islands further
identified Príncipe and São Tomé as the only group of islands where the number of
species, colonizations, and within-archipelago speciation all exceeded the predictions of the global model (Valente et al. 2020).
Why So Many Endemic Birds?
The 29 endemic species of the oceanic islands of the Gulf of Guinea belong to
20 distinct evolutionary lineages from 16 families. This means that the current
diversity of the endemics required at least 20 independent colonization events
from the mainland. Hence, the impressive level of bird endemism is spread across
independent phylogenetic lineages rather than being concentrated within speciesrich genera from just a few colonizations, such as in the well-known adaptive
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radiations that have occurred in other archipelagos. In the Galapagos, six colonizations gave rise to the 22 extant endemic species, dominated by the radiation of
Darwin’s finches (Grant and Grant 2008), and in the Hawaiian archipelago, six
colonizations diversified into more than 40 endemic species, dominated by the
Hawaiian honeycreepers (Pratt 2005). The factor underlying these distinct patterns
is geography. These two archipelagos are much farther from the mainland than the
Gulf of Guinea oceanic islands. The oceanic islands of the Gulf of Guinea constitute
an ‘intermediate island system’ (Melo 2007; Ricklefs and Bermingham 2007),
whose biogeographical characteristics lie between very isolated and virtually independent systems, and those so close to the mainland that their diversity patterns are
determined mostly by ecological factors. In addition, the diverse and species-rich
ecosystems of West Africa and the Congo Basin to the north and east, respectively,
provide ample sources for potential colonization to the Gulf of Guinea oceanic
islands. This “surrounding landmass proportion” is not only very large, but it
consists mostly of habitats that are similar to those of the islands themselves—the
two most important parameters associated with an increased likelihood of successful
colonization (Weigelt and Kreft 2013).
The linear arrangement of the Gulf of Guinea islands and the relatively large
distances between them, which are similar to their distances from the African
continent, appear to have favored independent colonizations from the mainland
relative to dispersal between islands. Colonization by so many mainland species is
expected to increase inter-specific competition, reducing the chances for adaptive
radiation (Schluter 2000; Ricklefs and Bermingham 2007). Nevertheless, white-eyes
(Zosteropidae) represent a five-species radiation in these islands (Melo et al. 2011—
Box 21.2). Other instances of inter-island dispersal events leading to speciation
include the Giant and Príncipe Golden weavers (Valente et al. 2020), and the
Príncipe Sunbird Anabathmis hartlaubi and the Sao Tome Sunbird Dreptes
thomensis (Rauri Bowie, unpublished data: sister species relationship supported by
mitochondrial and nuclear markers.; MM and Luís Valente, unpublished data: sister
species relationship supported by mitochondrial sequence data). Inter-island dispersal has also resulted in the differentiation of the Príncipe Seedeater into three
subspecies (Jones and Tye 2006; Melo 2007). The distinct species of green-pigeons
(Pereira 2013), scops-owls (Freitas 2019), thrushes (Melo et al. 2010), and
Crithagra canaries (Melo et al. 2017) present on different islands may have been
derived either from independent colonizations from the African continent or from
inter-island dispersal. The same applies to the island subspecies of the Lemon Dove
Columba larvata (Pereira 2013), and the Malachite Kingfisher (Melo and Fuchs
2008).
Although the proximity to a species-rich continent does increase the chances of
successful colonizations, it also increases the probability that gene flow between
island and mainland populations is maintained at levels that will prevent population
divergence and eventual speciation. Hence, the most likely reason that the oceanic
islands of the Gulf of Guinea support the highest concentration of endemic birds
worldwide is their unique geographic location: they are close enough to the African
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The Avifauna of the Gulf of Guinea Oceanic Islands
573
continent to be colonized by a diverse array of species, but far enough to allow
successful immigrants to evolve in isolation.
In summary, bird speciation in the oceanic islands of the Gulf of Guinea has in
most cases occurred by independent divergence in allopatry (allospeciation: Mayr
and Diamond 2001), when an immigrant population from the mainland reached one
island and evolved there in isolation. This is the overwhelmingly dominant route for
bird speciation on islands (Ricklefs and Bermingham 2007; Valente et al. 2020) and
for birds in general (Price 2008). In addition, molecular data have now revealed
previously unrecognized radiations on the islands, most remarkably among the
white-eyes (Box 21.2). Although comprising only five species, this radiation may
be the third largest globally for birds inhabiting small oceanic islands, and further
stands out by having the fastest speciation rates recorded in birds and one of the
highest in vertebrates (Appendix 5 in Melo et al. 2011).
Box 21.2: The Radiation of the White-Eyes (Zosteropidae) of the Oceanic
Islands of the Gulf of Guinea
The spectacular radiations of the Hawaiian honeycreepers (Pratt 2005) and of
the Galapagos finches (Grant and Grant 2008) could mislead us into believing
that radiations are a common diversification process for birds on small oceanic
islands—when they are in fact a very rare exception (Valente et al. 2020). The
next largest oceanic island bird radiation worldwide is found in the Gulf of
Guinea, where the five white-eyes species descend from a single ancestor that
reached the islands within the last 0.7–1.1 my (Melo et al. 2011). Although
modest in size, the white eye radiation boasts one of the fastest rates of
speciation ever documented in vertebrates (Melo et al. 2011).
The radiation itself is a textbook example of the “archipelago radiation
model” developed originally for island birds (Lack 1947; Grant 2001; Petren
et al. 2005), which is also in agreement with current views of the speciation
process (Rundle and Nosil 2005; Nosil 2012), where inter-specific competition
is the engine of phenotypic diversification (numbers refer to photos below):
(I) Descendants of the original colonization (6: mainland relative), islandhop and diverge in isolation (1, 3, 5).
(II) Presumably because they occupy similar habitats, phenotypic changes
are not pronounced—as illustrated by the Príncipe and São Tomé whiteeyes (1, 3), which are indistinguishable in the field (Hering et al. 2018).
(III) Inter-island dispersal events bring diverging populations together, setting
the stage for inter-specific competition.
(IV) The pressure of resource competition is felt more strongly in the
outnumbered new arrivals. These undergo the most phenotypic change
and at very fast rates. The most aberrant species of the group (2, 4)
represent the most recent speciation events: they may have diverged from
one another less than 0.3 mya and from a typical white-eye less than 0.5
(continued)
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M. Melo et al.
Box 21.2 (continued)
mya—a timeframe typical of intra-specific but not inter-specific divergence in birds (Melo et al. 2011). This process of asymmetric divergence
driven by resource competition has been predicted by theory (Doebeli
and Dieckmann 2000) and is now empirically supported by the radiation
of Darwin’s finches (Petren et al. 2005) and of the Gulf of Guinea whiteeyes.
(1) Príncipe White-eye Zosterops ficedulinus. (2) Príncipe Speirops Z. leucophaeus. (3) São
Tomé White-eye Z. feae. (4) Black-capped Speirops Z. lugubris (São Tomé). (5) Annobón
White-eye Zosterops griseovirescens. (6) Northern Yellow White-eye Z. senegalensis, the
closest mainland relative with the typical white-eye phenotype. Photo credits: (1–4) Lars
Petersson, (5) Martim Melo, (6) Jake Selby
21
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Systematics of the Endemic Birds: New Insights from
Molecular Data
The taxonomy and systematics of the endemic birds of the Gulf of Guinea were
mostly addressed by Amadon (1953) and Naurois (1994) and later summarized by
Jones and Tye (2006). Evolutionary inferences were still then dependent on phenotypic data, and particularly on morphological traits, which are often adaptive and can
quickly lose their phylogenetic signal. This issue is particularly problematic in birds
(Bock 1967; Hafner et al. 1984) and on oceanic islands, where both rapid phenotypic
evolution (Millien 2006; Melo et al. 2011; Garcia-Porta et al. 2016; Sendell-Price
et al. 2020) and phenotypic convergence (Fleischer et al. 2008; Covas 2016;
Benítez-López et al. 2021) are common. Molecular phylogenies are expected to
constitute better hypotheses of evolutionary history than phenotype-based phylogenies, as they use genetic markers that are mostly independent from phenotypic traits,
and not under direct selection (Bromham et al. 2002; Davies and Savolainen 2006).
The most important insight brought by molecular phylogenies was that most bird
speciation events in the Gulf of Guinea islands are recent, having occurred since the
late Pliocene (2.5 Ma—Table 21.4). The exceptions so far are the Príncipe and São
Tomé thrushes and the Sao Tome Short-tail, which may have speciated in the
mid-Pliocene (c. 3.5–4.0 Ma), and Dohrn’s Thrush-Babbler Sylvia dohrni, which
may date back to the Miocene (c. 8 Ma—Table 21.4). Even without estimates of
speciation times for some of the endemics, it is safe to conclude that the present
species are all much more recent than the emergence of the islands they inhabit,
which range from 31 to 6 Ma (Ceríaco et al. 2022). This pattern indicates that the
oceanic islands of the Gulf of Guinea constitute a speciation center rather than a
stable refuge for species that went extinct on the mainland. The absence of old
species is nevertheless surprising and could be due to the recent and intense volcanic
history of the islands (Lee et al. 1994; Barfod and Fitton 2014; Ceríaco et al. 2022).
The patterns of genetic variation of the lizard Trachylepis thomensis within São
Tomé have been linked to the impact of volcanic activity, with the extent of this
variation being much lower than expected from the age of the island (Jesus et al.
2005). Likewise, volcanic activity on São Tomé has been linked to the evolutionary
history of two sister caecilian lineages—Schistometopum ephele and S. thomense
(O’Connell et al. 2021). In the absence of (sub)fossil evidence, it is not known if
cycles of sea-level rise during post-glacial periods may have caused extinctions
(Jones and Tye 2006; Ceríaco et al. 2022). Príncipe is likely to have been the most
affected, having lost almost 90% of its land area as recently as 12,000 years ago
(Norder et al. 2018). Likewise, during glacial periods Annobón was eight times
larger, whereas the size of São Tomé did not change greatly. In any case, the
relatively small sizes of the islands and their proximity to the mainland might
make them susceptible to more rapid species turnover, which may further help
explain the young age of most endemic bird species.
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M. Melo et al.
The main taxonomic consequence of the fast rates of phenotypic divergence
inferred from molecular phylogenies is that all the endemic genera have been
found invalid. This includes the Dohrn’s Thrush-Babbler and the Sao Tome Shorttail, formerly placed in the monotypic genera Horizorhinus and Amaurocichla,
respectively, whose peculiar traits obscured to which families they belonged (i.e.,
classified as incertae sedis). Dohrn’s Thrush-Babbler, from Príncipe, is sister to a
clade including the African Hill Babbler Sylvia abyssinica, an Afromontane forest
species present also in the neighboring land-bridge island Bioko and Mount Cameroon (Voelker et al. 2009). In the case of the Sao Tome Short-tail, several of its
traits, such as nine primaries (albeit a vestigial tenth primary is present) and ten
rectrices with a protruding shaft, led to the suggestion that it could share an ancestor
with the South-American Furnariidae (Naurois 1982). In actuality, it represents a
recent speciation event from continental Africa, derived from the same ancestor as
the Mountain Wagtail Motacilla clara, with which it shares the ecological niche of
forest streams, and the Cape Wagtail M. capensis (Alström et al. 2015). The São
Tomé Grosbeak, a Crithagra canary (Fringillidae) sister to the co-occurring Príncipe
Seedeater (Moreau 1962; Melo et al. 2017), was originally placed in the monotypic
genus Neospiza, and was often classified as a weaver (Ploceidae) (e.g., Bocage
1888b—he later placed it in Fringillidae: Bocage 1904; Sclater 1924; Bannerman
1953; Moreau 1962). The Sao Tome Weaver Ploceus sanctithomae, formerly in the
endemic monotypic genus Thomasophantes (Amadon 1953; Moreau 1960; Naurois
1994), is now considered sister to the clade including the Forest Weaver Ploceus
bicolor and the Red-headed Weaver Anaplectes rubriceps (Anaplectes being invalid
as well; De Silva et al. 2019). The Sao Tome Sunbird is currently still classified
under the only remaining endemic genus, Dreptes, which is known to be invalid,
since the species is sister to the Príncipe Sunbird (genus Anabathmis) (Rauri Bowie,
pers comm.; MM and Luís Valente, unpublished data). Finally, the genus Speirops,
endemic to the Gulf of Guinea, is also no longer considered valid (Melo et al. 2011).
It used to group four species of “aberrant” white-eyes (Zosteropidae): Black-capped
Speirops Zosterops lugubris (São Tomé), Príncipe Speirops Z. leucophaeus, Bioko
Speirops Z. brunneus, and Cameroon Speirops Z. melanocephalus (Mount Cameroon). However, molecular data show that the four species are not monophyletic and
that the “aberrant” characters are the result of fast phenotypic divergence. On the
oceanic islands, aberrant species represent the most recent speciation events (Box
21.2; Melo et al. 2011), rather than being derived from the oldest colonizations as
previously assumed (Amadon 1953; Moreau 1957).
Conservation
The importance of the islands for conservation was first noted when the southwestern forests of São Tomé were identified as the second most important for bird
conservation in Africa (Collar and Stuart 1988). As a result, an IUCN-funded
21
The Avifauna of the Gulf of Guinea Oceanic Islands
577
mission surveyed plants and vertebrates of São Tomé and Príncipe confirming the
high endemism and the global importance of the biological diversity of the oceanic
islands (Jones and Tye 1988; Jones et al. 1991; Jones 1994). For birds, each of the
oceanic islands is listed by BirdLife International as an independent Endemic Bird
Area (Stattersfield et al. 1998; BirdLife International 2021a). More recently, the
moist lowland forests of Príncipe, São Tomé, and Annobón were identified as the
third most important in the world for the conservation of forest birds (Buchanan et al.
2011), and the endemic birds were the main factor for the protected areas of São
Tomé and Príncipe combined to be considered globally as the 17th most important
protected area for the conservation of threatened species (Le Saout et al. 2013).
Some of the endemic birds were already extremely rare early in the twentieth
century and remain at high risk, but only the Príncipe subspecies of the Olive Ibis
Bostrychia olivacea rothschildi became extinct (de Lima and Melo 2021). The most
recent assessment listed 14 threatened bird taxa for the islands (IUCN 2021): five
Critically Endangered, including the Annobón Scops-Owl Otus feae—which we
treat as a subspecies of O. senegalensis following Clements et al. (2021); four
Endangered, including the Gray Parrot, which is common on Príncipe and the only
non-endemic threatened bird on the islands (Valle et al. 2021); and five Vulnerable
(Tables 21.2 and 21.3).
The number of threatened taxa has increased since 2000, when only nine were
listed: three Critically Endangered (the Annobón Scops-Owl and the Príncipe
Thrush were not recognized as species by IUCN), none Endangered (the Maroon
Pigeon Columba thomensis was Vulnerable, the Príncipe and São Tomé white-eyes
were treated as conspecific and Vulnerable, and the Sao Tome Green-Pigeon Treron
sanctithomae and the Gray Parrot were Least Concern), and six were Vulnerable
(including the Principe and Sao Tome white-eyes treated as the same taxon). Most of
these changes have been due to improved knowledge and not necessarily to a
deterioration of the situation of the species, despite indications that conditions
might be worsening for several taxa (IUCN 2021). The conservation status of each
bird species is reviewed every year (BirdLife International 2021b) and thus further
changes are expected. Other taxa await assessment, namely all endemic subspecies
and putative new species, many of which are likely to be threatened. These include
the Boné de Jóquei Islet subspecies of the Principe Seedeater Crithagra rufobrunnea
fradei, which has a highly restricted range (Melo 2007), the elusive Gulf of Guinea
Band-rumped Storm-Petrel (Flood et al. 2019), and the Príncipe Scops-Owl, which
is still being described but will likely classify as Critically Endangered (Freitas
2019).
Habitat loss, overexploitation, and introduced species are key threats to native
birds both globally (IUCN 2021) and in the Gulf of Guinea. Given the habitat
associations described in the previous section, forest loss and degradation are the
main threats to the birds on these islands (e.g., Dallimer et al. 2012; Soares et al.
2020). Most of this habitat loss can be attributed to agricultural expansion and
intensification (Oyono et al. 2014), both to supply the local markets (notably
578
M. Melo et al.
horticulture) and to produce export cash crops (e.g., cocoa, palm oil, and coffee).
Logging, fire, mining, infrastructure development, urban and tourism expansion,
livestock, and silviculture (e.g., oil palm wine and medicinal plants) also contribute
to habitat loss. To halt ongoing habitat loss, it is vital to ensure the effective
implementation of existing protected areas, and their possible expansion, since
some important forests are not yet formally protected (BirdLife International 2020;
de Lima et al. 2022). Furthermore, environmentally friendly practices should be
promoted in extractive and agricultural activities to ensure that complex vegetation
structures are not lost and that introduced species are kept under control (de Lima
et al. 2014; Carvalho 2015).
Most bird species are hunted, but the effects of direct exploitation are more
noticeable on larger species (de Lima et al. 2013), such as the Sao Tome Ibis
(Sampaio et al. 2016; de Lima et al. 2017), pigeons (Palmeirim et al. 2013; Carvalho
2015; Fundação Príncipe 2019) and the Brown Booby (Bollen et al. 2018). The
diffuse nature of hunting coupled with the rugged terrain makes it extremely difficult
to enforce existing laws that regulate this activity (Albuquerque and Carvalho
2015a, b; de Lima et al. 2022). Given that bird hunting is mostly a cultural,
commercial, and recreational activity that contributes little to protein intake, diverting hunting efforts to instead control populations of introduced mammals could have
a dual positive effect on bird conservation (Carvalho 2015).
Introduced bird species are thought to be strongly associated with land-use
intensification, having little or no impact on the native avifauna (Soares et al.
2020). On the other hand, the effects of introduced mammals (Dutton 1994) and
plants (Figueiredo et al. 2011) have long been identified as potential threats, even
though their impacts remain poorly understood (BirdLife International 2014a, b;
Fundação Príncipe et al. 2021). Feral pigs and cows feed on understory plants and
turn over the soil, disturbing key forest habitats that evolved in the absence of large
terrestrial mammals. Rats Rattus sp. and Mona Monkeys Cercopithecus mona are
likely to have direct effects through nest predation (Guedes et al. 2021). Introduced
mammal and plant species also have the potential to change forest structure in the
long term, namely through the disruption of seed dispersal and other processes
linked to forest regeneration (Heleno et al. 2021).
Other factors, such as pollution and climate change have also been identified as
potential threats to the endemic-rich avifauna of these islands (IUCN 2021). For
example, the intensive use of insecticides was claimed to be responsible for a severe
population crash of the Sao Tome Paradise Flycatcher Terpsiphone atrochalybeia in
the 1970s (Naurois 1984a).
Because most threats to biodiversity act synergistically and often occur as a result
of habitat loss, protecting the remaining native forest is the single most important
measure to secure the future of these species (de Lima 2012). Fortunately, all the
islands have significant proportions of their territory already dedicated to biodiversity conservation (UNEP-WCMC and IUCN 2021), and the protected area network
is soon expected to expand to cover additional important habitats (BirdLife
21
The Avifauna of the Gulf of Guinea Oceanic Islands
579
International 2020; de Lima et al. 2022). However, weak enforcement of environmental legislation remains a major concern (de Lima et al. 2017). Improving our
knowledge of species ecology and of pervasive threats, such as hunting, invasive
species, and climate change, will also be key to designing effective species-specific
conservation measures. In this regard, conservation priorities in São Tomé and
Príncipe have been identified through extended discussions, both for protected
areas (Albuquerque and Carvalho 2015a, b) and for all Critically Endangered bird
species (BirdLife International 2014a, b; Fundação Príncipe et al. 2021). Despite not
being entirely fulfilled, these have been extremely useful in guiding conservation
action, and continued revision will be essential. The success of ongoing conservation
efforts ultimately relies on engaging the inhabitants of the islands, a process that is
still in its infancy (de Lima et al. 2022). In this regard, birds are also being used to
raise awareness locally and globally for the value of the unique biodiversity of the
islands (e.g., Rebelo 2021; Ayres et al. 2022).
Concluding Remarks
The oceanic islands of the Gulf of Guinea constitute an outstanding example of an
intermediate island system for birds, whose geographical location and rich
rainforests maximize the accumulation of bird endemism. As such, they offer a
valuable suite of phylogenetically independent replicates for testing hypotheses
about evolutionary processes in speciation and adaptation. Knowledge gaps persist
regarding Annobón and the status of some species, including potential undescribed
endemics, past extinctions, and the origins of putative non-native species. Birds are
still the best-known taxon in the archipelago, however, making them ideal exemplars
that can guide future work on other groups. Our knowledge of environmental
constraints and the history of human occupation of these islands also make them
excellent models for understanding ecological processes and testing conservation
strategies that can be used in a wider context, for instance in other small forested
islands.
Acknowledgments MM was supported via the European Union’s Horizon 2020 research and
innovation program under grant agreement 854248. Fundação para a Ciência e a Tecnologia (FCT,
Portugal) provided structural funding to CIBIO (UIDB/50027/2021: to MM) and to cE3c
(UID/BIA/00329/2021: to RFL). We thank Lars Petersson, Jake Selby, and Paul van Giersbergen
for permission to use their excellent photos. We thank the reviewers Peter Ryan, Jacob Cooper, and
the editor Rayna Bell for their helpful comments and suggestions.
580
M. Melo et al.
Appendix
Checklist of bird species on the oceanic islands of the Gulf of Guinea, excluding
vagrant and unconfirmed species (de Lima and Melo 2021). Islands: P, Príncipe; S,
São Tomé; A, Annobón. Status: E, endemic species; I, probably non-native; R,
native non-endemic resident; S, endemic subspecies; X, extinct; B, breeding
migrant; M, non-breeding migrant; ?, uncertain. Subspecies are only identified
when they are endemic. Taxonomy and nomenclature follow Clements et al. (2021)
Higher taxonomy
Order Galliformes
Family Numididae
Numida Linnaeus, 1764
Family Phasianidae
Coturnix Garsault, 1764
Pternistis Wagler, 1832
Gallus Brisson, 1760
Order Columbiformes
Family Columbidae
Columba Linnaeus, 1758
Streptopelia Bonaparte, 1855
Treron Vieillot, 1816
Order Cuculiformes
Family Cuculidae
Chrysococcyx Boie, F., 1826
Order Caprimulgiformes
Family Apodidae
Zoonavena Mathews, 1918
Apus Scopoli, 1777
Cypsiurus Lesson, R., 1843
Order Gruiformes
Family Rallidae
Paragallinula Sangster, Garcia-R &
Trewick, 2015
Species/subspecies
S
A
N. meleagris (Linnaeus, 1758)
I
I
C. delegorguei histrionica
(Hartlaub, 1849)
P. afer (Müller, PLS, 1776)
G. gallus (Linnaeus, 1758)
S
C. livia Gmelin, 1789
C. thomensis Bocage, 1888
C. malherbii Verreaux & Verreaux,
1851
C. larvata inornata (Reichenow,
1892)
C. l. principalis (Hartlaub, 1866)
C. l. simplex (Hartlaub, 1849)
S. senegalensis (Linnaeus, 1766)
T. sanctithomae (Gmelin, 1789)
T. calvus virescens Amadon, 1953
P
I
I
I
E
I
E
E
E
S
E
E
I
E
I
S
C. cupreus insularum Moreau &
Chapin, 1951
S
S
Zoonavena thomensis (Hartert,
1900)
A. affinis bannermani Hartert, 1928
C. parvus (Lichtenstein, 1823)
E
E
S
I
S
I
P. angulata (Sundevall, 1851)
?
?
S
(continued)
21
The Avifauna of the Gulf of Guinea Oceanic Islands
Higher taxonomy
Gallinula Brisson, 1760
Order Charadriiformes
Family Scolopacidae
Numenius Brisson, 1760
Actitis Illiger, 1811
Tringa Linnaeus, 1758
Family Laridae
Anous Stephens, 1826
Onychoprion Wagler, 1832
Order Phaethontiformes
Family Phaethontidae
Phaethon Linnaeus, 1758
Order Procellariiformes
Family Oceanitidae
Hydrobates Boie, F., 1822
Order Suliformes
Family Sulidae
Sula Brisson, 1760
Family Phalacrocoracidae
Microcarbo Bonaparte, 1856
Order Pelecaniformes
Family Ardeidae
Egretta T. Forster, 1817
Bubulcus Bonaparte, 1855
Butorides Blyth, 1852
Family Threskiornithidae
Bostrychia G. R. Gray, 1847
Order Accipitriformes
Family Accipitridae
Milvus Lacépède, 1799
Order Strigiformes
Family Tytonidae
Tyto Billberg, 1828
Family Strigidae
Otus Pennant, 1769
581
Species/subspecies
G. chloropus (Linnaeus, 1758)
P
R
S
R
A
R
N. phaeopus (Linnaeus, 1758)
A. hypoleucos (Linnaeus, 1758)
T. nebularia (Gunnerus, 1767)
M
M
M
M
M
M
M
A. stolidus (Linnaeus, 1758)
A. minutus Boie, F., 1844
O. fuscatus (Linnaeus, 1766)
O. anaethetus (Scopoli, 1786)
B
B
B
?
B
?
?
?
B
B
?
B
P. lepturus Daudin, 1802
P. aethereus Linnaeus, 1758
B
?
B
B
H. cf. castro (Harcourt, 1851)
S. leucogaster (Boddaert, 1783)
?
B
Microcarbo africanus (Gmelin,
J. F., 1789)
B
?
R
E. gularis (Bosc, 1792)
B. ibis (Linnaeus, 1758)
B. striata (Linnaeus, 1758)
R
R
R
B. olivacea rothschildi (Bannerman,
1919)
B. bocagei Chapin, 1923
X
M. migrans (Boddaert, 1783)
R
R
R
R
R
E
R
T. alba thomensis (Hartlaub, 1852)
S
O. hartlaubi (Giebel, 1849)
O. senegalensis feae (Salvadori,
1903)
Otus sp. nov.
E
S
E
(continued)
582
M. Melo et al.
Higher taxonomy
Order Coraciiformes
Family Alcedinidae
Corythornis Kaup, 1848
Halcyon Swainson, 1821
Ceryle F. Boie, 1828
Order Psittaciformes
Family Psittaculidae
Agapornis Selby, 1836
Family Psittacidae
Psittacus Linnaeus, 1758
Order Passeriformes
Family Oriolidae
Oriolus Linnaeus, 1766
Family Dicruridae
Dicrurus Vieillot, 1816
Family Monarchidae
Terpsiphone Gloger, 1827
Family Laniidae
Lanius Linnaeus, 1758
Family Cisticolidae
Prinia Horsfield, 1821
Family Hirundinidae
Hirundo Linnaeus, 1758
Family Sylvidae
Sylvia Scopoli, 1769
Family Zosteropidae
Zosterops Vigors & Horsfield, 1827
Family Sturnidae
Onychognathus Hartlaub, 1849
Lamprotornis Temminck, 1820
Family Turdidae
Turdus Linnaeus, 1758
Species/subspecies
C. cristatus thomensis (Salvadori,
1902)
C. cristatus nais (Kaup, 1848)
H. malimbica dryas Hartlaub, 1854
C. rudis (Linnaeus, 1758)
P
S
S
S
S
?
A. pullarius (Linnaeus, 1758)
P. erithacus princeps Alexander,
1909
I
S
I
O. crassirostris Hartlaub, 1857
D. modestus modestus Hartlaub,
1849
E
S
T. atrochalybeia (Thomson, 1842)
T. rufiventer smithii (Fraser, 1843)
E
L. newtoni Bocage, 1891
E
P. molleri Bocage, 1887
E
H. rustica (Linnaeus, 1758)
M
S
S. dohrni (Hartlaub, 1866)
E
Z. ficedulinus Hartlaub, 1866
Z. griseovirescens Bocage, 1893
Z. feae Salvadori, 1901
Z. lugubris (Hartlaub, 1848)
Z. leucophaeus (Hartlaub, 1857)
E
O. fulgidus fulgidus (Hartlaub,
1849)
L. splendidus (Vieillot, 1822)
L. ornatus (Daudin, 1800)
T. xanthorhynchus Salvadori, 1901
T. olivaceofuscus Hartlaub, 1852
A
E
E
E
E
S
R
E
E
E
(continued)
21
The Avifauna of the Gulf of Guinea Oceanic Islands
Higher taxonomy
Family Nectariniidae
Anabathmis Reichenow, 1905
Dreptes Illiger, 1811
Cyanomitra Reichenbach, 1853
Family Ploceidae
Ploceus Cuvier, 1816
Quelea Reichenbach, 1850
Euplectes Swainson, 1829
Family Estrildidae
Nigrita Strickland, 1843
Estrilda Swainson, 1827
Uraeginthus Cabanis, 1851
Spermestes Swainson, 1837
Family Viduidae
Vidua Cuvier, 1816
Family Motacillidae
Motacilla Linnaeus, 1758
Family Fringillidae
Crithagra Swainson, 1827
a
583
Species/subspecies
P
A. hartlaubii (Hartlaub, 1857)
A. newtonii (Bocage, 1887)
D. thomensis (Bocage, 1889)
C. olivacea (Smith, 1840)
E
S
E
E
R
P. princeps (Bonaparte, 1851)
P. velatus Vieillot, 1819
P. cucullatus (Müller, 1766)
P. grandis (G. R. Gray, 1844)
P. sanctithomae (Hartlaub, 1848)
Q. erythrops (Hartlaub, 1848)
E. hordeaceus (Linnaeus, 1758)
E. aureus (Gmelin, 1789)
E. albonotatus (Cassin, 1848)
E
N. bicolor (Hartlaub, 1844)
E. astrild (Linnaeus, 1758)
U. angolensis (Linnaeus, 1758)
S. cucullata (Swainson, 1837)
R
I
I
I
E
E
?
I
I
I
I
I
I
I
V. macroura (Pallas, 1764)
I
Motacilla bocagii (Sharpe, 1892)
E
C. mozambica (Müller, 1776)
C. rufobrunneaa (Gray, 1862)
C. concolor (Bocage, 1888)
A
I
I
E
E
C. rufobrunnea is represented by three endemic subspecies (Table 21.3)
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Chapter 22
Current Knowledge and Conservation
of the Wild Mammals of the Gulf of Guinea
Oceanic Islands
Ana Rainho, Christoph F. J. Meyer, Sólveig Thorsteinsdóttir, Javier Juste,
and Jorge M. Palmeirim
Abstract Oceanic islands are usually difficult for mammals to colonize; consequently, the native mammal fauna is typically species-poor, often consisting of just a
few species of bats. The oceanic islands of the Gulf of Guinea are no exception to
this pattern. Still, the known mammal richness is relatively high for the small size of
the islands. Out of a total of 13 native species, including 11 bats and 2 shrews, at
least 7 species and 3 subspecies are single-island endemics. In addition to native
species, at least 6 other wild mammals have been introduced to the islands purposely
or accidentally by humans. Some of these are among the world’s most notorious
invasive species and cause damage to native species, ecosystems, and humans.
Predation by exotic species can threaten native island mammals, which are especially sensitive due to their small populations and limited ranges. These impacts are
likely worsened by other threats, such as forest degradation and climate change, and
a general lack of knowledge about the natural history of most species also hampers
the implementation of conservation measures. Therefore, fostering further research
on the endemic-rich mammal fauna of these islands is vital to ensure their
persistence.
A. Rainho (*) · S. Thorsteinsdóttir · J. M. Palmeirim
Center for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências,
Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon,
Portugal
e-mail: amrainho@fc.ul.pt
C. F. J. Meyer
Environmental Research and Innovation Centre, School of Science, Engineering and
Environment, University of Salford, Salford, UK
J. Juste
Department of Evolutionary Biology, Estación Biológica de Doñana (CSIC), Seville, Spain
CIBER de Epidemiología y Salud Pública (CIBERESP), Instituto de Salud Carlos III, Madrid,
Spain
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_22
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Keywords Annobón · Introduced species · Islands · Mammals · Príncipe · São
Tomé
Introduction
Large expanses of ocean are often extreme barriers to mammal dispersal, and even
some bat species are known to be reluctant to fly over open bodies of water (Castella
et al. 2000). Therefore, it is not surprising that oceanic islands typically host a small
number of native mammals, usually only a few species of bats (Whittaker and
Fernández-Palacios 2007). How non-flying mammals overcome this obstacle to
naturally reach oceanic islands is a controversial topic. The most frequent explanation, natural rafting, makes assumptions that sometimes seem impossible to meet,
particularly in the case of small animals with high metabolic rates and freshwater
requirements (Ali and Vences 2019; Mazza et al. 2019). In addition, as humans
colonized oceanic islands, they usually brought with them a large number of
mammal species, which often came to exceed the number of native mammals
(Tennyson 2010). As a result of this process, humans have caused the extinction
of several mammals native to oceanic islands and also biotic homogenization
(Longman et al. 2018).
The oceanic islands of the Gulf of Guinea are an excellent example of these
processes of natural and human-mediated colonization. Considering the small size of
the islands, they host a surprisingly large number of mammal species. Of the
19 known wild species (Appendix), 13 are native and, of these, at least 7 species
and 3 subspecies are single-island endemics. Most endemic and native species are
bats (Juste and Ibáñez 1994a; Rainho et al. 2010), but there are also two endemic
shrews (Bocage 1887; Ceríaco et al. 2015). Their presence on oceanic islands at such
a long distance from the mainland is still puzzling (Heim de Balsac and Hutterer
1982; Ceríaco et al. 2015). Even with the potential ability to use torpor in situations
of food scarcity (McKechnie and Mzilikazi 2011), shrews would have had substantial limitations to obtain freshwater during the long dispersal trip to the islands.
Furthermore, the number of reproducing individuals reaching the islands would be
expected to be far too small to sustain a viable population.
The remaining six species of mammals were introduced by humans (Dutton
1994), either purposely or accidentally. Two of these, the house mouse Mus
musculus Linnaeus 1758 and the ship rat Rattus rattus (Linnaeus, 1758), are
among the 100 worst invasive species globally, due to the impacts they cause on
ecosystems when they are introduced (Lowe et al. 2000). Thus, their abundance on
the Gulf of Guinea islands is concerning for the native flora and fauna. Although
there are also domestic and feral mammals on these islands, such as dogs, cats, pigs,
goats, cows, horses, and others that might have arrived at the islands more recently,
these species will not be addressed in detail in this chapter.
Knowledge is the basis of conservation, and this chapter aims to compile the
information available to date on the species of wild mammals that occur on the
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islands of Príncipe, São Tomé, and Annobón. Threats to endemic and native species
and knowledge gaps will also be discussed.
A Brief History of Mammal Research
Records of the presence of mammals on the oceanic islands of the Gulf of Guinea
date to the first manuscripts of the first Portuguese travelers to these islands. An
example of this is the excerpt presented by Sousa (1888) of a manuscript entitled
“Da viagem de dom Francisco d’Almeyda primeiro visorey da Índia” [The journey
of Dom Francisco d’Almeyda, India’s first viceroy] dated ca. 1505. In this text, it is
mentioned that “n’esta ilha ha gatos d’algalia que criam que fugiram aos
armadores que trouxerom da terra firme” [on this island there are breeding civets
that fled from the shipowners who brought them from the mainland] confirming the
presence of the African civet Civettictis civetta (Schreber, 1776) in São Tomé
already at the beginning of the sixteenth century.
More systematic surveys of mammals began much later. During the nineteenth
century, Richard Greeff visited São Tomé and Rolas Islet between 1879 and 1880.
Although this expedition did not focus on mammals, it confirmed the presence of
two bat species Cynonycteris stramineus—currently Eidolon helvum (Kerr, 1792)—
and Phyllorhina caffra—currently Hipposideros ruber (Noack, 1893). Greeff also
confirmed the presence of the least weasel Mustela nivalis Linnaeus 1766 in São
Tomé, based on a specimen found in the digestive tract of a cobra-preta Naja
(Boulengerina) peroescobari Ceríaco et al. 2017 (Greeff 1884; Bocage 1905).
These observations were further confirmed by A. F. Nogueira who also listed
monkeys, bats, civets, weasels, and many rats in São Tomé (Nogueira 1885). In
1885, a botanical survey of São Tomé led by Adolpho F. Möller was commissioned
by the Botanical Gardens of the University of Coimbra. Although focusing on
botanical matters, some animal specimens were also collected. A list published by
L. Vieira (1886) included mona monkey Cercopithecus mona (Schreber, 1774),
Viverra civetta (currently C. civetta), Cynonycteris stramineus (currently E. helvum),
Phyllorhina caffra (currently H. ruber), Mus ducomanus (currently Rattus
norvegicus (Berkenhout, 1769)), Mus rattus (currently Rattus rattus), and Mus
musculus.
Between 1885 and 1895, Francisco Newton was hired by the National Museum
of Lisbon to conduct a zoological survey in the Gulf of Guinea. This survey included
all the Gulf of Guinea islands, being the first known zoological survey in Annobón
(Peris 1961). The mammal specimens were studied by J. V. Barbosa du Bocage, at
the time director and curator of Zoology at the National Museum of Lisbon, resulting
in several papers describing new species for the islands (see Bocage 1905). Such was
the case of the São Tomé shrew Crocidura thomensis (Bocage, 1887), Newton’s
long-fingered bat Miniopterus newtoni Bocage 1889, the São Tomé horseshoe bat
Phyllorhina (Commersoni) thomensis (currently Macronycteris thomensis (Bocage,
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1891)) and the São Tomé collared fruit bat Cynonycteris brachycephala (currently
Myonycteris brachycephala (Bocage, 1889)).
In 1954, a scientific expedition to São Tomé was undertaken by researchers from
the Centro de Zoologia da Junta de Investigação do Ultramar. A report lists the bat
specimens collected during this expedition (Lopes and Crawford-Cabral 1992),
deposited in the collection of the Portuguese Institute of Scientific and Tropical
Research. In 1955, Father Aurelio Basilio remained in Annobón for 3 months,
reporting the presence of R. norvegicus for the first time on this island (Peris 1961).
During the 1970s, the French zoologist Henri Heim de Balsac took advantage of
the presence of Father René de Naurois on the islands and asked him to collect
pellets of Barn owl Tyto alba (Scopoli, 1769) during his ornithological surveys.
Heim de Balsac believed that this would be an easy way to identify the spectrum of
micromammals present on the island. Despite the high number of pellets collected,
the diet of the barn owl proved to be composed essentially of ship rats R. rattus, and
other than those, only one bird and one house mouse were found. Further efforts
were made, and finally, some shrews were captured in São Tomé by R. Naurois, and
in Príncipe by R. Naurois and Daniel Nunez, confirming the presence of Crocidura
thomensis in São Tomé and identifying the species present in Príncipe as C. poensis
(Fraser, 1843) (Heim de Balsac and Hutterer 1982). This mammal family was further
reviewed by John Dutton and Jan Haft, based on the results of three expeditions, two
German and one British, that visited São Tomé between 1989 and 1991 (Atkinson
et al. 1994; Dutton and Haft 1996).
During the early 1990s, bats were the focus of Spanish investigators who started
working in this region. This team made a massive contribution to the knowledge of
this group, publishing several papers focusing on bat taxonomy (Juste and Ibáñez
1992, 1993b; Juste et al. 2007), morphology, and genetics (Juste and Ibáñez 1993a;
Juste et al. 1996, 2000) and even echolocation (Guillén et al. 2001). They also
described one new species, the São Tomé free-tailed bat Chaerephon tomensis (Juste
and Ibáñez, 1993) and discovered the presence of an undescribed pipistrelle of the
genus Pseudoromicia Monadjem et al. 2020 in Príncipe (Juste and Ibáñez 1993c,
1994a).
During the first decade of the twentieth century, bats were again the focus of
research on the islands. In 2002, a study of the abundance of E. helvum in Príncipe
was carried out by a team of English researchers (Dallimer et al. 2006). In 2010, a
team from the University of Lisbon studied the status and distribution of bats on São
Tomé (Rainho et al. 2010), adding a new species for São Tomé, the tricolored
mouse-eared bat Myotis cf. tricolor (Temminck, 1832). In 2012, Peel and colleagues
published a study on the persistence of several viruses on the isolated population of
E. helvum in Annobón (Peel et al. 2012).
Among the studies published recently, it is worth highlighting the reviews on the
species of Crocidura in São Tomé (de Lima et al. 2016) and Príncipe (Ceríaco et al.
2015), the latter describing the shrew of Príncipe as Crocidura fingui Ceríaco et al.
2015, and demonstrating that it is endemic to the island. Ecological studies have also
included information on the mammals of the oceanic islands of the Gulf of Guinea;
for example, studies on the hunting of wild species in São Tomé (Carvalho et al.
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2015a, b; Hayman and Peel 2016), and the study of seed dispersal networks on this
island (Mendes 2017; Coelho 2018; Heleno et al. 2021). Studies of broader geographical scope also addressed some mammal species from the Gulf of Guinea
islands. This is the case of the work by Peel and colleagues (e.g., Shi et al. 2014;
Peel et al. 2016, 2017), who studied ecology, traits, genetics, and possible zoonosis
associated with E. helvum, and hypothesized on colonization and movements of this
species between the islands. Rodrigues and colleagues (2017) have investigated the
origin and process of invasion of the least weasel on the Atlantic islands, including
São Tomé. Finally, a recent expedition was carried out in 2019 by a team from the
University of Lisbon on the bats of Príncipe Island (JMP and ST, pers. obs). Their
main results are included in the following sections of this chapter.
Current State of Knowledge
Order Primates
Family Cercopithecidae
Only one species of non-human primate occurs on the islands. The mona monkey
was introduced in São Tomé and Príncipe 150–500 years ago (Glenn and Bensen
2013). The reason for its introduction is not fully known, but it is possible that it was
used as food by enslaved plantation workers or, more likely, sailors and slavers kept
them as pets (Denham and Denham 1987). The mona monkey was also introduced
on the Caribbean island of Grenada, with animals originating from São Tomé and
Príncipe (Glenn and Bensen 2013). No reference was found to the historical or
contemporary presence of monkeys in Annobón.
The mona monkey is a forest species native to West Africa. Once common across
its native range, it has become rare and even extirpated in some areas due to habitat
loss and over-hunting by humans (Goodwin et al. 2020). Where it is still common, its
densities vary between 15 and 49 ind/km2 (Glenn et al. 2014). It is common on the
islands, with estimates of 19 ind/km2 in São Tomé and 21 ind/km2 in Príncipe
(Glenn 1998; Glenn et al. 2014), even though it is also hunted for human consumption on both islands (Carvalho et al. 2015a). The mona monkey is considered a
generalist because it uses various types of forest, has a very diverse diet, and has
been successful in colonizing forests outside its native range (Glenn et al. 2014). In
Príncipe, this species seems to be particularly abundant in the transition zones
between the forest and the agricultural areas where food is plentiful (JMP pers.
obs. and Filipa Soares pers. comm.). It mainly feeds on fruits and arthropods but also
eats leaves, flowers, small lizards, and bird eggs and chicks (Glennet al. 2014). Mona
monkeys are among the introduced species that may affect the seed dispersal
networks on São Tomé because they favor plant species with large fruits and seeds
(Heleno et al. 2021). They are often regarded as agricultural pests. Dutton (1994)
mentioned that they can impact forest regeneration, and Carvalho et al. (2015a)
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suggested that monkeys can potentially become significant predators of small
vertebrates, particularly of endemic birds that have low resilience and small
populations. Their predation of bird nests has recently been confirmed (Guedes
et al. 2021), but further work is required to determine the impacts on bird
populations.
Order Rodentia
Family Muridae
São Tomé and Príncipe support populations of all three introduced murid rodents in
Africa: the ship rat, the brown rat, and the house mouse. Both the house mouse and
the brown rat occur and are abundant also on Annobón (Bocage 1893; Peris 1961;
Jones and Tye 2005; Fry 2008; Martim Melo pers. comm.).
These commensal species may have reached the islands as stowaways in boats
arriving from Europe. The ship rat and the house mouse are likely to have been
accidentally introduced with the arrival of Portuguese ships to the islands during the
fifteenth century. According to Dutton (1994), the brown rat only reached the islands
during the eighteenth century, when it became abundant in the ports of western
Europe (Atkinson 1985).
Given their invasive character, even in mainland Africa (Denys et al. 2009;
Dalecky et al. 2015), these three species are likely to occur across the three islands
and to be most abundant in anthropogenically-modified environments. Atkinson
(1994) confirmed the presence of all three rodents around villages in São Tomé
and referred to the occurrence of rats at the margins of the primary forest and in the
secondary forest along the Quija River. They also highlighted the capture of several
young brown rats in Lagoa Amélia and Morro Esperança (Atkinson et al. 1994). A
recent pilot study was performed in São Tomé, confirming the presence and high
abundance of ship rats throughout the island, while recording only one brown rat in
the capital city (Ward-Francis et al. 2017). Ship rats seem to be abundant in Príncipe
(Fundação Príncipe 2019, Martim Melo pers. comm.), where the presence of brown
rats has recently been confirmed in the south of the island (JMP and ST pers. obs.).
These species can also be a problem to the human inhabitants of the islands. For
instance, in 2004, the farmers of Annobón faced huge crop damages caused by an
overabundance of rats on the island (Martim Melo pers. comm.).
Other Species
In 2019, a non-identified rodent was observed and photographed at Lagoa Amélia on
São Tomé island (Fig. 22.1, 1; Leonel Viegas and Francisco Alamô pers. comm.).
The overall external morphology of the observed individual (reddish fur, long snout,
black dorsal stripe, long tail) suggests it may belong to the sub-Saharan genus
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Fig. 22.1 Some of the poorly known mammal species of the islands of the Gulf of Guinea: (1)
Small rodent probably belonging to the genus Dendromus; (2) Hypsignathus monstrosus; (3)
Myotis cf. tricolor; (4) Pseudoromicia sp., a novel species occurring in Príncipe; (5) Crocidura
thomensis; (6) Myonycteris brachycephala; (7) Miniopterus newtoni; (8) Civettictis civetta. Photo
credits: (1) Leonel Viegas, (3, 7) Ana Rainho, (4) Jorge Palmeirim and Sólveig Thorsteinsdóttir, (5)
Ricardo de Lima, (6) Javier Juste, (2, 8) unknown photographer
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Dendromus Smith, 1829 (Family Nesomydae). This is a tentative identification, by
no means conclusive, particularly taking into consideration the confusion that still
prevails in the field of African rodent taxonomy and the frequent lack of external
morphological characters separating taxa (Monadjem et al. 2015). Further research is
necessary to clarify the identity, distribution, and natural history of this species.
Order Eulipotyphla
Family Soricidae
Two species of shrew are known to occur on the oceanic islands of the Gulf of
Guinea: the São Tomé white-toothed shrew Crocidura thomensis (Fig. 22.1, 5)
endemic to São Tomé, and the Príncipe White-Toothed Shrew Crocidura fingui
endemic to Príncipe (Heim de Balsac and Hutterer 1982; Dutton and Haft 1996;
Ceríaco et al. 2015; de Lima et al. 2016). No shrews have been found on Annobón
(Heim de Balsac and Hutterer 1982).
Crocidura thomensis was described by Bocage (1887) based on a specimen
captured by Francisco Newton in 1886 at Roça Minho. A few years later, it was
also captured by Newton and António Lobo de Almada Negreiros at Santa Maria and
another unknown location (Bocage 1905). By the end of the twentieth century, the
species had been recorded from fewer than ten locations (Dutton and Haft 1996).
Recent data suggest, however, that it may not be as rare as initially suspected.
Without directed sampling effort, this species was recorded 23 times in 15 new
locations in recent years (de Lima et al. 2016). It seems to be widely distributed,
occurring from near sea level to high mountainous areas (Fig. 22.2), inhabiting
humid areas across a variety of habitats ranging from mist forests to lowland
plantations (Dutton and Haft 1996; de Lima et al. 2016). The use of humid habitats
may result from the higher availability of arthropod prey (Dutton and Haft 1996;
de Lima et al. 2016). Crocidura thomensis is listed as Endangered in the IUCN Red
List of Threatened Species (Kennerley 2016). This status is due to its reduced extent
of occurrence and the continuing decline in the extent and quality of the available
habitat. Other possible threats are predation by introduced species, use of pesticides,
and agricultural intensification (Dutton and Haft 1996; de Lima et al. 2016). If
confirmed, the dependence on humid habitats may make this species vulnerable to
climate change (de Lima et al. 2016).
The taxonomic status of the shrew species occurring in Príncipe has undergone
several changes since its first records. It was first identified as C. thomensis by
Bocage (1887) based on a specimen captured by F. Newton at Oquê Nazareth in
1894. A century later, Heim de Balsac and Hutterer (1982) identified the species as
C. poensis, a species also occurring in West Africa, based on 12 new specimens (plus
4 young) captured on the island by R. de Naurois and Daniel Nunez. Four other
individuals were captured in 2013 (Ceríaco et al. 2015). The morphological and
molecular analysis of these latter specimens led Ceríaco et al. (2015) to conclude that
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Fig. 22.2 Locations where different wild mammal species were recorded on the island of São
Tomé. Sources: Lopes and Crawford-Cabral (1992), Juste and Ibáñez (1994a), Rainho et al. (2010),
de Lima et al. (2016), Peel et al. (2017), and ACR (2020)
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Fig. 22.3 Locations where different wild mammal species were recorded on the islands of Príncipe
and Annobón. Sources: Lopes and Crawford-Cabral (1992), Juste and Ibáñez (1994a), Ceríaco et al.
(2015), Peel et al. (2017), ACR (2020), Juste (2020), and JMP and ST (pers. obs.)
this is indeed a distinct species, endemic to Príncipe, that they named C. fingui.
Based on molecular clock estimates, this island endemic diverged from the CentralEast African lineage of C. poensis ~1.0–1.2 Ma (Nicolas et al. 2019). The distribution of C. fingui has not been studied, but so far, it has only been recorded in the
northern part of the island (Fig. 22.3). It seems to be versatile in terms of habitat,
occurring both near human settlements and in forest (Ceríaco et al. 2015). Due to the
lack of knowledge about the distribution of this species, its ecological requirements,
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and potential threats, it is listed as Data Deficient in the IUCN Red List of Threatened
Species (Ceríaco et al. 2019).
Order Chiroptera
Family Pteropodidae
Three species of fruit bats occur in the oceanic islands of the Gulf of Guinea. In
2019, photos of a fourth species, a male hammer-headed bat Hypsignathus
monstrosus H. Allen, 1862, allegedly captured in the town of São Tomé, appeared
on social media (Fig. 22.1, 2). Since we have not been able to collect more
information, we refrain from commenting on this observation.
The conspicuous and noisy African straw-colored fruit bat, Eidolon helvum, is the
largest bat and probably one of the most abundant native mammals on the islands.
Dallimer et al. (2006) estimated the density of this species on Príncipe at between
82 and 111 ind/km2. Peel et al. (2017) produced a slightly higher estimate for
Príncipe at between 156 and 159 ind/km2 and estimated a density between 94 and
176 ind/km2 for Annobón. All estimates show that this species reaches densities
similar to those found in mainland Africa (Dallimer et al. 2006). Eidolon helvum is
commonly seen flying with slow strokes high above the canopy in forests, plantations, and even city gardens and orchards, foraging on native and planted fruits (all
authors, pers. obs.).
Eidolon helvum is migratory on the African mainland, where it is considered
monotypic despite its broad distribution (O’Toole 2019). Conversely, all three island
populations are considered non-migratory (Juste et al. 2000; Peel et al. 2016, 2017).
The populations of E. helvum from São Tomé, Príncipe, and Annobón show genetic
differentiation in a clear geographic pattern (Peel et al. 2013). Genetic and demographic analyses provide evidence that E. helvum of Príncipe and São Tomé are
broadly part of the same genetic population cluster, though dispersal between the
islands is rare (Juste et al. 2000; Peel et al. 2013). By contrast, the Annobón
population is recognized as a taxonomically distinct entity (E. helvum annobonense
Juste et al. 2000). It exhibits island dwarfism, with individuals being significantly
smaller than those of the other two islands (Juste et al. 2000; Peel et al. 2016, 2017).
Despite its high density on the Gulf of Guinea islands, E. helvum was classified as
Vulnerable on São Tomé because of its reduced range and habitat degradation
(Rainho et al. 2010). Moreover, it is hunted in large numbers on São Tomé (Carvalho
et al. 2015b; Hayman and Peel 2016; Peel et al. 2017) and on Príncipe (Hayman and
Peel 2016, JMP and ST pers. obs.). Hayman and Peel (2016) quantified the effects of
hunting on the demographic structure of the population on São Tomé but did not find
detrimental impacts on Príncipe. Increased hunting pressure may result in the
unsustainable exploitation of this species, a problem compounded by the frequent
disturbance of its colonies (Rainho et al. 2010; Peel et al. 2017). Globally, E. helvum
is Near Threatened on the IUCN Red List due to a significant decline of its
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population and over-harvesting, making this species close to qualifying for Vulnerable status (Cooper-Bohannon et al. 2020).
The Egyptian rousette, Rousettus aegyptiacus (Geoffroy, 1810), is found on
Príncipe and São Tomé islands (Figs. 22.2 and 22.3). The genus Rousettus Gray
1821 is unique among Old World fruit bats for its echolocation capacity (Holland
et al. 2004; Table 22.1), allowing roosting in total darkness in caves and buildings.
The populations on Príncipe and São Tomé are clearly differentiated morphologically and genetically from other African forms and recognized as endemic at
subspecies rank (Juste and Ibáñez 1993b). These two subspecies represent classic
examples of island dwarfism in the case of R. aegyptiacus princeps Juste and Ibáñez
1993 on Príncipe and gigantism by R. aegyptiacus tomensis Juste and Ibáñez 1993
on São Tomé (Juste and Ibáñez 1993b; Juste et al. 1996). Still, both forms share
features (like their massive dentition) that point to a common evolutionary history
(Juste and Ibáñez 1993b). Rousettus aegyptiacus is a cave-dwelling species that
forages in multiple habitats on the islands, feeding on native and cultivated fruits
(Rainho et al. 2010). On São Tomé, it was observed sharing a roost with H. ruber
and M. newtoni in a large marine cave (Rainho et al. 2010). On Príncipe, a small
colony was found roosting in a cliff in Pico Papagaio (Juste 1990). Rousettus
a. tomensis is listed as Vulnerable because of its small range and projected habitat
degradation (Rainho et al. 2010). Although harvested for human consumption, it
remains relatively common on both Príncipe and São Tomé (Rainho et al. 2010; JMP
and ST pers. obs). However, an increase in harvesting, aggravated by the disturbance
of the colonies in their roosts, may become a threat (Rainho et al. 2010).
A third fruit bat species, the São Tomé collared fruit bat Myonycteris
brachycephala (Fig. 22.1, 6) is only found on São Tomé (Fig. 22.2). This endemic
species is unique in having lost a lower incisor, hence displaying the only asymmetrical dental formula known in any mammal (Juste and Ibáñez 1993a). It is very
elusive, and despite netting efforts, it is only known from two localities beyond the
type locality (Cascata, São Tomé), both in a rugged landscape, one (Morro Palmira)
in montane forest and the other (Belavista) in lowland cocoa plantations (Juste and
Ibáñez 1994a). It is considered Endangered (Juste 2016).
Family Hipposideridae
The family Hipposideridae comprises many insectivorous species spread throughout
the Old World tropics, all featuring a highly complex leaf-nose. The oceanic islands
of the Gulf of Guinea host two species: Hipposideros ruber and Macronycteris
thomensis. The latter is endemic to São Tomé and was described by Bocage (1891)
based on specimens from Ribeira Peixe and Roça Saudade. It is a large microbat
(forearm (FA) ~85 mm, weight ~56 g) and is part of a group of leaf-nosed bat species
that were recently moved from the genus Hipposideros to Macronycteris (Foley
et al. 2017). Very little is known about the biology of this species; however, it is
presumably somewhat similar to that of M. gigas (Wagner, 1845), a close relative
present on Bioko (Juste and Ibáñez 1994a) and the adjacent mainland (Happold
22
Species
Rousettus aegyptiacus
Hipposideros ruber
Macronycteris thomensis
Myotis cf. tricolor
Miniopterus newtoni
Taphozous mauritianus
Chaerephon pumilus
Chaerephon sp.
Fmin
(kHz)
9.3 2.4
4.1–11.9
139.7 0.2
139.3–139.8
66.0 0.8
64.3–66.8
39.3 2.0
36.6–41.6
50.3 1.3
47.8–52.2
24.2 0.7
23.4–25.2
24.9 2.7
19.8–29.4
21.0 1.1
19.0–22.4
Fmax
(kHz)
110.5 48.0
44.0–150.0
141.5 0.4
140.8–141.9
68.0 1.0
66.8–70.2
117.3 3.3
112.0–120.8
101.7 16.7
69.6–119.0
31.9 0.6
31.4–32.5
36.0 8.7
24.7–51.5
23.0 1.1
20.4–25.5
FmaxE
(kHz)
–
140.9 0.3
140.4–141.1
67.2 0.4
66.4–68.0
78.4 2.1
76.4–81.8
55.9 2.7
53.2–61.0
28.3 0.2
28.1–28.4
28.4 2.3
23.4–31.5
22.1 1.0
19.9–24.1
Duration (ms)
0.33 0.12
0.2–0.5
5.9 0.2
5.7–6.1
20.7 4.0
15.6–28.6
1.84 0.1
1.74–1.92
4.8 2.1
2.3–7.8
14.8 1.7
12.8–16.8
13.6 3.0
8.1–18.6
16.3 1.7
12.7–19.9
Interval
(ms)
122.5 28.7
81.7–165.0
14.1 4.2
10.4–22.1
66.8 17.4
43.2–106.4
82.7 16.2
58.4–102.6
61.4 23.6
31.8–105.7
77.4 6.4
70.7–86.4
258.4 156.5
62.8–472.0
350.7 97.2
137.0–558.5
N
8
6
10
5
14
5
32
26
Values indicate mean, standard deviation and range of observed values. Fmin, minimum pulse frequency; Fmax, maximum pulse frequency; FmaxE, maximum
energy frequency. Note that the values indicated for Chaerephon sp. may refer to Chaerephon pumilus or another species of the same genus (e.g., Ch. tomensis)
Adapted from Rainho et al. (2010)
Current Knowledge and Conservation of the Wild Mammals of the Gulf. . .
Table 22.1 Characteristics of the echolocation calls of different bat species present in São Tomé
605
606
A. Rainho et al.
2013a; Foley et al. 2017). Macronycteris thomensis looks like a dwarf form of
M. gigas. A colony of several hundred individuals was found in an underground
roost, and a single individual was observed roosting under the leaves of a palm tree.
It is common throughout the island but much less so than H. ruber (Rainho et al.
2010).
Hipposideros ruber is a small leaf-nosed bat (FA ~50 mm, weight ~11 g) with
two very distinct color forms: dull brown and orange. The species is part of a species
complex present across much of Africa (Patterson et al. 2019) and is common
throughout Príncipe and São Tomé. On both islands, the species is mostly associated
with primary and secondary forests, but it is also present in other ecosystems. On São
Tomé, it seems to be somewhat less common in the dryer northeast of the island than
in the well-forested and humid center and south (Rainho et al. 2010). It uses a wide
variety of roost types and has been found in caves and abandoned buildings on
Príncipe (JMP and ST pers. obs.). On São Tomé, in addition to these types of roosts,
it uses artificial tunnels (Rainho et al. 2010). On the mainland, it is known to also
roost in tree hollows (Happold 2013b) and likely does so on the islands as well.
Hipposideros ruber has very broad wings and highly maneuverable flight, capable of
foraging by hawking and gleaning in cluttered forest habitats (Happold 2013b). Both
foraging behaviors have been observed on the islands. Its diet has not been studied
on São Tomé or Príncipe, but on the mainland, it feeds on a variety of insects,
including beetles, moths, dipterans, and isopterans (Happold 2013b). An unusual
feature of the population of H. ruber on São Tomé is its daytime flying habits.
Although most of its activity takes place during the night, it is common to find this
bat flying and foraging in the forest during the day (Russo et al. 2011). São Tomé and
Príncipe populations produce constant frequency (CF) calls that are typical for the
family and include two harmonics, where the second and higher-pitched one is the
information carrier (Guillén et al. 2001). The resting frequency is the same as that
reported for bats from the mainland and averaged 136.6 and 136.1 kHz for females
and 139.7 and 136.7 kHz for males on São Tomé and Príncipe, respectively (Guillén
et al. 2001). Although H. ruber is classified as Least Concern globally (Monadjem
et al. 2017), it was considered Near Threatened in São Tomé due to the probable
decline in the number of individuals and colonies resulting from the reduction of
roost availability (Rainho et al. 2010).
Family Emballonuridae
The Mauritian Tomb bat Taphozous mauritianus (Geoffroy Saint-Hilarie, 1818) is
the only emballonurid species known to be present on the Gulf of Guinea oceanic
islands. This species, originally described from the island of Mauritius, is quite
common across sub-Saharan Africa (Bonaccorso 2019). As an open-space forager,
T. mauritianus is quite good at colonizing islands (Bonaccorso 2019). In mainland
Africa, its diet consists of aerial insects such as Lepidoptera, Isoptera, and
Coleoptera (Dengis 1996 and references therein). It typically roosts at the base of
the crown of leaves in coconut trees. It was found at several sites along the northern
22
Current Knowledge and Conservation of the Wild Mammals of the Gulf. . .
607
coast of São Tomé (Fig. 22.2) and is presumably common across other coastal areas
of the island (Juste and Ibáñez 1994a). It has not been collected on Príncipe, but its
presence there has recently been confirmed acoustically (JMP and ST pers. obs.;
Fig. 22.3) Finally, T. mauritianus seems to be very rare on Annobón (Fig. 22.3),
where a single specimen was found dead and is now housed at the Estación
Biológica de Doñana (EBD-CSIC) collections in Seville (Juste 2020). In São
Tomé, it was classified as Endangered, given its reduced area of occupancy, the
number of known locations, and projected decline in habitat quality (Rainho et al.
2010).
Family Molossidae
Two species of molossids occur on the islands and both are insectivorous, the São
Tomé free-tailed bat Chaerephon tomensis endemic to São Tomé (Juste and Ibáñez
1993c), and the little free-tailed bat Chaerephon pumilus (Cretzschmar, 1826),
which is found on both São Tomé and Príncipe (JMP and ST pers. obs.). The latter
is an abundant habitat generalist, widely distributed across Africa and the islands
around the continent and is currently classified as Least Concern (Bouchard 1998;
Mickleburgh et al. 2019). By contrast, C. tomensis is classified as Endangered,
reflecting its small extent of occurrence and likely decreasing population trend as a
result of habitat loss associated with coastal development and land conversion for
agricultural use, and possibly competition with its much more abundant congener
(Monadjem et al. 2019).
During recent island-wide surveys, Rainho et al. (2010) captured several dozen
individuals of C. pumilus on São Tomé, in shade cocoa plantations, coconut groves
and at roosts (Fig. 22.2). On Príncipe, JMP and ST (pers. obs.) captured it at a roost
in the roof of a house near Porto Real and recorded its calls at several locations in the
NE of the island (Fig. 22.3). By contrast, C. tomensis seems to be so rare that recent
extensive trapping efforts have failed to document it. The only records to date are the
type series of three specimens captured in two lowland localities, in a coastal lagoon
at Praia das Conchas in the drier northern area of São Tomé and at the mouth of a
river in cocoa plantations in Água Izé (Juste and Ibáñez 1993c). Acoustic sampling
further confirmed the ubiquitous presence of C. pumilus on São Tomé (Table 22.1).
In addition, these data revealed that Chaerephon emits vocalizations that fall into
two distinct groups that differ in a number of call characteristics (Table 22.1). The
first can unequivocally be assigned to C. pumilus (FmaxE 28 kHz), while the
second group (FmaxE 22 kHz) could potentially correspond to C. tomensis
(Rainho et al. 2010), thus offering a glimmer of hope that this species still occurs
on the island.
608
A. Rainho et al.
Family Vespertilionidae
In São Tomé and Príncipe, this large family of insectivorous bats is represented by
one species on each island. On São Tomé, recent surveys led to the detection of a
species of mouse-eared bat, Myotis Kaup, 1829 (Rainho et al. 2010). While its
general morphology suggests the species is a tricolored mouse-eared bat
(Fig. 22.1, 3), M. cf. tricolor, genetic and morphological comparisons, as well as
its echolocation calls (Table 22.1), indicate differentiation from mainland specimens
(authors’ unpublished data). An integrative taxonomic assessment is underway to
establish its phylogenetic placement with respect to other Afrotropical Myotis.
Rainho et al. (2010) captured several individuals in a single roost in a coastal cave
at Ponta Figo, south of Neves, comprised of several dozen individuals of M.
cf. tricolor and several thousand M. newtoni (described below). No other roosts of
the species were found, the species has not been captured elsewhere on the island,
and has merely been recorded acoustically at one other location (Bom Sucesso,
Fig. 22.2) attesting to its overall rarity (Rainho et al. 2010).
The island of Príncipe is home to a very small pipistrelle bat that is considered an
endemic form for the island (Fig. 22.1, 4). Although first reported over 30 years ago
(Juste 1990; Juste and Ibáñez 1994b), its formal description is still pending, and its
phylogenetic placement in one of the most entangled African bat groups requires
clarification. Its general dark brown morphology, baculum characteristics, and
genetic comparisons indicate that the pipistrelle belongs to the Neoromicia group
(JJ pers. obs.) and possibly to the recently described genus Pseudoromicia
(Monadjem et al. 2020). The species is abundant and ecologically eclectic, having
been captured or recorded in urban, agricultural, and forest areas (JMP and ST pers.
obs.). As is the case for other bat species, the distribution map suggests that the
species is more common in the northern part of Príncipe (Fig. 22.3), but this is
mostly a result of biased sampling due to difficulty accessing the southern part of the
island.
Family Miniopteridae
Only one species of this family occurs on the Gulf of Guinea oceanic islands,
Miniopterus newtoni. It has only been recorded on São Tomé (Fig. 22.2), and was
first reported for the island and described as a new species by Bocage (1889, 1903).
The original material used by Bocage was lost in a fire in Lisbon, and Juste and
Ibáñez (1992) provided a neotype from Santa Catarina. These authors distinguished
the species morphologically from the mainland western (occidentalis) and eastern
(minor) little Miniopterus forms, all considered subspecies of M. minor Peters, 1867.
A subsequent genetic assessment confirmed the specific rank of this endemic (Juste
et al. 2007). The species seems relatively common across São Tomé (Juste and
Ibáñez 1994a; Rainho et al. 2010) and was found in modified habitats (e.g., foraging
around streetlamps in urban areas) as well as in primary lowland forests, from sea
22
Current Knowledge and Conservation of the Wild Mammals of the Gulf. . .
609
level up to 1300 m in Morro Palmira (Juste 1990). It appears to roost strictly in caves,
water mines, and tunnels. It can form colonies of thousands of individuals, often with
other species. Miniopterus newtoni emits low duty cycle frequency-modulated
echolocation calls with maximum energy of around 56 kHz (Table 22.1). It was
locally considered Near Threatened due to a probable decline in the number of
individuals and locations because of the destruction and/or disturbance of underground roosts (Rainho et al. 2010). However, it is listed as Data Deficient in the
IUCN Red List (Juste 2019).
Order Carnivora
Family Mustelidae
One of the wild carnivores present on São Tomé is the least weasel (Bocage 1895;
Dutton 1994). To the best of our knowledge, this species was not reported for
Príncipe or Annobón. Although the Portuguese were most likely responsible for
the introduction of the least weasel on São Tomé, genetic analyses by Rodrigues
et al. (2017) revealed that the animals that occur on this island do not appear to be
closely related to mainland Portugal populations. Instead, they are identical to those
from the Azores (a Portuguese volcanic archipelago in the mid-Atlantic), which, in
turn, are thought to have been introduced from the Balearic Islands in the Mediterranean. Morphological similarity between individuals of São Tomé and the Azores
had already been highlighted by Bocage (1895), and Barrett-Hamilton (1904)
mentioned that the animals of São Tomé might have been imported from the Azores.
There is little information about the abundance and distribution of the least weasel
on São Tomé and Príncipe. Atkinson et al. (1994) observed weasels both at Fernão
Dias and Ribeira Peixe. The least weasel feeds mainly on rodents, both in its native
and introduced range, but can also consume birds and their eggs, small reptiles, and
invertebrates, particularly if the rodent population declines or if an easy predation
opportunity arises (Sheffield and King 1994 and references therein; King et al.
2001). According to Dutton (1994), the abundance of rodents on the islands may
reduce the impact of weasels on other animal groups. However, shrews are frequently part of the weasel’s diet and the endemic shrews might thus be vulnerable to
its presence (Sheffield and King 1994).
Family Viverridae
The African civet (Fig. 22.1, 8) is endemic to sub-Saharan Africa, occurring between
latitudes 15 N and around 29 S (Ray 2013). It is naturally present on Zanzibar but
absent from other offshore African islands (Ray 2013). It is likely that the Portuguese
introduced the African civet to both São Tomé and Príncipe (Bocage 1905; Dutton
1994; Fundação Príncipe 2019), not only for the control of rodents but also for the
610
A. Rainho et al.
exploitation of its musk (Frade 1958). No reference was found to the presence of this
species on Annobón.
The African civet is a solitary, silent species that is active only at night. Thus it is
not easy to observe, and information on its distribution and abundance is scarce.
Atkinson et al. (1994) observed a fresh civet hole in a secondary forest between
Santo António and São Miguel, and JJ (pers. obs.) recorded this species near São
Tomé and at Cantagalo, Monte Belo, Monte Café, and Praia das Conchas in the early
1990s. During the last decade, the species has been observed across São Tomé, from
the savannas in Morro Peixe to Monte Café and Monte Carmo, and from the road to
the native forest (Ricardo de Lima pers. comm.). In Príncipe, it was camera-trapped
at Morro Leste (Fundação Príncipe 2019). In mainland Africa, this species does not
usually dwell in primary forests, but will use this habitat if accessible by logging
roads (Ray and Sunquist 2001). African civets are omnivorous and opportunistic,
feeding mainly on fruit, arthropods, mammals, and, less frequently, on birds and
reptiles (Ray 2013 and references therein). The African civet is not a good climber or
digger (Ray 2013), so tree-dwelling species should be relatively safe from civet
predation (Dutton 1994). The potential impact on native ground-dwelling fauna is
not known.
Conservation
The long-term isolation of Príncipe, São Tomé, and Annobón allowed the differentiation of insular populations, resulting in a very high level of endemism and an
exceptional mammal conservation value. The taxonomy of these mammals is still in
flux but of the 13 native species currently recognized, 7–9 are endemic species, and
3–4 are endemic subspecies, with no endemism shared between islands (Appendix).
Most of these native and endemic species are bats (Appendix), though Príncipe and
São Tomé each have an endemic species of shrew, and São Tomé may have a yet
undescribed rodent. All the remaining mammals were introduced by humans.
Little is known about the threats faced by these species, although they should all
be considered somewhat fragile due to their very small ranges (Le Breton et al.
2019). In particular, further deforestation and forest degradation would likely result
in a potentially threatening situation for several mammal species. All the endemics
likely evolved in humid forest, and several species show some level of association to
this habitat (e.g., Ch. tomensis, E. helvum annobonense and H. ruber). Although
much of the forest on the three islands has, at some point in the past, been converted
to plantation agriculture or profoundly altered, there are still areas of relatively
undisturbed habitat in rugged parts of the islands (Jones and Tye 2005; de Lima
et al. 2022). The remaining primary forest is mostly in protected areas and, along
with complementary areas of secondary forest, is likely to provide suitable habitat to
maintain populations of all native mammals. The area of native forest on Annobón is
very small, but the only mammal that is endemic to this island, the subspecies
E. helvum annobonense, also uses secondary habitats (JJ pers. obs.).
22
Current Knowledge and Conservation of the Wild Mammals of the Gulf. . .
611
Hunting of E. helvum and R. aegyptiacus for food is common on São Tomé
(Carvalho et al. 2015b; Peel et al. 2017) and on Príncipe (Peel et al. 2017; JMP and
ST pers. obs.). Still, both species remain quite numerous, presumably because these
frugivorous species take advantage of the increase in fruit resources due to agriculture. The endemic M. brachycephala, however, is quite rare and it may be caught in
traps set up to capture the two more abundant species, so hunting is a potentially
significant threat to this species.
Some carnivorous mammals, both wild and domestic, have been introduced in
São Tomé, all of which are also widespread in Príncipe, except for the least weasel.
Although the impact of these species on the native wildlife has not yet been studied,
they are all known to consume small mammals, so they are potential predators of the
native shrews. Rats prey on smaller mammals and may thus also prey on both shrew
species and potentially bats (Racey and Entwistle 2003).
Because so little is known about the real impact of the various potential threats to
native mammals on these islands, it is not possible to formulate very specific
conservation recommendations. However, it is evident that the protection of forest
is essential. The expansion of conservation management to areas of well-preserved
secondary forest and increased surveillance and enforcement are necessary to ensure
the continuity of the forests on the islands and all the biodiversity they sustain.
Integrated management actions directed at the control of exotic predators are also
urgently needed, within the forest but also in anthropogenic systems (Courchamp
et al. 2003). Alien invasions are recognized as a significant cause of species
endangerment and extinction, and the rodents present on the islands are among the
most damaging invasive alien species (Lowe et al. 2000). Their devastating effects
on natural systems, particularly on islands, and impacts on human activities and
health have been thoroughly documented around the globe (Dutton 1994; Drake and
Hunt 2009; Harris 2009; Russell et al. 2017).
In the case of bats, cave-dwelling species are always of particular concern,
because the availability of suitable underground roosts is limited and the concentration of bats in these roosts exposes them to additional risks. Five cave-dwelling bat
species are known to occur on São Tomé, two of which have populations also on
Príncipe. It is thus essential to take measures to ensure that these roosts are adequately identified and protected. The importance of each roost should be evaluated,
using criteria based on the number of individuals and number of species using the
site and their conservation status. High-ranking roosts should be identified, regularly
monitored, and human access physically limited if necessary (Rainho et al. 2010).
Frugivorous bat species are considered pests by many farmers because they consume
planted fruits. In extreme damage and food-loss situations, the use of wildlifefriendly exclusion nets to protect individual trees or fruits may be licensed and
supported (Tollington et al. 2019). However, this conflict should be managed with
care and in partnership with farmers.
Educational outreach about the value of biodiversity is needed to provide citizens
with a better understanding of the importance of their local mammal species. In the
case of bats, for instance, highlighting their importance in seed dispersal and in the
control of insects that are agricultural pests as well as vectors of diseases. Finally, it
612
A. Rainho et al.
is important to highlight the need to carry out more research on which to base the
conservation of the endemic-rich mammalian fauna of the islands.
Challenges and Future Research
Although recent efforts have advanced our understanding of the mammal fauna and
in particular the bat fauna of São Tomé and Príncipe (Rainho et al. 2010), the
preceding sections clearly highlight that our knowledge is fragmented, and important
gaps remain to be addressed in future research. Detailed taxonomic assessments that
integrate multiple lines of evidence based on craniometric, morphological, genetic,
and (for bats) acoustic data are needed to resolve the identity and taxonomic
relationships of several species, specifically M. cf. tricolor in São Tomé,
Pseudoromicia sp. in Príncipe and of the putative Dendromus species recently
discovered in São Tomé.
At least 7 of the 19 wild mammal species occur only on one of the Gulf of Guinea
islands, including 3 Endangered and 2 Data Deficient species (Appendix). The longterm conservation of this large number of single-island endemics, such as the bats
Ch. tomensis and M. brachycephala or the shrews C. fingui and Cr. thomensis,
constitutes a fundamental challenge. In this regard, further detailed surveys of the
islands are needed, to gather reliable data to assess the ecology, distribution, threats,
and current status of populations. In particular, Annobón should be targeted since it
has not been surveyed for decades. Ideally, such surveys should be conducted at
regular intervals to be able to monitor population trends (Meyer et al. 2010) and to
trigger appropriate management interventions if needed. Such detailed surveys are
also urgently needed to fill important knowledge gaps concerning basic biology and
ecological requirements—information that is scant or lacking for many species (e.g.,
Ch. tomensis, M. thomensis, M. newtoni). Finally, further field surveys are needed to
assess the population status of the invasive species, particularly the murid rodents,
and to quantify their impact on the Gulf of Guinea island ecosystems.
Acknowledgments We are most grateful to Ricardo de Lima for supplying the geographical data
on Cr. thomensis distribution in São Tomé and providing a photo, relevant papers and reports. We
also thank Leonel Viegas for sharing his photo and Kristofer Helgen (Australian Museum Research
Institute) for the suggested identification of Dendromus sp. Alison Peel and Luís Ceríaco provided
valuable comments on an early version of the text. Finally, we are grateful to Filipa Soares and
Martim Melo for providing information concerning introduced mammals in Príncipe and Annobón.
22 Current Knowledge and Conservation of the Wild Mammals of the Gulf. . .
613
Appendix
List of the wild terrestrial mammals of the Gulf of Guinea oceanic islands. Occurrence status per island: E, endemic; R, resident; I, introduced; ?, uncertain. IUCN
Red List category: NE, not evaluated; DD, data deficient; LC, least concern; NT,
near threatened; VU, vulnerable; EN, endangered; CR, critically endangered
Higher taxonomy
Order Primates
Family Cercopithecidae
Cercopithecus Linnaeus,
1758
Order Rodentia
Family Muridae
Mus Linnaeus, 1758
Rattus Fischer, 1803
Order Eulipotyphla
Family Soricidae
Crocidura Wagler, 1832
Order Chiroptera
Family Pteropodidae
Eidolon Rafinesque, 1815
Rousettus Gray, 1821
Myonycteris Matschie, 1899
Family Hipposideridae
Macronycteris Gray, 1866
Hipposideros Gray, 1831
Family Emballonuridae
Taphozous É. Geoffroy,
1818
Species/subspecies
P
ST
Cercopithecus mona (Schreber,
1775)
I
I
Mus musculus Linnaeus, 1758
Rattus rattus (Linnaeus, 1758)
Rattus norvegicus (Berkenhout,
1769)
I
I
I
I
I
I
Crocidura fingui Ceríaco et al 2015
Crocidura thomensis (Bocage, 1887)
E
Eidolon helvum (Kerr, 1792)
E. helvum annobonense Juste et al.,
2000
Rousettus aegyptiacus (É. Geoffroy,
1810)
R. aegyptiacus tomensis Juste and
Ibáñez, 1993
R. aegyptiacus princeps Juste and
Ibáñez, 1993
Myonycteris brachycephala
(Bocage, 1889)
R
Macronycteris thomensis (Bocage,
1891)
Hipposideros ruber (Noack, 1893)
Taphozous mauritianus É. Geoffroy,
1818
A
IUCN
NT
I
?
I
LC
LC
LC
DD
EN
E
R
NT
E
NT
E
E
E
EN
E
LC
R
R
LC
R
R
R
LC
(continued)
614
Higher taxonomy
Family Molossidae
Chaerephon Dobson, 1874
Family Vespertilionidae
Myotis Kaup, 1829
Pseudoromicia Monadjem
et al., 2020
Family Miniopteridae
Miniopterus Bonaparte,
1837
Order Carnivora
Family Mustelidae
Mustela Linnaeus, 1758
Family Viverridae
Civettictis Pocock, 1915
A. Rainho et al.
Species/subspecies
P
ST
Chaerephon pumilus (Cretzschmar,
1826)
Chaerephon tomensis (Juste and
Ibáñez, 1993)
R
R
LC
E
EN
Myotis cf. tricolor (Temminck, 1832)
Pseudoromicia sp.
A
IUCN
R
E
NE
Miniopterus newtonii Bocage, 1889
E
DD
Mustela nivalis Linnaeus, 1766
I
LC
I
LC
Civettictis civetta (Schreber, 1776)
I
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Chapter 23
Cetaceans of São Tomé and Príncipe
Inês Carvalho, Andreia Pereira, Francisco Martinho, Nina Vieira,
Cristina Brito, Márcio Guedes, and Bastien Loloum
Abstract The Gulf of Guinea is a marine biodiversity hotspot, but cetacean fauna in
these waters is poorly studied and our knowledge is documented mostly from
opportunistic (sightings and strandings) and whaling data. This chapter presents a
short review of historical whaling in the Gulf of Guinea and an update of cetacean
biodiversity in the waters of São Tomé and Príncipe. Observations since 2002 have
confirmed the presence of 12 species of cetaceans, 5 of them new to the region
(Striped Dolphin, Rough-toothed Dolphin, Risso’s Dolphin, Pygmy Killer Whale,
and Dwarf Sperm Whale). The archipelago seems to be an important area for
cetaceans, with some species (Bottlenose Dolphin and Pantropical Spotted Dolphin)
being present throughout the year. The volcanic origin of the archipelago produces
great depths very close to the coast, which may favor the approach of pelagic species
I. Carvalho (*)
Population and Conservation Genetics Group, Instituto Gulbenkian de Ciência, Oeiras, Portugal
APCM, Associação para as Ciências do Mar, Lisbon, Portugal
e-mail: icarvalho@igc.gulbenkian.pt
A. Pereira
APCM, Associação para as Ciências do Mar, Lisbon, Portugal
Instituto Dom Luiz, Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal
F. Martinho
APCM, Associação para as Ciências do Mar, Lisbon, Portugal
Ecco Ocean, Benfica, Portugal
N. Vieira
APCM, Associação para as Ciências do Mar, Lisbon, Portugal
CHAM, Centro de Humanidades, Faculdade de Ciências Sociais e Humanas, Universidade
NOVA de Lisboa, Lisbon, Portugal
C. Brito
CHAM, Centro de Humanidades, Faculdade de Ciências Sociais e Humanas, Universidade
NOVA de Lisboa, Lisbon, Portugal
M. Guedes · B. Loloum
ONG MARAPA, São Tomé, Sao Tome and Principe
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_23
621
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I. Carvalho et al.
like Sperm Whales, Killer Whales, and Short-finned Pilot Whales. Bays and shallow
waters may also serve as protection or rest areas for particular groups, like mother
and calf pairs of Humpback Whales. Major anthropogenic threats to cetaceans in São
Tomé and Príncipe include habitat degradation due to overfishing, fisheries interactions, possibly some occasionally directed takes and, more recently, oil and gas
prospecting. Consistent and dedicated research to inform national legislation,
together with increasing environmental awareness and local engagement, would
help to identify effective cetacean conservation strategies in the archipelago.
Keywords Conservation · Dolphins · Gulf of Guinea · Whales · Whaling
Introduction
Top predators, such as cetaceans, are known to seek and associate with predictable
regions of high biological activity (“hotspots”). Oceanic islands are topographic
features that result in localized upwellings, eddies, and convergence zones, which in
turn may cause enhanced primary productivities that promote biomass accumulation
and congregate biodiversity in their vicinity (Doty and Oguri 1956; Caldeira et al.
2002; Palacios 2002).
The Gulf of Guinea is a globally important region that hosts high concentrations
of rare, range-restricted, and threatened marine species, such as sea turtles, elasmobranchs, and marine mammals (Weir 2010; Lucifora et al. 2011; Selig et al. 2014;
Polidoro et al. 2017) and is considered a marine biodiversity hotspot (Roberts et al.
2002). The waters of the Gulf of Guinea support key life-history stages for several
cetacean species (Jefferson et al. 1997; Weir 2010, 2011). However, the cetacean
fauna along the west coast of Africa, as well as of the oceanic islands of the Gulf of
Guinea, is incompletely described and, despite historical information and verbal
descriptions of great diversity, there is relatively little scientific information about
the ecology of species from this group occurring in the region (Hoyt 2005; Weir
2010).
The nation of São Tomé and Príncipe is composed of two main islands and
several small islands and islets. Due to their volcanic origin, the islands display high
relief and the littoral surrounding fringe is very narrow with depths of around 200 m
close to the shore (Afonso et al. 1999). The country has an Exclusive Economic
Zone (EEZ) of almost 165,000 km2, and a strong dependence on fishing; however,
knowledge related to its marine fauna is limited, and only a few studies have been
conducted in recent years (e.g., Afonso et al. 1999; Maia et al. 2018; Hancock et al.
2019; Quimbayo et al. 2019).
This chapter provides a brief summary of historical whaling activity in the Gulf of
Guinea region, an updated review of the occurrence of cetaceans in the waters of São
Tomé and Príncipe (no studies available for Annobón), and a brief history of
cetacean research in the archipelago. It also identifies priorities for future research
and conservation of cetaceans in the region.
23
Cetaceans of São Tomé and Príncipe
623
Cetacean Occurrences Based on Historical Whaling Data
Background on Historical Whaling in the Gulf of Guinea
Early written references to cetaceans in the Gulf of Guinea include observations of
“big fishes such as porpoises” (Dias 1934 in Brito 2009) and “many whales, large
and small, that it is a wonderful thing to say” (Anonymous 1812). As with other
Atlantic islands and the coast of the African mainland, cetaceans stranded on the
shore were probably used by local people and settlers, who consumed the meat and
transformed blubber into fuel (Brito et al. 2017; Vieira 2020).
By the second half of the eighteenth century, the Governor of São Tomé and
Príncipe reported the presence of English vessels hunting whales around Cap Lopez
(Gabon) and Fernando Po (Bioko) Island (Ferreira 1773). Those operations followed
“American whaling” techniques, which included the persecution of animals from
open boats and hand harpooning (Macy 1835; Townsend 1935). Humpback Whales
Megaptera novaeangliae (Borowski, 1781) were one of the main targets along
equatorial West Africa, due to their seasonal migratory movements, preference for
coastal waters during migration and breeding, and slower swimming speed compared with other baleen whales (Townsend 1935; Tønnessen and Johnsen 1982).
The combination of these factors made this species an easy target for coastal whaling
globally during the nineteenth century (Reeves and Smith 2006), including in the
waters of São Tomé and Príncipe, for instance during the voyage of the Vessel
Admiral Blake. The Vessel arrived at São Tomé on June 22, 1869, and anchored on
Príncipe Island on June 24, 1869. The crew went on “bay whaling” until the end of
August hunting humpback cow and calf pairs (Anonymous 1869–70).
Starting in the mid-1800s, whaling became dramatically more effective due to
several innovations, including explosive harpoons and modern steam-driven whaling boats (Tønnessen and Johnsen 1982; Clapham and Baker 2002). This allowed
the capture of previously unattainable fast-swimming species, especially
Balaenoptera whales including Blue Whale Balaenoptera musculus (Linnaeus,
1758), Sei Whale Balaenoptera borealis (Lesson, 1828), Bryde’s whale
Balaenoptera edeni (Anderson, 1879), and Fin Whale Balaenoptera physalus
(Linnaeus, 1758).
In the early twentieth century, engine-powered Norwegian floating factories
(moored near shore or working in the open sea) accompanied by fleets of catcher
boats with deck-mounted harpoons began operations in the Gulf of Guinea. During
this time whaling went through periods of expansion and crisis (Rocha et al. 2015).
Despite the breaks in whaling activity resulting from World Wars I and II, after years
of intense captures, the following seasons were significantly less successful. Pelagic
and coastal whaling operations were conducted from Cap Lopez (Gabon) in 1912
and took place in 1912–1914, 1922–1926, 1930, 1934–1937, 1949–1952, and 1959.
Whaling operations took place mostly between the end of June and November, with
a peak in July/August (Budker and Collingon 1952), corresponding to the breeding
period of Humpback Whales, the main target of the catch. Bryde’s, Sei, Sperm
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Physeter macrocephalus (Linnaeus, 1758) and Fin whales were also taken (Budker
1953; Tønnessen and Johnsen 1982). During the whaling seasons, high fluctuation
of total catches, with a substantial decline not only in numbers but in the mean length
of the individuals caught indicated the depletion of the Humpback Whale stock
(Budker and Collignon 1952; Budker 1953).
In the late 1960s, overexploitation was notorious, and almost every whale stock
was depleted or had already collapsed. The International Whaling Commission
(IWC), an intergovernmental organization established in 1946 to provide conservation of whale stocks and management of the whaling industry, began to impose
restrictions on whale catches. Restrictions for Blue and Humpback whales were
imposed in the 1960s, Sei and Fin whales in the 1970s, and in 1986 the moratorium
went into effect with zero catch quota for both pelagic and coastal whaling (Clapham
and Baker 2002). In the 1970s, illegal captures, mostly of Bryde’s and Sei whales,
continued by the catcher/factory vessel Run/Sierra in the Gulf of Guinea (Tønnessen
and Johnsen 1982; Best 2001).
In addition to commercial whaling, an aboriginal whaling operation in Annobón
has been reported since the late nineteenth century (Doce 1932, 1951; Aguilar 1985),
and with recent evidence of continuing until today (Collins et al. 2019; Fielding and
Barrientos 2021). The Annobonese retained the skills and practices of hunting
whales from their experience on foreign whaling vessels, and the activity was
integrated into local culture. Small rowing boats with two rowers and one harpooner
were used in July and August, targeting coastal Humpback Whales, mainly calves
(Aguilar 1985). However, the status of this hunt is uncertain and more information is
needed.
Industrial Whaling in São Tomé and Príncipe
First attempts to promote modern whaling in São Tomé using a factory-ship and
catchers date to the 1930s (Henriques 2016) but not much is known from that period.
From 1945, the company Grémio dos Armadores da Pesca da Baleia of Lisbon,
regulated the activity in mainland Portuguese waters and overseas (Henriques 2016).
There are some references on whaling operations off São Tomé and Príncipe in
the 1940s. Tenreiro (1961) mentioned that local fishermen and Norwegian companies established on São Tomé hunted Sperm Whales and sharks. He notes that 1946
was an excellent year when they caught 100 cetaceans, which generated 1079 tons of
oil, produced in the factory in the town of Neves (Fig. 23.1, 1). In 1951, a decree
granted a Norwegian company the right to hunt whales in the archipelago for a
period of 10 years, with one of several conditions being the distribution of whale
meat to the local population (Henriques 2016). The operation was supported by the
modern factory in Praia Rosema (Neves), in the northeast of São Tomé Island
(Figueiredo 1960; Henriques 2016). Among the workforce were local people,
Portuguese, and foreigners (Boletim Semanal 1951). The factory operated between
July and October of 1951, processing an average of seven animals per day, with a
23
Cetaceans of São Tomé and Príncipe
625
Fig. 23.1 Whaling industry on São Tomé: (1) Whaling factory at Praia Rosema (Neves, São Tomé;
Tenreiro 1961); (2–5) Remains of the whaling factory in 2005. Photo credits: (2–5) Inês Carvalho
total of 714 animals: 336 Bryde’s Whales, 323 Humpback Whales, 53 Sperm
Whales, and 2 Fin Whales (Figueiredo 1960).
The Humpback Whales killed in the waters of São Tome and Príncipe belong to
the Gabon stock that by 1951 the IWC had already identified as being depleted.
626
I. Carvalho et al.
Nevertheless, at the time, Portugal was not a member of the IWC (joining only in
2002) and despite the criticism, whaling was allowed in STP waters (Budker and
Collignon 1952). However, with increasing international criticism, the competition
with French enterprises in the Gulf waters, and the low number of captures, the
factory closed in that same year (Budker and Collignon 1952; Henriques 2016). Its
remains are still part of the São Tomé seascape (Figs. 23.1, 2–5).
Historical Catches of Cetaceans in the Gulf of Guinea Region
Whaling data provides valuable information on species identification, distribution,
migration, life history, and population status of whale stocks around the world (e.g.,
Townsend 1935; Josephson et al. 2008; Gregr 2011; Smith et al. 2012). To gather
information on the occurrence and distribution of cetacean species in the eastern
Gulf of Guinea area during the whaling period, two databases were used. The first
was the American Offshore Whaling Logbook database (Lund et al. 2021), which
includes information from 1381 logbooks from American offshore whaling voyages
(1784–1920) extracted from original whaling logbooks from three different sources:
Matthew Maury (1850s), Townsend (1930s), and the Census of Marine Life project
(Barnard et al. 2002). The second database was the IWC compilation of worldwide
whale catches since 1900 (Allison 2016a, b). The IWC data is continually updated
(Allison and Smith 2004) and consequently, the total number of catches reported has
changed over time (e.g., Findlay 2000; Best 2001; Weir 2010). Whaling records and
species identifications were accepted as published, despite the likely
misidentification between Sei Whale and Bryde’s Whale in the whaling statistics
(Best 2001). Prior to 1960, whalers could not reliably distinguish between the two
species (Best 2001; Weir 2010). This led to records of “Sei Whales” along the coast
of West Africa likely being misidentified Bryde’s Whales; thus, records of the two
species were merged. Since several cetacean catches are represented by the same
geographic positions, the data were separated into two seasons for better visualization (Fig. 23.2): June to October, representing the breeding season for Humpback
Whales; and November to May.
Humpback Whale was the main target species of whaling in the Gulf of Guinea
region with more than 10,000 animals captured mostly near the coast of Gabon and
around Príncipe Island between June and October (Fig. 23.2, top). Bryde’s/Sei
Whales were caught throughout the year, mainly off the southern coast of Gabon,
the offshore waters off the west coast of São Tome, and between the islands of São
Tomé and Annobón (Fig. 23.2). Sperm and Fin Whale catches were more infrequent
and spread in offshore waters across the entire region, while catches of other
cetacean species were rare (Fig. 23.2).
23
Cetaceans of São Tomé and Príncipe
627
Fig. 23.2 Distribution of whale catch positions around the Gulf of Guinea Islands. Data from
American Offshore Whaling Logbook database (https://whalinghistory.org/av/logs/aowl/) and IWC
database (Allison et al 2016b), representing N ¼ 11845 catches (10553 Humpback whales; 1010
Bryde’s/Sei whales; 261 Sperm whales; 15 Fin whales; 2 Pilot whales; 1 Blue whale; 1 Right whale
628
I. Carvalho et al.
Recent Data from Fieldwork on São Tomé and Príncipe
There is limited information about the spatial and temporal patterns of the distribution and abundance of cetaceans in the Gulf of Guinea, and most of the available
information is based on whaling data (e.g., Townsend 1935; Budker and Collignon
1952), reports on strandings, by-catch data, and some dedicated cetacean research
(e.g., Walsh et al. 2001; Van Waerebeek et al. 2009; Segniagbeto and Van
Waerebeek 2010; Weir et al. 2010; Weir 2011; Sohou et al. 2013; Rosenbaum
et al. 2014; Escalle et al. 2015; De Boer et al. 2016; Collins et al. 2019; Trew
et al. 2019).
In 2002, the first field study dedicated to cetaceans of São Tomé Island started
with the objective of collecting baseline data on the occurrence of cetaceans in these
waters. The fieldwork of this project was based at Rolas Islet, and the boat surveys in
2002 and 2003 were conducted in the south region of São Tomé. Data on occurrence,
movements, seasonality, and behavior (including acoustic behavior) of several
species were collected and analyzed (Picanço et al. 2009). In 2004, a PhD focusing
on the population structure of the Humpback Whale on the West African coast was
initiated, in collaboration with the Wildlife Conservation Society and the American
Museum of Natural History. Fieldwork was conducted between 2004 and 2006 in
São Tomé waters to collect data on the occurrence, distribution, behavior, and
genetics of humpback whales (Carvalho et al. 2011, 2014; Carvalho 2012; Kershaw
et al. 2017). In 2012, a partnership between the NGOs MARAPA (São Tomé) and
Associação para as Ciências do Mar (APCM; Portugal) started the project
“Operação Tunhã.” The aim of the project was to establish a program to collect
systematic baseline data on cetaceans in São Tomé, to assess the local capacity to
develop a sustainable whale watching activity, and at the same time to raise
awareness among stakeholders on local cetacean conservation.
In Príncipe Island, data collection about cetaceans has been more limited. Some
sighting and stranding records have been collected intermittently over the years by
Fundação Príncipe (Vanessa Schmitt pers. comm.). In 2020, between August and
November, a field survey was carried out in the archipelago’s waters to collect visual
and acoustic data on cetaceans, for the South Atlantic Cetacean project by the
Edmaktub Association (Sesani et al. 2020).
Fig. 23.2 (continued) (Eubalaena australis Desmoulins, 1822); 1 Minke whales; 1 Killer whale).
Top map-whaling catches between June-October, Bottom map-whaling catches between
November-May. The symbol ○ (on top map in red) represents the records without specific
geographic coordinates provided by IWC. Blue, Right and several Humpback whale catches were
recorded with this point, which indicates that they were caught in the area but there was no specific
location
23
Cetaceans of São Tomé and Príncipe
629
Fig. 23.3 Cetacean sightings and strandings in São Tomé Island recorded from 2002 to 2006 and
from 2012 to 2015 (N ¼ 215; Picanço et al. 2009; Carvalho et al. 2014; Collins et al. 2019;
Associação para as Ciências do Mar, Portugal unpublished data)
Cetacean Species Recorded in São Tomé and Príncipe Waters
To date, the presence of 12 cetacean species has been confirmed (Fig. 23.3, Appendix), based on data collected by the authors during 2002–2006 and 2012–2015
around São Tomé Island. Five of those species were only confirmed recently by
the authors: Striped Dolphin Stenella coeruleoalba (Meyen, 1833), Rough-toothed
Dolphin Steno bredanensis (Lesson, 1828), Risso’s Dolphin Grampus griseus
(G. Cuvier, 1812), Pygmy Killer Whale Feresa attenuata (Gray, 1874), and Dwarf
Sperm Whale Kogia sima (Owen, 1866).
Megaptera novaeangliae Humpback Whales (Fig. 23.4, 1) in the Southern Hemisphere migrate between summer feeding areas in the nutrient-rich waters of the
Southern Ocean and winter breeding areas in tropical waters (Townsend 1935). The
Gulf of Guinea region is known as a breeding area for the Humpback Whale B stock
(IWC 2001). Catch histories and recent genetic data suggest that this stock may be
sub-structured (Findlay 2000; Carvalho et al. 2014) with some temporal and spatial
segregation; Humpback Whales use two different migration corridors and different
feeding areas, in South Africa and Antarctica (Barendse et al. 2011; Rosenbaum
et al. 2014; Carvalho et al. 2014). Between 2002 and 2014, 74 sightings of Humpback Whales were collected around São Tomé waters (Carvalho et al. 2011; APCM
unpublished data). In 2020, 63 sightings were collected mostly around Príncipe
Island (Sesani et al. 2020). The sightings were collected between July and late
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I. Carvalho et al.
Fig. 23.4 Cetacean species photographed in São Tomé waters: (1) Humpback Whale; (2)
Bottlenose Dolphin; (3) Pantropical Spotted Dolphin; (4) Rough-toothed Dolphin; (5) Killer
Whale; (6) Pygmy Killer Whale; (7) Short-finned Pilot Whale; (8) Sperm Whale. Photo credits:
(1) Maria Pimentel, (2, 5, 7) Inês Carvalho, (3) Cristina Picanço, (4, 6, 8) Bastien Loloum
23
Cetaceans of São Tomé and Príncipe
631
November. São Tomé appears to be used primarily by mother/calf pairs, as a calving,
nursing, and resting area. This is suggested by the high frequency of observed groups
with a calf present (more than 70%) and long occupancy of several weeks in the area
by these groups (Carvalho et al. 2011; Sesani et al. 2020). Female Humpback
Whales with calves prefer shallow waters (Ersts and Rosenbaum 2003), being
sighted mostly around Rolas Islet (sometimes very close to the shore), near São
Tomé city (northeast), and around Príncipe Island (Picanço et al. 2009; Carvalho
et al. 2011; Sesani et al. 2020).
Physeter macrocephalus The Sperm Whale (Fig. 23.4, 8) is a cosmopolitan species
but shows differential sex-and age-related distributions. Females and immature
individuals inhabit primarily warm waters in tropical to subtropical areas (Whitehead
2002). As males get older, they disperse from these warmer areas to higher latitudes
(Whitehead 2002). There are three stranding records of Sperm Whales in São Tomé
(2002, 2010 and 2013; Fig. 23.4) and one in Príncipe in 2014 (Collins et al. 2019).
Two sightings of single animals were recorded off the north coast of São Tomé
Island, one reported in 2005, at 1500 m depth (Picanço et al. 2009), and another one
in 2013 at 980 m depth (APCM unpublished data). These records suggest the
occurrence of the expected “nursery groups,” as young calves were recorded from
strandings and immature animals and adults were recorded from sightings. Sesani
et al. (2020) described a sighting of two individuals in 2020, 80 km off the east coast
of São Tomé Island at 2500 m depth, with no information on age and sex.
Kogia spp. Two Kogia species are currently recognized: the Dwarf Sperm Whale
(Kogia sima) and the Pygmy Sperm Whale Kogia breviceps (de Blainville, 1838)
(Rice 1998). Both occur in deep temperate and tropical waters worldwide, with
overlapping distributions, and they are very difficult to distinguish. The Dwarf
Sperm Whale is smaller and has a more prominent dorsal fin, whereas the Pygmy
Sperm Whale is slightly larger and has a smaller and rounded dorsal fin. There were
two confirmed records of the Dwarf Sperm Whale off São Tomé, one sighting in
February 2012, off the northwest coast, at around 150 m depth, and one a by-catch
record in the southern region in February of 2014 (APCM unpublished data). Four
additional sightings of Kogia spp. were recorded off the north region of São Tomé
Island, two in March and April of 2012 and two in January of 2014 (APCM
unpublished data), but the species could not be fully confirmed.
Orcinus orca (Linnaeus, 1758) The Killer Whale (Fig. 23.4, 5) is distributed across
oceans (Rice 1998), but reports are less common in tropical waters (Weir et al.
2010). Six sightings were reported around São Tomé (Picanço et al. 2009; Weir et al.
2010): one in November, four in December, and one in January. Four of the six
sightings occurred around Rolas Islet, in the south, and the remaining on the east and
northwest coasts (Fig. 23.4). Four sightings occurred in shelf edge habitat
(270–790 m), one in shallow waters (55 m) and another one in deep-water
(1200 m; Weir et al. 2010). The average group size was estimated at six animals
and included adults and calves. Weir et al. (2010) photo-identified 13 animals. Two
animals were first photo-identified together in 2002, and then in 2004; one of these
632
I. Carvalho et al.
individuals was also photographed in 2003. The four sightings during December
2002 were the result of repeated encounters on successive dates with a single group
of Killer Whales. A predation event was observed off São Tomé during January
2003, when an adult–calf pair of killer whales was observed feeding on an Ocean
Sunfish Mola mola (Linnaeus, 1758) at the surface (Weir et al. 2010). Repeated
sightings of the same group of killer whales around São Tomé suggested the regular
use of that area (at least seasonally) by a particular group of animals. In 2020, there
were two recorded sightings off western São Tomé, one individual in October and
two individuals in November (Sesani et al. 2020). The three individuals were photoidentified, but there was no cross-checking with photographs from previous years.
Steno bredanensis The Rough-toothed Dolphin (Fig. 23.4, 4) inhabits primarily
warm oceanic waters worldwide (Rice 1998). Four sightings of this species were
recorded, off the north coast of São Tomé Island, in August and September of 2012
and within the 200 m bathymetry. Three of the sightings comprised average groups
of eight individuals, all adults. The fourth sighting was a larger group of around
20 adults and juveniles sighted together with a group of 8–10 Pygmy Killer Whales,
at around 2 km from the coast and depths under 100 m (APCM unpublished data). In
October of 2008, there was one offshore sighting of a group of 35 individuals, west
of São Tomé at 3271 m depth (Weir 2011).
Grampus griseus The Risso’s Dolphin inhabits temperate and tropical waters
worldwide and generally prefers deeper offshore waters, especially close to the
continental shelf edge and slope (Jefferson et al. 2008). One individual was stranded
on the north coast of São Tomé (Fig. 23.3) in February 2015 (Collins et al. 2019).
Pseudorca crassidens (Owen, 1846) The False Killer Whale inhabits primarily
tropical to subtropical waters, and sometimes also occurs in warm temperate waters
(Rice 1998). The first record of this species was a sighting of 6–8 adult animals
engaged in feeding activities (some animals had fish in their mouths) off the north
coast of São Tomé Island in April 2012 (APCM unpublished data). The two
subsequent records, in 2013 and 2014, came from strandings in the same coastal
region (Collins et al. 2019). The most recent sightings were recorded in 2020, one
south of Rolas Islet (on São Tomé) and another on the southwestern coast of Príncipe
(Sesani et al. 2020). The estimated group size of these sightings was 30 and
20 individuals, respectively. The group observed off Príncipe was composed of
adults and calves (Sesani et al. 2020). All the sightings of this species were within the
250 m bathymetry.
Feresa attenuata The Pygmy Killer Whale (Fig. 23.4, 6) occurs mainly in deep
warm tropical waters (Rice 1998). Off the north of São Tomé Island, two groups of
eight (in August) and 12 animals (in December) were recorded in 2012 (APCM
unpublished data). The eight Pygmy Killer Whales were sighted together with
rough-toothed dolphins at less than 100 m depth. The other 12 animals were sighted
around 450 m deep.
Globicephala macrorhynchus (Gray, 1846) There are two species of pilot whales:
the Short-finned Pilot Whale (Fig. 23.4, 7), which is mostly found in tropical waters,
23
Cetaceans of São Tomé and Príncipe
633
and the Long-finned Pilot Whale, Globicephala melas (Traill, 1809), which inhabits
colder waters. Picanço et al. (2009) reported a sighting in January 2003 of around
20 pilot whales as Long-finned Pilot Whales, mixed with Bottlenose Dolphins, off
the southeast coast of São Tomé, over the shelf edge (975 m). During this sighting,
eleven individuals were identified by photographs of the dorsal fins. The second
sighting of pilot whales was recorded in February 2012, a group of eight Shortfinned Pilot whales, including calves, traveling off the east coast of São Tomé
(APCM unpubl. data). Photographs confirmed that both sightings refer to Shortfinned Pilot Whales and that the most conspicuous individual identified in 2003 was
re-sighted after 9 years, suggesting long-term site fidelity that could also apply to
other individuals of the group.
Stenella attenuata (Gray, 1846) The Pantropical Spotted Dolphin (Fig. 23.4, 3)
occurs in tropical and subtropical waters (Rice 1998). This species is one of the most
frequently observed cetaceans in São Tomé, and it is present throughout the year.
Since 2002, a total of 37 sightings have been recorded off São Tomé Island;
14 sightings recorded by Picanço et al. (2009) and 23 afterward. Most sightings
were recorded over the slope (400–2000 m) to the north of São Tomé (APCM
unpublished data). More recently, this species was also recorded around Príncipe,
with five sightings (Sesani et al. 2020). The Pantropical Spotted Dolphin can form
large groups, ranging from a few animals to several hundred animals. The majority
of the sightings were groups of more than 100 animals. In 2012, one animal died
from by-catch in the south of São Tomé (Collins et al. 2019).
Stenella coeruleoalba The Striped Dolphin is a mostly oceanic species and occurs
in deep warm temperate, subtropical, and tropical waters worldwide (Rice 1998).
There was a single record of one stranded individual in March 2012, off the east
coast of São Tomé (Collins et al. 2019).
Tursiops truncatus (Montagu, 1821) The Common Bottlenose Dolphin (Fig. 23.4,
2) is a cosmopolitan species with a worldwide distribution in tropical and temperate
regions (Rice 1998). It is the most commonly sighted small cetacean species around
São Tomé and occurs regularly throughout the year (Pereira et al. 2013). The average
group size for this species was estimated at 45 individuals. Calves and juveniles were
sighted regularly with adults. Pereira et al. (2013) photo-identified 140 individuals
during sightings from 2002 to 2006 and 2012 around São Tomé. The sightings
occurred mainly around Rolas Islet and to the northeast of São Tomé (adjacent to
São Tomé city), sometimes very close to shore. Most sightings around São Tomé
were recorded below the 200 m bathymetry. Some of the individuals identified
showed a degree of site fidelity (Pereira et al. 2013). Eight individuals recorded
from 2002 to 2006 were resighted in 2012, and one of them was sighted in every
survey year. On several occasions, Bottlenose Dolphins were sighted in mixed
groups with other species, such as Sperm Whales (on two occasions), Pantropical
Spotted Dolphins, and Short-finned Pilot Whales. In 2020, there were five sightings
of this species along the northeastern coast of São Tomé, around the 250 m bathymetric, but none around Príncipe (Sesani et al. 2020).
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Threats, Conservation Needs, and Future Research
The Gulf of Guinea is one of the 18 global hotspots for marine biodiversity
conservation (Roberts et al. 2002). Globally, it is also one of the fastest developing
marine regions, and a highly productive ecosystem, that includes some of the most
productive coastal and offshore fisheries (Aryeetey 2002). This region also has
substantial oil and gas reserves. Marine species are therefore subject to a range of
pressures, such as incidental capture (by-catch) in fisheries, overfishing of their prey,
direct catch (meat and other products), as well as habitat loss and pollution, namely
linked to intense deep-water oil and gas exploration (Weir and Pierce 2013; Escalle
et al. 2015). The expansion of offshore hydrocarbon extraction activity has been a
concern for the populations using the waters of central Africa and the eastern Gulf of
Guinea (Findlay et al. 2006). Seismic surveys use high-amplitude sound sources,
that can have negative impacts on acoustically-sensitive animals such as cetaceans,
which can result in changes in habitat use, including spatial avoidance (Weir 2008;
Kavanagh et al. 2019), and behavioral changes (Cerchio et al. 2014; Dunlop et al.
2017). In recent years, several seismic surveys have been conducted in the EEZ of
São Tomé and Príncipe for future oil exploration (e.g., Anonymous 2018). Although
there was no assessment of the impact seismic surveying had on cetaceans in the
area, it is most likely that such extended surveys resulted in some degree of
responses by the animals.
In São Tomé and Príncipe, fishing provides more than 80% of the animal protein
consumed by the population (Maia et al. 2018). From 1955 to 2010, the number of
artisanal fishers in the archipelago increased by about 116%, from 1127 to 2428
(Maia et al. 2018). Moreover, catches by national semi-industrial fishing and foreign
industrial fishing (by the European Union, Japan, and China) have continued to
increase during recent decades (Carneiro 2011; EU 2019), despite a reduced capacity
for monitoring, control, and surveillance by national authorities (Belhabib 2015).
Maia et al. (2018) suggested a potential decline in the catch trends (mainly coastal) in
São Tomé and Príncipe’s artisanal fisheries. Declining catches and increasing fishing
efforts can lead fishermen to expand their fishing grounds further offshore, use
destructive fishing practices (such as explosives and grenades), use illegal gillnets,
and sometimes target different species (Santos 2017). Most sightings of cetaceans in
northern and southern São Tomé coincide with areas of intense artisanal fisheries.
Episodes of cetacean by-catch (Collins et al. 2019) and direct hunting of cetaceans
(APCM unpublished data) have been described in recent years. Fishermen themselves recognize that the problem of overexploitation of marine resources should be
addressed through the creation of marine reserves (Maia et al. 2018). So far, São
Tomé and Príncipe has not created any marine protected areas (MPAs), but presently
efforts are being made by local and international NGOs together with the government to propose a network of co-managed coastal MPAs (de Lima et al. 2022). Wellmanaged MPAs have been reported to lead to increases in marine biodiversity,
abundance, and biomass (Ballantine 2014; Grorud-Colvert et al. 2021), benefit
fisheries (Harrison et al. 2012), and improve the local economy.
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Cetaceans of São Tomé and Príncipe
635
In 2018, at the 67th IWC meeting, several countries from the Gulf of Guinea (São
Tomé and Príncipe included) voted, along with whaling nations, to re-establish
appropriate catch limits for some stocks/species, and voted against the proposal to
create a Whale Sanctuary in the South Atlantic (IWC 2018). Cetaceans in the waters
of São Tomé and Príncipe have no specific legal protection, although there are laws
regarding general aspects of environmental protection (Brito et al. 2010; DecreeLaw N 11/1999—Fauna and Flora conservation and protected areas; Decree-Law
N 6/2014—Marine turtles protection and Decree-Law N 22/XI/5a/2021—new
fisheries law mentions the creation of protected areas for cetaceans in important
regions for migration and/or feeding). There is a clear need for action at national and
regional levels to quantify the impact of human activities (especially by-catch and
direct take) and to implement legislation and measures for the protection of
cetaceans.
Cetacean research in the Gulf of Guinea has focused mostly around São Tomé
waters and in coastal areas, with some research on Príncipe and none at all on
Annobón. Broadening the survey area to include the islands of Príncipe and
Annobón, and covering a wider temporal window, may provide important information on the level of population structure, habitat use, and seasonal dynamics of
several cetacean species. In addition, extending the survey area to offshore waters
will provide new information on the more oceanic species (Bryde’s and Sperm
Whales, for example) that are present in other regions of the Gulf of Guinea, and
are expected to occur around the archipelago. Establishing the year-round monitoring of species composition, distribution, and abundance as well as identifying critical
habitats for cetacean survival and its overlap with human activities (specially
by-catch and direct takes) should be a priority for future research. This is especially
important since whale catches and recent sightings indicate that the region may be
important for several cetacean species (Picanço et al. 2009; Carvalho et al. 2011).
For the implementation of long-term population monitoring, it will be essential to
promote greater conservation efforts by involving local biologists and NGO technicians in training programs that include species identification, photography techniques, and collection of samples from stranded animals. Moreover, it is crucial to
engage with the local population and fisheries communities by developing conservation campaigns and targeting different stakeholders. By allying consistent research
and local awareness it will be possible to better understand and protect the cetaceans
of this region.
Acknowledgments We would like to thank the following people and institutions: the Government
of São Tomé and Príncipe for permission to conduct the studies, especially the former GeneralDirector for the Environment, Arlindo Carvalho. Vanessa Schmitt and Estrela Matilde from
Fundação Príncipe provided valuable information for Príncipe. Tim Collins and Howard
Rosenbaum, from the Wildlife Conservation Society, offered logistic and scientific support. Herbert
Maia, Cristina Picanço, Maria Pimentel, Carlos Carvalho, João Mendes, and Hipólito Lima were
invaluable in the field, as was the logistic support from the NGO MARAPA. We acknowledge
funding from: Rolas Island Resort, EU ECOFAC program, Wildlife Conservation Society, PPL
crowdfunding, French Facility for Global Environment (FFEM)—IUCN. IC was supported by the
Portuguese Foundation for Science and Technology, FCT (SFRH/BD/18049/2004, SFRH/BPD/
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I. Carvalho et al.
97566/2013, and IGC-DL57NT-32). AP was supported by FCT (UIDB/50019/2020 – IDL) and the
project AWARENESS (PTDC/BIA-BMA/30514/2017). NV was supported by CHAM (NOVA
FCSH / UAc), through the strategic project sponsored by FCT (UIDB/04666/2020). We would like
to thank Graham John Pierce and Caroline Weir for their helpful comments and suggestions, which
significantly improved this manuscript.
Appendix
Cetacean species confirmed for São Tomé and Príncipe. IUCN conservation status
(IUCN 2021): data deficient (DD); least concern (LC); near threatened (NT);
vulnerable (VU)
Higher taxonomy
Family Balaenopteridae
Megaptera Gray, 1846
Family Physeteridae
Physeter Linnaeus, 1758
Family Kogiidae
Kogia Gray, 1846
Family Delphinidae
Orcinus Fitzinger, 1860
Steno Gray, 1846
Grampus Gray, 1828
Pseudorca Reinhardt,
1862
Feresa Gray, 1870
Globicephala Lesson,
1828
Tursiops Gervais, 1855
Stenella Gray, 1866
Species
English name
IUCN
Megaptera novaeangliae
(Borowski, 1781)
Humpback Whale
LC
Physeter macrocephalus
(Linnaeus, 1758)
Sperm Whale
VU
Kogia sima
(Owen, 1866)
Dwarf Sperm Whale
LC
Orcinus orca
(Linnaeus, 1758)
Steno bredanensis
(Lesson, 1828)
Grampus griseus
(Cuvier, 1812)
Pseudorca crassidens
(Owen, 1846)
Feresa attenuata
(Gray, 1874)
Globicephala
macrorhynchus
(Gray, 1846)
Tursiops truncatus
(Montagu, 1821)
Stenella attenuata
(Gray, 1846)
Stenella coeruleoalba
(Meyen, 1833)
Killer Whale
DD
Rough-toothed Dolphin
LC
Risso’s Dolphin
LC
False Killer Whale
NT
Pygmy Killer Whale
LC
Short-finned Pilot Whale
LC
Common Bottlenose
Dolphin
Pantropical Spotted
Dolphin
Striped Dolphin
LC
LC
LC
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Cetaceans of São Tomé and Príncipe
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Chapter 24
Biodiversity Conservation in the Gulf
of Guinea Oceanic Islands: Recent Progress,
Ongoing Challenges, and Future Directions
Ricardo F. de Lima, Jean-Baptiste Deffontaines, Luísa Madruga,
Estrela Matilde, Ana Nuno, and Sara Vieira
Abstract The biodiversity of the oceanic islands of the Gulf of Guinea is valued
internationally for its uniqueness and locally for its contribution to human welfare,
but it is under growing anthropogenic pressure. We provide an overview of recent
progress, ongoing challenges, and future directions for terrestrial and marine conservation. The islands were colonized in the late fifteenth century and have since
relied heavily on international markets. Nevertheless, the livelihoods of many
islanders depend directly on local natural resources, and growing human populations
R. F. de Lima (*)
Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências,
Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon,
Portugal
Gulf of Guinea Biodiversity Centre, São Tomé, Sao Tome and Principe
J.-B. Deffontaines
Gulf of Guinea Biodiversity Centre, São Tomé, Sao Tome and Principe
BirdLife International, Cambridge, UK
L. Madruga
Fauna & Flora International, Cambridge, UK
Fundação Príncipe, Santo António, Sao Tome and Principe
E. Matilde
Fundação Príncipe, Santo António, Sao Tome and Principe
A. Nuno
Interdisciplinary Centre of Social Sciences (CICS.NOVA), School of Social Sciences and
Humanities, NOVA University Lisbon, Lisbon, Portugal
Centre for Ecology and Conservation, College of Life and Environmental Sciences, University
of Exeter, Penryn, UK
S. Vieira
Center of Marine Sciences (CCMAR), University of Algarve, Faro, Portugal
Associação Programa Tatô, São Tomé, Sao Tome and Principe
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_24
643
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and economies are intensifying the use of these resources, including timber, land,
and fisheries. Here we summarize conservation initiatives on the islands, including
pivotal projects and achievements, as well as the rise of civil society and governmental engagement. We also review species and site-based conservation priorities
and highlight the need for continuous updating based on ongoing research. Engagement in conservation has increased steadily in recent decades but not fast enough to
counteract the growth of anthropogenic pressure on biodiversity. Fostering capacity
building, environmental awareness, and research is thus urgent to ensure a thriving
future for the islands, able to reconcile economic development and biodiversity
conservation.
Keywords Endemics · Nature–human interactions · Prioritization · Protected areas ·
Research · Threatened species
Introduction
The oceanic islands of the Gulf of Guinea (Príncipe, São Tomé, and Annobón) are
widely recognized as global priorities for biodiversity conservation. Considering
their small size, they have exceptionally high numbers of endemic and threatened
species (Jones 1994). They are part of the “Guinean Forests of West Africa”
biodiversity hotspot (Myers et al. 2000) and of the “Cameroon-Guinea” Centre of
Plant Diversity (WWF and IUCN 1994). These islands also retain a high proportion
of natural vegetation cover (WWF 2019) compared to other oceanic islands (e.g.,
Norder et al. 2020), having relatively large extents of well-preserved native vegetation across lowland, montane, and mist forests (Exell 1944). Among the islands, mist
forests are exclusive to São Tomé and hold especially high numbers of endemic and
threatened plant species (Dauby et al. 2022; Stévart et al. 2022). Being mountainous,
the islands function as ecological and evolutionary refugia, offering a wide variety of
stable environments whose climates are buffered by the ocean (Ceríaco et al. 2022a).
Príncipe and São Tomé also have a few mangrove areas, which despite their small
size provide important ecosystem services (Afonso et al. 2021; Cravo 2021). The
islands are situated within one of the 18 global hotspots for marine conservation
(Roberts et al. 2002) and the most important marine biodiversity hotspot of the
“West African Coast” (Polidoro et al. 2017), which connects the eastern and western
Atlantic marine faunas (Wirtz et al. 2007). Their marine environments include areas
that are key for the life cycles of seabirds, marine megafauna (cetaceans, sea turtles,
rays, and sharks), and large, commercially valuable, pelagic, migratory fish species.
Here, we provide an overview of terrestrial and marine conservation in the
oceanic islands of the Gulf of Guinea. We start by describing the links between
biodiversity and livelihoods on the islands, focusing on the direct dependence of
people on natural resources, and on their unsustainable use, to understand current
threats to biodiversity. Then, we provide a brief history of conservation initiatives on
the islands, summarizing the history of conservation movements and providing an
overview of species conservation statuses and of sites prioritized for conservation.
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Biodiversity Conservation in the Gulf of Guinea Oceanic Islands:. . .
645
Finally, we highlight important lessons and ongoing challenges to define priorities
for the future of conservation on these unique islands.
People and Biodiversity: Close Together on Small Islands
The oceanic islands of the Gulf of Guinea are thought to have been uninhabited until
Portuguese sailors reached São Tomé on 21 December 1471, Príncipe on 17 January
1472, and Annobón on 1 January 1473 (Seibert 2016). European colonization of the
islands started during the fifteenth century and focused on the slave trade and on
exploiting cash crops, such as sugar cane, coffee, and cocoa (Eyzaguirre 1986). The
peoples of the islands thus derive mostly from a mixture of African and European
settlers (Hagemeijer and Rocha 2019; Almeida et al. 2021). The relatively recent
colonization and economic reliance on intensive agriculture are reflected in the
somewhat superficial connection to local nature when compared to other African
cultures, and instead bear stronger similarity with other colonial-based cultures, such
as those of many Caribbean islands (Eyzaguirre 1986). A connection with nature is
nevertheless embedded in the traditions of islanders, namely in the cuisine
(Gonçalves et al. 2014), medicine (Roseira 1984; Madureira et al. 2008), beliefs,
and worldviews (Valverde 2000).
The human population is unevenly split between islands: Príncipe is 139 km2 and
has 8778 inhabitants (65/km2), São Tomé is 857 km2 and has 201,462 inhabitants
(235/km2—INESTP 2019), and Annobón is 17 km2 and has 5314 inhabitants
(313/km2—INEGE 2018). The rugged terrain of the islands has meant that, up
until today, most people live by the coast (Norder et al. 2020), benefiting from
resources provided by both the ocean and the forest (e.g., Torres 2005; Pereira
2021). In addition, human activities are concentrated in the drier and flatter coasts
in the north of the islands, whereas the mountainous south and center are still
dominated by rainforest (Jones and Tye 2006). These contrasting landscapes provide
ecosystem services that are key for human wellbeing in the islands, and that islanders
recognize as essential: forests are important for pure air, water, foraged foods,
medicinal plants, and tourism, while plantations are key for agriculture, livestock,
and fruits (BirdLife International 2021a).
The economy of Annobón is mostly focused on services and relies on national
income resulting from oil revenues (INEGE 2018), while that of Príncipe and São
Tomé is heavily dependent on foreign aid and on export crops (INESTP 2019). All
islands are heavily reliant on imports, even though internal markets and the subsistence of most islanders are strongly based on agriculture and other activities on the
primary sector. Fisheries (Dias 2013), fuelwood and charcoal (Nuno 2021), and
timber (do Espírito et al. 2020) are essential to meet basic needs, and thus natural
resources are viewed as a primary source of protein, energy, and shelter that also
create diverse job opportunities. Some natural resources might play a small role in
subsistence overall, such as hunting (Carvalho et al. 2015a) and medicinal plants
(Madureira et al. 2008), but their significance should not be overlooked, even if it is
646
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predominantly cultural. Economic and cultural importance ascribed to introduced
species, some of which are invasive, also has relevant implications for conservation.
For instance, the West African giant land snail, Archachatina marginata (Swainson,
1821), is an important source of protein and income, particularly among vulnerable
social groups (Pereira 2021). More broadly, there is also a greater awareness of the
economic benefits and uses of introduced species than of the endemic-rich native
biodiversity, which might hinder willingness to adopt conservation measures
(Carvalho et al. 2015b; Panisi et al. 2022).
Having an economy largely based on cash crops has been, and still is, the defining
factor for the extent and severity of anthropogenic impacts on the environment.
Historically, deforestation and other key components of human impacts on the
islands have been decoupled from population size (Norder et al. 2020). This is
because human populations on the islands are heavily reliant on external markets,
producing agricultural goods to export and then importing much of what is consumed on the islands (Eyzaguirre 1986). Nevertheless, both the economy and the
human population have been rapidly growing in recent times. These increases are
most notable in São Tomé, which has rapidly been growing since the 2000s (MuñozTorrent et al. 2022) when malaria infections were greatly reduced (Lee et al. 2010).
The impacts of this growth are noticeable in the depletion of many natural resources
(Fig. 24.1), including timber (do Espírito et al. 2020), land conversion to agriculture
(de Lima 2012; Soares 2017), quarry species (Carvalho 2015), and fisheries
(Belhabib 2015; Maia et al. 2018; Nuno et al. 2021). The underlying effects of
less direct anthropogenic impacts, such as introduced species and climate change
remain largely unstudied (but see Brito 2013; Heleno et al. 2022).
Major threats to the conservation of terrestrial biodiversity identified by local
stakeholders include tree logging, land-use changes derived mostly from agricultural
pressure, hunting and collection of threatened and endemic species, invasive introduced species, and the development of macroprojects (BirdLife International 2019).
These threats strongly coincide with those that had already been identified for the
islands (Jones et al. 1991; Oyono et al. 2014; Ndang’ang’a et al. 2014a, b), and
largely match the most salient factors threatening species globally: habitat loss and
degradation; overexploitation; invasive species; pollution, and global climate change
(Vié et al. 2009).
Less is known about threats in marine environments. The overexploitation of
fisheries is certainly relevant: the Marine Trophic Index in São Tomé and Príncipe
scored 14.5 in a 0–100 range (Wendling et al. 2020), indicating that species higher in
the food web might have been fished out and that fishing is now targeting lower
trophic levels. Fisheries in São Tomé and Príncipe consist of small-scale activities
focused on the territorial sea, and of European-dominated industrial fleets that
extract most of the volume of fish removed from the Exclusive Economic Zone
(Porriños 2021). The evaluation of fish stocks and the control of fishing have been
almost inexistent, even though fishing agreements with the European Union represent 40% of the non-fiscal revenues of the country and are meant to promote
sustainable fishing (FAO 2019). Increased pressure on marine resources is leading
to the use of destructive practices that maximize catch in the short-term, but that
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Biodiversity Conservation in the Gulf of Guinea Oceanic Islands:. . .
647
Fig. 24.1 Examples of threats to the endemic-rich biodiversity of the oceanic islands of the Gulf of
Guinea: (1) Fire and agriculture shape the landscape in the driest portions of northern São Tomé;
(2, 3) Small plots of horticulture around Bom Sucesso threaten the endemic-rich montane forests of
São Tomé, encroaching on São Tomé Obô Natural Park; (4) Illegal selective logging is widespread
on São Tomé; (5) Several introduced species, such as the Mona Monkey Cercopithecus mona
(Schreber, 1774) threaten ecosystem function; (6) Charcoal production is widespread but particularly intensive in the drier north of São Tomé; (7) Hunting threatens several endemic birds, such as
the Endangered Sao Tome green-pigeon Treron sanctithomae (Gmelin, 1789); (8) Longline fishing
(baited hooks linked to short lines attached to a long main line) is a damaging practice that destroys
the ocean floor and results in bycatch and discarded fishing gear. Photo credits: (1–3, 6) JeanBaptiste Deffontaines, (4, 5) Ricardo F. de Lima, (7) Ricardo Rocha, (8) Luísa Madruga
648
R. F. de Lima et al.
threaten biodiversity, the livelihoods of coastal communities, and food security on
the islands in the long term. The exploration of mineral resources in the oceans is
increasingly a threat since large deposits of petroleum were found offshore in
the 1990s. These are yet to be extracted but are already boosting the economy of
the island (Frynas et al. 2003). Finally, there is also evidence that the waters around
Annobón have been used to dump large quantities of toxic waste and that these
activities have affected its marine life (Wood 2004).
Conservation Initiatives
Early in the twentieth century, several authors expressed concerns about the environmental implications of deforestation linked to the expansion of cocoa plantations
on the islands, mentioning several actions to ensure the future of remaining forests,
such as the protection of mountaintops (e.g., Campos 1908; Henriques 1917). These
might be the first conservation safeguards known to take place on the islands.
However, the collapse of the economy based on export crops (Eyzaguirre 1986),
the focus of colonial scientific research on agricultural production, the poor local
capacity and, later on, political instability linked to the post-independence period
(Cruz 2014) meant that, for many decades biodiversity research was fairly limited
(Ceríaco et al. 2022b). Only in the late 1980s, the first initiatives based on modern
principles of conservation (Soulé 1985) started taking shape, following a few
successful expeditions to the islands (Jones and Tye 1988; Jones et al. 1991;
Atkinson et al. 1991).
In 1993, a workshop took place in Jersey (United Kingdom), bringing together
several scientists to assess knowledge on the biodiversity of the Gulf of Guinea
islands (including Bioko) and define priorities for future research and conservation
action (Juste and Fa 1994). The Gulf of Guinea Conservation Group emerged from
this meeting and was the umbrella under which many scientists visited the islands
over the next two decades, in great part thanks to the efforts of Angus Gascoigne,
who resided in São Tomé and facilitated links to local institutions (Melo 2012).
Also, in 1993, the European Commission started funding the ECOFAC program,
aiming to promote the conservation and sustainable use of forest ecosystems in
central Africa (Table 24.1). Besides promoting numerous studies, ECOFAC was
fundamental to many of the conservation efforts that have since taken place in São
Tomé and Príncipe (Fig. 24.2), such as the establishment of terrestrial protected areas
and other environmental legislation, the creation of the Bom Sucesso Botanical
Garden and São Tomé and Príncipe National Herbarium (STPH; NYBG 2021),
and the training of many islanders and foreigners that still work toward conservation
on the islands. The Global Environment Facility has been another key source of
funding for conservation on the islands over the last two decades (Table 24.1). More
recently, other sources of funding, such as the Critical Ecosystem Partnership Fund
(CEPF 2021) or the Rufford Small Grants for Nature Conservation (The Rufford
Foundation 2021) have allowed smaller projects to develop important
Period
Funding
1992–1997 783 k€ + Technical Assistance (European
Commission)
ECOFAC.2—Establish the
management structure of the
Obô Natural Park
1997–2001 645 k€ + Technical Assistance (European
Commission)
Programa Tatô
1998–
ongoing
GEF-2—Biodiversity Strategy, Action Plan and First
National Report and Clearing
House Mechanism
2000–2005 163 k$ (through The World
Bank)
Department for the
Environment
ECOFAC.3—Development
of tourist activities and support for the promotion of sites
2001–2005 600 k€ + Technical Assistance (European Commission) + 250 k€ (AFD)
AGRECO + SECA +
CIRAD Forêt
Currently c. 250 k€/year
(USFWS + Oceanário de
Lisboa + Tusk Conservation
+ FFEM + private sector)
Implementation
AGRECO + CIRAD Forêt
Description
Preparatory work for the designation of a protected area;
research program—inventory
& management-oriented, and
evaluation of the area.
Protected Area Management
AGRECO + BDPAPlan & Management StrucSCETAGRI + SECA +
ture, including research &
CIRAD Forêt + FFI
ecological monitoring, and
institutional support to the
forest
Associação Programa Tatô + Sea turtle conservation program in São Tomé Island
MARAPA (1998–2002:
ECOFAC; 2002–2017:
MARAPA)
Source
Muriel Vives (pers.
comm.)
Muriel Vives (pers.
comm.)
Betânia FerreiraAiraud (pers.
comm.); Associação
Programa Tatô
(2021)
GEF (2021)
(continued)
649
Enable the Government of
São Tomé and Príncipe to
develop a biodiversity strategy in compliance with CBD
and to identify priority
actions for biodiversity conservation and management
Development of ecotourism Muriel Vives (pers.
activities. Support to the Obô comm.)
Natural Park. Botanical Garden. Scientific research for
the conservation of marine
turtles, gray parrots. Conservation measures to limit
charcoal, sand extraction, etc.
Biodiversity Conservation in the Gulf of Guinea Oceanic Islands:. . .
Project
ECOFAC.1—Support the
creation of the Obô Natural
Park
24
Table 24.1 Key conservation projects in São Tomé and Príncipe. The details of equivalent programs that have focused on Annobón are not known
650
Table 24.1 (continued)
Project
ECOFAC.4—São Tomé and
Príncipe Obô Natural parks
Period
Funding
2007–2010 595 k€ (European
Commission)
Implementation
BRL Ingenieurie + GFA
Consulting Group + DFS
GEF-5—Integrated ecosystem approach to biodiversity
mainstreaming and conservation in the Buffer Zones
2011–2017 2.4 M$ (through IFAD)
Directorate of Environment
+ Directorate of Agriculture
and Rural Development
ECOFAC.5—Strengthen
eco-tourism around São
Tomé Obô Natural Park
2012–2015 200 k€ (European
Commission)
ONG Alisei + MARAPA
Protetuga
Currently c. 150 k€ / year
(OAK Foundation, Kosmos,
HBD, Rufford, USFWS,
YWPF, CEPF)
2016–2019 295 k£ (Darwin Initiative)
Fundação Príncipe
University of Exeter +
Fundação Príncipe
Improved food security,
increased gender equality,
and poverty reduction in
coastal communities in
Príncipe, through a socialecological approach to
enhance marine resource
management and diversify
livelihood opportunities
Source
David Bruguière
(pers. comm.)
GEF (2021)
Bastien Loloum
(pers. comm.)
Estrela Matilde
(pers. comm.);
Fundação Príncipe
(2021a)
Darwin Initiative
(2021); Fundação
Príncipe (2021d)
R. F. de Lima et al.
Omali Vida Nón 1—Improving Marine Biodiversity and
Livelihood of coastal communities in Príncipe
2015–
ongoing
Description
Natural Parks (São Tomé
Obô natural Park, Príncipe
Natural Park), and respective
buffer zones management
Rehabilitate degraded ecosystems in STP to provide
ecosystem services and habitat for endemic species of
flora and fauna of global
importance
Strengthen the
co-management of the conservation systems of the Obô
Natural Park and its periphery, particularly around the
Malanza and Jalé mangroves
Sea turtle conservation program in Príncipe Island
Blue Action Fund—
Establishing a network of
marine protected areas across
São Tomé and Príncipe
through a co-management
approach
Taking action for Príncipe’s
threatened trees
Action for sustainable landscape management in São
Tomé and Príncipe
Contribute to sustainable
fisheries, conservation of
marine biodiversity, and food
security for the Santomean
population
Natural Parks (São Tomé
2018–2022 2 M€ (European
BirdLife International +
Obô natural Park, Príncipe
Commission)
Oikos + RSPB + SPEA+
Natural Park), and respective
Plataforma de Turismo
buffer zones, through landResponsável e Sustentável
scape approaches
2018–2023 2.59 M€ (Blue Action Fund + Fauna & Flora International Support the designation of
Arcadia Fund)
+ Oikos + Fundação Príncipe the first co-managed Marine
Protected Areas across São
+ MARAPA
Tomé and Príncipe
2019–2022 104 K£ (Global Trees
Campaign)
2021–2024 2.32 M€ (European Union)
Oikos + MARAPA
Missouri Botanical Garden,
Herbarium of Université
Libre de Bruxelles, University of Coimbra, FFI,
Fundação Príncipe, Institut
de Recherche pour le
Développement
Oikos + BirdLife International + Zatona-ADIL
Oikos and
MARAPA (2021)
EC (2021);
ECOFAC6 (2021)
BAF (2018);
Fundação Príncipe
(2021d); Oikos and
MARAPA (2021)
Generate data and build local Estrela Matilde
(pers. comm.)
capacity for research and
conservation through field
surveys, monitoring and
threat assessment for three
threatened tree species
EU (2021)
Improve the use of natural
resources through integrated
landscape management, for
sustainable access to food,
wealth, and the preservation
of the Obô Natural Park and
São Tomé High Conservation
Value forests
651
(continued)
Biodiversity Conservation in the Gulf of Guinea Oceanic Islands:. . .
ECOFAC.6—São Tomé and
Príncipe Obô Natural Parks
2017–2020 581 k€ (European Union +
Instituto Camões)
24
Kike da Mungu 1—Sustainable co-management of fisheries in the south of São
Tomé Island
652
Table 24.1 (continued)
Project
GEF-6—Enhancing Biodiversity Conservation and
Sustainable Land and Natural
Resource Management
Period
Funding
2021–2025 4.28 M$ (through UNDP)
Implementation
General Directorate for the
Environment
GEF-7—Improving biodiversity mainstreaming in the
agro-forestry and fishery sectors in São Tomé and
Príncipe
Concept
approved
Ministry of Agriculture,
Fisheries, and Rural
Development
3.55 M$ (through IFAD)
Description
Source
Safeguard globally signifiGEF (2021)
cant terrestrial biodiversity
and ecosystems services by
strengthening national capacities and frameworks for biodiversity and natural resource
management (. . .)
Mainstream biodiversity con- GEF (2021)
servation (. . .) to minimize
the negative impacts of the
agro-forestry and fishery sector development while
enhancing the contribution of
ecosystem services to livelihoods in São Tomé and
Príncipe
R. F. de Lima et al.
24
Biodiversity Conservation in the Gulf of Guinea Oceanic Islands:. . .
653
Fig. 24.2 Examples of conservation initiatives that have been taking place in the oceanic islands of
the Gulf of Guinea: (1) Sign marking the boundary of the São Tomé Obô Natural Park; (2) Small
trees being distributed in a school in the buffer zone of the São Tomé Obô Natural Park; (3) An Obô
guardian surveying the forests of São Tomé; (4) The orchidarium at the Bom Sucesso Botanical
Garden in São Tomé; (5) Sea turtle hatcheries are used to protect nests at risk from feral animal
predation, poaching and beach erosion in São Tomé and Príncipe; (6) Inspection of illegal logging
activities in a forest in Príncipe; (7) Freshwater macroinvertebrates surveys in Rio Papagaio,
Príncipe; (8) Young parabotanist surveying tree diversity in Príncipe. Photo credits: (1) Ricardo
F. de Lima, (2) Raphaela Nazaré, (3, 4, 6) Jean-Baptiste Deffontaines, (5) Maria Branco, (7, 8)
Vasco Pissarra | Fundação Príncipe
654
R. F. de Lima et al.
complementary tools for conservation. Previous phases of ECOFAC have also
covered Equatorial Guinea, where it coincided with the EU-funded project of
Conservation and Rational Use of Forest Ecosystems (Conservación y Utilización
Racional de los Ecosistemas Forestales—CUREF 1996–2001), aiming to describe
ecosystems, to promote sustainable use of natural resources, and to create a network
of protected areas (García and Eneme 1997, Angela Formia pers. comm.). However,
it is unclear how these have contributed to creating the Annobón Nature Reserve or
any other conservation initiative on the island.
Since 2016, there has been a noticeable and much needed increased investment in
coastal and marine conservation, focusing on sustainable fisheries through engagement with coastal fishing communities (Table 24.1), namely through the Omali vida
nón project in Príncipe (Nuno 2019; FFI et al. 2021; Fundação Príncipe 2021d), and
the Kike da mungu project in São Tomé (Oikos and MARAPA 2021). Building on
these, since late 2018, Fauna & Flora International, in close collaboration with the
government authorities, has partnered with Fundação Príncipe, Oikos, and
MARAPA to establish a network of co-managed marine protected areas across
São Tomé and Príncipe (BAF 2018). There have been significant efforts for the
conservation of sea turtles on both of these islands (Associação Programa Tatô 2021;
Fundação Príncipe 2021a; Ferreira-Airaud et al. 2022). There has also been some
research on cetaceans in São Tomé (MARAPA 2021b), and in June 2021 a project
has been approved to study the little known but highly threatened shark populations
of São Tomé and Príncipe (NGANDU 2021).
Parallel to increased funding, civil society awareness toward conservation has
also greatly increased over the past few decades, which is clearly reflected in the
number and impact of local environmental non-governmental organizations (Ayres
et al. 2022). MARAPA has been active in marine conservation initiatives for São
Tomé Island, promoting sustainable fisheries and environmental education since its
creation in 1999 (MARAPA 2021a). Associação Monte Pico emerged in 2006 from
a group of Santomeans trained by ECOFAC; it has been working for sustainable
ecotourism and rurality, and supporting scientific research and the management of
protected areas (Associação Monte Pico 2021). Founded in 2015, Fundação Príncipe
focuses on marine and terrestrial biodiversity conservation and the socio-economic
development of Príncipe Island, in close partnership with regional authorities and
communities (Fundação Príncipe 2021b). Since 2017, Rede.Bio has brought
together seven environmental NGOs from São Tomé and Príncipe to promote
integrated and sustainable development based on the protection and valorization of
the natural heritage of the country, namely by reinforcing the participation of civil
society in environmental governance (Rede.Bio 2021). Most recently, on October
16, 2020, the Gulf of Guinea Biodiversity Center had its inaugural meeting, bringing
together national and international scientists and conservationists in an initiative that
aims to facilitate research, education, and conservation of the unique diversity of the
plants and animals of the islands (GGBC 2021).
Several international environmental organizations have also increased their presence in São Tomé and Príncipe. BirdLife International has had a long-term interest in
these islands and has been increasing its presence especially since 2012, working
24
Biodiversity Conservation in the Gulf of Guinea Oceanic Islands:. . .
655
with park authorities and other governmental institutions, and with communities to
promote research, conservation, and empowerment. In 2018, BirdLife opened an
office in country (BirdLife International 2021d). Fauna & Flora International has
been working closely with Fundação Príncipe since its inception in 2015, to build
conservation capacity, conduct research, raise environmental awareness, and diversify the livelihoods of communities on Príncipe (FFI 2021). Oikos—Cooperação e
Desenvolvimento has had a growing presence in São Tomé and Príncipe since 2015,
working toward the rational use of natural resources and enhanced livelihood in
communities (Oikos 2021). In 2018, the international NGO Associação Programa
Tatô was created to continue the work on marine conservation focusing on sea turtles
that had been initiated by ECOFAC and MARAPA on São Tomé (Associação
Programa Tatô 2021).
Little is known about conservation initiatives on Annobón, besides a few small
conservation projects led by the national NGO Amigos de Natureleza y Desarollo de
Guinea Ecuatorial (ANDEGE).
Over the last few decades, the São Tomé and Príncipe and Equatorial Guinea
governments have also shown a strong national and international commitment to
developing policies aiming to ensure the conservation of biodiversity (Appendix). In
São Tomé and Príncipe, environmental responsibilities are split between the General
Directorate for the Environment (part of the Ministry of Infrastructures, Natural
Resources and Environment), the Fisheries Directorate, and the Forest and Biodiversity Directorate (both part of the Ministry for Agriculture, Fisheries and Rural
Development). Príncipe is an autonomous region that has its own Regional Government, where environmental responsibilities are also split but following a distinct
organization. This complex administrative structure, which often changes when a
new government takes power, hinders progress and post-project sustainability of
conservation initiatives. In Equatorial Guinea, the National Institute for Forestry
Development and Protected Areas Management (INDEFOR-AP) from the Ministry
of Agriculture and Forests has developed a national network of protected areas and is
responsible for environmental and wildlife conservation but little is known about the
local government structure in the province of Annobón.
Threatened Species
The oceanic islands of the Gulf of Guinea hold several hundred endemic species, a
number that will certainly increase as new endemics are still being described every
year, even among the best-known taxonomic groups (de Lima 2016). Many of the
endemic species are at risk of extinction and only terrestrial vertebrate species have
been thoroughly evaluated (IUCN 2021). Out of 67 endemic species of terrestrial
vertebrates, 58 have been assessed, and 18 are threatened. These include 11 birds
(Melo et al. 2022), three mammals (Rainho et al. 2022), one reptile (Ceríaco et al.
2022c), and three amphibians (Bell et al. 2022). Of these species, four are Critically
Endangered, ten are Endangered, and four are Vulnerable. Among terrestrial
656
R. F. de Lima et al.
vertebrates, there are also seven Data Deficient, seven Near Threatened, and nine
species that are not recognized or have not been assessed. Finally, both Príncipe and
São Tomé have populations of the non-endemic Endangered Gray Parrot Erithacus
psittacus Linnaeus, 1758.
Scientific research in coastal and marine environments is still scarce and mostly
dedicated to studies of ichthyofauna. Fishes are the only non-terrestrial vertebrate
group with endemic species (but see Flood et al. 2019). Out of 15 endemic species
(Costa et al. 2022), only eight have been assessed (IUCN 2021): three Vulnerable
and five Data Deficient. There are also large numbers of non-endemic fish species
that are threatened including 6 Critically Endangered (all cartilaginous fishes),
15 Endangered (only two bony fishes), and 28 Vulnerable species (of which
16 are bony fishes). Additionally, 58 species are Data Deficient (all bony fishes)
and nine are Near Threatened (including three cartilaginous fishes). The remaining
threatened marine vertebrates are the Critically Endangered Hawksbill Turtle
Eretmochelys imbricata (Linnaeus, 1766), the Endangered Green Turtle Chelonia
mydas (Linnaeus, 1758), the Vulnerable Sperm Whale Physeter macrocephalus
Linnaeus, 1758, and three Vulnerable sea turtle species (Ferreira-Airaud et al.
2022). Additionally, there are also the Data Deficient Killer Whale Orcinus orca
(Linnaeus, 1758), the Near Threatened False Killer Whale Pseudorca crassidens
(Owen, 1846), and ten Least Concern cetacean species (Carvalho et al. 2022).
Very few endemic terrestrial invertebrates have been assessed by the IUCN: four
mollusks, two crabs, one butterfly, and one dragonfly species, of which half are Data
Deficient, two Near Threatened, one Least Concern, and only the Vulnerable Búziod’Obô Archachatina bicarinata (Bruguiere, 1792) is classified as threatened.
Among the endemic marine invertebrates, only 23 species of mollusks have been
assessed, all of which are Data Deficient, apart from the Vulnerable Haliotis geigeri
Owen, 2014.
Among plants, 272 species have been assessed (IUCN 2021) out of a total that
should exceed 1700 species (Garcia et al. 2022; Stévart et al. 2022). Out of almost
200 endemic plant species, only 49 have been assessed. These include two Extinct,
two Critically Endangered, 14 Endangered, 22 Vulnerable, and 7 Near Threatened.
Additionally, there are seven Endangered, 11 Vulnerable, 6 Near Threatened, and
1 Data Deficient plant species that are not endemic. Considering ongoing work,
especially focusing on describing and red-listing seed plant species (Fundação
Príncipe et al. 2021), it is evident that these numbers will greatly increase soon
(Stévart et al. 2022). The situation is even more dire when it comes to fungi, a group
for which Red List evaluations are scarce, with none of the species of the oceanic
islands of the Gulf of Guinea assessed so far (Desjardin and Perry 2022).
In 2004, amphibians, mammals, and birds were fully assessed for the first time
(IUCN 2021). At that point, there were 38 recognized endemic species in these
taxonomic groups, of which there were 14 threatened species (five Critically Endangered, three Endangered, and six Vulnerable), compared to the current 17 threatened
species (four Critically Endangered, nine Endangered, and four Vulnerable) out of
45 recognized endemics. These trends reflect mostly an improvement of knowledge,
showing that even among some of the best-studied groups there have been major
24
Biodiversity Conservation in the Gulf of Guinea Oceanic Islands:. . .
657
changes not only in the Red List status but also in taxonomy. The high numbers of
species that are still being described, that have not yet been assessed, or that remain
Data Deficient attest to the urgent need for future work in the region. There has been
an attempt to list species at the national level in São Tomé and Príncipe (Gascoigne
1995), but in recent years all assessments have been directly linked to the IUCN Red
List because most species of interest are endemic, and therefore national assessments
are also global.
In addition to the IUCN Red List, there are other tools to define priorities for
species conservation. The EDGE of Existence is an example that combines the
IUCN Red List status with the amount of unique evolutionary history represented
by species of terrestrial vertebrates, cartilaginous fishes, and corals (EDGE 2021).
This program has identified 31 species on the islands, including 16 cartilaginous
fishes, one amphibian, three sea turtles, one cetacean, and ten birds as high priority.
The Critically Endangered Dwarf Olive Ibis Bostrychia bocagei (Chapin, 1923), and
the Endangered Newton’s Grassland Frog Ptychadena newtoni (Bocage, 1886)
ranked the highest among terrestrial species, while the Critically Endangered
Hawksbill Turtle and the Endangered Whale Shark Rhincodon typus Smith, 1828
ranked the highest in the ocean.
After identifying priority species for conservation, it is also essential to define
strategies for conservation action. In these islands, so far only the Critically Endangered birds (Ndang’ang’a et al. 2014a, b—currently under review, Fundação
Príncipe 2021c) and the Vulnerable Búzio-d’Obô (Panisi et al. 2020) have Species
Action Plans dedicated to defining priority activities for conservation, further
highlighting the long road ahead toward defining conservation priorities and
implementing effective conservation action.
Site-Based Conservation
Several assessments have identified areas of global conservation relevance in the
oceanic islands of the Gulf of Guinea (Fig. 24.3). The islands include three Alliance
for Zero Extinction sites: “Príncipe Forests” (5712 ha), “Sao Tome Uplands”
(28,660 ha), and “São Tomé Lowland Forests” (21,833 ha—AZE 2019). These
largely coincide with Key Biodiversity Areas (“Príncipe Forests”: 5708 ha; “São
Tomé Montane and Cloud-forests”: 4839 ha; and “São Tomé Lowland Forests”:
21,832 ha—currently under review), of which there are five more on the islands:
“Annobón” (2891 ha), “Tinhosas Islands” (18 ha), “São Tomé Northern Savannas”
(526 ha), “Parque Natural Obô de São Tomé e Zona Tampão” (45,132 ha), and
“Zona Ecológica dos Mangais do Rio Malanza” (231 ha—BirdLife International
2021c). The Tinhosas are a Ramsar site, due to their important seabird colony, as is
the whole island of Annobón and surrounding waters (230 km2), mostly due to the
threatened species and ecological assemblages it supports (Ramsar 2021). As part of
the “Congolian Coastal Forests,” the “São Tomé, Príncipe and Annobón moist
lowland forests” (WWF 2019) are listed as Critical or Endangered Terrestrial
658
R. F. de Lima et al.
Fig. 24.3 Map of sites prioritized for conservation in the oceanic islands of the Gulf of Guinea: (1)
Príncipe Biosphere Reserve (UNESCO 2021); (2) São Tomé Key Biodiversity Areas (BirdLife
International 2021c); (3) São Tomé Obô Natural Park, buffer zone and preliminary High Conservation Value areas (BirdLife International et al. 2020; UNEP-WCMC and IUCN 2021); (4)
Annobón Nature Reserve (UNEP-WCMC and IUCN 2021). The nuclear terrestrial area of the
Príncipe Biosphere Reserve corresponds to the Príncipe Natural Park, and the buffer corresponds to
the buffer of the Natural Park. To the southwest of Príncipe Island, the marine protected areas
demarcated around the Tinhosas Islets are a Ramsar site and a Key Biodiversity Area. The
boundaries of the São Tomé lowland forests Key Biodiversity Area are not aligned with the contour
of the island and will be revised in the ongoing national reassessment of Key Biodiversity Areas
Ecoregions of the World (Olson and Dinerstein 2002) and have been identified
among the most important ecoregion for the conservation of forest-dependent birds
worldwide (Buchanan et al. 2011). Due to the unique assemblage of bird species,
each of the main islands is a separate Endemic Bird Area, and they rank on the three
highest priority categories of this assessment: São Tomé is critical, Príncipe is
urgent, and Annobón is high (Stattersfield et al. 1998; BirdLife International
24
Biodiversity Conservation in the Gulf of Guinea Oceanic Islands:. . .
659
2021b). Since 2012, Príncipe has been recognized as a UNESCO Biosphere Reserve
that includes the Tinhosas, all other islets around the main island, and 576 km2 of
surrounding marine environment (UNESCO 2021).
As a result of its rich and productive marine life, the region has three Ecologically
or Biologically Significant Marine Areas: “Tinhosas Islands,” “Lagoa Azul and
Praia das Conchas,” and the “Equatorial Tuna Production Zone” (CBD 2021).
At the national level, each island has one protected area: the Annobón Natural
Reserve, created in 2000 includes the whole island and surrounding marine environments (230 km2), the São Tomé Obô Natural Park (252 km2), and the Príncipe
Obô Natural Park (45 km2), both created in 2006, the latter also including a strip of
coastal ecosystems (Fig. 24.3, Appendix—UNEP-WCMC and IUCN 2021). The
last two cover the wettest and most rugged portions of each island, where the bestpreserved forests remain and are critical for the survival of many endemic species,
especially the most threatened (e.g., de Lima et al. 2017; Soares 2017; Fundação
Príncipe 2019; Soares et al. 2022). Taken together, they were assessed as the 32nd
most important protected area in the world for the conservation of mammals, birds,
and amphibians, the 17th if only threatened species are considered, and the 2nd ex
aequo if only threatened bird species are counted (Le Saout et al. 2013). Unfortunately, despite having management plans (Albuquerque and Carvalho 2015a–d—
currently under review) and receiving significant funding (Table 24.1), the effective
implementation and success of both parks is lacking, largely due to a lack of stable
and reliable sources of funding (BirdLife International 2019). A sustainable finance
plan for protected areas and biodiversity is currently assessing best-revenue options,
while several initiatives are already promoting implementation (Natural Strategies
2021). In São Tomé and Príncipe, the first efforts to create marine protected areas are
only now taking place (Table 24.1—FFI et al. 2021).
There have been several national initiatives in recent years aimed at identifying
additional areas that are relevant for conservation, beyond the strict concept of
protected areas (Fig. 24.3). The laws that created both Obô Natural Parks (Appendix)
envisaged the existence of a buffer zone, which would extend at least 250 m around
the park boundaries, whenever possible, to work as a transition zone that would
minimize the impact of human activities in the core protection area. These buffer
zones are widely recognized and have received international funding (Table 24.1),
but their boundaries and regulations were never clearly defined, and seem to have
limited success at minimizing human impacts (Ward-Francis et al. 2017). Since
2018, BirdLife International has been leading the identification of High Conservation Values areas in São Tomé terrestrial and coastal ecosystems (BirdLife
International et al. 2020), an initiative that is now being extended to Príncipe
(D’Avis 2022). Since 2016, the Ministry of Infrastructures, Environment and Natural Resources of São Tomé and Príncipe, funded by the African Development Fund
(Table 24.1) has been working on a national land planning initiative, which has
identified large extents around the protected areas on each island as Conservation
Areas (MIRNASTP 2021).
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These initiatives should be continuously revised, since current knowledge on the
distribution of biodiversity is still limited (Dauby et al. 2022; Soares et al. 2022).
Ideally, these should be mostly based on the prioritization of ecosystem types to
ensure that the best-preserved and most unique components of biodiversity are
maintained. So far, the typification of ecosystems on the islands is not yet well
established (Dauby et al. 2022). Areas at higher altitudes harbor endemic-rich and
threatened ecosystems, even though biased sampling has limited our understanding
of patterns along the altitudinal gradient (Stévart et al. 2022). The characterization
and distribution of spatially restricted ecosystems, such as wetlands and coastal or
rupicolous forests, constitutes a particularly pertinent challenge, since these hold
specific plant associations (Diniz and Matos 2002; Dauby et al. 2022) and have
unique ecologies that ensure key ecosystem services (e.g., Afonso et al. 2021) and
thus deserve targeted conservation action. The peculiar palustrine system of Lagoa
Amélia in São Tomé is one such example, holding several species that have highly
restricted ranges (e.g., Stévart and Oliveira 2000) and the source of the springs that
feed all main rivers in the north of the island. In this regard, the newly developed
IUCN Red List for Ecosystems (Keith et al. 2015) might prove an invaluable tool.
Concluding Remarks
Príncipe, São Tomé, and Annobón are widely recognized as global priorities for
biodiversity conservation, mostly due to their extraordinary number of endemic
species. The value of their biodiversity is also promptly acknowledged by the
islanders for the valuable services they provide and is engrained in the local culture.
Nevertheless, the fast-growing population and economy, heavily reliant on the
exploitation of natural resources, are threatening the long-term persistence of this
precious natural heritage. Knowledge, awareness, attitudes, and investment in the
conservation of the endemic-rich biodiversity of the islands have improved in recent
decades but not fast enough to counteract the growth of anthropogenic pressure on
natural resources. Remoteness and insularity, a colonial past and conflicting land
tenure structures since independence, inadequate legal frameworks, weak institutional capacity to monitor and enforce laws, social inequity, and poor governance, all
contribute to the environmental deregulation that threatens the biodiversity of the
islands. While natural resources, like forests and fisheries are state-controlled in
theory, high rates of non-compliance mean that these are de facto open access.
Although our knowledge of the biodiversity of the islands is still very incomplete,
key priorities for conservation are mostly clear and should be the focus of future
conservation activities. The exceptions are marine environments and Annobón,
where biodiversity remains particularly understudied. Current knowledge must be
used to expand the network of protected areas in marine and terrestrial environments,
and to ensure effective protection of the best-preserved and keystone ecosystems.
24
Biodiversity Conservation in the Gulf of Guinea Oceanic Islands:. . .
661
Likewise, management mechanisms that enhance the role of biodiversity for development, for instance through ecotourism, sustainable extraction of forest products,
or payment for ecosystem services should be implemented. More broadly,
biodiversity-friendly practices and alternative livelihoods should be mainstreamed
into the economic and social development of communities to reduce pressure on
natural resources by maintaining diverse agroforests, promoting sustainable levels of
resource exploitation (e.g., fisheries, hunting, or timber logging), or even enhancing
the biodiversity value of sites through business-based restoration mechanisms. More
specific activities might also be necessary and highly beneficial for sensitive species
or ecosystems, as is the case of restoring degraded wetlands, protecting sea turtle
breeding sites, controlling invasive species, or even promoting conservation ex situ
of highly threatened species.
There have also been an increasing number of initiatives aiming to improve
environmental awareness on the islands (Ayres et al. 2022), which is vital to boost
public support and locally-led initiatives, ultimately contributing toward more robust
conservation. In addition, making biodiversity information more accessible (e.g.,
GBIF 2021) will strengthen local capacity and engagement in conservation. All
these actions would benefit from continued research, but enough is already known to
make biodiversity conservation a political priority and to improve conservation
management.
The success of conservation on the islands will ultimately rely on public support,
therefore it is pivotal to continue listening, informing, training, and engaging island
inhabitants and institutions, to ensure that conservation projects are inclusive. Much
has already been done in this regard, and conservation initiatives are increasingly
moving toward integrating local needs and sensibilities, particularly through
enhanced investment in in-country leadership for successful conservation. Nevertheless, there is still a difficult road ahead, as it is not always straightforward to
balance biodiversity conservation with human needs to find truly sustainable development models. Reaching economic development and conservation goals must
center on empowerment and equity, while considering trade-offs in a transparent
and participatory approach. Only by promoting the involvement of diverse stakeholders working toward a shared vision, and through the co-development of integrative strategies, will we be able to ensure a thriving future for the unique
biodiversity and human inhabitants of the islands.
Acknowledgments We want to thank Bastien Loloum, Betânia Ferreira-Airaud, David Bruguière
and Muriel Vives for sharing information used to create Table 24.1, and Angela Formia for sharing
information on Annobón. RFL benefitted from cE3c structural funding by the Portuguese Government through “Fundação para a Ciência e a Tecnologia” (FCT/MCTES – UID/BIA/00329/2021),
who also supported SV with a PhD grant (SFRH/BD/05970/2020). AN acknowledges the support
of the European Union’s Horizon 2020 research and innovation program under the Marie
Skłodowska-Curie grant agreement SocioEcoFrontiers No. 843865.
662
R. F. de Lima et al.
Appendix: International Agreements and National
Legislation and Strategies Relevant to Biodiversity
Conservation
International agreements adhered to by the Democratic Republic of São Tomé and
Príncipe (STP) and the Republic of Equatorial Guinea (EG):
• Framework Convention on Climate Change (1992 – STP; 2000 – EG)
• Convention on International Trade in Endangered Species of Wild Fauna and
Flora (1992 – EG; 2001 – STP)
• Convention to Combat Desertification (1994 – EG; 1995 – STP)
• Convention on Biological Diversity (1995 – EG; 1998 – STP)
• Kyoto Protocol (2000 – EG; 2008 – STP)
• Bonn Convention on the Conservation of Migratory Species of Wild Animals
(2001 – STP; 2010 – EG)
• Ramsar Convention on Wetlands of International Importance Especially as
Waterfowl Habitat (2003 – EG; 2006 – STP)
• Convention concerning the Protection of the World Cultural and Natural Heritage
(2006 – STP; 2010 – EG)
• Agreement on Port State Measures to Prevent, Deter and Eliminate Illegal,
Unreported and Unregulated Fishing (2016—STP)
• Nagoya Protocol on Access and Benefit Sharing (2017 – STP)
Biodiversity conservation legislation—STP (Carvalho and Baía 2012):
Law 10/99 – Basic Law for the Environment
Law 11/99—Conservation of Fauna, Flora and Protected Areas
Decree-Law 37/99—Environmental Impact Assessment Process
Law 5/01—Forests
Law 9/11—Fisheries and Fishery Resources (currently under revision)
Law 6/06—São Tomé Obô Natural Park
Law 7/06—Príncipe Obô Natural Park
Regional Decree 3/09—Protection and Conservation of Sea Turtles
Decree Law 6/14—Capture and commercialization of sea turtles and their
products
• Decree Law 1/16—Hunting regulation
•
•
•
•
•
•
•
•
•
Biodiversity conservation legislation—EG (Osono et al. 2015):
•
•
•
•
•
•
•
•
Law 8/88—Wild Fauna, Hunting, and Protected Areas
Law 1/97—Forest Use and Management
Law 1/00—Taxation on timber exports
Law 4/00—Protected Areas
Law 7/03—Environment
Law 10/03—Fishing
Law 3/07—Water and Coasts
Law 4/09—Land tenure
24
Biodiversity Conservation in the Gulf of Guinea Oceanic Islands:. . .
663
• Decree Law 130/04—Fishing
• Decree Law 171/05—Biodiversity Conservation National Strategy and
Action Plan
• Decree Law 172/05—Trade of wild threatened species of flora and fauna
• Decree Law 173/05—Environmental inspection
• Decree Law 61/07—Timber exportation
• Decree Law 72/07—Primate hunting, selling, consumption, and ownership
• Decree 60/02—National Institute for Forest Development and Management of
the National Protected Area Network
National strategies for biodiversity conservation—STP:
• National Environmental Plan for Sustainable Development (RDSTP 1998)
• Strategic Plan for Tourism Development (UNDP 2001)
• National Forest Development Plan (Salgueiro and Carvalho 2001; Carvalho et al.
2017)
• National Action Plan for Climate Change Adaptation (NAPA 2006)
• Fisheries Master Plan (MAPDRSTP 2010)
• Strategy and National Action Plan for Developing the Sector of Non-Timber
Forest Products (Bonfim et al. 2016)
• Multisectoral Investment Plan to Integrate Climate Change Resilience and the
Risk of Catastrophes in Coastal Management (Carrasco et al. 2017)
• National Land Use Plan (MIRNASTP 2021)
• Sustainable Development Plan for the Autonomous Region of Príncipe: Príncipe
2030 (UNDP 2019)
• National Plan for Forest and Landscape Restoration (António et al. 2021)
National strategies for biodiversity conservation—EG (Osono et al. 2015):
•
•
•
•
•
•
•
•
•
•
2020 National Plan for Economic and Social Development
National Plan for Environmental Management
Biodiversity Conservation National Strategy and Action Plan
National Land Use Plan
National Protected Area Network
National Forest Policy Plan
National Climate Change Adaptation Plan
National Action Plan for Coastal and Marine Ecosystems
National Hydrological Plan
National Education Plan
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Chapter 25
Environmental Education in São Tomé
and Príncipe: The Challenges of Owning
a Unique Biodiversity
Roberta Ayres, José Carlos Aragão, Mariana Carvalho, Francisco Gouveia,
Estrela Matilde, Martina Panisi, Jormicilesa Sacramento,
and Vanessa Schmitt
Abstract The islands of São Tomé and Príncipe host extraordinary biodiversity that
evolved over millions of years without human presence. In the fifteenth century, the
colonization of the islands created a society of migrants, associated with extensive
land-use change and generally low knowledge and stewardship of autochthonous
biodiversity. Formal education became widely accessible after the country’s independence but the curriculum has never been aligned with the natural heritage of the
islands. Informal environmental education started in the 1990s alongside the pioneer
conservation initiatives involving the scientific community. In the last decade, these
efforts have multiplied, in line with the need to engage and involve local actors to
promote stewardship and ensure the success of conservation efforts. Some changes
were made recently at a formal level with the inclusion of environmental education
R. Ayres (*)
Gulf of Guinea Project, Department of Herpetology, California Academy of Sciences, San
Francisco, CA, USA
e-mail: rayres26@gmail.com
J. C. Aragão
Projeto Escola +, São Tomé, Sao Tome and Principe
M. Carvalho
Tropical Biology Association, Cambridge, UK
F. Gouveia
Arribada Initiative, Cheshire, UK
E. Matilde · J. Sacramento · V. Schmitt
Fundação Príncipe, Santo António, Príncipe Island, Sao Tome and Principe
M. Panisi
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon,
Portugal
Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências,
Universidade de Lisboa, Lisbon, Portugal
Alisei Onlus NGO, São Tomé, Sao Tome and Principe
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_25
671
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curricula and new manuals. In addition, several initiatives and improvements are
being developed in the private education sector. However, limited access to
resources for educators reduces motivation and capacity to implement longer-term
improvements. Most environmental education activities are still promoted by NGOs
and mainly focus on endemic or threatened species and target school-age audiences.
Other initiatives focusing on specific demographic groups have provided interesting
results but are more intermittent and their impacts have largely not yet been
evaluated. Improving formal assessments for current and future projects to assess
impacts and refine future approaches will be essential moving forward. In addition,
ensuring the involvement of local actors, coordination between different initiatives,
and the use of diversified approaches will ensure that environmental education
engages the widest possible audiences.
Keywords Civil society · Environmental education curriculum · Formal education ·
Gulf of Guinea · Informal education · Oceanic islands
Brief Historical Background of Environmental Education
in São Tomé and Príncipe
How the Landscape and History Shaped Environmental
Education
Príncipe, São Tomé, and Annobón are remote oceanic islands with a unique and
understudied biodiversity, which evolved over millions of years without human
interaction. We were unable to find information about local perspectives on environmental education for Annobón and thus, here we will solely focus on São Tomé
and Príncipe.
When the Portuguese discovered São Tomé and Príncipe in 1470, the islands
were uninhabited. The human population of the islands was mostly brought from
other parts of Africa, and, to a lesser extent, from Europe, in two main colonization
periods. The first was associated with the slave trade and the second with contracted
labor for the coffee and cocoa plantations (Seibert 2015). The islands have a history
of extensive plantation agriculture that is closely related to the degradation of vast
areas of forest in São Tomé and Príncipe and possibly with the extinction of endemic
species before they were formally described to science. Early scientific studies to
describe the biodiversity of São Tomé and Príncipe were conducted by European
naturalists during the nineteenth and early twentieth centuries (Ceríaco et al. 2022).
The natural ecosystems of the islands, nowadays recognized for the uniqueness of
their species, were poorly known and of little use for the newly established human
population. The local plants and animals were unfamiliar and few edible plants and
animals from the native forest were known or used (e.g., Seibert 2015). Thus, landuse change was promoted with the introduction of species and the conversion of the
native ecosystems to agricultural land with introduced plants and animals that could
be exploited. Some of the native ecosystems endured, due to their remoteness and
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Environmental Education in São Tomé and Príncipe: The Challenges of. . .
673
difficulty of access, and the biodiversity within remained largely unknown to most
people living on the islands.
Santomeans had limited access to primary education before independence and
opportunities were divided between a nearly-formal setting in the plantations, which
provided basic education to the workers’ children, and an informal setting called
“bush school” (“escola do mato”), which took place in villages without any official
context or support (Amado 2018). Secondary school only appeared in the mid
twentieth century, first with a private status and later open to the wider public, but
still restricted to just one school. Education was fully structured according to the
norms of the hierarchical and centralized colonial administrative model. It was
designed to impose civilizational standards and the European culture on students,
disregarding and discriminating against the “sons of the land” and their culture
(Amado 2021).
From Independence to Strategic Environmental Education
Options
After centuries of colonialism, São Tomé and Príncipe achieved independence on
July 12, 1975, inheriting an educational system marked by low literacy, only one
post-primary school, and the absence of professional education (Barreto 2012).
During the first phase of the post-independence period, called “First Republic”
(also known as “Single Party Period”), from 1975 to 1990, the government made
education a priority with mass literacy one of its main objectives (Cardoso 2004). In
the year of independence, the illiteracy rate was 80%. Fifteen years later, it fell to
30% (MECF 2012). Today, São Tomé and Príncipe report that 92.8% (2018) of the
population over 15 years old is literate, representing the best index among African
countries in which Portuguese is the official language (UNESCO 2021). Despite
important progress, illiteracy remains a problem, especially in some areas of the
country, such as the southern and northern regions of São Tomé Island, affecting
mostly the female portion of the rural population. The Santomean government has
set the goal of eradicating illiteracy by 2022 (MECF 2012).
The democratic reforms and the opening of the country in the late 1980s marked
the start of the “Second Republic” (“Multiparty Democracy”), bringing important
interventions with the aim to establish a better framework for education. The
institution of democracy gradually created opportunities for the national curriculum
to become more open to incorporate the pedagogical innovations and guidelines
coming from international organizations such as UNESCO, UNICEF, and UNDP
(MEC 2002). In 1986, an educational reform began in the country with support from
the Calouste Gulbenkian Foundation (Portugal) and the World Bank, focusing on the
production and editing of textbooks for the first 6 years of basic education. However,
the program never reached its final objectives, and only a few manuals were
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produced. These manuals were used for over 20 years without being updated (MeiaOnça 2013).
The country has always been concerned with the quality of its educational system
(Cotrim 2019). All the reforms sought to accompany changes in Santomean society
and keep pace with the rest of the world, but the educational system was not ready
for the new challenges facing the country (Cardoso 2004). The Basic Law of the
Education System (Law 2/2003) introduced only two significant changes: an
increase in compulsory schooling from 4 to 6 years and the inclusion of the 12th
grade (MECJD 2006). Despite many attempts to develop a national curriculum
adapted to the context and needs of the country, it was not until the last decade
that the sciences received more attention. Today the curriculum is still insufficiently
adapted to its audience and fails to reflect the natural heritage of the islands.
Nevertheless, the environmental education needs of the country were widely
recognized and highlighted by the scientific and conservation communities, with
strong and significant efforts starting in the 1990s. In 1992, São Tomé and Príncipe
received assistance from the EU’s European Development Fund in support of the
Forestry Commission’s efforts to prevent harvesting in primary forests and to
promote efforts to educate the public about forest conservation. Under the ECOFAC
Programme, an EU-funded regional program for the conservation and rational use of
forest ecosystems in Central Africa, this work is still ongoing on the islands and lead
to the establishment of the protected areas network of São Tomé and Príncipe. This
network covers roughly one-third of the islands and culminated with the creation of
two Natural Parks in 2006 (Lima et al. 2022). Meanwhile, an Action Statement on
biodiversity conservation in the four Gulf of Guinea islands arose from a workshop
held in 1993. This document reviewed the state of the main habitats on all the
islands, current threats, and existing institutions and management actions taken so
far (Juste and Fa 1994). This work led to the formation of an international group of
scientists and a special issue of the journal Biodiversity and Conservation (vol
3, 1994). These events were key for synthesizing biodiversity knowledge and
conservation actions for the islands, and also for igniting local actions to engage
Santomeans in protecting their natural heritage.
The first environmental education activities emerged with ECOFAC around sea
turtles (with Programa Tatô, still active as an independent NGO since 2018) and gray
parrots. These were some of the better-known species at the time, highly pressured
by the capture of individuals and eggs for food, trade, and crafts (AGRECO –
SECA – CIRAD 2005). As the scientific knowledge of other groups and species
increased and diversified, the need to involve the local population in environmental
initiatives grew and has been a strong driver for most of the ongoing programs. The
islands’ potential for ecotourism has also been an important driver for the expansion
of environmental outreach activities to reach the whole population and foreign
visitors.
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The Current State of Environmental Education in São Tomé
and Príncipe
Formal Education: Environmental Education in Public
and Private Schools
The public school system on São Tomé and Príncipe had the subject of Environmental Education (EE) formally introduced in 2010, but only to the eighth grade
curriculum (Barreto 2012). Most private schools use EE in their lessons, formally or
informally, linked to their internal curricula or to international curricula, such as the
EE benchmarks provided by the Portuguese Ministry of Education.
Public Schools
Before 2010, environmental education content could be found in the Natural Science
manuals but was not considered a priority. With the educational reform in the
country, teachers of basic education inserted themes related to environmental education, namely on how to protect the environment from pollution or on how to
conserve the fauna and flora, through the subjects of “Physical and Social Environment” for classes from the first cycle. Classes from the second cycle worked by the
“Student Manual” in the science module, in which information and /or small themes
were adjusted to include environmental education.
In 2010, the NGO MARAPA (Mar, Ambiente e Pesca Artesanal), CTA (Centro
Técnico de Cooperação Agrícola e Rural), and ACP-EU (African, Caribbean and
Pacific Group of States-European Union) sponsored the publication of the manual
“Ecologia, Ambiente e Educação Ambiental em São Tomé e Príncipe” (“Ecology,
Environment and Environmental Education in São Tomé and Príncipe”) to be used
by teachers of the fifth and sixth grade (Carvalho et al. 2010). The manual includes
simple environmental education modules together with different practical activities
and teaching tools to be used by teachers of all subjects. Teachers from across the
country were trained but there was no formal assessment of the program’s efficacy or
impact. The manual was then used to support the elaboration of the EE curriculum
for the eighth grade (under Projeto Escola+) when, after 2010, EE as a subject was
inserted as part of a separate enrichment to the curriculum. Three different areas were
introduced in high schools in both São Tomé and Príncipe: “Environmental Education” was introduced to eighth grade students, incorporating group work and other
interactive activities to the lectures; “Health Education” to the seventh grade; and
“Civic Training” for ninth graders.
The curriculum content was developed by a select group of secondary school
teachers under the supervision of the Secondary Education Directorate. The educators from Projeto Escola+, coordinated by the Instituto Marquês de Valle Flôr,
supported by several European partnerships, and approved by the Ministry of
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Education and Culture, made the school manuals available along with a series of
structured training events held to promote the development of key stakeholders in
the second cycle educational network (Barreto 2012). After publication, the manual
was made available for teachers to use in the classroom, along with regular training
offered on how to integrate the manual into the environmental education curriculum
by the First Cycle Board. The curriculum was not widely adopted by teachers but
achieved greater use on the island of São Tomé and was included sporadically in
classes on Príncipe.
In 2014, following the inclusion of environmental education in the school
curriculum, along with a dedicated teacher’s manual, actions were focused on the
eighth grade students. This resulted in the production of a new EE student manual
(Eloy et al. 2014). This material was intended to alert and prepare young people to
the worsening environmental situation in the country, and to the need to promote
sustainable economic development while preserving the islands’ biodiversity. Due
to various limitations after its publication, very few people knew about the existence
of this material, including teachers and students in São Tomé and Príncipe.
Private Schools
Based on a sample (n ¼ 5) of private schools (pre-k to 12 grade) interviewed in São
Tomé in 2020 and 2021, environmental education (EE) is part of the curriculum but
it is not adapted to the context of the islands and does not use examples of the local
biodiversity and habitats. Four schools used the curriculum published by the Portuguese Ministry of Education: Referencial de Educação Ambiental para a
Sustentabilidade (Environmental Education Benchmark for Sustainability). Some
schools teach about the history and geography of São Tomé and Príncipe first and
then proceed with the Portuguese curriculum. Only one school incorporated a few
EE topics related to the islands with the support of local NGOs. Príncipe recently
opened its first private pre-k school on the island. The school integrates EE activities
such as Earth Day, but EE is not yet connected to a formal curriculum.
The EE topics taught by the private schools depend on how closely they follow
the Portuguese benchmarks, covering preschool to secondary level, to develop
lessons and activities that aim to contribute directly to the personal and social
development of their students. The ninth grade of a particular school we interviewed
added “environmental sustainability,” which incorporates first-hand experiences.
For instance, in one of their modules students go into the field to test water quality,
using knowledge acquired in the classroom to interpret their results and reach
conclusions.
Another school took a step further and incorporated EE (using a mix of both
Santomean and Portuguese concepts) into their mission statement, consequently
linking all their curricular activities toward raising children’s awareness about the
importance of protecting and appreciating the natural world. Children as early as
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Environmental Education in São Tomé and Príncipe: The Challenges of. . .
677
12 months old have exposure to activities both in and outside of the classroom, with
the purpose of promoting values and actions that can later result in the development
of environmental stewardship in São Tomé and Príncipe. This particular school uses
beach cleanup as its “beacon activity” to introduce the issue of trash pollution, which
chronically impacts the islands’ local beaches and city centers. Their aim is to
reinforce the notion that children can be an important part of the solution and they
also play an active role in teaching behavioral changes to family members and civil
society.
Informal Education: Past and Ongoing Efforts
The basis for informal environmental education in São Tomé and Príncipe has been
built upon the recent scientific work on the species-rich and under-explored biodiversity of the islands. A project by Veríssimo et al. (2012) aimed to understand the
knowledge and attitudes of key stakeholders toward biodiversity, sustainability, and
natural resource management, revealed that there is still the need to improve
engagement and communication with local actors. International institutions and
researchers need to invest time and resources to develop effective ways to better
communicate their scientific findings through environmental education. Nevertheless, major efforts on EE have been made to raise awareness about the conservation
of these unique islands over the past 23 years, with several national and international
projects being held in the country that reach local residents and tourists alike
(Table 25.1).
The lack of a centralized database to track records of early EE programs in São
Tomé and Príncipe makes it difficult to assemble a complete assessment of the
diversity of the project aims, target populations (TP), and outputs, but there has
clearly been increased investment in long-term projects over the last decade
(Fig. 25.1). Based on four “one-off” and 11 currently “ongoing” informal EE projects, five take place on both islands, five exclusively in São Tomé, and five
exclusively in Príncipe, although collaborations are frequent between organizations
from both islands. The establishment of a larger number of NGOs in the country
contributed to the increase in longevity of the programs, funding, and creation of
training and employment opportunities for members of the civil society. The main
topic covered is biodiversity conservation, especially focusing on the valorization of
threatened species and ecosystems. Projects address a wide range of taxa and
ecosystems, although some focus on a specific taxon (e.g., marine turtles, bees,
and terrestrial mollusks) or topics (e.g., recycling and illegal hunting). Twelve
projects target schools and local communities, but the target audience can be project
specific, depending on the main aims (e.g., fishermen and fishmongers for marine
ecosystem conservation or hunters for terrestrial ecosystem conservation).
Projects
Arribada Club: Arribada initiative | Fundação Príncipe
Period
2017 –
present
Place
P
BirdLife International Partners Programme: RSPB |
SPEA
2015–2017 |
(under
ECOFAC
6 as of 2018)
2016–2019
ST
Bumbu D’Iê: Terrestrial Conservation Programme |
Fundação Príncipe
Main theme
STEM | biodiversity | endemic
species | conservation technology | conservation | protection
Biodiversity | endemic species |
conservation not hunting |
protection
Target population
Primary school
P
Bees | biodiversity | ecology |
conservation | protection | sustainable business practices |
income-generating activity
Primary school | community |
general public | NGO agent
Community | community
leader | NGO agent | Nat’l park
staff
Hunter | primary school | community | community leader |
general public | eco guide
March–June
2010
STP
Biodiversity | endemic species |
conservation | ownership
ECOFAC 6 (Obô Ôvyô
Campaign): BirdLife International | Oikos
2018 –
present
STP
Environmental Education
Manual: MARAPA | CTA |
ACP-EU
Forest Giants: Alisei Onlus
NGO | FCUL
August
2010–June
2011
2018 –
present
STP
Biodiversity | endemic species |
conservation | protection | sustainable business practices |
effective land management |
protected areas | National Parks
| natural heritage | ecotourism
Biodiversity | ecology | conservation | environmental education principles & didactic tools
Terrestrial mollusks | biodiversity | endemic species | conservation | protection | ecology |
snail husbandry
ST
STP
Teacher | community | NGO
agent | nature Club
Teacher | primary school |
community | general public |
NGO agent | eco guide
Methodology
After-school program | lecture
| multimedia communication |
hands-on activity
Outreach | training | hands-on
activity
Product development and
distribution | outreach | lecture
| training | workshop | multimedia communication | field
trip | hands-on activity
Outreach | training | multimedia communication | hands-on
activity
Outreach | training | workshop
| multimedia communication |
field trip | hands-on activity
Product development and
distribution | training | meeting | hands-on activity
Outreach | lecture | training |
workshop | meeting | multimedia communication | field
trip | hands-on activity
R. Ayres et al.
ECOFAC 4: PNOST |
Zuntabawê
Hunter
678
Table 25.1 Summary of environmental education projects in São Tomé (ST), Príncipe (P) and both in São Tomé and Príncipe (STP)
Missão Dimix Association
2017 –
present
Omali Vida Nón 1 & 2: University of Exeter, UK | FP |
DRAPP | DGP | Principe Island
UNESCO Biosphere Reserve |
FFI | Oikos | MARAPA
Phase 1
July 2016–
March 2019
Phase 2
2018 –
present
2018 –
present
Príncipe Thrush: Terrestrial
Conservation Programme |
Fundação Príncipe
Programa Tatô: ECOFAC
(1998–2002); MARAPA
(2002–2018); Associação
Programa Tatô (2018 –
present)
Protetuga: Fundação Príncipe
Biodiversity | endemic species |
conservation | protection |
ownership | stewardship
Teacher | primary school |
community | general public
ST
Arts | biodiversity | marine life |
conservation | protection |
stewardship
Primary school | secondary
school
P
STP
Phase 1 | better Management of
Marine Resources | sustainable
practices
Phase 2 | creation of marine
protected areas | conservation |
protection
Principe thrush | ecology |
population size & distribution |
conservation | protection
Sea turtles | conservation | protection | biodiversity | marine
life | ownership | stewardship |
income-generating activities
Fisherman | fishmonger |
community
P
1998 –
present
ST
2015 –
present
P
Fisherman | fishmonger | kindergarten | primary school |
secondary school | community
| general public | eco guides |
tourists | NGO agents |
government
Kindergarten | primary school |
secondary school | community
| general public | NGO agent |
eco guide | tourist | government
Outreach | lecture | multimedia communication | hands-on
activity
Product development and
distribution | outreach | lecture
| workshop | training | meetings | multimedia communication | exhibition | guided
Tours | museum interpretive
activities | field trip | theater
play production | museum |
hands-on activity |
Outreach | lecture | training |
meeting | multimedia communication | guided Tours |
museum interpretative activity | museum | field trip |
hands-on activity
(continued)
679
Sea turtles | biodiversity |
marine life | conservation |
protection | ownership | stewardship | income-generating
activity
Primary school | community |
general public | NGO agent
Product development and
distribution | outreach | training | workshop | multimedia
communication | hands-on
activity
After-school program | lecture
| multimedia communication |
exhibition | field trip | handson activity
Outreach | multimedia
communication
Environmental Education in São Tomé and Príncipe: The Challenges of. . .
2010 –
present
25
Gulf of Guinea: California
Academy of Sciences
680
Table 25.1 (continued)
Projects
RaizArte: BLI support
Period
2019 –
present
Place
ST
Water & Recycling: Fundação
Príncipe
2013–2015
P
Main theme
Performing arts | biodiversity |
endemic species | ecology |
nature themes | conservation |
protection | ownership |
stewardship
Plastic bottle recycling | reusable water bottle | water filling
station | waste management |
stewardship
Target population
Secondary school | general
public
Methodology
After-school program | lecture
| training | multimedia communication | theater play production | hands-on activity
Primary school | community |
general public | tourist
Outreach | hands-on activity
ACP-EU: African, Caribbean and Pacific Group of States-European Union – BLI: BirdLife International, UK – CTA: Technical Centre for Agriculture and
Rural Cooperation, European Union – DGP: Direcção Geral das Pescas, STP – DRAPP: Direcção Regional da Agricultura, Pesca e Pecuária, STP – FCUL:
Faculdade de Ciências da Universidade de Lisboa, Portugal – FFI: Fauna & Flora International, UK – FP: Fundação Príncipe, STP – MARAPA: Mar, Ambiente
e Pesca Artesanal, STP – PNOST: Parque Natural Obo de São Tomé – RSPB: Royal Society for the Protection of Birds, UK – SPEA: Sociedade Portuguesa para
o Estudo das Aves, Portugal
R. Ayres et al.
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Environmental Education in São Tomé and Príncipe: The Challenges of. . .
681
Approaches to Informal Environmental Education
Outreach in primary public schools is the preferred method used by the informal EE
programs, possibly due to the fact that primary school students have very little
exposure to environmental sciences. Informal EE projects are addressing some of
the existing gaps by using a variety of hands-on methodologies and approaches
within or outside the classroom. In 2011, the California Academy of Sciences
pioneered a large-scale education effort based on scientific research to raise awareness about the islands’ unique biodiversity in both São Tomé and Príncipe (Drewes
2012). The Gulf of Guinea Project uses a unique approach for content assimilation,
following the same cohort of students from third to fifth grades, aiming to promote
knowledge and stewardship about biodiversity in students’ own “backyard.” The
project distributes to each student and their teachers captivating take-home educational materials after every lesson (Fig. 25.1 (6)), using the main message: “Only
Here! São Tomé and Príncipe, Our Special Islands, and Nowhere else in the World!”
The opportunities for meaningful learning outside of the classroom in the public
school system are almost non-existent on the islands and 20% of the EE projects are
organized as after-school programs to address this limitation. The Protetuga Project
in Príncipe, for example, incorporates their turtle conservation program through the
Zero Capture campaign into the school calendar, creating the unique opportunity to
organize field trips to their Kaxí Tetuga Museum at Praia Grande, where students
visit a biodiversity museum and participate in the release of turtle hatchlings into the
ocean amongst other educational activities (Fig. 25.1 (7)). The Arribada Club, in
Príncipe, introduces primary school students to computers and conservation technology, such as GPS trackers and audio recording devices (Fig. 25.1 (1)). The Forest
Giants Project creates debates with students and rural communities to raise awareness about biodiversity conservation, using the story of the rapid decline of the
threatened Obô Giant Snail Archachatina bicarinata and provides hands-on teaching and training opportunities for learning about local species and for interacting
with the Obô Giant Snail at the Botanical Garden of Bom Sucesso, São Tomé
(Fig. 25.1 (5)). Other projects create awareness using visual or performing arts.
Missão Dimix Association organizes student art exhibitions made with recycled
materials showcasing their focus on marine life conservation, in addition to their
regular after-school programs and camps. RaizArte works with teenagers on playwriting, stage design, and performing art techniques using biodiversity, conservation, and other nature-related themes (e.g., the Se o Obô Falasse theater play
addresses species conservation in São Tomé and Príncipe; Fig. 25.1 (8)). Programa
Tatô develops an array of educational printed materials, such as the story book A
viagem da visitante mais antiga de São Tomé e Príncipe (The journey of the oldest
visitor of São Tomé and Príncipe), the activity book Livro de atividades para os dias
de chuva (Activity book for rainy days), and an annual booklet Ngê di Omali (Sea
people), which is distributed to primary schools with a different theme every year.
The peer teaching and learning experiences, along with facilitated themed discussions and activities, can create paths to promote a sense of ownership and
682
R. Ayres et al.
Fig. 25.1 Examples of environmental education projects in São Tomé and Príncipe: (1) Arribada
Club Project computer science class, Príncipe; (2) ECOFAC 4 “Net of Life” activity in Claudino
Faro rural community, São Tomé; (3) ECOFAC-6 plant nursery activity with students at Diogo Vaz
primary school, São Tomé; (4) Bumbu D’Iê classroom program about bee conservation, Príncipe;
(5) Forest Giants Project lesson to primary school students about terrestrial biodiversity conservation and the decline of the Obô Giant Snail Archachatina bicarinata, São Tomé; (6) Gulf of Guinea
Project primary school outreach program “Our Special Birds” about the endemic species of birds
from São Tomé and Príncipe, São Tomé; (7) Protetuga Project hatchling release activity with school
25
Environmental Education in São Tomé and Príncipe: The Challenges of. . .
683
valorization of the natural resources. Projects that work with specific audiences (e.g.,
fishermen, fishmongers, hunters, loggers, National Park staff, school teachers, and
students that live in the vicinity of protected areas) used “train the trainer” methods
to capacitate community leaders to conduct training sessions with their own communities using a variety of hands-on activities and facilitation tools (e.g., photo
montage, films, role play, games, sports championships, cooking competitions,
fairs). This method is proven to be efficient to raise environmental awareness and
well accepted among communities. In a pilot study in the scope of ECOFAC
4 (Fig. 25.1 (2)), focusing on communities around São Tomé Obô Natural Park,
the “train the trainer” method was shown to be a potentially strong tool to develop
and promote increased knowledge toward endemic biodiversity and nature conservation. In 2018, the ECOFAC 6 project investment is working in the buffer zones of
the natural parks of both São Tomé and Príncipe, developing training to promote
sustainable use of natural resources for income-generating activities, imperative to
generate real results toward the conservation and valorization of natural heritage,
biodiversity, and ecosystems (Fig. 25.1 (3)).
The Omali Vida Nón project works with the government and coastal communities
to create a network of marine protected areas across both islands through a
co-management approach. It aims to create awareness and promote the adoption of
alternative sustainable methods as a way of balancing human impact with the
subsistence living of the communities. Likewise, to promote sustainable honey
practices, the Bumbu D’Iê project provided training to beekeepers for an alternative
model of honey production that does not involve bee-burning in the forest, combined
with EE hands-on activities (Fig. 25.1 (4)).
Multimedia communication is used by nine of the projects to reach wider and
more diverse audiences, which is frequently amplified by content productions on
TV, radio, and social media. Even some of the most rural parts of the islands have
radios and television sets (plugged-in to generators) available at home or at the local
kiosk. Community members tend to congregate in such venues, to socialize and
watch TV or listen to the radio at the end of the workday, in the evenings, and
especially over the weekends. The Programa Tatô, for example, uses local media
celebrities on educational radio soap operas on São Tomé to raise awareness about
their sea turtle conservation program. Fauna and Flora International (2019) concluded that the use of posters and radio was an efficient and cost-effective method to
reach and engage large numbers of people. The report cautioned, however, that a
high level of engagement does not necessarily translate into effective dissemination
of the underlying message.
⁄
Fig. 25.1 (continued) children at Praia Grande, Príncipe; (8) RaizArte “Se o Ôbo Falasse” play
written, directed, and performed by high school students, São Tomé. Photo credits: (1, 4, 7)
Fundação Príncipe, (2) Mariana Carvalho, (3) Raphaela Nazaré, (5) Vasco Pissarra, (6) Andrew
Stanbridge, (8) BirdLife International
684
R. Ayres et al.
Evaluation of Projects
Evaluation is a very important tool to determine what works well and what could be
improved; however, only six of the EE projects (40%) have an evaluation tool in
place. This makes it difficult to measure the real impact of the programs, which may
compromise reporting to stakeholders and limit funding opportunities relative to
projects that use quantitative data to assess impact.
EE projects that use evaluation tools commonly use questionnaires with adults,
and drawings, games, or simple question-answer sheets with children, to evaluate
knowledge gain and understanding of the concepts being taught. Oral interviews are
commonly used to obtain direct feedback from stakeholders such as governmental
authorities, teachers, school administrators, and students. ECOFAC 6 is the first
project to use a more comprehensive method of evaluation, defining project indicators (e.g., days of training vs. number of people trained, number of people trained in
green economy and entrepreneurship, number of followers on social media, number
of students involved in awareness activities, and percentage of people with correct
understanding of basic environmental concepts) to determine success. Programa
Tatô has made big strides toward evaluating the impact of their conservation
marketing campaign Tataluga – Mém di Omali on the consumption of sea turtle
meat and eggs in São Tomé (Thomas-Walters et al. 2020).
A recent study on the use of children’s drawings to evaluate the impacts of
environmental education activities (Sinclair 2020), carried out by researchers at the
University of Exeter (UK) in partnership with the Protetuga project by Fundação
Príncipe, provided useful insights to inform efforts for sea turtle conservation on the
island. The study demonstrated that using drawings as a tool for assessing levels of
knowledge about the biodiversity of Príncipe and evaluating change in children’s
knowledge over time can be useful to inform interventions, is highly engaging, and
has low-cost implementation on-the-ground. This assessment method demonstrated
that Protetuga’s EE activities over 4 years resulted in increased knowledge of
conservation issues and solutions among children.
These findings are particularly promising, as they validate some of the progress
undertaken through informal education efforts in the past years and provide valuable
guidance for future monitoring and recognition of the EE projects.
Challenges and Lessons Learned
One of the biggest challenges concerning formal education in the public system is
the fact that EE is only part of the eighth grade curriculum, and not present in any
other grade. Thus, much of EE falls under informal education, which is not offered
systematically and is not connected to formal education. Furthermore, teachers are
not motivated to embrace EE in and outside the classroom, due to the lack of a
support system, namely proper training and resources to promote extracurricular
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685
activities. Such challenges become a serious roadblock toward making any substantial advances.
More than 60% of the local teachers from first to sixth grade have no formal
educational training (MECCC 2016), and the required qualifications for filling
teacher vacancies in primary and secondary education in the country are low. For
example, it is possible for someone who has just finished high school to start
teaching eighth grade students. This is the result of a fast-growing society built on
a job market with very limited options for young people entering the workforce or
pursuing a university degree. The University of São Tomé was formally founded
only in 2014, after many years of existence as several different independent educational institutions. Other international universities, like the University of Évora or the
Lusíada University (both from Portugal), have a branch on São Tomé, offering
higher education courses. However, the tuition is typically far beyond the financial
means of the target demographic, contributing to the scarcity of professionals with
formal academic training. Individuals that obtain a college degree in another country
rarely return to São Tomé and Príncipe due to the low salaries and scarce job
opportunities. In some cases, teachers also hold appointments in other governmental
departments and teaching is a second job, which means that their availability and
engagement in the teaching role may be low. Institutions like the World Bank
occasionally finance and provide teacher-training opportunities led by the local
government in partnership with different Portuguese institutions, or private sectors.
However, these opportunities are rare and generally cover small groups or a small
percentage of teachers in the country.
For Príncipe residents, the conditions are even more challenging, as only recently
(2012/2013) was it made possible for students to finish high school on the island. Up
to a few years ago, students from Príncipe had to attend high school in São Tomé,
resulting in a high percentage of youths without a high school degree. On the other
hand, even with the governmental “isolation allowance” (financial incentive),
Príncipe still struggles to find teachers willing to move to the island due to the
high cost of living and isolation.
In March of 2021, we interviewed 10 primary and secondary school teachers from
Príncipe and six from São Tomé, all working in the public system, to learn about
their perception regarding their job experience satisfaction and knowledge about
local biodiversity. The results showed that 56% have chosen this profession because
they enjoy teaching and 37% due to a lack of options. When asked about the
availability of opportunities and the kind of limitations they are confronted with
regarding career advancement, they shared their concerns about the limitations
imposed on career advancement, which are linked to the lack of the schools’ basic
needs (e.g., electricity, water, sewage, and nutritious meals), and the absence of a
recognition system for different teaching categories, with salary compensation
dependent on the amount of training. Teachers interviewed in São Tomé did not
receive any specific training on local biodiversity or environmental issues, but in
Príncipe only one said that he had not received some type of training, either through
other teachers, universities, or NGOs. Only one teacher in Príncipe and one in São
Tomé stated that before becoming a teacher they did not have any knowledge about
686
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the importance of biodiversity and other issues related to the protection of the
environment in São Tomé and Príncipe. All teachers we interviewed recognize the
importance of the environmental issues on the islands and emphasize the role of
biodiversity in maintaining the health of ecosystems.
As in the public school system, opportunities for private school teacher training
on EE adapted specifically to the local context are very rare. Only one of the private
schools we interviewed invested time and resources to keep their teachers connected
to the subject by either bringing professionals from different areas of environmental
sciences or organizing field trips to different NGOs. Overall, the support system to
either train teachers, or to facilitate access to EE materials pertaining to the local
fauna and flora is underdeveloped, but it exists. Willing teachers can work with
informal environmental educators, biologists, technicians or NGOs to complement
and explore different local EE topics.
Various EE projects have observed that the schools in the capital of São Tomé
have higher student and teacher engagement during program delivery than in rural
areas. Schools situated in very remote areas not only have lower engagement but also
have difficulty in understanding basic concepts and the overall message of the
content. It is also in these rural communities that children most often have to support
their household with domestic tasks, making it very hard for them to be available for
activities outside the school period. In addition, conditions in rural schools such as
an excessive number of students per classroom, no electricity, and malnutrition, can
make learning more difficult. The socio-economic situation on the islands clearly
reflects the degree of knowledge and understanding of the communities about the
importance of their unique biodiversity. It is extremely difficult to convey nature
conservation messages when the basic needs of the local communities are not met.
A recent study was conducted with 361 students from both rural and urban
primary schools in São Tomé to assess children’s knowledge of local biodiversity
(Panisi et al. 2022). It showed that students’ wildlife knowledge improved among the
male student population of impoverished rural schools, and that threatened endemic
species were less often recognized than non-native species. Students in São Tomé
preferred to protect species according to their attractiveness or profitability (e.g.,
species that can be eaten or sold). These findings reveal existing disparities in
children’s knowledge about biodiversity among genders, economic backgrounds,
and reasons to protect wildlife. A lack of targeted and well-planned EE actions can
result in the progressive extinction of knowledge about the unique fauna and flora of
the island by the younger generation, especially in more urbanized areas (Soga et al.
2018).
Despite the fact that different generations have the opportunity to experience EE
through programs and activities, in many cases, ownership or follow-up is still
missing. This could be the result of poor planning (e.g., time constraints, budget,
personnel), type of language used (e.g., low involvement of local educators to ensure
educational tools are locally adapted), and insufficient long-term engagement to
create continuity. The very few existing published reports from past efforts are not
comprehensive enough to prevent repeating the same errors, which may deter further
development of EE in the country. Until today, the majority of EE actions happening
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Environmental Education in São Tomé and Príncipe: The Challenges of. . .
687
on São Tomé and Príncipe have been conducted informally and under the responsibility and leadership of international NGOs, with engagement of local civil society.
In recent years, EE has been growing and progressively led by national organizations, with several recognized Santomean educators who keep their engagement with
the dissemination of conservation messages throughout the years in different projects and in their own communities and networks.
During 2020, the COVID-19 pandemic was a global challenge, and education
was one of the sectors that suffered the most. In the majority of developed countries,
the online system was a solution to keep children and youth engaged, while in
non-developed countries, where access to electricity and the internet is limited, this
global crisis resulted in a complete stop of the education process. The limits to social
gatherings and the lack of virtual platforms also impaired projects working with
communities or other target groups. Consequently, all formal and informal EE
programs and activities also came to a halt in both São Tomé and Príncipe. In
2021, the EE activities (formal and informal) are slowly starting as schools are back
in session and meeting restrictions are starting to be lifted.
Looking into the Future
There are many political, economic, and social challenges on São Tomé and Príncipe
that directly impact the general quality of the education system. Consequently, the
subject of EE, including the focus on the importance of the islands’ local biodiversity, is less of a priority to the country. In today’s world, issues related to the
environment and education are more relevant than ever. Scientific knowledge of
the endemic and unique biodiversity of the islands has significantly increased in the
last few decades, and the national policies are starting to see biodiversity as a
development tool through tourism. Príncipe has been at the forefront of creating a
model for sustainable development, with the island being recognized as a UNESCO
Biosphere Reserve in 2012 and the development of the Plan for Sustainable Development “Príncipe 2030.” São Tomé seems eager to follow these steps with work
being done to achieve UNESCO Biosphere Reserve status as well. However, this
fragile and recent understanding of the importance of the local biodiversity is not yet
evident in the education system. Without the support and leadership of
non-governmental national and international organizations, the local knowledge of
the environmental relevance of São Tomé and Príncipe would be still precarious.
Teachers’ feedback indicated that a national education reform paired with a
dedicated budget is imperative to increase and sustain the investment on training
local teachers, improving schools’ basic conditions, and promoting the inclusion of
EE in all grades of the public system. EE has to be seen as a priority, and integrating
children with an environmental agenda is an investment in creating future adults
engaged with the conservation of the country’s natural resources. In parallel with the
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integration of the EE curriculum in all grades of public education, the private
education system should enhance the use of their resources, and dedicate a budget
to strengthen the efforts made to promote more EE activities. Integration of local
partners and stakeholders and the use of materials with messages and content tailored
to the local reality are also key elements to the future of EE on the islands.
Going forward, it is highly recommended that all organizations promoting EE
(public, private, informal) in the country monitor and evaluate their activities, and
commit to share their results to ensure the growth and advancement of EE on São
Tomé and Príncipe. The development of an evaluation protocol to be used nationally
could be of great benefit to accomplish such an important task. Additionally, a
potential development of an online database of EE initiatives in the country could
serve as an important learning tool for anyone planning or currently working in the
country, and promote exchanges with other regions or educators. There are few
meaningful opportunities for teachers, students, and civil society to engage and
network with local and international professionals in the field of EE, as most of
the communication and materials are done in languages other than Portuguese. In the
last decade, the islands have hosted several events related to environmental education in Lusophone countries. These conferences and meetings, although limited in
time, represent opportunities to exchange and develop ideas, establish collaborations
and keep people inspired and motivated by EE.
It is evident that there is an urgent need to create a strong and well-defined joint
strategy with local governmental support between public, private, formal, and
informal educational institutions, to ensure a successful integration of EE on São
Tomé and Príncipe, and to generate positive, long-lasting results on the islands’
biodiversity conservation. Education is the most effective way to achieve greater
public support and establish solid goals to preserve the fragile and threatened
biodiversity of these islands. This is urgent to ensure the future of both people and
biodiversity. Past EE efforts left a legacy in transmitting knowledge, motivating and
training people, and developing valuable materials that are currently addressing
critical environmental issues. Present and future EE efforts will inspire and engage
the next generation of national leaders to take a more critical and active role in
shaping the future of the unique biodiversity of the Gulf of Guinea oceanic islands.
Acknowledgments First, many thanks are due to those that gave their time to read and edit our
chapter. This chapter was made possible by the contributions from all the amazing professionals that
work on São Tomé and Príncipe leading projects dedicated to the protection and conservation of the
islands’ unique biodiversity. As such, they also carry on the important mission of educating the
future generations of environmental stewards, and awakening in each individual the responsibility
to live in a sustainable way. Thank you to all the school principals, teachers, and other professionals
in the field of education that contributed with invaluable data collected via a series of in-person,
virtual, and email interviews. We are also indebted to the national and regional governmental
entities of both São Tomé and Príncipe for their continuous support. Finally, we thank the
institutional support linked to all the authors involved in this chapter, including Fundação para a
Ciência e a Tecnologia (FCT/MCTES–PD/BD/140814/2018 and UID/BIA/00329/2021—to
Martina Panisi).
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689
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Open Access This chapter is licensed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits use, sharing,
adaptation, distribution and reproduction in any medium or format, as long as you give appropriate
credit to the original author(s) and the source, provide a link to the Creative Commons license and
indicate if changes were made.
The images or other third party material in this chapter are included in the chapter’s Creative
Commons license, unless indicated otherwise in a credit line to the material. If material is not
included in the chapter’s Creative Commons license and your intended use is not permitted by
statutory regulation or exceeds the permitted use, you will need to obtain permission directly from
the copyright holder.
Chapter 26
A Thriving Future for the Gulf of Guinea
Oceanic Islands
Rayna C. Bell, Luis M. P. Ceríaco, Ricardo F. de Lima, and Martim Melo
Abstract The oceanic islands of the Gulf of Guinea hold extraordinary levels of
endemism across many taxonomic groups. Biodiversity surveys are still uncovering
species new to science, and much work remains to be done on the evolution,
ecology, and conservation of this unique biological heritage. The next 10 years
will be crucial to find and implement development strategies that can respond to the
needs of the islands’ inhabitants while sustaining the biodiversity and
R. C. Bell (*)
Department of Herpetology, Institute for Biodiversity Science and Sustainability, California
Academy of Sciences, San Francisco, CA, USA
e-mail: rbell@calacademy.org
L. M. P. Ceríaco
Museu de História Natural e da Ciência da Universidade do Porto, Porto, Portugal
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório
Associado, Universidade do Porto, Vairão, Portugal
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, Vairão, Portugal
Departamento de Zoologia e Antropologia (Museu Bocage), Museu Nacional de História
Natural e da Ciência, Universidade de Lisboa, Lisbon, Portugal
R. F. de Lima
Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências,
Universidade de Lisboa, Lisbon, Portugal
Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon,
Portugal
Gulf of Guinea Biodiversity Centre, São Tomé, São Tomé and Príncipe
M. Melo
Museu de História Natural e da Ciência da Universidade do Porto, Porto, Portugal
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório
Associado, Universidade do Porto, Vairão, Portugal
BIOPOLIS Program in Genomics, Biodiversity and Land Planning, Vairão, Portugal
FitzPatrick Institute of African Ornithology, University of Cape Town, Rondebosch,
South Africa
© The Author(s) 2022
L. M. Pires Ceríaco et al. (eds.), Biodiversity of the Gulf of Guinea Oceanic Islands,
https://doi.org/10.1007/978-3-031-06153-0_26
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ecosystem functions on which they depend. We outline seven priority areas that need
to be addressed on the path for a thriving future for both people and biodiversity.
Keywords Biodiversity databases · Capacity · Exploration · Natural history
collections · Outreach · Small islands developing states · Sustainable development
Earth’s islands collectively hold the greatest concentration of biodiversity that exists
on our planet. Although islands have long served as important models for understanding the ecology and evolution of biodiversity, islands have also been recognized as epicenters of extinction with approximately 75% of all recent bird, reptile,
amphibian, and mammal extinctions occurring on islands. Much of the remaining
global island diversity is threatened, with up to 85% of remaining reptile, amphibian,
and mammal species, along with nearly half of island birds, at risk of extinction
today. Similar figures are expected for other taxonomic groups, for which global
assessments are currently missing. This biodiversity crisis is particularly notable on
tropical oceanic islands, where species evolved in stable and isolated conditions and
are especially vulnerable to the fast pace of ongoing environmental change. As
extinctions multiply, island ecosystems begin to crumble and further cascades of
species extinction will follow. As a result, the human inhabitants who depend on
these ecosystems will lose their livelihoods and ways of life. At the same time,
because island ecosystems are relatively simple, they also offer an opportunity to
understand how to stop this crisis, and to alter the course of our relationship with
biodiversity.
This edited volume provides an important summary of over 200 years of biological research on the oceanic islands of the Gulf of Guinea, highlighting the archipelago’s extraordinary endemism across the tree of life. Much of this diversity is still
being formally described to science, and the conservation status of most endemic
species has not yet been formally assessed. Likewise, our understanding of species
natural history, interactions among species, and characteristics of the islands’ diverse
ecosystems is still woefully incomplete. Importantly, these gaps in knowledge
hinder our ability to halt biodiversity loss on the islands and to secure a thriving
future for the islands’ human inhabitants. In support of the United Nations Small
Island Developing States commitment to reach sustainable development, the following activities should be a top priority for the oceanic islands of the Gulf of Guinea
over the next 10 years:
• Field surveys and taxonomic research that target specific taxonomic and geographic gaps in knowledge. Key knowledge gaps are discussed in more detail in
each of the taxonomic chapters, but we also note that for some branches of the
tree of life, the current state of knowledge for the oceanic islands of the Gulf of
Guinea is so sparse that we could not provide a chapter and/or checklist for that
particular group. This includes algae, lichens, and several groups of terrestrial
(e.g., annelids, bees, flies) and aquatic invertebrates (e.g., crustaceans, corals,
echinoderms, sponges). For much of the archipelago’s biodiversity, this work will
26
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•
•
•
•
A Thriving Future for the Gulf of Guinea Oceanic Islands
693
also necessitate a better understanding of regional species diversity and evolutionary relationships. Molecular techniques will continue to prove an invaluable
tool for advancing taxonomy and systematics in these lesser known groups.
Mobilizing existing natural history collections and their data to democratize
knowledge and expedite biodiversity research. Biodiversity surveys over the
last two centuries have resulted in extensive natural history collections that
document the diversity and distribution of the archipelago’s terrestrial and aquatic
ecosystems. Most of these collections are housed in Europe and the USA, and
many have not yet been curated, georeferenced, digitized, and made available to
the local or global research community. This critical work must continue and take
advantage of the growing availability and accessibility of online platforms for
collections data.
Integrating data from targeted field surveys and existing collections to map
species distributions. The distributions of most species in the oceanic islands of
the Gulf of Guinea are unknown, which limits our inference of species richness
and endemism across the islands’ ecosystems. Existing natural history collections
already hold much of this information, and future surveys should be designed to
fill conspicuous gaps in knowledge. These spatial data can be combined with
maps of current protected areas and estimates of future climate and land-use
change to inform sustainable development and conservation planning that centers
biodiversity resilience.
Promoting the islands as models for ecological studies. Biodiversity is dynamic
and relies on complex interactions at multiple levels of organization that are
challenging to study. As the species and ecosystems of the Gulf of Guinea
oceanic islands become more completely documented, hypothesis-driven studies
to promote a deeper understanding of their ecology are becoming possible.
Although few such studies have been conducted, it is already clear that the islands
are valuable mesocosms to test and develop advanced ecological theories, including population dynamics, community ecology, species interactions, ecosystem
resilience, and the impact of human activities on biodiversity.
Bolstering local taxonomic expertise and resources for biological research. An
increasing number of Santomean and Equatoguinean researchers are contributing
to biodiversity science, but this community is still small and largely under
resourced. Local institutions, including universities, herbaria, botanical gardens,
and libraries, need an influx of funding and training to support the growth in
taxonomic expertise and leadership that is essential for islanders to direct the next
phase of biodiversity research and environmental stewardship.
Augmenting resources for island residents of all ages to learn about their local
biodiversity. Effective biodiversity conservation requires a well-informed and
engaged local community. Currently, science literacy in the Gulf of Guinea
oceanic islands is limited and formal curricula do not feature the islands’ unique
biological heritage. Developing widely available, accessible references and environmental learning opportunities for those with less scientific training will be vital
to stimulate environmental stewardship and to recruit more local naturalists.
These resources can also serve to advertise the islands as a destination for
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sustainable tourism. The contents of this book can serve as a baseline reference
for updating school and university science curricula to focus on local biodiversity,
ecosystems, and environmental stewardship. Likewise, this book can serve as a
reference for developing taxon-focused field guides with illustrations, distribution
maps, natural history accounts, identification keys, and interactive tools. Finally,
featuring local biodiversity in community spaces through art, music, and theatrical performances can further extend the reach of biodiversity knowledge and
stewardship.
The next 10 years will be critical to set the stage for biodiversity conservation and
sustainable development in the oceanic islands of the Gulf of Guinea. Building on a
foundation of more than two centuries of biodiversity science, robust commitments
from local leadership, and strong cross-sector partnerships, this unique archipelago
is well situated to change course from cascades of species extinction towards a
thriving future for biodiversity. Most powerfully of all, the islands can teach us how
to assess and support healthy ecosystem function and scale these approaches to
Earth’s larger systems.
Open Access This chapter is licensed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits use, sharing,
adaptation, distribution and reproduction in any medium or format, as long as you give appropriate
credit to the original author(s) and the source, provide a link to the Creative Commons license and
indicate if changes were made.
The images or other third party material in this chapter are included in the chapter's Creative
Commons license, unless indicated otherwise in a credit line to the material. If material is not
included in the chapter's Creative Commons license and your intended use is not permitted by
statutory regulation or exceeds the permitted use, you will need to obtain permission directly from
the copyright holder.