Antarctic Seaweeds Diversity, Adaptation and Ecosystem Services

Iván
Gómez
Pirjo Huovinen Editors
Antarctic
Seaweeds
Diversity, Adaptation and Ecosystem
Services
Antarctic Seaweeds
Iván Gómez • Pirjo Huovinen
Editors
Antarctic Seaweeds
Diversity, Adaptation and Ecosystem Services
Editors
Iván Gómez Pirjo Huovinen
Instituto de Ciencias Marinas y Instituto de Ciencias Marinas y
Limnológicas, Facultad de Ciencias Limnológicas, Facultad de Ciencias
Universidad Austral de Chile Universidad Austral de Chile
Valdivia, Chile Valdivia, Chile
Research Center Dynamics of High Latitude Research Center Dynamics of High Latitude
Marine Ecosystems, (IDEAL) Marine Ecosystems, (IDEAL)
Valdivia, Chile Valdivia, Chile
ISBN 978-3-030-39447-9 ISBN 978-3-030-39448-6 (eBook)

https://doi.org/10.1007/978-3-030-39448-6
© Springer Nature Switzerland AG 2020

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Preface
In 2002, Christian Wiencke and Margaret Clayton published the book Antarctic
Seaweeds in the series Synopsis of the Antarctic Benthos edited by J.W. Wägele. To
our knowledge, this volume represents the most recent and comprehensive guide
dedicated exclusively to Antarctic macroalgae, which has made it an obligate refer-
ence for further studies. Nearly two decades later, we believe that it is timely and
urgently needed to bring to light an update on the present state of the art of these
important organisms in a rapidly changing world. Therefore, we invited various
Antarctic researchers to contribute chapters covering recent advances in a variety of
related topics. The list of contributors reflects well the currently active role of South
American research groups in this field. Originally, the focus of the book was on the
contributions from the South America; however, the invitation was expanded to
some distinguished colleagues from other regions in order to improve the coverage
of the thematics. It is clearly not possible to include all the topics, but we believe
that a representative view of the current state of knowledge on the most relevant
aspects is given, providing useful information for both undergraduate and postgrad-
uate students as well as for scientific community. The book is organized in 5 parts
with a total of 18 chapters. Part 1 gives a brief overview of the individual chapters
and outlines the major gaps and challenges as well as the new directions in the study
of Antarctic seaweeds. The following parts summarize the recent advances in diver-
sity and biogeography (Part 2); physiology, productivity, and environmental
responses (Part 3); biological interactions and ecosystem processes (Part 4); and
chemical ecology of Antarctic seaweeds (Part 5). Many of the chapters discuss the
topics in the context of environmental threats, especially climate change that is
already affecting these ecosystems. Thus, unavoidably, there is some overlapping of
these themes in different chapters, however, from distinct points of view and in
other context.
We are grateful to all the colleagues who kindly accepted the invitation to con-
tribute a chapter. We would also like to warmly thank our colleagues Chuck Amsler,
Kai Bischof, Bernardo Broitman, Gabriela L. Campana, Marie-Laure Guillemin,
Patrick Neal, Ellie Poulin, Martin Thiel, Nelson Valdivia, Christian Wiencke and
Katharina Zacher for dedicating their time and expertise for peer review and
v
vi Preface
improving the chapters of this book at their manuscript stages. We greatly acknowl-
edge Prof. Christian Wiencke for contributing the foreword as one of the leading
experts in polar seaweeds. Finally, we would like to thank the Universidad Austral
de Chile, the Comisión Nacional de Investigación Científica y Tecnológica
(CONICYT), and the Instituto Antártico Chileno (INACH) for permanent support
of our research activities in the Antarctic and to the publisher for giving us the
opportunity to make this volume. This publication is within the frame of the scien-
tific program of the Research Center Dynamics of High Latitude Marine Ecosystems
(IDEAL).
Valdivia, Chile Iván Gómez

Pirjo Huovinen
Foreword
Seaweeds represent a group of photoautotrophic organisms of vital importance for

the function of coastal ecosystems. They provide diverse habitats and breeding
areas for uncountable numbers of organisms including crustaceans and fishes and
represent an important food source not only for herbivores but also for detritivores
feeding on degraded seaweed biomass. About 10% of the global oceanic production
is based on seaweeds, a value similarly high as that of tropical rain forests. We knew
for long that seaweed communities are well developed in the temperate regions of
the world, but recent research shows that this is also true for the submarine seaweed
forests of Antarctica: single species can attain biomasses of over 10 kg wet weight
per square meter.
The exploration of Antarctic seaweeds began in 1817 with the expeditions of
Gaudichaud, Bory, Montagne, Hooker, and Harvey. In a second phase of intensive
research during the first two decades of the twentieth century, Gain, Skottsberg, and
Kylin made important taxonomic studies on Antarctic seaweeds. In the 1960s, scuba
diving investigations started and so, by the early 1980s, basic knowledge was avail-
able on taxonomy, geographic distribution, and depth zonation of Antarctic sea-
weeds. During the expeditions of Clayton and Wiencke in the 1980s and 1990s,
numerous species of Antarctic seaweeds were isolated and taken in culture, allow-
ing the description of algal life histories and the performance of physiological
experiments in temperature-controlled rooms in the home laboratories. An impor-
tant side product was a monograph on Antarctic seaweeds containing the first iden-
tification key.
These studies were a booster for scientists especially from South America, but
also from Europe, Australia, and North America, to work further on the investiga-
tion of these interesting biotas growing in this remote, harsh, and unique environ-
ment. Purely descriptive surveys came to an end, and scientists applied the latest
available methods to study distribution and biodiversity, metabolic adaptations to
the extreme Antarctic environment characterized by low temperatures and long
periods of darkness, the importance of the seaweeds as primary producers for
Antarctic near-shore ecosystems, and the effects of global climate changes, in par-
ticular the increase of UV-B radiation due to stratospheric ozone depletion and the
vii
viii Foreword
increase of the water temperatures in the Antarctic Peninsula region and their influ-
ence on zonation patterns and geographic distribution. Besides traditional studies,
scientists used new approaches to study photosynthesis and carbon balance, genetic
diversity, transcriptomic responses, and trophic interactions by experimental ecol-
ogy and ecological network analysis, just to mention some.
To my knowledge, this is the first multi-authored book exclusively focused on
Antarctic seaweeds and their role in coastal ecosystems in Antarctica with respect
to their reaction to a changing environment from the metabolic, cellular, and organ-
ismic level to the level of communities. I am proud to say that I have supported
many studies and interacted with almost all authors of the book. The book repre-
sents the present state of the art in this research area and as such will serve as an
important baseline for future research.
Bremerhaven, Germany Christian Wiencke

Contents
Part I Introduction
1 Antarctic Seaweeds: Biogeography, Adaptation,
and Ecosystem Services �� 3
Iván Gómez and Pirjo Huovinen
1.1 Introduction: The Historical Context�� 4
1.2 Antarctic Seaweeds in the Wake of Climate Change�� 7
1.3 The Book�� 8
1.4 Gaps, Emerging Challenges, and Future Directions �� 15
References�� 17
Part II Diversity and Biogeography

2 Diversity of Antarctic Seaweeds�� 23
Mariana C. Oliveira, Franciane Pellizzari, Amanda S. Medeiros,
and Nair S. Yokoya
2.1 The Antarctic Environment�� 24
2.2 Seaweeds in Antarctica: Definition and Importance �� 25
2.3 Seaweed Taxonomic Studies in Antarctica: Toward a New Species
Compilation�� 27
2.4 Molecular Taxonomy for the Study of Antarctic Seaweed Diversity 35
2.5 Seaweed Distribution in Antarctica�� 37
2.6 Concluding Remarks: Gaps and Prospects for the Future�� 38
References�� 39
3 Biogeographic Processes Influencing Antarctic
and sub-Antarctic Seaweeds �� 43
Ceridwen I. Fraser, Adele Morrison, and Pamela Olmedo Rojas
3.1 Antarctica’s Place in the World: An Isolated Continent?�� 44
3.2 Physical Oceanographic Processes Influencing Movement
of Seaweeds into or out of the Antarctic �� 46
ix
x Contents
3.3 Hitch-Hiking to the Antarctic: Passengers on Seaweed Rafts�� 50

3.4 Concluding Remarks�� 54
References�� 54
4 Detached Seaweeds as Important Dispersal Agents Across
the Southern Ocean�� 59
Erasmo C. Macaya, Fadia Tala, Iván A. Hinojosa,
and Eva Rothäusler
4.1 Introduction�� 60
4.2 Detached Seaweeds in Antarctica �� 62
4.3 Abiotic Factors Influencing Floating Seaweeds�� 69
4.4 Biotic Factors Affecting Floating Seaweeds �� 71
4.5 Physiology of Floating and Drifting Seaweeds:
Traspassing Thermal Barriers �� 72
References�� 75
5 Biogeography of Antarctic Seaweeds Facing Climate Changes�� 83
Franciane Pellizzari, Luiz Henrique Rosa, and Nair S. Yokoya
5.1 The Abiotic Setting of the Southern Ocean�� 84
5.2 Biogeographic Patterns �� 85
5.3 Seaweed Assemblages: Are Antarctic Seaweed
Diversity and Richness Changing? �� 87
5.4 The Physiological Bases of Macroalgal Shifts �� 89
5.5 Deception Island: A Case Study of Opportunistic,
Alien, Cryptic and Cryptogenic Species�� 90
5.6 Reevaluating Eco-Regions, Isolation,
and Endemism in the Southern Ocean�� 93
5.7 Concluding Remarks: Prospects for the
Future Marine Flora of the Southern Ocean �� 97
References�� 98
6 Comparative Phylogeography of Antarctic Seaweeds:
Genetic Consequences of Historical Climatic Variations �� 103
Marie-Laure Guillemin, Claudio González-Wevar, Leyla Cárdenas,
Hélène Dubrasquet, Ignacio Garrido, Alejandro Montecinos, Paula
Ocaranza-Barrera, and Kamilla Flores Robles
6.1 Historical Isolation of Antarctic Marine Macroalgae �� 104
6.2 Antarctic Marine Macroalgae: Surviving Quaternary
Glacial Cycles in Situ�� 106
6.3 Persistence in Multiple Isolated Glacial Refugia Versus
a Single Antarctic Refugium�� 108
6.4 Antarctic Macroalgae Genetic Diversity:
COI and TufA Sequences Data Sets �� 109
6.5 Brown, Red and Green Macroalgae: Sharing a Common Pattern
of Glacial Impact and Postglacial Populations Recovery? �� 111
References�� 121
Contents xi
Part III Physiology, Productivity and Environmental Reponses

7 Underwater Light Environment of Antarctic Seaweeds�� 131
Pirjo Huovinen and Iván Gómez
7.2 Optics of Antarctic Coastal Waters �� 132
7.3 Adaptations of Antarctic Seaweeds
to Extreme Light Conditions�� 137
7.4 Consequences for Light Field Under Current
and Future Threats�� 140
8 Production and Biomass of Seaweeds in Newly Ice-Free Areas:
Implications for Coastal Processes in a Changing Antarctic
Environment �� 155
María L. Quartino, Leonardo A. Saravia, Gabriela L. Campana,
Dolores Deregibus, Carolina V. Matula, Alicia L. Boraso,
and Fernando R. Momo
8.1 Introduction: Seaweeds in Coastal Marine Ecosystems �� 156
8.2 Macroalgae and Carbon Fluxes in Antarctic Coastal Areas�� 157
8.3 Macroalgal Biomass Studies in Antarctica �� 159
8.4 The Ecosystem of Potter Cove: An Outstanding Case Study �� 160
8.5 A Dynamic Growth Model for Antarctic Macroalgae
Under a Fast-Changing Environment�� 162
8.6 Seaweed Production in Present and Future Warming Scenarios�� 166
8.7 Future Prospects�� 167
9 Carbon Balance Under a Changing Light Environment�� 173
Dolores Deregibus, Katharina Zacher, Inka Bartsch, Gabriela
L. Campana, Fernando R. Momo, Christian Wiencke, Iván Gómez,
and María L. Quartino
9.2 Carbon Balance: A Case Study in Potter Cove �� 178
9.3 New Scenarios and Their Implications
for Algal Photosynthesis �� 183
9.4 Concluding Remarks and Future Prospects�� 185
10 Life History Strategies, Photosynthesis, and Stress Tolerance
in Propagules of Antarctic Seaweeds�� 193
Nelso Navarro, Pirjo Huovinen, and Iván Gómez
10.1 Seasonal Strategies and Life History Cycles�� 194
10.2 Photosynthetic Light Requirements of Early Stages�� 199
10.3 Effects of Environmental Factors
on the Biology of Propagules�� 205
xii Contents
10.4 Concluding Remarks: Biology of Propagules under Climate

Change�� 211
11 Form and Function in Antarctic Seaweeds:
Photobiological Adaptations, Zonation Patterns,
and Ecosystem Feedbacks �� 217
11.1 Brief Overview of Form and Function in Seaweeds �� 218
11.2 Functional Groups of Seaweeds in the Antarctic�� 219
11.3 The Vertical Zonation of Antarctic Seaweeds:
A Paradigm of Spatial Distribution
of Different Morpho-functional Traits�� 222
11.4 Light Use Characteristics as a Major Factor
Delineating Physiological Thallus Anatomy of Seaweeds �� 225
11.5 Form and Function in the Context of Life Strategies
and Stress Tolerance�� 227
11.6 Functional Traits of Seaweeds and Properties of Benthic
Communities �� 229
Part IV Biological Interactions and Ecosystem Processes

12 Successional Processes in Antarctic Benthic Algae �� 241
Gabriela L. Campana, Katharina Zacher, Fernando R. Momo,
Dolores Deregibus, Juan Ignacio Debandi, Gustavo A. Ferreyra,
Martha E. Ferrario, Christian Wiencke, and María L. Quartino
12.2 Structural Patterns and Changes in Algal Community
Composition during Succession�� 244
12.3 Ecological Factors Influencing Antarctic Algal Succession �� 248
12.4 Experimental Approaches to Study In Situ Succession
of Antarctic Benthic Algae�� 253
12.5 Concluding Remarks and Perspectives �� 254
13 Seaweed-Herbivore Interactions: Grazing as Biotic
Filtering in Intertidal Antarctic Ecosystems �� 265
Nelson Valdivia
13.1 Biological Invasions and Their Impact on the Ecology
of Antarctic Coastal Systems�� 266
13.2 Recent Introductions of Exotic Macroalgae in Antarctica�� 267
13.3 Can Grazers Control Alien Macroalgae in Antarctica?�� 268
13.4 Ulva intestinalis as a Case Study in a Simple,
Two-Species Assembly Model�� 270
Contents xiii

14 Diversity and Functioning of Antarctic Seaweed Microbiomes�� 279
Juan Diego Gaitan-Espitia and Matthias Schmid
14.1 Introduction: Environment and Antarctic Seaweed Host-
Microbiome�� 280
14.2 Functional Interactions of Antarctic Seaweeds
and Their Associated Microbiota�� 281
14.3 Deciphering the Structure and Diversity of Seaweed
Microbiomes �� 282
14.4 Variation of Bacterial Community Diversity in Antarctic
Seaweeds�� 284
14.5 Conclusions and Future Perspectives�� 287
15 Seaweeds in the Antarctic Marine Coastal Food Web�� 293
Fernando R. Momo, Georgina Cordone, Tomás I. Marina, Vanesa
Salinas, Gabriela L. Campana, Mariano A. Valli, Santiago R. Doyle,
and Leonardo A. Saravia
15.2 Food Webs and Seaweeds �� 295
15.3 Network Dynamics and Robustness �� 299
15.4 Non-Trophic Interactions�� 302
15.5 Final Remarks �� 304
16 Trophic Networks and Ecosystem Functioning�� 309
Marco Ortiz, Brenda B. Hermosillo-Núñez, and Ferenc Jordán
16.2 Macroscopic Ecosystem-Network Properties �� 318
16.3 Keystone Species Complex (KSC) �� 322
16.4 Contribution of Keystone Species Complex
to Macroscopic Network Properties�� 327
16.5 Constrains and Perspectives�� 328
Appendix 16.A�� 330
Part V Chemical Ecology

17 Chemical Mediation of Antarctic Macroalga-Grazer
Interactions�� 339
Charles D. Amsler, James B. McClintock, and Bill J. Baker
17.2 Feeding Bioassay Methodology�� 340
17.3 Antarctic Macroalgal Resistance to Herbivory �� 341
xiv Contents
17.4 Macroalga-Invertebrate Interactions on the Western Antarctic

Peninsula �� 352
17.5 Overview�� 355
18 Brown Algal Phlorotannins: An Overview
of Their Functional Roles�� 365
18.2 Synthesis and Cellular Localization
of Phlorotannins: Dual Functions as Secondary
Metabolites and Structural Compounds�� 369
18.3 Phlorotannins as UV-Screening Substances�� 370
18.4 Phlorotannins as Active Antioxidant Compounds�� 372
18.5 Phlorotannins in Antarctic Seaweeds�� 374
Index�� 389
Part I
Introduction
Chapter 1
Antarctic Seaweeds: Biogeography,
Adaptation, and Ecosystem Services
Abstract Seaweeds (macroalgae) represent the most striking benthic organisms in

the Antarctic near-shore ecosystems. Their abundance, relevant roles as primary
producers, and foundation organisms were recognized since the first Antarctic
explorations. Furthermore, especially since the 1960s, improvements in the sub-
aquatic survey techniques and laboratory facilities expanded considerably our
knowledge on ecology, reproduction, and environmental adaptation of seaweeds
whose biological processes determine much of the biogeochemical cycles in the
Antarctic coastal systems. In recent years, the imminence of the climate change and
the direct impact of human activities, which are affecting vast regions of the
Antarctica, have highlighted the importance of seaweeds as central components
shaping the structure, functions, and supporting services of benthic ecosystems
under changing polar environment. The present book is aimed to put together the
knowledge and experience gained in recent years by diverse research groups. Many
of these research efforts have long tradition, while others have brought more recently
important new approaches in the study of these organisms with benefits for the
whole polar science. We believe that this initiative is timely and urgently needed in
order to improve our scientific knowledge on these fascinating organisms. In this
chapter, we describe the book’s framework, summarizing the most important
advances in areas related with diversity, biogeography, ecophysiology, biological
interactions, and chemical ecology of Antarctic seaweeds. Finally, considerations
regarding the major gaps and challenges as well as the new directions in the study
of Antarctic seaweeds are outlined.
Keywords Antarctic · Climate change · Antarctic marine flora · Ecosystem

functions
I. Gómez (*) · P. Huovinen

Instituto de Ciencias Marinas y Limnológicas, Facultad de Ciencias,
Universidad Austral de Chile, Valdivia, Chile
Research Center Dynamics of High Latitude Marine Ecosystems, (IDEAL), Valdivia, Chile
e-mail: igomezo@uach.cl; pirjo.huovinen@uach.cl
© Springer Nature Switzerland AG 2020 3

I. Gómez, P. Huovinen (eds.), Antarctic Seaweeds,
https://doi.org/10.1007/978-3-030-39448-6_1
4 I. Gómez and P. Huovinen
1.1 Introduction: The Historical Context
In recent decades, important advances have been demonstrated in different areas of

knowledge on Antarctic seaweeds, from organisms to ecosystems. However, in
order to understand the roles and services of seaweed communities in Antarctica
currently marked by climate change, it is essential to go back to the history of this
endeavor. The first explorations of Antarctic seaweeds in the nineteenth century
(Gaudichaud 1826; Hooker 1847) had already documented the exuberant presence
of benthic seaweeds and recognized their importance for the coastal ecosystems in
the Antarctic, especially around the Antarctic Peninsula. In his book The Botany of
the Antarctic Voyage of H.M. discovery ships “Erebus” and “Terror” in the years
1839–1843, under the command of Captain Sir James Clark Ross (Fig. 1.1), one of
most complete records of marine and terrestrial flora of the Southern Ocean, the
British botanist Joseph D. Hooker disclosed much of the extraordinary conditions
that characterize the habitat of many Antarctic seaweeds. Later, another important
researcher, Karl Skottsberg, expanded this information from different Antarctic
expeditions in the early twentieth century (e.g., Skottsberg 1907). During the 1960s
and 1970s, descriptions based on scuba diving surveys carried out by Neushul
(1965), Delépine et al. (1966), Zaneveld (1966), and Lamb and Zimmermann
(1977), among others, confirmed this, highlighting the dominance of large endemic
Desmarestiales at depths >10 m, where they occupy similar role as kelps as the
dominant seaweed group in the Northern Hemisphere and the Arctic. The unique
characteristics of the Antarctic marine flora reflect the complex biogeographic and
evolutionary processes that followed the formation of the Antarctic Circumpolar
Current (ACC) around 30–35 Ma and consequent full glaciation of the Antarctica
(Clayton 1994). Diverse surveys across different sites in the Antarctic, including
communities growing under ice shelves, expanded considerably our knowledge on
vertical distribution, biomass, and diversity of seaweeds (Zielinski 1981, 1990;
Amsler et al. 1995; Klöser et al. 1993, 1996; Brouwer et al. 1995).
Due to the harsh climatic conditions and logistic restrictions in Antarctica,
advances in our knowledge on reproduction, phenology, and acclimation to the
polar environment were only possible since the 1980s. Using cultured material,
Moe and Henry (1982) described for the first time various aspects of the develop-
ment of early phases of Ascoseira mirabilis. The first studies unraveling the sea-
sonal development, life history, and physiological performance of Antarctic
seaweeds were based on algae grown under cultivation conditions simulating the
Antarctic light regime (Wiencke 1990). Based on these findings, two main growth
strategies were defined: the season responders start growth and reproduction when
environmental conditions are optimal in spring and summer, while the season antic-
ipators develop during late winter and spring. Thereafter, the number of investiga-
tions focused on physiology of photosynthesis, growth, chemical ecology, etc.,
increased (revised in Wiencke 1996). A noticeable finding was that various endemic
Antarctic brown algae, such as Ascoseira mirabilis, Cystosphaera jacquinotii,
Desmarestia anceps, and Himantothallus grandifolius, exhibit thallus anatomical
1 Antarctic Seaweeds: Biogeography, Adaptation, and Ecosystem Services 5
Fig. 1.1 Cover page of Hooker’s publication describing the flora of the Southern Oceans
and functional characteristics resembling those of large kelps from the Northern
Hemisphere (Drew and Hastings 1992; Gómez et al. 1995; Fig. 1.2). Here, the most
remarkable morpho-functional adaptations of large Antarctic brown algae are their
very low light demands for growth and photosynthesis and an efficient operation of
light-independent carbon fixation (LICF) at the meristematic zones, which allow
these organisms to display positive carbon balance at depth close to 30 m (Gómez
et al. 1997). The knowledge on these structural and functional aspects of
Fig. 1.2 Large endemic brown algae are the most representative components of the Antarctic
costal systems. (a) Himantothallus grandifolius, (b) Desmarestia anceps, (c) Cystosphaera jac-
quinotii. (Photos by Ignacio Garrido)
p hotosynthetic responses had important implications for understanding the biologi-

cal interactions between seaweeds and their associated biota (Zacher et al. 2007;
Iken et al. 2009; Amsler et al. 2011).
In the last decades, the Antarctic ozone depletion and associated increase in
UV-B radiation, as well as the environmental shifts driven by climate change, ori-
ented the research of Antarctic seaweeds. In this context, various studies have exam-
ined the effects of changing irradiance on different algal assemblages across
Antarctica (Schwarz et al. 2003; Zacher et al. 2007; Huovinen and Gómez 2013;
Clark et al. 2017; Deregibus et al. 2016). At an ecosystem level, seaweeds have been
commonly recognized as important sentinels of climatic change in the Antarctic,
highlighting the remarkable capacity of these organisms to adapt to new habitats
(Quartino et al. 2013), and also providing some key ecological ecosystem properties
that permit the maintenance of species richness and biomass (Valdivia et al. 2015).
Through their ecosystem engineering functions, especially large endemic brown
algae are able to minimize environmental variability enhancing the resilience of the
whole system (Ortiz et al. 2017).
Despite these advances, much of the predictions related with adaptation and fate
of Antarctic seaweeds are limited by scarce molecular evidence. From this perspec-
tive, the findings of an increasing number of cryptic species with Antarctic/sub-
Antarctic or even more vast joint distribution (van Oppen et al. 1993; Hommersand
et al. 2009; Billard et al. 2015) challenge some traditional concepts related with the
evolution and biogeographic patterns of the Antarctic marine flora (Crame 1992;
Clayton 1994). According to current predictions, climatic anomalies, e.g., enhanced
temperature, increased storms, and winds, will be able to break the ecological isola-
tion of Antarctica and facilitate the arrival of temperate species (Fraser et al. 2018),
with impacts on diversity and genetic configuration of local communities yet not
well understood.
1.2 Antarctic Seaweeds in the Wake of Climate Change
The climate, oceanography, and related ecosystem processes in Antarctica and its
surrounding oceanic system have been changing rapidly in the last decades
(reviewed in Constable et al. 2014). Accelerated regional warming was reported
especially in the WAP region almost 20 years ago (Vaughan et al. 2003). According
to the IPCC scenarios, the mean annual air temperature in this region was predicted
to increase by 1.4–5.8°C until 2100 (Clarke et al. 2007), although strong natural
variability seems characteristic in this region (Turner et al. 2016). The surface
waters of the Bellingshausen Sea have warmed by 1°C in summer since the 1950s
(Meredith and King 2005), while Schloss et al. (2012) reported an increase of more
than 2°C in winter sea surface temperature between 1991 and 2006 in Potter Cove
(King George Island). This tendency and the possible effects on the polar system
were recently highlighted in the last IPCC report (IPCC 2019). As a synthesis the
report indicates that the Southern Ocean (area corresponding to 25% of world’s
oceans) has been warming at alarming rates, being responsible for 45–62% of the
global ocean warming during the period 2005–2017. Although no clear overall
trends in Antarctic sea ice cover were evident for the period 1979–2018, a strong
decline has been observed recently (2016–2018), which can pose threats to the pho-
tosynthetic organisms due to unpredictable changes in the light regime (see Chap. 7
by Huovinen and Gómez). In the Arctic, massive ice-sheet losses, exceeding the
rates of modeled estimations, have been observed (Bronselaer et al. 2018). Here, the
role of albedo-reducing light-absorbing impurities in ice and snow fields exacerbat-
ing ice loss has been emphasized (Benning et al. 2014; Tedesco et al. 2016; Tedstone
et al. 2017). Dark snow phenomenon has recently also been associated with
decreased albedo in Maritime Antarctic (Huovinen et al. 2018). Recently, the active
role of ice sheets and icebergs in the global carbon cycle has been recognized
(reviewed by Barnes et al. 2018; Wadham et al. 2019) and can have important con-
sequences for the adjacent marine realm in areas like Maritime Antarctic (Hood
et al. 2015). Although various impacts of these changes are broadcasted for pelagic
realms, their implications for the processes occurring in the Antarctic shallow ben-
thos are much less known (Barnes and Conlan 2012; Constable et al. 2014).
The increasing number of volumes devoted to the present and projected impacts
of global climate changes on the Southern Ocean and their different ecosystems
(e.g., Bargagli 2005; Bergstrom et al. 2006; Rogers et al. 2012; Tin et al. 2014;
Kanao et al. 2018) is a clear evidence of the importance of understanding their
global consequences. Antarctica can be regarded as a natural laboratory where its
physical environment brings the adaptation capacities of organisms to an extreme
limit. In this context, seaweeds, as fundamental components of the Antarctic coastal
systems, can give important insights into the structure and functioning of the biota
in the new scenarios driven by climate change.
1.3 The Book
Based on recent quantitative, observational, and experimental evidences, this book

updates the state of art about the diversity and geographic distribution of seaweeds
as well as their biological interactions and responses to the environment, which is
fundamental for understanding the coastal processes in a changing Antarctica. The
main themes and the overall scientific framework discussed in the book can be sum-
marized in Fig. 1.3.
1.3.1 Diversity and Biogeography
Compared to other biogeographical regions in the Southern Hemisphere, e.g.,

southern Australia, New Zealand, and the southern Chilean coast, the diversity of
seaweeds in the Antarctic has been traditionally considered low. Based on Wiencke
and Amsler (2014), the number of species is 124, showing high endemism (35%).
In their chapter (Chap. 2), Oliveira et al. indicate that the richness of Antarctic sea-
weeds has been underestimated. Based on previous information and recent molecu-
lar surveys, the authors report a diversity of 151 species of which 85 are Rhodophyta,
32 Chlorophyta, and 34 Ochrophyta (most of them brown algae). Likewise, this
update decreased the percentage of endemism to 24%. Overall, the increase in the
number of catalogued species can be explained by improvements in the identifica-
tion tools, e.g., the use of DNA barcoding, more complete gene databases, and more
efficient approaches to detect, e.g., cryptic species. However, a conclusive outcome
of this diversity is far from definitive: a lack of baseline datasets in order to accu-
rately detect local loss of native species, or their replacement by alien assemblages,
still persists. Thus, extending the geographical range and number of surveys, adjust-
ing better the inventories of phylogenetic markers, and deepening the examination
of less conspicuous algal groups, such as crustose and endophyte species, a hidden
diversity normally overlooked, are suggested.
The Antarctic Circumpolar Current has defined the structure, diversity, and func-
tioning of the biomes of the Southern Ocean. Fraser et al. (Chap. 3) make a compre-
hensive analysis of environmental and oceanographic conditions that characterize
Antarctic from the sub-Antarctic regions, the dual role of ACC acting as an efficient
Fig. 1.3 Schematic presentation of the major drivers, organismal processes, and biological inter-
actions of Antarctic seaweeds. The framework is based on the conclusions of the different chapters
in this book
barrier and also as a bridge connecting marine assemblages and the requisites of
organisms permitting their dispersal across these environmental gradients. Rafting
of floating seaweeds driven by prevailing winds across the different fronts in the
Southern Ocean appears as a central mechanism promoting transoceanic connec-
tions, not only of seaweeds but also invertebrates. The definitive establishment and
persistence of new taxa in these zones will depend on different environmental fil-
ters, e.g., physical and biological constraints, and also on various organismal fea-
tures related with reproductive viability, physiological capacities, etc.
Probably the extent of exchange of species and hence genetic fluxes between
sub-Antarctic and Antarctic regions lie in the diversity of taxa that can be trans-
ported across long distances and their ability to remain alive during their journey.
Macaya et al. (Chap. 4) indicate that a total of 39 species (3 Chlorophyta, 14
Ochrophyta, and 22 Rhodophyta) have been reported drifting, stranded or floating
in Antarctica or crossing the Antarctic Polar Front (APF). Considering that many
cold and cold-temperate species at both sides of the ACC show remarkable physio-
logical adaptions to biotic and abiotic factors, e.g., grazing, UV radiation, and
t emperature, they could be able to arrive and colonize different locations around the
Southern Ocean. An example is the floating large brown algae commonly used by
different hitchhiking biota (e.g., barnacles, amphipods, algae). Interestingly, the
authors suggest that various Antarctic seaweeds, some with floating or buoyancy
capacity, have the physiological potential to travel out of the Antarctic.
In their chapter (Chap. 5), Pellizari et al. indicate that the diversity and biogeo-
graphic patterns of Antarctic seaweeds have begun to change. Here, the changing
environmental scenarios in the Southern Ocean, related mostly with circulation and
warming, will determine the new seaweed diversity. Using the seaweed assemblages
of Deception Island in the South Shetlands as a case study, the authors describe an
important presence of species with broad geographical distribution, especially
Chlorophyceans, indicative of recent arrival. Apparently, areas like this character-
ized by peculiar physicochemical conditions could become key places to study the
new Antarctic biodiversity, its biogeographic divergences and connections.
The Antarctic continental margins or peri-Antarctic islands are zones that evi-
dence the long evolutionary history of seaweeds within the Southern Ocean.
Guillemin et al. (Chap. 6) analyzed the sequences of mitochondrial and chloroplast
markers in eight Antarctic species of green, brown, and red seaweeds in order to
determine the genetic patterns in the context of the quaternary climatic oscillations
(QCO). The haplotype network revealed that the studied Antarctic seaweeds show
very low genetic diversity, and significant signatures are indicative of a recent popu-
lation expansion after a massive constriction during the Last Glacial Maximum
(20 Ka). Thus, the authors agree with a theory that this marine flora survived in situ
in a unique refugium and subsequently recolonized the multiple postglacial open
areas using the ACC as a predominant driving force.
In all, Antarctica is not a physically isolated continent, and in a scenario of
increasing warming, the influx of marine organisms arriving, e.g., via rafting to its
coasts, can find new opportunities for colonization, which finally will modify the
local diversity (Fig. 1.3). Here, the examination of large-scale patterns of seaweeds
may provide clues to evaluate aspects of endemism, biological corridors, and expan-
sion of geographical distribution of various algal species. In this context, an account
of the genetic footprints of past diversity can help to understand not only the large-
scale processes that occurred along the evolution of the Antarctic flora, but also its
future genetic structure.
1.3.2 Environment and Ecophysiology
Due to the harsh environmental conditions, the Antarctic has commonly been
regarded as an inhospitable place for living organisms. Antarctic biota has adapted
to these conditions and thrives in different types of habitats, some marked by
extreme physical variability. However, the new environmental features as a conse-
quence of regional warming and related phenomena occurring in the cryospheric
realm, as well as direct anthropogenic pressures, are challenging the adaptive strate-
gies of seaweeds in manners still not well understood.
Light is probably the most important environmental factor determining the phe-
nology, spatial distribution, and productivity of Antarctic seaweeds. In Chap. 7,
Huovinen and Gómez describe the underwater optics in the context of present and
future variability and its importance for seaweed photobiology. The optical proper-
ties of the coastal waters, including their light absorbing and scattering components,
define the underwater light environment at ecologically relevant depths (down to
40 m). Despite Antarctic seaweeds being regarded as shade-adapted organisms, they
also show a striking capacity to acclimate to sudden increases in solar radiation.
However, the natural variability in light regimes is being altered due to earlier sea
ice breakup, enhanced runoff from the terrestrial and glacial melting, enhanced
UV-B levels as a result of ozone depletion, etc. These new scenarios are accompa-
nied by emergent stressors (e.g., local freshening, acidification, increasing contami-
nant load) whose influence on the underwater light climate in the Antarctic up to
now is not well understood.
Probably one of the most striking signals of warming in the Antarctic is the
retreat of glaciers, which is creating new ice-free habitats for benthic organisms.
The question of how the future coastal scenarios driven by climate change will
affect the colonization and fate of seaweeds was addressed by Quartino et al. (Chap.
8). In fact, the increased seaweed biomass will enhance the carbon flux and hence
the organic matter towards the higher trophic levels. Due to some species attaining
biomass values close to 10 kg m−2 wet weight, a strong impact on the coastal pro-
ductivity can be expected. However, in these highly dynamic new habitats, reflected
in the model system of Potter Cove in King George Island, seaweed colonization
follows the sharp gradients set by the light penetration, which are strongly modified
by enhanced sedimentation. Considering their great abundance and functional role
as ecosystem engineers, benthic seaweeds can become important carbon sink in
these systems. For instance, it has been estimated that seaweeds can account for a
global net primary production of ca. 1.5 Tg C yr−1 (Krause-Jensen and Duarte 2016),
thus forming part of the “blue carbon” components.
Low water transparency in the new ice-free areas affects the physiological per-
formance of seaweeds in different ways. Deregibus et al. (Chap. 9), based on long-
term records in areas nearby a retreating glacier at Potter Cove, describe the
photosynthetic carbon balance of seaweeds (the gain of C in photosynthesis versus
that lost in respiration) and its changes in relation with the light climate. Considering
light requirements and photosynthetic efficiency estimated from P-E curves, the
authors indicate that vertical distribution limits of some seaweed species changed as
a result of enhanced turbidity. Accuracy of the carbon balance estimations requires
a robust temporal set of solar irradiance data; thus, the importance of permanent in
situ monitoring accounting for variations at short (hours, days) and long (monthly,
inter-annual) timescale was highlighted.
The performance of seaweed populations under changing environmental regimes
depends on the survivorship of their early reproductive stages. However, life cycle
stages (e.g., spores, microscopic gametophytes, embryonic sporophytes, etc.) can
be highly sensitive to environmental stressors. In Chap. 10, Navarro et al. make a

thorough review of the aspects of the physiology of propagules of Antarctic sea-
weeds and how they respond to major physical factors, e.g., solar radiation, and
temperature, considering present and future settings. UV effects are in many cases
modified by temperature, showing interactions of factors. The response mechanisms
and degree of tolerance of early developmental stages mirror those observed in the
parental individuals. For example, differential responses to UV radiation deter-
mined in adult populations of congeneric and conspecific species from distinct
depth zones (e.g., subtidal versus intertidal) or geographical origin (e.g., Antarctic
versus sub-Antarctic) have also been observed in their propagules.
Antarctic seaweeds can be very abundant in terms of biomass and account by
more than 50% of the coastal primary productivity, especially around the Antarctic
Peninsula. Much of this ubiquity is strongly linked with efficient morpho-functional
adaptations that have permitted these organisms to occupy niches characterized by
sharp physical gradients. In Chap. 11, Gómez and Huovinen discuss the importance
of the form and function of seaweeds. In general, the functional forms are well dis-
tributed along the major groups of Antarctic seaweeds: coarsely branched and leath-
ery species, which can be regarded as the most robust and large-sized forms,
represent 49% of the total number of species. In this group, endemic brown and red
algae dominate, mainly growing at the subtidal zone. Filamentous, finely branched
and foliose species (41%) belong mostly to green and red algae, common at shallow
and intertidal sites, and are geographically widely distributed. Each of these morphs
are integrated in different life strategies and hence distinct ecosystem functions. For
example, perennial canopy-forming species show competitive abilities for light and
substrate, but in general prevail less in sites subject to strong physical perturbation.
Here, small colonizers and opportunistic species dominate in virtue of rapid meta-
bolic adjustments and turnover rates.
The different chapters reveal that the abiotic environment of Antarctica is chang-
ing in extent that is already affecting several aspects of the physiology of marine
biota in general and seaweeds in particular. The emergence of new habitats available
as the glaciers retreat is modifying the composition, structure, and trophic relations
of the benthic communities dominated by seaweeds. Apparently, a strategic factor
underlying these responses is the ability of adult plants and their propagules to
acclimate, via different functional traits, to the environmental shifts.
1.3.3 Ecological Functions
The ecological succession in Antarctic benthos determines the structure of the

mature community and its biological network. Different types of positive and nega-
tive interactions between algal assemblages, invertebrates, fish, and microorgan-
isms can be identified as the community develops. Based on in situ experiments,
Campana et al. (Chap. 12) describe the successional stages and their biotic interrela-
tions in a coastal site near Potter Cove. During the first three months, the incipient
community is dominated by microorganisms and benthic diatoms, which apparently

promote the development of small ephemeral filamentous green algae. The assem-
blage is successively enriched by the presence of various foliose and crustose forms
of red algae and during late algal succession (after 4 years) by some perennial spe-
cies of Desmarestia. The different components of the succession respond differently
to environmental factors such as UV radiation, grazing, glacier retreat, and sea ice,
and hence the structure and the biotic relations change dynamically within this early
community.
Grazing is probably the most important biotic factor controlling the structure and
composition of seaweed-dominated communities. In Antarctic benthic systems, the
early successional stages dominated by small-sized seaweeds and periphyton repre-
sent excellent models to study how grazing modifies different ecological properties
not only of native assemblages but also of alien species, whose arrival and establish-
ment will be stimulated by climate warming. In Chap. 13, Valdivia determined by
means of mathematical simulations the impact of mesograzers in sub-Antarctic and
Antarctic sites connected by dispersal. Ulva sp. was regarded an alien species, being
highly competitive in the Antarctic but not in the sub-Antarctic littoral. The results
indicated that Antarctic mesograzers have a deterministic and marked effect on the
biomass of the alien seaweeds; however, projected climate-change-driven shifts in
temperature or pH could decrease the potential of, for example, amphipod grazers
to control the development of invaders.
Antarctic seaweeds harbor complex and intricate microbiomes, which exert
important influence on different molecular and biochemical processes of the algal
host. Hitherto much of the coevolutionary processes of this association have been
little studied. However, it is reasonable to argue that microbiota plays important
functional roles in the ecology of Antarctic seaweeds. Gaitan-Spitia and Schmid
(Chap. 14) review various aspects of structure, diversity, and functioning of Antarctic
microbiomes and their implications for seaweeds. Members of phylum Actinobacteria
show high diversity and persistence among different seaweed species, while
Firmicutes are less represented. In general, the microbiomes associated to seaweeds
are different from those found in the surrounding environment, which suggest that
the bacterial composition is regulated by the seaweed host. Apparently, this feature
reflects adaptive strategies to respond to multiple environmental conditions, e.g.,
antioxidation, antimicrobial activity, photoprotection, etc.
Seaweeds and microphytobenthos represent the basis of the Antarctic coastal
food web. Because coastal areas can become highly perturbed, the dynamics and
stability of the interspecific interrelations have fundamental influence on the whole
benthic ecosystem at different spatial and temporal scales. Momo et al. (Chap. 15)
determined that the food web at Potter Cove is based on 24 seaweed species and
diverse other photosynthetic organisms, such as epiphytic and benthic diatoms and
phytoplankton as well as their detritus. The system is also hyperconnected indicat-
ing multiple energy pathways. Considering extinction thresholds, this network can
be regarded as relatively resilient to local losses of seaweed species. Similarly, using
as a model Fildes Bay, a coastal system geographically close to Potter Cove, Ortiz
et al. (Chap. 16) analyzed different keystone species complexes, which contribute
importantly to the emergent network properties, such as growth, organization,

development, maturity, and health of the ecosystem. The theoretical framework
(based on network analysis, ascendency, and loop analysis) identified detritus, the
phyto-zooplankton complex, sea stars, sea urchins, and seaweeds as the major com-
ponents determining the overall structure and function of this system. Similar to
Potter Cove, Fildes Bay appears to be a less developed system compared to other
cold-temperate system, but being highly resilient to physical perturbations.
The described examples on the ecology of the coastal system in the Maritime
Antarctic reveal complex biological interactions between, e.g., algae, microbiota,
invertebrates, and fish, which are strongly regulated by the physical environment. In
this scenario, seaweeds are identified as key components from the early stages of
succession to the consolidate communities. Due to the strong influence of physical
factors from terrestrial, freshwater, cryospheric and atmospheric processes, the
structure, function, and trophic interrelations in these communities are in general
very resistant to disturbances (Fig. 1.3). Thus, it seems that there are internal mech-
anisms operating at individual (e.g., efficient growth strategies, multiple anti-stress
mechanisms) as well as at population and community (e.g., filters controlling native
and alien species, high biological complexity based on species and biomass rich-
ness) levels, providing the system with a high resilience.
1.3.4 Chemical Ecology
The trophic relations in the Antarctic benthic system show a balance between con-
sumption by herbivores and their deterrence. Amsler et al. (Chap. 17) review the
recent advances in relationship between seaweeds and, e.g., amphipods, gastropods,
and fish. Diverse halogenated monoterpenes and phlorotannins (phenolic com-
pounds found in brown algae), and probably various other compounds, confer many
species of Antarctic seaweeds unpalatability to different kinds of herbivores.
Interestingly, the relationship between some seaweeds and various species of
amphipods includes mutualism, in which chemically defended algae offer protec-
tion from, e.g., omnivorous fish, while amphipods reduce the biofouling and epi-
phytic load of the thalli.
Chemical defenses based on phlorotannins operate not only against grazing, but
also form part of a wide suite of constitutive anti-stress mechanisms. In Chap. 18,
Gómez and Huovinen summarize the different aspects that determine the synthesis
and accumulation of these substances, which in some Antarctic brown algae can
represent up to 12% of the dry weight. These compounds have different functions as
grazing deterrents, reactive oxygen species (ROS) scavenging agents, and metal
chelators and can be allocated in different thallus parts to optimize defense. Although
phlorotannins are regarded as UV screening substances, no evidence on UV induc-
tion in Antarctic seaweeds has been reported. However, the antioxidant capacity
increases substantially along with increasing phlorotannin concentrations in algal
extracts, even in algae not naturally exposed to UV radiation.
The high prevalence of chemical defenses observed in Antarctic seaweeds is

remarkable and suggests their central role in defining their dominance and biologi-
cal interactions in the Antarctic coastal ecosystems (Fig. 1.3). Particularly, the con-
stitutively high levels of phlorotannins measured in various dominant brown algae
(e.g., Desmarestia anceps, Himantothallus grandifolius) open interesting questions
about the activation of anti-stress mechanisms based on chemical substances with
multiple primary and secondary functions. For seaweed assemblages subjected to
climate-change-driven environmental shifts, such defenses could confer ecological
advantages.
1.4 Gaps, Emerging Challenges, and Future Directions
The different chapters throughout this book update the current knowledge and pro-
vide novel insight into various aspects on diversity, ecophysiology, and ecology of
Antarctic seaweeds, with particular emphasis on their responses to the changing
polar environment. However, several gaps still persist and new questions require
attention in the near future.
• Long-term assessment: Due to logistical constraints, research in Antarctica is
normally restricted to the spring-summer season. This time frame clearly does
not permit covering the entire environmental variability to which Antarctic
organisms, especially annual and perennial species, are exposed. For example,
many gaps exist on the metabolic performance of seaweeds (e.g., carbon and
nutrient metabolism, use and remobilization of photoassimilates, etc.) during the
long Antarctic winter. In fact, the few studies addressing photosynthesis in win-
ter or under ice cover suggest that seaweeds are at their physiological limit dur-
ing this period (Gutkowski and Maleszewski 1989; Drew and Hastings 1992;
Schwarz et al. 2003). These studies should be complemented with long-term
monitoring of annual and inter-annual physical fluctuations in order to delimit
the ranges of acclimation and adaptation of organisms. Because most of the mon-
itoring platforms deployed around the Antarctica are designed to record changes
in the open ocean, long-term or real-time baseline information of near coastal
processes is still very limited. In this context, the long-term observations focused
on the impact of the retreating Fourcade Glacier in Potter Cove (King George
Island) represent an important effort in gaining insights into the responses of
benthos at ecological scales (Meredith et al. 2018; see Chap. 8 by Quartino et al.
and Chap. 9 by Deregibus et al. and references therein).
• Molecular ecology: Although remarkable improvements in biomolecular tools
have considerably expanded our capacities to record and elucidate the taxonomi-
cal status of Antarctic species (Held 2014), many seaweeds are still not well
classified, are cryptic or due to their life form (e.g., epiphytes, endophytes or
prostrates) remain undiscovered. Another important limitation challenging the
efforts to expand not only the genetic inventories, but also the general knowledge
on Antarctic organisms, is that the surveyed areas are strongly biased towards
some regions, especially around the Antarctic Peninsula and in sites in direct
proximity to research stations, while other coasts, e.g., from the East Antarctic,
have been scarcely visited (Mormède et al. 2014). Thus, it is assumed that in the
near future, along with the advances in phylogeography and population genetics
as well as in geographic coverage, the number of Antarctic seaweed species, both
native and recently arrived, will increase (see Chap. 2 by Oliveira et al.).
There a considerable lags in our understanding of gene expression and regula-
tion. This is probably one of the weakest areas in the study of seaweeds in general
and Antarctic species in particular. Thus, use of molecular tools such as transcrip-
tomic analysis will help identify the metabolic pathways and adaptive strategies that
Antarctic seaweeds exhibit beyond their tolerance threshold. For example, recently
high and constitutive gene expression of various physiological reactions, including
photochemical and inorganic carbon utilization components, from RNA-Seq analy-
sis was reported for the first time for an Antarctic endemic species (the brown alga
Desmarestia anceps; Iñiguez et al. 2017). Clearly this type of techniques open new
avenues for the identification of transcripts that are differentially expressed under
different stress conditions. On the other hand, the new molecular tools together with
improved physiological methodologies are fundamental to predict whether key
Antarctic seaweeds exhibit the molecular machinery to respond to ongoing and
near-future impacts of climate change.
• Ontogenetic development and life cycle responses: Developmental phases (e.g.,
spores, gametes, and embryonic sporophytes) are highly sensitive to environ-
mental changes (reviewed in Chap. 10 by Navarro et al.). However, they are often
overlooked due to their small size or because the logistical constraints associated
with their isolation, culture, and experimentation in Antarctica (Wiencke 1988).
Considering that the fate of these cells determine the structure and dynamics of
further life phases, it is urgent to conduct research focused on the acquisition of
stress tolerance capacity at different developmental stages and how this resil-
ience is “transferred” over generations. Following important developments in the
identification and visualization techniques in microalgae, e.g., fluorescence cell-
based sensing and “omics” approaches (metabolomics, proteomics, genomics), it
is now possible to quantify in real time the effects of different stressors on cel-
lular structures of early stages of seaweeds. Thus, it will be possible to track the
progressive expression of anti-stress mechanisms along the ontogeny or life
cycle phases, an essential approach to understand the adjustments in response to
environmental changes at an organismal level.
• Direct anthropogenic impacts and interaction of multiple stressors: Warming
and ozone depletion are not the only threats to Antarctic biota. Among other
concerns are ocean acidification and local decreases in salinity (freshening) due
to enhanced melting of glaciers. Furthermore, increase of pollution in the
Antarctic environment is generating new and not well-understood threats to
these ecosystems. As the identification of sources, concentrations, and persis-
tence of inorganic and organic pollutants poses considerable challenges (reviewed
in Caroli et al. 2001; Bargagli 2005), their effects on seaweeds and their com-
munities are hitherto widely unknown. Moreover, many contaminants are reac-
tive to other environmental factors (e.g., UV radiation), which may enhance their
detrimental impact on biota. Because all these different variables are changing
simultaneously, the research on the impact of their interactive effects (synergis-
tic, antagonistic, additive, etc.) is challenging (see Chap. 7 by Huovinen and
Gómez).
Finally, the contents of this book are in agreement with the increasing awareness
of the importance of Antarctic and its biota in global processes and the urgency to
improve our understanding on the role and sentinel responses of seaweeds to global
climate change. We believe that a comprehensive account of the progress made in
the last decades is timely and urgent in order to put into perspective how diversity,
ecophysiological adaptations, and ecosystem relations of seaweeds will be molded
in the future Antarctica.
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Part II
Diversity and Biogeography
Chapter 2
Diversity of Antarctic Seaweeds
Mariana C. Oliveira, Franciane Pellizzari, Amanda S. Medeiros,

and Nair S. Yokoya
Abstract Antarctica is characterized by extremes of climate and biogeographic iso-

lation from other continents by distance, high depths, and the Antarctic Circumpolar
Current. Even under these harsh conditions, macroalgae thrive in different coastal
ecosystems contributing to primary production and serving as habitat and food for a
variety of species of marine fauna. However, it is known that the Antarctic marine
flora presents low species richness compared to other biogeographical regions: until
the past decade a number of 120 Antarctic seaweeds had been reported. On the other
hand, long geographical isolation and extreme climatic and oceanographic conditions
justify their high degree of endemism (ca. of 33–40%). A new compilation of the
Antarctic seaweed diversity is presented in this chapter, reporting a list of 151 species
cited to the entire Antarctica, comprising 85 Rhodophyta, 34 Ochrophyta
(Phaeophyceae and Chrysophyceae), and 32 Chlorophyta with an endemism degree
of 27%, lower than in previous reports. Molecular approaches based on different
markers (ITS, UPA, COI-5P) are being used to assist species identification. The col-
lection of marine specimens in Antarctica is expensive and still very difficult, and
therefore, the occurrence for many species can become inaccurate. The difficult
access to samples is another limitation, which could explain that most of the best
known species are concentrated around scientific stations. Consequently, the mac-
roalgal diversity in Antarctica and its distribution is probably underestimated. A bet-
ter knowledge on this diversity and its distribution is urgent, as the region is facing
significant climate changes that may drive shifts on the assemblages of macroalgae.
M. C. Oliveira (*) · A. S. Medeiros

Department of Botany, Institute of Biosciences, University of São Paulo,
São Paulo, SP, Brazil
e-mail: mcdolive@ib.usp.br
F. Pellizzari
Laboratório de Ficologia e Qualidade de Água Marinha, Universidade Estadual do Paraná,
Campus Paranaguá, Paranaguá, PR, Brazil
e-mail: franciane.pellizzari@unespar.edu.br
N. S. Yokoya
Institute of Botany, São Paulo, SP, Brazil
e-mail: nyokoya@pq.cnpq.br

https://doi.org/10.1007/978-3-030-39448-6_2
24 M. C. Oliveira et al.
Keywords Benthic algae · Diversity · Endemic species · Maritime Antarctica ·

Molecular taxonomy
2.1 The Antarctic Environment
Antarctica is characterized by extremes of climate, which makes its habitats and

biogeographic context quite unique. It is isolated from other continents by distance,
high depths, and oceanographic currents, mainly by the Antarctic Circumpolar
Current (Barker and Thomas 2003) (Fig. 2.1). Broad variations in temperature and
salinity can occur in the Antarctic habitat, with high incidence of alternating ultra-
violet radiation with long periods of absence of light, freezing, and thawing cycles
that determine highly variable physical mosaics (Wynn-Williams 1996; Vincent
2000; Clarke et al. 2005). However, few attempts have been made to provide sub-
Fig. 2.1 Schematic map showing Antarctica and surroundings, Africa (AF), Australia (AU), New
Zeeland (NZ), and South America (SA). King George Island (South Shetland Islands) is marked
by ∗ and Adelaide Island is marked by ★. The Antarctic Circumpolar Current is represented by a
black line and arrowheads. (https://freevectormaps.com/globes/antarctica/GLB-AN-01-0001)
2 Diversity of Antarctic Seaweeds 25
stantial insight into the implications of these gradients of abiotic factors for the
spatial distribution of biodiversity (Convey et al. 2014).
Low temperatures, high salinities, and the occurrence of long periods of ice
cover in coastal regions can characterize the Southern Ocean. The seasonality of
irradiance levels and photoperiod, as well as the ice cover, exert a strong effect on
supralittoral, eulittoral, and sublittoral communities (Hempel 1987; Drew and
Hastings 1992). The alternation of annual ice cycles impacts the physical and chem-
ical environment in many ways and, consequently, the local biota as a whole. The
effects of ice cover are most obvious in the intertidal zone and in the upper sublit-
toral due to the physical action of the displacement of ice blocks that remove sessile
organisms, including macroalgae. Ice formation, as well as summer melting, signifi-
cantly alters salinity and light penetration, exposing benthic organisms to extreme
values of these parameters.
Even so, the Southern Ocean is known to afford living space for high abundance
of benthic organisms compared to other regions of the world. Since the first studies
carried out in the region, the high densities and relatively high diversity of benthic
communities have been demonstrated (Clarke 1990).
2.2 Seaweeds in Antarctica: Definition and Importance
Similar to the terrestrial plants, seaweeds – or marine macroalgae – are photosyn-

thetic organisms that form underwater forests on consolidated or hard substrate. In
virtue of their diversity and biomass, seaweeds play a key role in sustaining the
primary production in coastal ecosystems and are important food sources, espe-
cially to the rockfish, Notothenia coriiceps; echinoderms, e.g., Odontaster validus
and Sterechinus neumayeri; and amphipods, e.g., Gondogeneia antarctica.
Moreover, macroalgae serve as shelter and substrate for the growth and reproduc-
tion of several marine organisms (Nedzarek and Rakusa-Suszcewski 2004, see also
Chap. 15 by Momo et al. and Chap. 16 by Ortiz et al.).
Antarctic seaweeds belong to the major divisions of algae: golden-brown and
brown (Ochrophyta: Chrysophyceae and Phaeophyceae, respectively), green
(Chlorophyta), and red algae (Rhodophyta). The morphology of Antarctic macroal-
gae varies from crustose forms or delicate filamentous forms of few centimeters to
large foliaceous, terete, and leathery forms that may reach several meters long
(Fig. 2.2). Some species deposit calcium carbonate in their cell walls, presenting a
rigid thallus. These calcareous species provide substrate for other marine species
(see also Chap. 11 by Gómez and Huovinen). Specific groups of algae are protected
against predation by synthesizing chemical compounds that make them unpalatable
(see Chap. 17 by Amsler et al.). The synthesis and accumulation of these bioactive
compounds is the result of a long and complex evolutionary and ecological process.
Some of these substances, especially for the species adapted to extreme polar eco-
systems, may have biotechnological and pharmaceutical applications. The repro-
ductive sexual and/or asexual cells of Antarctic seaweeds are well adapted to the
Fig. 2.2 Macromorphology of Antarctic seaweeds. (a) Crustose calcareous red alga

Clathromorphum sp. (Rhodophyta). (Photo by F. Pellizari); (b) monostromatic saccate green alga
Monostroma hariotii (Chlorophyta); (c) terete red alga Plocamium sp. (Rhodophyta). (Photos by
A.S. Medeiros); (d) leathery brown alga Himantothallus grandifolius (Phaeophyceae), with an
approximate length of 3.7 m. (Photo by E.C. Oliveira)
environmental conditions marked by low temperature and limited solar radiation.

These cells, either an asexual stage, a gamete, or a zygote (after gametes fusion),
will float within the marine currents and settle and develop on a suitable substrate,
in a dynamic tuned with the seasonal Antarctic variability (see also Chap. 10 by
Navarro et al.).
In the Southern Ocean, macroalgae together with the phytoplankton are respon-
sible for 30–50% of the dissolved O2 released in the marine habitats surrounded by
the Southern Ocean (data retrieved from visibleearth.nasa.gov). In particular, the
robust and perennial endemic brown algae (Phaeophyceae), such as Himantothallus
grandifolius and Desmarestia spp., are well represented in terms of biomass and are
the main primary producers in these areas (Amsler et al. 1995; Wiencke et al. 2014).
2.3 S
eaweed Taxonomic Studies in Antarctica: Toward
a New Species Compilation
Antarctic seaweed communities have been characterized by low diversity and high
levels of endemism (Lamb and Zimmermann 1977; Wiencke et al. 2014). The first
reports date back to the nineteenth century when seaweeds were collected during
cruises of the corvettes Uranie and Physicienne (Gaudichaud 1826). However, the
first compilations on diversity of Antarctic seaweeds along the Antarctic Peninsula
were published much later by Skottsberg (1906, 1941, 1953, 1964), who is consid-
ered the pioneer of the Antarctic phycology. The first scuba diving surveys were
conducted by Neushul (1959, 1961, 1963, 1965, 1968) and Skottsberg and Neushul
(1960). Skottsberg (1964) estimated the occurrence of 96 species of Antarctic sea-
weeds (16 Chlorophyta, 19 Phaeophyceae, and 61 Rhodophyta). In later surveys,
higher species richness was documented: 100 species (Papenfuss 1964; Moe 1985),
120 species (Clayton 1994), and 117–123 species (Wiencke and Clayton 2002). The
most recent review on seaweed diversity for the entire Antarctica reported a total of
124 taxa, comprising 80 species of Rhodophyta, 27 species of Phaeophyceae, and
17 Chlorophyta (Wiencke et al. 2014).
Different researchers have broadly studied seaweed communities from the South
Shetland Islands, mainly from the King George Island, including Zielinski (1990),
Quartino et al. (2005), Oliveira et al. (2009), Valdivia et al. (2014), and Gómez et al.
(2019). The macroalgal diversity from Deception Island and Livingston Island was
studied by Ramírez (1982), Clayton et al. (1997), and Gallardo et al. (1999).
Medeiros (2013) generated a set of sequences of macroalgal DNA barcodes and
phylogenetic markers from Admiralty Bay (King George Island), contributing to a
molecular database useful for future investigations on the diversity of Antarctic sea-
weeds. Molecular data were obtained for 8 species of Chlorophyta, 9 species of
Phaeophyceae, and 14 species of Rhodophyta. Prasiola sp., Protomonostroma rosu-
latum (Chlorophyta), Chordaria linearis (Phaeophyceae), Acanthococcus antarcti-
cus, and Plumariopsis peninsularis (Rhodophyta) are new records for Admiralty
Bay, and Callophyllis sp. is possibly a new species for science.
Mystikou et al. (2014) analyzed the seaweed diversity in the Southwestern
Antarctic Peninsula (Adelaide Island) over records of 35 years, reporting 41 spe-
cies. This part of the Antarctic Peninsula is a key region affected by contemporary
climate change, but has been rarely studied. Sanches et al. (2016) performed multi-
variate analyses of Antarctic and sub-Antarctic seaweed distribution patterns focus-
ing on a new evaluation of the role of the Antarctic Circumpolar Current. Regarding
species diversity, in this study the authors identified 129 and 145 macroalgal spe-
cies, respectively, for the Southern Antarctic Circumpolar Front (SACF) and for the
Polar Front (PF) and considering genera, 95 and 101, for the SACF and PF,
respectively.
Pellizzari et al. (2017) recorded a total of 104 species of benthic marine algae
along the South Shetland Islands (28 Phaeophyceae, 24 Chlorophyta, and 52
Rhodophyta), representing 82% of all seaweed taxa described in Antarctica. The
authors also reported nine new records, mainly previously recorded at other lati-
tudes (Protomonostroma rosulatum, Monostroma grevillei, Cladophora coelothrix,
Chaetomorpha irregularis, Dictyota decumbens, Asteronema ferruginea,
Microzonia velutina, Cladodonta lyalli, Rhodophyllis centrocarpa) and two puta-
tive new species of Prasiola sp. and Callophyllis sp. (see also Medeiros 2013).
Spatial variation in the species diversity was observed among the collecting sites:
Livingston Island and King George Island showed the highest diversity. Deception
Island, an area with geothermal activity and intense tourism, was dominated by
opportunistic and broadly distributed filamentous green algae (see also Chap. 5 by
Pellizzari et al.).
A new compilation of the Antarctic seaweed diversity is presented in this chap-
ter, based primarily on data reported by Wiencke and Clayton (2002), Oliveira et al.
(2009), Wiencke et al. (2014), Mystikou et al. (2014), and Pellizzari et al. (2017).
This survey reports a species richness of 151 species, comprising 85 Rhodophyta
(plus one uncertain species), 34 Phaeophyceae, and 32 Chlorophyta to the entire
Antarctic region (Tables 2.1, 2.2, and 2.3, based on Guiry and Guiry (2019) for
taxonomical nomenclature).
Antarctic marine flora can be characterized by a high number of endemic spe-
cies, approximately 33% (Wiencke and Clayton 2002), 35% (Neushul 1968; Wulff
et al. 2009; Wiencke and Amsler 2012), or 39.6% (Skottsberg 1964). However, this
percentage decreases to 27.1% of species restricted to areas within the Antarctic
Circumpolar Current, i.e., Antarctica and sub-Antarctic islands (with latitude higher
than 55°S) in the compilation of the present chapter (Tables 2.1, 2.2, and 2.3).
Considering the degree of endemism close to 27.1% calculated from a total of 41
endemic species, Rhodophyta represents 61% of endemic taxa, Phaeophyceae
29.3%, and Chlorophyta 9.7%. However, if we consider separately and proportion-
ally (total group richness/group endemic richness), the algal group with the highest
endemism degree is Phaeophyceae (35.3%), followed by Rhodophyta (29.4%), and
Chlorophyta (12.5%).
Large brown seaweeds of the order Laminariales (kelps) are common structuring
species in cold-temperate coasts in the southern and northern hemisphere and also
in the Arctic, while in Antarctica this order is substituted by the Desmarestiales,
Table 2.1 Compiled taxa list of Chlorophyta

South King
Shetland George Adelaide
Species Antarcticaa Islandsb Islandc Islandd
Acrosiphonia arcta (Dillwyn) Gain 1912 X X X
Blidingia minima (Nägeli ex Kützing) Kylin X X
1947
Chaetomorpha irregularis (Zaneveld) X X
Cormaci, Furnari & Alongi 2014 (as Lola
irregularis) (E)
Chaetomorpha mawsonii Lucas 1919 X X
Cladophora coelothrix Kützing 1843 X
Cladophora repens Harvey 1849 X
Endophyton atroviride O’Kelly in Ricker X X
1987
Entocladia maculans (AD Cotton) X
Papenfuss 1964
Lambia antarctica (Skottsberg) Delépine X X
1967 (E)
Monostroma grevillei (Thuret) Wittrock X
1866
Monostroma hariotii Gain 1911 X X X X
Prasiola sp. (SP428305) X
Prasiola crispa (Lightfoot) Kützing 1843 X X X
Protomonostroma rosulatum X
Vinogradova (E)
Protomonostroma undulatum (Wittrock) X
Vinogradova 1969
Pseudothrix groenlandica (Agardh) Hanic X
& SC Lindstrom 2008 (as Capsosiphon
groenlandicus)
Rhizoclonium ambiguum (Hooker & X
Harvey) Kützing 1849
Rhizoclonium riparium (Roth) Harvey 1849 X
Spongomorpha pacifica (Montagne) X X
Kützing 1854 (as Acrosiphonia pacifica)
Ulothrix australis Gain 1911 (E) X X X
Ulothrix flacca (Dillwyn) Thuret in Le Jolis X X
1863
Ulothrix subflaccida Wille 1901 X
Ulothrix zonata (Weber & Mohr) Kützing X
1833
Ulva sp. (foliose) X
Ulva compressa Linnaeus 1753 X X
Ulva hookeriana (Kützing) HS Hayden, X X X
Blomster, Maggs, Silva, Stanhope &
Waaland 2003 (as Enteromorpha bulbosa)
(continued)
Table 2.1 (continued)
South King
Ulva intestinalis Linnaeus 1753 X X
Ulva lactuca Linnaeus 1753 X
Ulva rigida C.Agardh 1823 X
Ulvella leptochaete (Huber) Nielsen, X
O’Kelly & Wysor in Nielsen et al. 2013
Ulvella viridis (Reinke) Nielsen, O’Kelly & X X
Wysor in Nielsen et al. 2013 (as Entocladia
viridis)
Urospora penicilliformis (Roth) Areschoug X X X X
1866
Based on aWiencke and Clayton (2002) and Wiencke et al. (2014), bPellizzari et al. (2017), cOliveira
et al. (2009), and dMystikou et al. (2014)
E = endemic species (restricted to Antarctic and sub-Antarctica)
Table 2.2 Compiled species list of Ochrophyta (Phaeophyceae and Chrysophyceae)

South King
Adenocystis utricularis (Bory) Skottsberg X X X X
1907
Antarctosaccion applanatum (Gain) X X X
Delépine (E)
Ascoseira mirabilis Skottsberg 1907 (E) X X X
Asteronema ferruginea (Harvey) X
Delépine & Asensi 1975
Australofilum incommodum (Skottsberg) X
AF Peters 2003
Chordaria linearis (Hooker & Harvey) X X
Cotton 1915
Cystosphaera jacquinotii (Montagne) X X X
Skottsberg 1907 (E)
Desmarestia anceps Montagne 1842 X X X
Desmarestia antarctica Moe & Silva X X X
1989 (E)
Desmarestia chordalis Hooker & Harvey X
1845
Desmarestia confervoides (Bory) X
Ramírez & Peters 1993
Desmarestia menziesii Agardh 1848 (E) X X X X
Dictyota decumbens (Ricker) Hörnig, X
Schnetter & Prud’homme van Reine
1992
(continued)
South King
Ectocarpus constanciae Hariot 1887 X
Ectocarpus siliculosus (Dillwyn) X
Lyngbye 1819
Elachista antarctica Skottsberg 1953 (E) X X X X
Geminocarpus austrogeorgiae Skottsberg X X X X
1907 (E)
Geminocarpus geminatus (Hooker & X X X X
Harvey) Skottsberg 1907
Halopteris corymbosa (Dickie) Draisma, X
Prud’homme & Kawai 2010
Halopteris obovata (Hooker & Harvey) X X
Sauvageau 1904
Haplogloia moniliformis RW Ricker X X
1987
Himantothallus grandifolius (A Gepp & X X X X
E Gepp) Zinova 1959 (E)
Leptonematella falklandica (Skottsberg) X
MJ Wynne 1969
Lithoderma antarcticum Skottsberg 1953 X X
(E)
Microzonia australe (Levring) Camacho X
& Fredericq 2018 (as Syringoderma
australe) (E)
Microzonia velutina (Harvey) Agardh X
1894
Petalonia fascia (Müller) Kuntze 1898 X X
Petroderma maculiforme (Wollny) X X
Kuckuck 1897
Phaeurus antarcticus Skottsberg 1907 X X X
(E)
Pylaiella littoralis (Linnaeus) Kjellman X X X X
1872
Ralfsia australis Skottsberg 1921 X X
Scytosiphon lomentaria (Lyngbye) Link X X
1833
Scytothamnus fasciculatus (Hooker & X X
Harvey) Cotton 1915
Utriculidium durvillei Skottsberg 1907 X X
a
Wiencke and Clayton (2002) and Wiencke et al. (2014), bPellizzari et al. (2017), cOliveira et al.
(2009), and dMystikou et al. (2014)
Table 2.3 Compiled taxa list of Rhodophyta

South King
Acanthococcus antarcticus Hooker & X X
Harvey 1845 (E)
Ahnfeltia plicata (Hudson) Fries 1836 X
Antarcticothamnion polysporum Moe & X
Silva 1979 (E)
Antarctocolax lambii Skottsberg 1953 (E) X
Ballia callitricha (C Agardh) Kützing 1843 X X X X
Ballia sertularioides (Suhr) Papenfuss 1940 X
Bangia fuscopurpurea (Dillwyn) Lyngbye X X
1819
Callophyllis sp. 1 X
Callophyllis sp. 2 X
Callophyllis atrosanguinea (JD Hooker & X X X
Harvey) Hariot 1887
Callophyllis pinnata Setchell & Swezy Xe
1923
Callophyllis tenera Agardh 1849 X
Callophyllis variegata (Bory) Kützing 1843 X X
Carlskottsbergia antarctica (Hooker & X
Harvey) Athanasiadis 2018 (as
Lithophyllum antarcticum)
Ceramium involutum Kützing 1849 X
Cladodonta lyallii (Hooker & Harvey) X
Skottsberg 1923
Clathromorphum sp. X
Clathromorphum obtectulum (Foslie) Adey X X
1970
Curdiea racovitzae Hariot in De Wildemann X X X X
1900 (E)
Delisea pulchra (Greville) Montagne 1844 X X X
Erythrotrichia carnea (Dillwyn) Agardh X
1883
Falklandiella harveyi (Hooker) Kylin 1956 X
(as Dasyptilon harveyi)
Gainia mollis Moe 1985 (E) X X
Georgiella confluens (Reinsch) Kylin 1956 X X X
(E)
Gigartina skottsbergii Setchell & Gardner X X X
1936
Gracilariopsis longissima (Gmelin) X
Steentoft, Irvine & Farnham 1995 (as
Gracilaria verrucosa)
(continued)
South King
Griffithsia antarctica Hooker & Harvey in X
Hooker 1847
Gymnogongrus antarcticus Skottsberg 1953 X X X
(E)
Gymnogongrus turquetii Hariot 1907 (E) X X X
Hildenbrandia lecannellieri Hariot 1887 X X X
Hydrolithon sp. X
Hymenocladia sp. X
Hymenocladiopsis prolifera (Reinsch) X X X
Wynne 2004 (as H. crustigena) (E)
Iridaea cordata (Turner) Bory de Saint- X X X X
Vincent 1826
Iridaea mawsonii Lucas 1919∗ X X
Leptophytum coulmanicum (Foslie) Adey X
1970 (E)
Lithothamnion granuliferum Foslie 1905 X X
Meiodiscus concrescens (KM Drew) X
Gabrielson in Gabrielson et al. 2000 (as
Audouinella concrescens)
Mesophyllum sp. X
Microrhinus carnosus (Reinsch) Skottsberg X X
1923
Myriogramme livida (Hooker & Harvey) X
Kylin 1924
Myriogramme manginii (Gain) Skottsberg X X X
1953 (E)
Myriogramme smithii (Hooker & Harvey) X X X
Kylin 1924
Nereoginkgo adiantifolia Kylin in Kylin & X X
Skottsberg 1919 (E)
Neuroglossum delesseriae (Reinsch) Wynne X X X
1997 (as N. ligulatum) (E)
Notophycus fimbriatus Moe 1986 (E) X X X X
Pachymenia orbicularis (Zanardini) Setchell X X X
& Gardner 1934
Palmaria decipiens (Reinsch) Ricker 1987 X X X X
Palmaria georgica (Reinsch) Ricker 1987 X X
Pantoneura plocamioides Kylin 1919 (E) X X X
Paraglossum lancifolium (Agardh) Agardh X X X
(as Delesseria lancifolia)
Paraglossum salicifolium (Reinsch) Showe X X X
in Fredericq & Hommersand 2012 (as
Delesseria salicifolia)
(continued)
South King
Peyssonnelia harveyana P Crouan & H X
Crouan ex Agardh 1851
Phycodrys antarctica (Skottsberg) X X X
Skottsberg 1923 (E)
Phycodrys austrogeorgica Skottsberg 1923 X X X
(E)
Phycodrys quercifolia (Bory) Skottsberg X X
1922
Phyllophora abyssalis Skottsberg in Kylin X
& Skottsberg 1919 (E)
Phyllophora ahnfeltioides Skottsberg in X X
Kylin & Skottsberg 1919 (E)
Phyllophora antarctica A Gepp & ES Gepp X X
1905 (E)
Leptophytum foecundum (Kjellmann) Adey X
Phymatolithon lenormandii (Areschoug) X
Adey 1966
Picconiella plumosa (Kylin) De Toni 1936 X X X
Plocamium cartilagineum (Linnaeus) Dixon X X X X
1967
Plocamium secundatum (Kützing) Kützing X X X X
1866
Plocamium hookeri Harvey in Hooker & X X X
Harvey 1845 (E)
Plumariopsis eatonii (Dickie) De Toni 1903 X
Plumariopsis peninsularis Moe & Silva X X
1983 (E)
Polysiphonia abscissa Hooker & Harvey X
1845
Pseudolithophyllum sp. X
Pterothamnion antarcticum (Kylin) Moe & X
Silva 1980
Pterothamnion simile (Hooker & Harvey) X
Nägeli 1862
Ptilonia magellanica (Montagne) Agardh X
1852
Porphyra plocamiestris Ricker 1987 (E) X X X
Porphyra umbilicalis Kützing 1843 X
Porphyra woolhouseae Harvey 1863 X
Pyropia endiviifolia (A Gepp & E Gepp) X X X
Choi & Hwang in Sutherland et al. 2011 (as
Porphyra endiviifolia) (E)
(continued)
South King
Rhodochorton purpureum (Lightfoot) X
Rosenvinge 1900 (as Audouinella purpurea)
Rhodophyllis centrocarpa (Montagne) X
Wynne
Rhodymenia coccocarpa (Montagne) X X X
Wynne 2007 (as Rhodymenia subantarctica)
Rubrointrusa membranacea (Magnus) X
Clayden & Saunders 2010 (as Audouinella
membranacea)
Sarcodia sp. X
Sarcodia montagneana (Hooker & Harvey) X X
Agardh 1852
Sarcothalia circumcincta (Agardh) X
Hommersand in Hommersand et al. 1993
Sarcothalia papillosa (Bory) Leister in X X
Hommersand, Guiry, Fredericq & Leister
1993
Adapted from aWiencke and Clayton (2002) and Wiencke et al. (2014), bPellizzari et al. (2017),
c
Oliveira et al. (2009), cMystikou et al. (2014), dMystikoy et al. (2014) and eYoneshigue-Valentin
et al. (2013)
*This species is considered uncertain in Algaebase (https://www.algaebase.org/GuiryandGuiry
2019), and therefore was not considered in the calculations for total and endemic species.
e.g., Himantothallus grandifolius and various Desmarestia spp. (Moe and Silva
1977; Clayton 1994). The fact that Laminariales do not reproduce at temperatures
below 0°C and/or the competition with Desmarestiales could explain the absence of
kelps in Antarctica (Peters and Breeman 1993).
2.4 M
olecular Taxonomy for the Study of Antarctic Seaweed
Diversity
Some Antarctic macroalgae exhibit phenotypic plasticity, which leads to identifica-

tion problems; therefore, it is important to use molecular markers (e.g., DNA bar-
coding) as an additional tool to gain accuracy in the classification (Medeiros 2013).
However, there are some difficulties in the applicability of this technique, due to the
occurrence of variability in the region of the primers, especially for cox1 DNA bar-
code, and the lack of effectiveness of this marker in the case of Chlorophyta. The
proposal of a quick, easy, and low-cost method for inventory of seaweed biodiver-
sity shows advantages over other techniques, since standardization of a DNA bar-
code in the identification and report of new records or new species facilitates the
exchange of information among laboratories around the world (Le Gall and
Saunders 2010).
Medeiros (2013) has successfully used three DNA barcodes for the identification
of the macroalgal assemblages of Admiralty Bay, despite some limitations. The
three used DNA barcodes (UPA, cox1, and tufA), although presented different rates
of divergence, were consistent with other markers used in the analyses. The main
advantage found in the amplification of the UPA marker (Sherwood et al. 2010) was
the universality of the primers, since a single pair of primers was used for the three
seaweed groups, whereas different combinations of primers were required to
amplify the cox1. However, the low variability in UPA sequences may underesti-
mate the species diversity, while cox1 presents a higher level of divergence, being
more suitable as a specific marker. The absence of universal primers can limit the
amplification in some groups of algae. In other instance, tufA showed to be very
promising for green algae, since it was possible to amplify this marker with a single
set of primers and the levels of divergence found were relatively higher than for
UPA and comparable to those found for cox1 in red and brown algae. Finally, the
use of the UPA can be a fast and efficient tool for biodiversity monitoring, mainly
of cryptogenic and cryptic seaweed species from Antarctica. Medeiros (2013) con-
clude that due to the analysis of only a few specimens per species in Admiralty Bay,
it was not possible to establish a reliable limit between the values of intraspecific
and interspecific divergences (barcode gap) for the distinct genera, which according
to Meier et al. (2008) is necessary for successful species identification.
Thus, further studies are needed to establish these limits in order to use the DNA
barcoding technique extensively in the identification and surveys of macroalgae
diversity from Antarctica. Although larger molecular markers such as rbcL, ITS and
SSUrDNA, which have more sequences available for comparison in global database,
are relevant to obtain. In addition, the use of GenBank data for molecular species
identification purposes is not totally reliable, since accurate species identification is
not always guaranteed and identification based on morphological characters is still
indispensable.
Seaweed species from Admiralty Bay, King George Island, exhibit affinities with
seaweeds from South America and New Zealand, as well as with cold and polar
regions from the northern hemisphere. In Hommersand et al. (2009), rbcL data
showed that the affinity between the Antarctic and South American Rhodophyta
species is complex, since the species groups are phylogenetically distant. Still,
according to Hommersand et al. (2009), there is a possibility that particularities in
the Antarctic climate caused a faster evolution of the rbcL gene, compared to tem-
perate waters from South America. This fact may justify the high divergence found
by Medeiros (2013) in sequences of rbcL for the species Iridaea cordata and
Plocamium aff. cartilagineum obtained in Antarctica, when compared to the same
species sampled in Chile. Finally, the author demonstrated that the DNA barcoding
tool, together with other markers, proved to be a very suitable approach for large-
scale application in biodiversity and conservation studies, providing information for
global database that would combine molecular, morphological, and distributional

data (see also Chap. 5 by Pellizzari et al.).
2.5 Seaweed Distribution in Antarctica
Seaweeds are conspicuous components of subtidal benthic communities; however,

their abundance and diversity vary strongly depending on the habitat characteristics
(Klöser et al. 1996). In many cases the hard-bottom substrata are often covered by
crustose red algae (e.g., Hildenbrandia lecannellieri and species of the order
Corallinales). Pebbles and boulders of granite, as well as volcanic outcrops, often
form the hard substrate. These formations are common on King George Island,
Penguin Island, Nelson Island, and Robert Island. Elephant Island, Livingston
Island, and Half Moon Island are formed of volcanic bedrocks and of pebbles in the
intertidal and subtidal zones. The slope and exposure to waves, ice melting, and
abrasion vary among Antarctic islands and the continental coast influencing directly
the recruitment of seaweeds (Pellizzari et al. 2017).
Large brown algae of the order Desmarestiales (e.g., Desmarestia anceps,
D. menziesii, and Himantothallus grandifolius) are dominant in the benthic com-
munities of Western Antarctica, growing in substrata below the zone affected by ice
scouring down to ≥30-m water depth (Wiencke and Clayton 2002). On the other
hand, red algae are dominant in the benthic communities at higher latitudes, as in
the Ross Sea. Many macroalgae may survive, after detached from the original sub-
strate, during long periods as free-floating thalli. Recent studies (synopsis in Fraser
et al. 2018) report that these robust free-floating specimens may also transport
hitchhiker species by rafting, including smaller epiphyte seaweed species and sev-
eral marine invertebrates. These floating seaweed masses anchor other species,
being recognized as vectors of introduction of alien/cryptogenic taxa around
Antarctica (see also Chap. 3 by Fraser et al. and Chap. 4 by Macaya et al.).
Intertidal seaweeds are filamentous (e.g., the green algae Urospora penicillifor-
mis and Ulothrix spp.), foliose (e.g., Monostroma hariotii, Pyropia endiviifolia), or
saccate (e.g., Adenocystis utricularis), or possess perennial basal attachments (e.g.,
Palmaria decipiens). Intertidal species are well developed in the milder climates of
the Antarctic maritime islands, especially in the South Shetland and the South
Orkney archipelagos (Wiencke and Clayton 2002; Oliveira et al. 2009). These
organisms display a suite of morpho-functional adaptations to cope with a high vari-
ability of physical factors, such as temperature, ice scour, light, salinity, etc. (Gómez
et al. 2019, see also Chap. 11 by Gómez and Huovinen).
In the Maritime Antarctica, which compress the Antarctic Peninsula and nearby
islands, the substrate availability, milder climate, and less marked seasonality per-
mit the colonization and persistence of a higher diversity of marine organisms
(Amsler et al. 1995). Here, more than 90% of all Antarctic species have been
reported (Clayton 1994). Species richness decreases in the East Antarctic Peninsula
(EAP), and only 7 and 17 species occurred, respectively, on the coasts of the Ross
Sea (Zaneveld 1966) and Terra Nova Bay (Cormaci et al. 1992). Generally, an
inverse relationship between species diversity and latitude is observed in Antarctic
seaweeds (Wiencke and Clayton 2002). A total of 104 taxa was identified in South
Shetland Islands (ca. 60°S) by Pellizzari et al. 2017, a species number higher than
in Adelaide Island (67°S) with 41 taxa (Mystikou et al. 2014) and Terra Nova Bay
(Ross Sea, above latitude 70°S) with 17 taxa (Cormaci et al. 1992). Only few spe-
cies grow in latitudes above 76°S, such as the red algae Iridaea cordata, Phyllophora
antarctica, Phycodrys antarctica, and Hildenbrandia lecannellieri, the green alga
Monostroma hariotii, and the brown alga Desmarestia menziesii (Wiencke and
Clayton 2002).
2.6 Concluding Remarks: Gaps and Prospects for the Future
The knowledge on the seaweed diversity throughout Antarctica is essential, as they

are fundamental as primary producers and their composition affects the structure of
the ecosystems. Species of seaweeds are bioindicators of environmental changes,
including climate change, invasive species, and seawater pollution, among others.
Therefore, knowledge on seaweed diversity throughout Antarctica is urgently needed.
There are some clear gaps in the knowledge on seaweed diversity from the
Antarctic region, especially in deeper water. As described above, species richness
tends to increase with the number of collections in a wide range of locations and in
different environments, but collection in Antarctica is expensive and difficult.
Furthermore, as mentioned above, little is known on the diversity fluctuations of the
marine flora and how those are influenced by environmental factors or anthropo-
genic activities. Regular monitoring of sites should be done, especially of those that
are subjected to human activities such as those from scientific bases or touristic visi-
tation (Hughes and Ashton 2017).
In Antarctica, some of the strongest environmental gradients on the planet can be
found, therefore providing an ideal study ground to test hypotheses related with
environmental variability and its impact on biodiversity. The most important physi-
cal driver of Antarctic marine communities is the oceanographic boundary of the
Polar Front. At smaller spatial scales, ice cover, ice scour, and salinity gradients are
clearly important determinants of diversity at habitat and community level. However,
stochastic and extreme events remain an important driving force, particularly in the
context of local extinction, colonization, or recolonization of Antarctic biota
(Convey et al. 2014).
Biogeographic barriers are known to be fundamental in macroecological and
evolutionary processes. Ocean circulation, considering present and past patterns of
continental drift, can isolate or connect many groups of marine organisms, includ-
ing seaweeds (see also Chap. 3 by Fraser et al. and Chap. 5 by Pellizzari et al.).
These benthic organisms release spores and propagules as planktonic stages that
drift with currents and/or tides and have been a sensible indicator of changes in
biogeographic distribution patterns (Sanches et al. 2016, see also Chap. 10 by
Navarro et al.). According to Pellizzari et al. (2017) and Fraser et al. (2018), the
Antarctic Circumpolar Current, previously considered a biogeographic barrier, may
become a new pathway for biota interconnectivity and deserves further investiga-
tion. Mystikou et al. (2014) discuss that Antarctic seaweeds display plasticity and
adaptability in response to extreme environmental conditions such as low tempera-
tures and limited light availability (Wiencke and Amsler 2012). Thus, it is relevant
to examine how environmental alterations, such as those caused by climate change,
will be affecting algal seasonality, richness, depth zonation, and latitudinal
distribution.
The higher seaweed diversity observed in the South Shetland Islands (Pellizzari
et al. 2017), a transitional area, bring the imminent need of long-term biological and
abiotic monitoring in order to establish conservation guidelines across the Antarctic
and sub-Antarctic zones, especially upon increasing tourism, global climate, and
oceanographic changes.
Moreover, laboratory culture techniques associated with morphological and
molecular analyses could reveal the hidden diversity of Antarctic marine flora, espe-
cially with respect to small species (e.g., epiphytes and endophytes), including
potential alien/cryptogenic species. Integrative taxonomical studies are needed to
less known groups, e.g., crustose algae, and molecular studies are essential to clar-
ify the phylogenetic and biogeographic relationships of Antarctic seaweeds.
Finally, a reference baseline database of seaweed diversity is urgently necessary.
This should integrate different inventories based on morphology and life cycles with
molecular data from fast, high-throughput, and low-cost methods, such as DNA
barcodes and/or metagenomics (Oliveira et al. 2018). Hence, researchers will be
enabled to effectively monitor environmental changes and help in the conservation
of this unique environment.
Acknowledgments We thank PROANTAR (Brazilian Antarctic Program 557030/2009-9,

407588/2013-2 and 442258/2018-2), INCT Criosfera 2, Brazilian Navy (Polar Ship Almirante
Maximiano–H41), Brazilian Air Force, MMA (Ministry of Environment), MCTIC (Ministry of
Science, Technology and Innovation), and CNPq (National Council of Research and Development;
for grant 310672/2016-3 to NSY and 301491/2013-5 to MCO). This study was financed in part by
the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance
Code 001.
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Chapter 3
Biogeographic Processes Influencing
Antarctic and sub-Antarctic Seaweeds
Ceridwen I. Fraser, Adele Morrison, and Pamela Olmedo Rojas
Abstract Antarctica has long been seen as biologically isolated, surrounded by the
vast Southern Ocean and its circumpolar oceanographic currents and fronts and
home to many endemic species. New evidence demonstrates, however, that buoyant
seaweeds can cross perceived oceanographic barriers in the Southern Ocean to
reach Antarctic coasts. These macroalgal rafts can carry diverse passengers, includ-
ing marine invertebrates and other, non-buoyant seaweeds. The stark differences
between Antarctic and sub-Antarctic near-coastal ecosystems are therefore more
probably the result of environmental differences than physical isolation. Modelling
indicates that algal rafts from the sub-Antarctic could reach Antarctic coasts every
month, providing an ongoing influx of marine propagules that are poised to colonise
as the climate warms. In this chapter, we review the following: (i) the evidence for
the isolation of Antarctica, (ii) the oceanographic processes that can hinder or pro-
mote passive dispersal into Antarctic waters and (iii) the characteristics of organ-
isms that could be rafting to Antarctic coasts with buoyant macroalgae.
Keywords Antarctic circumpolar current · Connectivity · Dispersal · Polar front ·

Stokes drift
C. I. Fraser (*) · P. Olmedo Rojas

Department of Marine Science, University of Otago, Dunedin, New Zealand
A. Morrison
Research School of Earth Sciences, and ARC Centre of Excellence
for Climate Extremes, Australian National University, Acton, ACT, Australia
e-mail: adele.morrison@anu.edu.au

https://doi.org/10.1007/978-3-030-39448-6_3
44 C. I. Fraser et al.
3.1 Antarctica’s Place in the World: An Isolated Continent?
Antarctica has long been seen as biologically isolated from the rest of the world
(Clarke et al. 2005; Fraser et al. 2012; Convey et al. 2014; Chown et al. 2015). The
opening of the Drake Passage between South America and Antarctica, around
41 million years ago (Scher and Martin 2006), and the subsequent onset of the
Antarctic Circumpolar Current (AAC), around 30 Ma (Scher et al. 2015), geo-
graphically isolated Antarctica. Along with declines in atmospheric CO2 in the
Cenozoic, the onset of the ACC enhanced cooling and glaciation of the Antarctic
(DeConto and Pollard 2003), resulting in marked reductions in diversity in some
marine groups (Clarke 1990). The ACC is the world’s largest ocean current, about
23,000 km long and up to 2000 km wide in some areas (Constantin and Johnson
2016); connects the Indian, Pacific and Atlantic Oceans; and extends up to 4–5-km
depth (Marynets 2019). There are several well-recognised circumpolar thermal
fronts in the Southern Ocean, including the Subantarctic Front and the Antarctic
Polar Front (see next section). These oceanic features, encircling Antarctica,
enhance the stark environmental differences between Antarctic and more northern
(sub-Antarctic or temperate) ecosystems. Biologically, the Southern Ocean with
its strong, eastward-flowing ACC and circumpolar fronts represents a major hur-
dle for some organisms to cross (Patarnello et al. 1996; Fraser et al. 2012;
Gonzalez-Wevar et al. 2012), particularly for passive dispersers. The observed
high-level endemism in the Southern Ocean marine biota (Barnes et al. 2006) and
the relatively low diversity and high endemism of terrestrial organisms in
Antarctica have largely been considered to result from long periods of evolution in
isolation (Fraser et al. 2012). However, we are increasingly recognising that the
Southern Ocean is not an impermeable biological barrier; dispersal events into the
Antarctic do occur (Clarke et al. 2005; Barnes et al. 2006) and at higher frequen-
cies than previously thought (Fraser et al. 2017; Fraser et al. 2018b). The distinc-
tive Antarctic biota is thus probably a result of adaptation to extreme environmental
conditions, rather than an inability of passively dispersing organisms to reach
the region.
3.1.1 A
daptations of Terrestrial Organisms to Antarctic
Conditions
Only around 0.2–0.3% of Antarctic land is currently ice-free (Convey and Stevens
2007; Burton-Johnson et al. 2016). Antarctic terrestrial organisms, restricted to
this ice-free land, have apparently persisted in Antarctica for millions of years
and have adapted to the extreme conditions including low temperatures, low win-
ter photoperiod and scarce food supply (Convey and Stevens 2007). Antarctic
terrestrial biodiversity is restricted mainly to microinvertebrates, bryophytes and
lichens; only two vascular plants occur, both restricted to the maritime Antarctica
3 Biogeographic Processes Influencing Antarctic and sub-Antarctic Seaweeds 45
(Ochyra et al. 2008). Lichens and mosses are the dominant flora of Antarctica –
there are ca 386 and 111 species of lichens and mosses identified, respectively
(Øvstedal and Lewis Smith 2001; Ochyra et al. 2008). Lichens have been
described as the organisms best adapted to Antarctic conditions (Ochyra et al.
2008) and have been reported to be photosynthetically active under suboptimal
temperatures (Kappen 2000). Antarctic mosses have also shown remarkable
physiological adaptations to both water availability and solar radiation. For
example, mosses can survive under long periods of both desiccation and submer-
gence (Wasley et al. 2006), including being frozen by glaciers for hundreds
(Cannone et al. 2017) and even thousands (Roads et al. 2014) of years, despite
water availability having been shown to be a key factor underpinning the abun-
dance and distribution of Antarctic terrestrial organisms (Kennedy 1993; Convey
and Stevens 2007; Robinson et al. 2018). The Antarctic terrestrial fauna is domi-
nated by microarthropods, such as springtails and mites (Convey and Stevens
2007). Glycerol in cell membranes might help arthropods inhabiting polar condi-
tions to survive freezing temperatures (Teets and Denlinger 2014). Additionally,
the small size of terrestrial organisms could assist with minimising moisture loss
in windy environments and maximising the use of limited nutrients (Kappen
et al. 1995).
3.1.2 A
daptations of Marine Organisms to Antarctic
Conditions
The contemporary marine biota of Antarctica has been strongly shaped by glacial
cycles (Allcock and Strugnell 2012; Fraser et al. 2012) and mainly comprises fish,
macroalgae and filter feeders such as sponges, small crustaceans, molluscs and
anemones (Clayton 1994; Griffiths 2010). Some taxa such as decapods, sharks and
skates are poorly represented in Antarctica (Aronson and Blake 2015). Up to 90%
of the Antarctic fishes and marine invertebrates (Barnes et al. 2006) and 35% of
macroalgae (Clayton 1994; Gómez 2015) are endemic to the region. Whereas some
Antarctic algal species are also present in nearby northern areas (such as Adenocystis
utricularis, Gigartina skottsbergii, Monostroma hariotii or Iridaea cordata, which
are found in both Antarctica and South America: Gómez 2015), others are unique
to the region but are closely related to taxa elsewhere. Sunlight is highly limited in
the Antarctic marine environment, but Antarctic macroalgae can survive at low
temperatures, photosynthesise under very low light conditions and can store
organic compounds to use in dark periods (Wiencke et al. 2007). Other marine spe-
cies also show adaptations to their extreme environment. Antarctic notothenioid
fish have developed antifreeze glycoproteins, which lower the internal freezing
point of most of their fluids, preventing freezing in sub-zero Antarctic waters
(DeVries 1988).
3.1.3 Evidence for Dispersal of Organisms into the Antarctic
Transoceanic dispersal mainly occurs either by active dispersal (e.g. swimming and
flying) or through passive dispersal such as through transport with ocean or wind
currents, or ‘hitch-hiking’ with larger animals, driftwood or seaweed (Muñoz et al.
2004; Gillespie et al. 2012; Moon et al. 2017). Some microbes appear to have
reached Antarctica via aerial dispersal with wind (Vincent 2000), and small arthro-
pods also appear capable of dispersing with wind (Hawes et al. 2007), although
long-distance dispersal of arthropods across the Southern Ocean via this mechanism
seems unlikely (Pugh 2003). Recently, Fraser et al. (2018b) reported that southern
bull kelp, Durvillaea antarctica, which grows in the sub-Antarctic but not in the
Antarctic, had travelled south across the Southern Ocean. These were the longest
biological rafting events ever recorded, >20,000 km, and were apparently driven by
strong winds and storms that pushed the kelp across Southern Ocean fronts (see
below). Similarly, in the last couple of decades, king crabs (Neolithodes yaldwyni)
have been found on the Antarctic continental shelf (Smith et al. 2012) and might
represent invasions from deeper water, although there has been some debate as to
whether the crabs are new immigrants (Thatje et al. 2005) or have been long-term
residents of the Antarctic and have simply gone undetected (Griffiths et al. 2013).
With global warming, many organisms are migrating poleward (Hickling et al.
2006; Chen et al. 2011; Fraser et al. 2012). Invasive (anthropogenically transported)
and naturally dispersing non-native species represent a major threat to Antarctic
biota (Frenot et al. 2005; Chown et al. 2012; Chown et al. 2015; Duffy et al. 2017).
Understanding how permeable the Southern Ocean ‘barrier’ is to dispersal of differ-
ent sorts of organisms will help us to understand how Antarctic biodiversity might
be affected by future colonisations (Fraser et al. 2017; Wauchope et al. 2019).
3.2 P
hysical Oceanographic Processes Influencing
Movement of Seaweeds into or out of the Antarctic
There has been a long-held perception that the fronts of the ACC act as oceano-
graphic barriers preventing movement of passively dispersing marine biota south-
ward into Antarctic waters (Hunt et al. 2016). Fronts are sharp transitions in
temperature, salinity and biogeochemical properties and align with the narrow, east-
ward currents of the ACC. Traditionally, three primary fronts have been identified in
the Southern Ocean – the Subantarctic Front, the Polar Front and the Southern
Antarctic Circumpolar Current Front (Orsi et al. 1995). Traversing southward
towards Antarctica, a front appears as a near step change from warmer, saltier waters
in the north to colder, fresher waters on the southern side. The separation of warm
and cold waters across the ACC fronts has cultivated the conceptual picture that
there is very little mixing or transport across the fronts. However, this is an overly
simplistic view of circulation in the Southern Ocean. Recent analysis of higher-
resolution observations shows that the ACC has a more complicated structure with
numerous fronts that merge and split around Antarctica (Sokolov and Rintoul 2009).
Mesoscale variability is also rich in the Southern Ocean, and eddies and jets that
meander in time can move objects away from the direction of the main currents
(Lehahn et al. 2011). An additional process that has recently been recognised as
extremely important for dispersal of floating surface material is non-linear a dvection
by surface waves, known as Stokes drift (Fraser et al. 2018b; Dobler et al. 2019).
Below we expand upon the most important processes influencing movement of sea-
weeds in the Southern Ocean: the mean northward drift of Ekman transport, tran-
sient north and south movement by eddies and storm-driven Stokes drift, in addition
to the predominantly zonal movement by the large-scale horizontal ocean currents.
3.2.1 Ekman Transport
The westerly winds over the Southern Ocean, also known as the ‘Roaring Forties’,
are the strongest average winds on the planet, with annual average speeds up to
10 m s−1 (Lin et al. 2018). The winds blow from west to east over a wide latitude
band covering approximately 30–65°S. Due to the Coriolis effect, which deflects
motion to the left in the Southern Hemisphere, the eastward wind stress on the
ocean drives a northward surface movement referred to as Ekman transport. Ekman
transport in the Southern Ocean extends to a depth of around 100 m and is surface
intensified. Observed northward speeds are up to ~2 cm s-1 at the surface (Lenn and
Chereskin 2009), which in isolation would result in floating objects moving more
than 600 km, or 6° of latitude northward in 1 year. Although the Southern Ocean
fronts provide a visible separation between the sub-Antarctic islands and Antarctica,
it is the constant northward drift of Ekman transport that represents the biggest
obstacle to southward movement of floating seaweeds.
3.2.2 Eddies
The Southern Ocean fronts are dynamically unstable, forming ubiquitous mesoscale
eddies and transient meanders in the ACC jets (Thompson Andrew 2008). Drifting
objects can be trapped inside coherent ring-like eddies and transported over long
distances away from the large-scale ocean currents (Lehahn et al. 2011). In the
Southern Ocean, eddies are ~10–100 km across and commonly last for longer than
4 months, over which time they can travel north or south by 5° or more of latitude
(Chelton et al. 2011). A drifting object would be unlikely to remain trapped for the
entire lifetime of an eddy, as eddies ‘leak’ as they stretch and interact with other
ocean circulation features (d’Ovidio et al. 2013). However, seaweeds may encoun-
ter a series of eddies over time, resulting in a net northward or southward transport.
Fraser et al. (2018b) showed that the inclusion of mesoscale variability was essen-
tial for modelled virtual particles to drift sufficiently southward to reach Antarctica.
3.2.3 Wave-Driven Stokes Drift
High wind speeds associated with atmospheric storms over the Southern Ocean
generate an intense wave climate and make it consistently the roughest ocean on
earth (Young 1999). The non-linear nature of surface ocean waves results in a net
advection of floating objects in the direction of the waves, known as Stokes drift.
While the average direction of waves in the Southern Ocean is eastward, the same
as the average wind direction, atmospheric storms result in large variability of the
wind direction and associated wave direction. Seaweeds can be transported south-
wards across fronts by large, individual storm events, during which the Stokes drift
is frequently as large as 0.3 m s−1 (Rascle and Ardhuin 2013). Fraser et al. (2018b)
showed that the influence of wave-driven Stokes drift is necessary for floating
objects to drift sufficiently southward to reach Antarctica (Fig. 3.1).
3.2.4 Surface Currents
The large-scale horizontal circulation in the open Southern Ocean is predominantly

eastward and therefore cannot in isolation drive floating objects southward.
Nonetheless, the ocean circulation is important to consider, as it largely determines
the locations where seaweeds approach Antarctica. While eddy processes and
Fig. 3.1 Simulated drift particle trajectories from South Georgia, as described in Fraser et al.
(2018a, b). More than 4.2 million virtual particles were released from South Georgia (red dot) and
advected for 3 years with simulated surface ocean velocities where (a) eddies, but not Stokes drift,
were included; (b) Stokes drift, but not eddies, was included; and (c) both Stokes drift and eddies
were included. Blue lines show trajectories for all particles located on the Antarctic shelf after
3 years. Brown lines show trajectories for a random sample (0.1%) of particles not satisfying this
condition. Black lines show positions of major fronts. Red arrows show the four major pathways
of approach to Antarctica, two aligned with southward deviations of the ACC and two associated
with the southward movement of the Weddell and Ross Gyres
Stokes drift are responsible for moving floating objects southward across the ACC
fronts, the large-scale meanders of the ACC and the subpolar gyres set the most
likely pathways of approach to Antarctica (Fraser et al. 2018b).
The eastward ACC dominates the ocean circulation in the Southern Ocean. The
ACC plays an important role in dispersing species zonally around the Southern
Ocean (Waters 2008) and in rapidly moving drifting objects to longitudes where
shorter routes to Antarctica are possible. The circumpolar path of the ACC is steered
by the underlying bathymetry and continental gateways. There are two close
approaches of the ACC to the Antarctic continental slope – along the West Antarctic
Peninsula and offshore from Wilkes Land in East Antarctica. In the recent Lagrangian
study of Fraser et al. (2018b), these two locations were preferred routes for south-
ward drifting particles to first make contact with the continent.
Two additional locations with high influx of floating objects to the Antarctic
coast are associated with the subpolar gyres (Fraser et al. 2018b). The Weddell and
Ross Gyres are clockwise circulation features between Antarctica and the ACC,
driven by Ekman divergence at the intersection of the westerly winds to the north
and easterly winds to the south. At the eastern edge of the Weddell and Ross Gyres
(~50°E and ~120°W, respectively), the flow is southward towards Antarctica. If
seaweeds are driven sufficiently southward across the ACC fronts through a combi-
nation of eddy and wave-driven processes (Fig. 3.2), the subpolar gyres can connect
dispersal pathways from the southern edge of the ACC to the Antarctic coast. Once
seaweeds reach the coast of Antarctica, circumpolar connectivity around the coast-
line is enabled by the westward Antarctic Coastal and Antarctic Slope Currents.
Fig. 3.2 Illustration of eddies and Stokes drift in the Southern Ocean. White lines show long-term
average fronts in the Southern Ocean. Purple colours show a snapshot of surface ocean current
speed, and green arrows show a snapshot of the additional surface velocity from wave-driven
Stokes drift. (All data are from sources listed in Fraser et al. 2018b)
3.3 H
itch-Hiking to the Antarctic: Passengers on Seaweed
Rafts
Buoyant macroalgae have long been recognised as potential vectors for the trans-
port of diverse other taxa (Thiel and Gutow 2005), including invertebrates (e.g.
Helmuth et al. 1994; Miranda and Thiel 2008; Nikula et al. 2010) and non-buoyant
seaweeds (e.g. Edgar 1987; Fraser et al. 2013; López et al. 2018). Indeed, entire
coastal communities can potentially travel long distances at sea via rafting with
seaweeds (Fraser et al. 2011). With new evidence that buoyant macroalgae can tra-
verse perceived oceanic ‘barriers’ and reach the Antarctic coast (Fraser et al. 2018b),
rafting events have the potential to enable diverse non-native species to reach
Antarctica. Currently, these taxa seem unable to establish, perhaps because the fre-
quent ice scour of rocky shores in Antarctica precludes establishment of the large
kelps these species require for habitat and food (Fraser et al. 2009; Fraser et al.
2018b). Antarctic coastal waters are warming, however, and some parts of the
Antarctic Peninsula could be comparable to present-day sub-Antarctic environ-
ments by the end of the century (Griffiths et al. 2017), facilitating establishment of
non-native species brought by kelp rafts.
3.3.1 Characteristics of Rafting Species
Shortly after detachment, there is a decline in the number of invertebrates associated

with kelp holdfasts (Edgar 1987; Hobday 2000; Gutow et al. 2009) – many indi-
viduals ‘jump ship’, including those that are commonly found on rafts at sea and are
apparently well suited to rafting (Miranda and Thiel 2008; Gutow et al. 2009).
There may be bet-hedging benefits for those species that have individuals that either
leave the detached kelp or remain, with departing individuals enhancing their
chances of remaining in suitable kelp habitats, and remaining individuals enhancing
their chances of colonising new territory (Gutow et al. 2009). Some species also
colonise already detached, drift macroalgae, enhancing raft diversity after the initial
decline (Edgar 1987).
Many marine invertebrates have pelagic larvae that can disperse only over rela-
tively short distances (hundreds to thousands of metres: Kinlan and Gaines 2003),
so a key benefit of dispersing with macroalgal rafts is the capacity to disperse longer
distances. Rafts can endure for hundreds of days, travelling up to tens of thousands
of kilometres (Fraser et al. 2011, 2018b), and macroalgal rafts provide both habitat
and food to many of their passengers (Thiel 2003a). Taxa that are long-lived, or that
brood offspring, are thus most likely to be able to take advantage of dispersal via
long-distance rafting journeys – direct-developing organisms have been noted to
make up an increasing proportion of the rafting community the longer a raft is at sea
(Thiel 2003a). Examples of such taxa include peracarid crustaceans (amphipods,
isopods and tanaids) and pulmonate gastropods (Thiel and Gutow 2005). In some
Fig. 3.3 Peracarid crustaceans including isopods and amphipods can brood their young within
kelp holdfasts, and are well suited to survive long rafting journeys. (a) The boring isopod Limnoria
stephenseni, (b) the amphipod Parawaldeckia kidderi, (c) a group of Parawaldeckia amphipods in
a tunnel in a dissected holdfast of Durvillaea antarctica bull kelp, (d) beached Durvillaea antarc-
tica bull kelp raft, with holdfast. (Photos by Ceridwen Fraser)
cases, these bore into kelp holdfasts, creating tunnels in which they are largely pro-
tected from exposure to harsh conditions in the open ocean and in which they can
nurture subsequent generations (e.g. the isopod genus Limnoria: Thiel 2003b)
(Fig. 3.3). Some other taxa that have been found associated with macroalgal rafts
that have dispersed long distances in the Southern Hemisphere include chitons, lim-
pets, bivalves, echinoderms and pycnogonids (Fraser et al. 2011), highlighting the
potential for macroalgal rafts to carry diverse new taxa to the Antarctic.
3.3.2 P
rocesses Affecting Establishment of New Taxa
in the Antarctic
Simulated dispersal of surface particles (e.g. buoyant macroalgal rafts) from sub-
Antarctic locations suggests that the vast majority are driven eastward and eventu-
ally northward, away from Antarctica. The proportions of particles able to reach the
Antarctic coast in simulations were relatively small – from 0.0001% to 0.1915%
(Fraser et al. 2018b). Estimates based on empirical surveys of kelp at sea suggest,
however, that there are tens of millions of macroalgal rafts adrift in the Southern
Ocean at any time; for Durvillaea antarctica, for example, there are estimated to be
about 70 million detached individuals at sea, with around 20 million of those still
bearing intact holdfasts (Smith 2002). If such estimates are correct and assuming
most rafts complete their journeys within 3 years (Fraser et al. 2018b), there could
be between a few and several thousand sub-Antarctic-origin D. antarctica rafts
reaching the Antarctic coast each month. For example, for releases from South
Georgia, approximately 0.19% of simulated particles reached the Antarctic coast
within 3 years (Fraser et al. 2018b), and this proportion of 70 million, over a period
of 36 months, amounts to close to 4000 per month, on average. Indeed, the finding
of D. antarctica on Antarctic beaches in 2017 (Fraser et al. 2018b) was not a one-off
event; D. antarctica samples had been collected from Antarctic waters previously,
but their significance was not immediately recognised. In 1989, for example, a spec-
imen was collected from Arthur Harbour at Anvers Island off the Antarctic Peninsula
(Herbarium of the University of California Berkeley, accession UC157330). Despite
this evidence for long-term, persistent transport of marine propagules from the sub-
Antarctic to Antarctica, the large kelps that dominate the sub-Antarctic near-shore
ecosystems (such as D. antarctica and Macrocystis pyrifera) and many of the inver-
tebrates associated with them have not yet been established in Antarctica.
There could be a range of factors that influence the chance of establishment of
these large macroalgae and their associated epifauna in Antarctica. The most obvi-
ous of these is ice scour – neither D. antarctica nor M. pyrifera currently occurs in
areas heavily affected by iceberg scour or sea ice (Fraser et al. 2009; Macaya and
Zuccarello 2010; Fraser 2012). Most Antarctic coasts are likely to be affected by ice
scour long into the future, but warming near the Antarctic Peninsula over coming
decades could make shallow marine environments in that region somewhat compa-
rable to contemporary sub-Antarctic environments by the end of this century
(Griffiths et al. 2017). If areas along the Peninsula, for example, bays and channels,
are partly protected from ice scour in this warmer environment, some large sub-
Antarctic macroalgae – and, subsequently, their associated epibionts – might have
an opportunity to establish.
Another consideration is the viability of dispersing seaweeds and other taxa on
reaching Antarctica. The viability of kelp rafts reaching Antarctica has yet to be
tested, but the two D. antarctica specimens found at King George Island in 2017
(Fraser et al. 2018b) were both male and had mature antheridia that appeared likely
to be viable. Furthermore, prior research indicates that the duration of survival and
viability of rafting macroalgae is greater in cooler, high-latitude waters versus
warmer, lower-latitude waters (Rothäusler et al. 2009). Establishment of dispersing
macroalgae can also be influenced by the presence or absence of competing conspe-
cific (Waters et al. 2013; Fraser et al. 2018a) or heterospecific (Valentine and
Johnson 2004) seaweeds. For Antarctic intertidal ecosystems, however, such com-
petition seems unlikely to play a major role in preventing the establishment of sub-
Antarctic-origin macroalgae, as Antarctic rocky shores generally are not densely
blanketed in algal cover (Fig. 3.4). Nonetheless, should ice scour become less
frequent in some areas, competitive processes could influence which macroalgae
can establish and survive on exposed rocky shores.
Fig. 3.4 Antarctic rocky shores are starkly different to sub-Antarctic shores. In the former, fre-
quent ice scour removes all but the hardiest organisms, and seaweeds tend to be small and/or have
biphasic life cycles. In the sub-Antarctic, large brown macroalgae create habitat for diverse other
taxa including invertebrates and other seaweeds. (a, b) show sub-Antarctic shores dominated by
Durvillaea antarctica bull kelp; (c, d) show Antarctic shores lacking large seaweeds; (e, f) show
small, hardy seaweeds that can occur in both the sub-Antarctic and Antarctic: Adenocystis utricu-
laris (e) and Bostrychia intricata (f). White scale bars represent approximately 20 cm. (Photos A,
B, E and F by Ceridwen Fraser, sub-Antarctic Marion Island and New Zealand; C by Carlos
Olavarria; D by Emma Newcombe, South Shetland Islands, Antarctica) (Figure modified from
Fraser et al. 2012).
3.4 Concluding Remarks
Antarctica has long been considered biologically isolated, but we now recognise
that the Southern Ocean and its fronts are not impermeable barriers to southward
dispersal of drifting objects. While there are no direct large-scale ocean currents
crossing the fronts, there are a number of both oceanic and directly wind-driven
processes that can move floating objects such as buoyant seaweed rafts north or
south across the fronts. Fraser et al. (2018b) showed that the combination of both
transient mesoscale variability and wave-driven Stokes drift is necessary for such
frontal traverses. Once floating objects have crossed to the southern edge of the
ACC, the large-scale horizontal ocean currents determine the locations of final
approach to Antarctica. Of the four primary regions where objects approach the
Antarctic coast (Fig 3.1), the region considered most feasible for future establish-
ment of sub-Antarctic macroalgae is the Antarctic Peninsula and nearby islands,
where warming is forecast to be most rapid. Should such establishment occur, there
could be drastic changes to Antarctic near-shore marine ecosystems, as drift mac-
roalgae can transport diverse other taxa including invertebrates and other seaweeds.
Acknowledgements We thank Richard Moe for alerting us to the existence of the D. antarctica
specimen from Antarctica in the UC Berkeley herbarium and Erasmo Macaya for discussions. CIF
was funded by a Rutherford Discovery Fellowship from the Royal Society of New Zealand (RDF-
UOO1803), AKM was supported by an Australian Research Council DECRA Fellowship
(DE170100184), and POR was supported by a Strategic Doctoral Scholarship from the Division of
Sciences at the University of Otago.
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Chapter 4
Detached Seaweeds as Important Dispersal
Agents Across the Southern Ocean
Erasmo C. Macaya, Fadia Tala, Iván A. Hinojosa, and Eva Rothäusler
Abstract After detachment from their substratum, many seaweeds can float or drift
at the mercy of currents and winds, thereby facilitating their dispersal and connec-
tivity. In Antarctica only one species possess floating structures (gas-filled vesicles),
the brown seaweed Cystosphaera jacquinotti. However, other species such as
Durvillaea antarctica and Macrocystis pyrifera that form abundant forests around
the sub-Antarctic islands can also remain at the sea surface once detached, provid-
ing a potential dispersal mechanism not only for the seaweeds but also for the asso-
ciated biota. Additionally, recent reports indicate that floating D. antarctica can
reach the Antarctic continent from sub-Antarctic regions. Herein, we collect
E. C. Macaya (*)
Laboratorio de Estudios Algales (ALGALAB), Departamento de Oceanografía, Universidad
de Concepción, Concepción, Chile
Millennium Nucleus Ecology and Sustainable Management of Oceanic Island (ESMOI),
Coquimbo, Chile
Research Center Dynamics of High Latitude Marine Ecosystems (IDEAL), Valdivia, Chile
e-mail: emacaya@oceanografia.udec.cl
F. Tala
Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del
Norte, Coquimbo, Chile
Centro de Investigación y Desarrollo Tecnológico en Algas, Facultad de Ciencias del Mar,
Universidad Católica del Norte (CIDTA-UCN), Coquimbo, Chile
e-mail: ftala@ucn.cl
I. A. Hinojosa
Millennium Nucleus Ecology and Sustainable Management of Oceanic Island (ESMOI),
Coquimbo, Chile
Departamento de Ecología, Facultad de Ciencias y Centro de Investigación en Biodiversidad
y Ambientes sustentables (CIBAS), Universidad Católica de la Santísima Concepción,
Concepción, Chile
e-mail: ihinojosa@ucsc.cl
E. Rothäusler
Centro de Investigaciones Costeras - Universidad de Atacama (CIC - UDA), Avenida
Copayapu 485, Copiapó, Chile
e-mail: eva.rothausler@uda.cl

https://doi.org/10.1007/978-3-030-39448-6_4
60 E. C. Macaya et al.
information about floating and drifting seaweeds in Antarctica, but also their biol-
ogy, physiology, and distribution within the sub-Antarctic sources. Up to now, only
a few species have been recorded floating in Antarctica, and mainly during the first
Antartic explorations. So far, most of the studies on detached seaweeds only high-
light their importance, when already stranded and serving as carbon sources for
benthic communities. However, some seaweed species are able to handle pres-
ent sea surface conditions in Antarctica and thus in the future when higher tempera-
tures, less ice and more available substrate are available, they might be able to
frequently travel and colonize this region, thereby representing an important disper-
sal mode.
Keywords Floating seaweed · Connectivity · Drifting · Rafting · Stranding

The two most striking vegetable productions of this island are a noble seaweed, called
Sargassum jacquinotii, and a Lichen. The first of these was not found attached, but floating
in the ocean among the ice, by which it was sometimes much mutilated. Though belonging
to a highly variable order, it is a perfectly distinct as well as conspicuous species. (James
Clark Ross 1847)
4.1 Introduction
The description above by the British Royal Navy Officer Sir James Ross onboard of
the HMS Erebus during the Antarctic exploration (January 1843) it is one of the first
records of floating seaweeds in Antarctica. In his report, Ross also mention the sur-
geon of the HMS Chanticleer, William Webster, who was the first naturalist in col-
lecting and describing such species at Deception Island: “the most common seaweed
was found floating. It was of a pale chocolate colour, stem and branches flat, quar-
ter of an inch in breadth, leaves equitant, thin, delicate, four of five inches long, and
at the base of each was a spherical air-cell the size of a grape. The mode of repro-
duction appeared to be from a cluster of buds appended to the terminal branches”
Webster (1834).
The seaweed observed by Webster and Ross is known today as Cystosphaera
jacquinotti and is endemic to the Antarctic. This brown seaweed species possesses
“pneumatocysts” (the size of a grape, according to Webster’s description) which are
floating structures and allow the seaweed to remain at the surface once being detached
from their primary substratum (Fig. 4.1). Although there are abundant records of
floating seaweeds around the world (e.g. Thiel and Gutow 2005a; Rothäusler et al.
2012; Macaya et al. 2016 and references therein), polar regions appear poorly rep-
resented. This may be due to the harsh environmental conditions onboard of a
research vessel, the limited accessibility to many regions, and the isolation of
Antarctica from the rest of the Southern Ocean. That is probably why most of the
information comes from microalgal aggregates (Cefarelli et al. 2011; Assmy et al.
4 Detached Seaweeds as Important Dispersal Agents Across the Southern Ocean 61
Fig. 4.1 The endemic Cystosphaera jacquinotti, black arrows indicate the gas filled structures
“pneumatocysts”. Right, a floating raft observed in Fildes Bay, King George Island. (Photos by
Erasmo C. Macaya)
2013; Katlein et al. 2015; Belt et al. 2018). As a result, few records of floating sea-
weeds have been reported in Antarctica, indicating only their importance as drifting
and stranding seaweeds, because they can serve as a carbon source for benthic com-
munities (e.g. Fischer and Wiencke 1992; Norkko et al. 2004; Braeckman et al.
2019; see also Chap. 8 by Quartino et al.). However recent records of non-native
positively buoyant kelps (Durvillaea antarctica and Macrocystis pyrifera) that
stranded on South Shetland Islands opened the discussion regarding the isolation of
Antarctica (Fraser et al. 2018; Avila et al. 2020). This is especially important in the
context of future warming scenarios, where long-distance dispersal might facilitate
connectivity with sub-Antarctic seaweed sources. In fact, long-distance dispersal
and connectivity within these vast areas of open oceans have been already demon-
strated for D. antarctica and Macrocystis pyrifera, with single haplotypes having a
wide sub-Antarctic distribution (Fraser et al. 2009; Macaya and Zuccarello 2010).
At the same time, these seaweeds serve as important dispersal vehicles for associ-
ated flora and fauna (Nikula et al. 2010; Wichmann et al. 2012; Nikula et al. 2013;
Cumming et al. 2014; Macaya et al. 2016), considering the large number of floating
D. antarctica rafts in the Southern Ocean (Smith 2002) (see also Chap. 3 by Fraser
et al.). In this chapter we give information about floating, drifting and stranded sea-
weeds in Antarctica in relation to their abundance and distribution. We also address
whether the extreme environmental conditions (irradiance and temperature) can
affect seaweed physiology, growth and thus survival mainly in floating conditions.
In addition, we give potential sources of seaweeds that may have the chance to
travel into Antarctica.
4.2 Detached Seaweeds in Antarctica
A total of 39 seaweeds species, including 3 Chlorophyta, 14 Ochrophyta, and 22

Rhodophyta–have been recorded drifting, stranding or floating in Antarctica or
crossing the Antarctic Polar Front APF (Table 4.1). From the 95 records included
herein, 75% reported about observations or studies of drifting seaweeds, followed
by a 17% of floating seaweeds, while only an 8% reported about stranded seaweeds.
To our knowledge, so far only brown but no red or green seaweed species have been
found floating in Antarctica. The brown seaweeds species include Cystosphaera
jacquinotti, Himantothallus grandifolius, Desmarestia anceps and Adenocystis
utricularis. Among them, only C. jacquinotti possesses floating structures and is
also the most frequent species observed. For instance, abundant seaweed pieces
were recorded floating during 1908–1909 in the Neumayer and Peltier Channels as
well as in the Bransfield and Gerlache Straits (Gain 1912). Fertile floating individu-
als were observed in Harmony Cove (Neushul 1963) and pieces up to 90 cm in
length were spotted among ice in Cockburn Island (Ross 1847). In contrast, A. utric-
ularis owes buoyancy when mature thalli become filled with air and individuals
have been found floating abundantly within the Fildes Bay (E. Macaya pers. obs).
Floating thalli but also holdfasts of H. grandifolius were observed within Admiralty
Bay (Zemko et al. 2015). Large numbers of floating kelps such as Macrocystis pyr-
ifera and Durvillaea antarctica were found floating south of the APF (Fraser et al.
2017) and floating D. antarctica pieces were recorded in the interior pass of
Deception Island (Gain 1912). Several records of floating seaweed were also carried
out by James Cook during his voyage towards the South Pole during 1770’s, he
described floating seaweeds at latitude 70°S, longitude 108°W: “We continued our
course to the south, and passed a piece of weed covered with barnacles, which a
brown albatross was picking off”. Those rafts might have been afloat for a while,
because of the barnacle presence (Thiel and Gutow 2005a).
Among the drifting red seaweeds, most of the species belong to the order
Ceramiales and Gigartinales, with seven and five species recorded, respectively.
Attached to the spines of the sea urchins Sterechnus neumayeri (Amsler et al. 1999;
Schwarz et al. 2003) or accumulated in hollows, a bundant biomass of drifting
Phyllophora antarctica were observed at 15–30 m depth in Cape Evans, McMurdo
Sound (Norkko et al. 2004). Interestingly, S. neumayeri uses drift pieces of P. ant-
arctica and Iridaea cordata as defense against its main predator, the anemone
Isotealia antarctica. At the same time, this retention of drifting seaweed pieces indi-
rectly supports to maintain the seaweed populations, if pieces are fertile and still
within the photic zone (Amsler et al. 1999). The most common drifting brown sea-
weeds belong to the order Desmarestiales. For instance individuals of Desmarestia
Table 4.1 Detached seaweeds reported drifting, floating or stranded in Antarctica. Floating kelps
crossing the Antarctic Polar Front are also included
Algal-
Phylum/order Species status Locality Reference
Chlorophyta
Prasiolales Prasiola crispa Drift Fildes Bay, King (Fischer and Wiencke
George Island 1992)
Ulothricales Monostroma Drift Admiralty Bay, (Oliveira et al. 2009)
hariotii King George
Island
Fildes Bay, King (Fischer and Wiencke
George Island 1992)
Stranded Fildes Bay, King (Westermeier et al.
George Island 1992)
Ulvales Ulva intestinalis Drift Whalers Bay, (Clayton et al. 1997)
Deception Island
Ochrophyta
Ascoseirales Ascoseira mirabilis Drift Fildes Bay, King (Müller et al. 1990;
George Island Sato et al. 1992; Tada
et al. 1996)
Drift Admiralty Bay, (Zielinski 1990)
King George
Island
Chrysomeridales Antarctosaccion Drift South Bay, (Gallardo et al. 1999)
applanatum Livingston Island
Desmarestiales Desmarestia anceps Drift Fildes Bay, King (Fischer and Wiencke
George Island 1992; Tada et al.
1996)
DeLaca Island (Amsler et al. 2012)
Signy Island, (Richardson 1979;
South Orkney Brouwer et al. 1995)
Islands
Admiralty Bay, (Zielinski 1990)
King George
Island
Floating, Bransfield Strait; (Gain 1912)
stranded Deception Island;
King George
Island
Desmarestia Drift Deception Island (Lastra et al. 2014)
antarctica
George Island 1992)
Desmarestia Drift Deception Island (Lastra et al. 2014)
menziesii
Signy Island, (Brouwer 1996)
South Orkney
Islands
(continued)
Algal-
George Island 1992)
Admiralty Bay, (Zielinski 1990)
King George
Island
Desmarestia sp. Stranded Deception Island (Gain 1912)
Himantothallus Floating Admiralty Bay, (Zemko et al. 2015)
grandifolius King George
Island
Drift Admiralty Bay, (Zielinski 1981, 1990)
King George
Island
South Orkney
Islands
Ectocarpales Adenocystis Drift, Fildes Bay, King (Westermeier et al.
utricularis George Island 1992; Tada et al.
1996)
Floating Fildes Bay, King (Erasmo Macaya pers.
George Island obs.)
Chordaria linearis Drift Admiralty Bay, (Oliveira et al. 2009)
King George
Island
Petalonia fascia Drift Whalers Bay, (Clayton et al. 1997)
Deception Island
Scytosiphon Drift Whalers Bay, (Clayton et al. 1997)
lomentaria Deception Island
Utriculidium Fildes Bay, King (Müller et al. 1992)
durvillei George Island
Fucales Cystosphaera Floating Deception Island (Hooker 1844)
jacquinotii
Cockburn Island (Ross 1847)
Antarctic (Montagne 1842;
Peninsula Skottsberg 1907)
Half Moon Island (Neushul 1963)
Fildes Bay, King (Gain 1912; Macaya
George Island E. Personal
Observation; Weykam
et al. 1996)
Gerlache Strait (De Wildeman 1935)
South Bay, Macaya E. Personal
Doumer Island Observation
Drift Admiralty Bay, (Zielinski 1981, 1990;
King George Oliveira et al. 2009)
Island
(continued)
Algal-
Drift Ardley Bay, King (Fischer and Wiencke
George Island 1992)
Drift, Half Moon Island (Neushul 1965)
stranded
Durvillaea Floating, Deception Island, (Gain 1912)
antarctica stranded King George
Island
Stranded Livingtone Island (Avila et al. 2020)
Floating South of New (Hooker 1844)
Zealand 65°S
South of the (Fraser et al. 2017)
Antarctic Polar
Front
Drift Livingston and (Pellizzari et al. 2017)
Elephant Islands
Stranded Fildes Bay, King (Fraser et al. 2018)
George Island
Laminariales Macrocystis Floating South of the (Fraser et al. 2017)
pyrifera Antarctic Polar
Front
Stranded Deception Island (Avila et al. 2020)
Rhodophyta
Balliales Ballia callitricha Drift South Bay, (Gallardo et al. 1999)
Livingston Island
Bangiales Porphyra Drift Cuverville Island (Clayton et al. 1997)
plocamiestris
Bonnemaisoniales Delisea pulchra Drift Admiralty Bay, (Oliveira et al. 2009)
King George
Island
Ceramiales Georgiella Drift Fildes Bay, King (Fischer and Wiencke
confluens George Island 1992)
Myriogramme Drift Livingston Island (Gallardo et al. 1999)
manginii
Deception Island (Gain 1912)
South Orkney
Islands
Neuroglossum Drift Fildes Bay, King (Fischer and Wiencke
delesseriae George Island 1992)
Pantoneura Drift Signy Island, (Brouwer 1996)
plocamioides South Orkney
Islands
South Bay, (Gallardo et al. 1999)
Livingston Island
(continued)
Algal-
Paraglossum Drift Admiralty Bay, (Oliveira et al. 2009)
lancifolium King George
Island
Phycodrys Drift Fildes Bay, King (Fischer and Wiencke
antarctica George Island 1992)
Phycodrys Drift Fildes Bay, King (Weykam et al. 1996)
quercifolia George Island
Gigartinales Cystoclonium Drift Byers Peninsula, (Hommersand et al.
obtusangulum Livingston Island 2009)
Gigartina Drift Fildes Bay, King (Fischer and Wiencke
skottsbergii George Island 1992)
Admiralty Bay, (Oliveira et al. 2009)
King George
Island
Iridaea cordata Drift Cape Evans, (Schwarz et al. 2003)
McMurdo Sound
George Island 1992)
McMurdo Sound (Amsler et al. 1999)
King George
Island
Stranded Fildes Bay, King (Westermeier et al.
George Island 1992)
Notophycus Drift Admiralty Bay, (Oliveira et al. 2009)
fimbriatus King George
Island
Phyllophora Drift Cape Evans, (Miller and Pearse
antarctica McMurdo Sound, 1991; Schwarz et al.
Ross Island 2003; Norkko et al.
2004)
McMurdo Sound (Amsler et al. 1999)
Gracilariales Curdiea racovitzae Drift Fildes Bay, King (Fischer and Wiencke
George Island 1992)
Halymeniales Pachymenia Drift Admiralty Bay, (Oliveira et al. 2009)
orbicularis King George
Island
Palmariales Palmaria decipiens Drift Half Moon Island (Neushul 1965)
Foster Bay, (Lastra et al. 2014)
Deception Island
George Island 1992)
(continued)
Algal-
Drift, Admiralty Bay, (Zielinski 1981;
stranded King George Westermeier et al.
Island 1992; Oliveira et al.
2009)
Plocamiales Trematocarpus Drift Fildes Bay, King (Fischer and Wiencke
antarcticus George Island 1992)
Plocamium Drift Fildes Bay, King (Fischer and Wiencke
cartilagineum George Island 1992)
King George
Island
South Orkney
Islands
Plocamium hookeri Drift South Bay, (Gallardo et al. 1999)
Livingston Island
Rhodymeniales Hymenocladiopsis Drift South Bay, (Gallardo et al. 1999)
prolifera Livingston Island
anceps and D. menziesii were observed at 10 to 40 m depth in Admiralty

Bay, where icebergs provoked their detachment (Zielinski 1990). Huge drifting
patches of D. anceps with up to 60 m3 were recorded between 5 and 20 m depth in
Fildes Bay. These, detached individuals represent an important habitat for a variety
of invertebrates such as gastropods (Nacella concinna), giant isopods (Glyptonotus
antarcticus) and gammaridean amphipods (Tada et al. 1996) (Fig. 4.2).
Similarly, high quantities of drifting D. anceps detached by ice and wave action
accumulated in hollows at Signy Island, South Orkney (Brouwer 1996). When
detached this species continued to grow and remained healthy for over
44 weeks, without changing its palatability (Brouwer 1996; Amsler et al. 2012). To
date, only 3 species of drifting green seaweeds have been reported in Antarctica,
namely: Monostroma hariotti, Prasiola crispa and the non-native Ulva intestinalis
(Fischer and Wiencke 1992; Clayton et al. 1997; Oliveira et al. 2009). Large inflated
thalli of U. intestinalis were found drifting in Whalers Bay (Deception Island),
which is probably a recent introduction, caused by shipping activities (Clayton et al.
1997), also this species has been reported as a common fouling organism in other
latitudes (Blomster et al. 1998). However, introduction via floating dispersal cannot
be ruled out because U. intestinalis can form massive floating mats, that are known
to tolerate severe winter conditions (Bäck et al. 2000) together with a rapid acclima-
tion to changes in salinity, nutrients and light (Cohen and Fong 2004). Similarly,
free floating Ulva linza acclimated rapidly to changing light conditions by develop-
ing effective mechanisms to cope with excessive irradiation (Häder et al. 2001).
Detached seaweeds washed ashore (Fig. 4.3) have been studied at different sites
with in Antarctica. Lastra et al. (2014) estimated 1545 tons of seaweeds that arrived
Fig. 4.2 Drifting seaweeds accumulated in hollows, Fildes Bay, King George Island. (Photo by
Ignacio Garrido)
to the shore in Foster Bay (Deception Island) within the period from November to

July, and only 3% of the detached seaweeds accumulated as wrack along the inter-
tidal. In Admiralty Bay, 1643 tons of stranded seaweeds were estimated between
February and November 1979, and especially after storms (Rakusa-Suszczewski
1980; Zielinski 1981). Stranded seaweeds remnants decompose with contact to air,
and within 20 d, more than 50% were transformed to organic matter (Rakusa-
Suszczewski 1980), a process that becomes accelerated by winds and waves
(Zielinski 1981). The wrack deposition can be highly variable with more than 50%
of replacement at each tidal cycle (Lastra et al. 2014), probably caused by the inter-
action between wind direction and coastal orientation (Rakusa-Suszczewski 1980;
Zielinski 1981; Rakusa-Suszczewski 1995; Lastra et al. 2014). Slow decomposition
rates due to the extreme environment, however facilitates the longevity of detached
seaweeds and constitute an important carbon source for higher trophic levels via the
detrital food web (Fischer and Wiencke 1992; Schwarz et al. 2003; see also Chap 8
by Quartino et al.).
Fig. 4.3 Stranded seaweeds at Fildes Bay, King George Island. Low left, Desmarestia antarctica
as epiphyte of stranded Curdiea racovitzae. (Photos by Erasmo C. Macaya)
4.3 Abiotic Factors Influencing Floating Seaweeds
Solar radiation (280–700 nm) and sea surface temperature (SST) are the main abi-
otic factors that determine the persistence and thus dispersal ability of floating sea-
weeds (Hobday 2000; Rothäusler et al. 2009, 2012; Graiff et al. 2013; Tala et al.
2016, 2019). In Antarctica and sub-Antarctic islands, there is a strong seasonal light
regime, especially at latitudes >70°S, where several months of darkness in winter
and of complete daylight in summer with up to 1700 μmol m−2 s−1of PAR, 44 W m−2
of UV-A, and 2.3 W m−2 of UV-B can prevail (Quartino et al. 2005; Zacher et al.
2007, 2009; see also Chap 7 by Huovinen and Gómez). Also SST varies from
warmer sub-Antarctic waters (4 °C to 14 °C) to colder, icier Antarctic waters
(−1.8 °C and 2.2 °C off the Antarctic Peninsula) (Drew and Hastings 1992; Klöser
et al. 1993; Kang et al. 2002; Mélice et al. 2003). Thus, depending on the latitude or
season when detached, and/or when occasionally become pushed through the APF,
seaweeds are confronting extreme different conditions during rafting.
In situ experiments carried out with two tethered kelp species in Tierra del Fuego
at 54°S, showed for the temperate M. pyrifera that its growth capacity is favored by
high light levels (~1000 μmol m−2 s−1) and moderate SSTs (~10 °C) in summer but
the high growth rates cannot be maintained in low light (~700 μmol m−2 s−1) com-
bined with low SST (~6 °C) in winter (Tala et al. 2016). In contrast, the
sub-Antarctic D. antarctica showed a reverse pattern with positive growth in winter

despite the low light and temperature conditions. Apparently, the potential for raft-
ing dispersal in D. antarctica appears to be less dependent on seasonal variations in
environmental conditions (Tala et al. 2019). Clearly, sub-Antarctic floating sea-
weeds perform well in cooler waters and under low solar radiation than their tem-
perate counterparts (Rothäusler et al. 2009; Graiff et al. 2013; Tala et al. 2016, 2019).
Seaweeds that are distributed in sub-Antarctic islands and Tierra del Fuego such
as D. antarctica and M. pyrifera typically grow in environments with large fluctua-
tions in seawater temperature and have thus a broad performance breadth (Eggert
2012). Consequently, if floating conspecifics have the chance to become pushed
through the APF (Fraser et al. 2017; Fraser et al. 2018) they possibly can acclimate
to cold-water temperatures more easily and thereby contributing to long distance
dispersal (Fraser et al. 2018). However, M. pyrifera may fail to establish in the
colder, icier Antarctic environment because it was shown that they lost biomass at
54°S in winter probably due to low light availability (Tala et al. 2016). Hence, abi-
otic conditions in polar waters >60 °S might temporarily, especially in winter, be
unfavorable for some cold-temperate floating seaweeds. This might be the reason
why M. pyrifera (> 1 m) has been reported in coexistence with the endemic Antarctic
H. grandifolius under the extreme environmental conditions in South Georgia
(Barnes et al. 2006). At the same latitude (54°S), but at Tierra del Fuego, floating
D. antarctica did not show biomass losses in winter and steadily grew, which was
not the case in summer (Tala et al. 2016). As a result its floating time exceeded
200 d in winter but in summer it dropped to 90 d (Tala et al. 2019). This suggests
that D. antarctica may survive and be successful when entering into icier SSTs at
the APF. Indeed, two mature thalli of D. antarctica were found stranded at the
Antarctic Peninsula (62°S) in summer 2017 with goose barnacles attached (Fraser
et al. 2018). Molecular studies showed that these seaweed pieces originated from
sub-Antarctic Islands and therefore the dispersal distances represented the longest
rafting events ever recorded, with trajectories between 20,000 and 25,000 km
(Fraser et al. 2018). This suggests that these pieces started their journey as rafts
consisting of several individuals because it was estimated that they travelled a maxi-
mum of 2 years and a minimum of 489 d in order to reach Antarctica from their
origins (Fraser et al. 2018). During this very long pelagic journey, rafts experienced
substancial fluctuations in the abiotic and biotic environment, thereby probably los-
ing biomass.
It is known that nutrient abundance stimulates seaweed growth and thus it has
been inferred to affect the persistence time of floating seaweeds (Rothäusler et al.
2012 and references therein). When seaweeds become occasionally pushed through
the APF and float in the open waters of the Southern Ocean, which are defined as
high nutrient environments, their growth and thus survival is unlikely to be restricted.
The same is true when seaweeds arrive to the coastal waters of the Antarctic
Peninsula, where high levels of nitrate and phosphate are present at the sea surface
throughout the year (reviewed in Zacher et al. 2009). There is still, however, very
little information available on the impact of nutrients on floating seaweeds.
4.4 Biotic Factors Affecting Floating Seaweeds
Large numbers of hitchhiking organisms have been reported from floating seaweeds
(Khalaman and Berger 2006; Vandendriessche et al. 2007a; Wichmann et al.
2012; Abé et al. 2013; Macaya et al. 2016; López et al. 2018). Many of these organ-
isms are grazers e.g. amphipods and isopods that mostly feed on vegetative parts
from the rafts, thereby removing photosynthetic tissue, and thus contribute to their
demise (Vandendriessche et al. 2007b; Rothäusler et al. 2009; Rothäusler et al.
2018). But also grazing by e.g. snails and sea urchins and fouling by bryozoans,
goose barnacles, and epiphytic seaweeds can limit their persistence at the sea sur-
face (Rothäusler et al. 2011b; Graiff et al. 2016; Rothäusler et al. 2018; see also
Chap. 17 by Amsler et al. about algal-grazers interactions in Antarctic seaweeds).
Especially, the overgrowth with sessile organisms can reduce buoyancy, because
epibionts contribute to an increase in the specific gravity of the floating seaweed
(Graiff et al. 2016). These biotic interactions are particularly important for seaweed
rafts because they will directly affect the persistence (and dispersal potential) of
rafts at the sea surface.
The destructive effect of herbivorous grazers on their rafts is dependent on water
temperature (Vandendriessche et al. 2007a; Rothäusler et al. 2009, 2018). In meso-
cosms but also in field studies it was shown that low temperatures (5–15 °C) slowed
amphipod and isopod consumption on floating M. pyrifera, Fucus vesiculosus, and
Ascophyllum nodosum, and that these seaweeds can compensate for grazer induced
tissue losses (Vandendriessche et al. 2007a; Rothäusler et al. 2009, 2018). For
instance, at 5 °C, F. vesiculosus and A. nodosum kept in mesocosms gained 3 times
their initial weight while afloat, but the weight gain was less in the presence of iso-
pods (Vandendriessche et al. 2007b). This is probably because herbivore metabo-
lism, which is strongly controlled by temperature (O’Connor 2009), slows down at
low SSTs and seaweed growth is favored under benign environmental conditions.
Similarly, in cold sub polar waters around Iceland (64°N), Ingólfsson (1998)
reported that fronds of A. nodosum, which were accidentally left afloat for 43 d, did
not show any signs of decay and were still in perfect condition. Consequently, float-
ing seaweeds are expected to be less grazed under cold SSTs.
Rafts serve as substratum for many sessile epibionts, including e.g. encrusting
bryozoans and goose barnacles (Hinojosa et al. 2006; Rothäusler et al. 2011a; Graiff
et al. 2016). Bryozoan growth and thus additional weight generally increase with
seaweed floating time, thereby negatively affecting seaweed persistence (Rothäusler
et al. 2011b for M. pyrifera at 30°S), which can finally result in their decay and sink-
ing (Graiff et al. 2016). However, recently, it was shown that maximum bryozoan
cover on tethered M. pyrifera (30°S) was reached earlier in spring/summer than in
autumn/winter (Graiff et al. 2016). In a study done with natural floating rafts of
M. pyrifera (30°S), the colonization by bryozoans increased with decreasing lati-
tudes, which coincides with warmer SSTs (Rothäusler et al. 2011a). This implies
that bryozoan growth is slowed down at lower SSTs. Hence, seaweeds carrying
epibionts and traveling in cold and icy sub-Antarctic or Antarctic waters may stay
afloat for substantially longer periods, which is also underlined by the fact that
D. antarctica thalli beached at Antarctica had goose barnacles attached (Fraser et al.
2018; E. Macaya Pers. Obs.). Preliminary observations on floating rafts of C. jac-
quinotti within the Antarctic Peninsula revealed very few epibionts (E. Macaya
pers. obs.).
Moreover, there is evidence from molecular studies, showing that hitchhiking
organisms, such as crustaceans, mollusks, seaweed parasites, and non-buoyant sea-
weeds, can travel vast distances (Nikula et al. 2010, 2013; Fraser and Waters 2013;
Fraser et al. 2013; Boo et al. 2014; Guillemin et al. 2014; Macaya et al. 2016). Some
of them even have a circum sub-Antarctic distribution, as has been reported for two
holdfast dwelling peracarid crustaceans (Nikula et al. 2010). However, there are no
studies from high latitudes determining whether these hitchhikers affect the floating
persistence of their rafts. Probably, under favorable conditions such as prevailing in
Tierra del Fuego, sub-Antarctic islands, and Antarctica, seaweeds can continuously
grow, and thus provide a long lasting substratum and food source for their associ-
ated hitchhikers, which in turn may have a decreased metabolic rate. Particularly,
high abundances of amphipods (up to 300,000 individuals m2) have been recorded
in benthic Antarctic seaweeds stands, such as Desmarestia antarctica, D. menziesii
and D. anceps (Huang et al. 2007; see also Chap. 17 by Amsler et al.), some of these
species have been found floating or drifting (Table 4.1) and might represent a dis-
persal vehicle for associated hitchhikers.
4.5 P
hysiology of Floating and Drifting Seaweeds:
Traspassing Thermal Barriers
Our knowledge about the physiological, reproductive and growth performance of

Antarctic seaweeds comes mainly from benthic populations and/or from seaweeds
kept under experimental conditions. Similarly, the performance of floating sea-
weeds at high latitudes has been almost exclusively studied under mesocosm condi-
tions. Generally, in Antarctic benthic seaweeds, photosynthetic and bio-optical
properties as well as UV and/or temperature stress tolerances are linked to their
vertical distribution and biogeographic affinity (Huovinen and Gómez 2013; Gómez
et al. 2019). These seaweeds are defined as shade-adapted, and hence are photosyn-
thetically and metabolically prepared to cope with extreme irradiance conditions
but also metabolically with very low temperatures (Gómez et al. 2009; Huovinen
and Gómez 2013; Rautenberger et al. 2015; Gómez et al. 2019). Hence, during
spring/summer, when irradiances, day length, and light penetration are suddenly
increasing, they can become stressful for many benthic seaweeds but also for their
community associated (Zacher et al. 2009). This is especially the case for subtidal
species, which are growing in a more stable environment compared to intertidal
species.
Upon detachment, floating seaweeds suffer a sudden environmental change from

the benthic (shaded) to the pelagic enviroment (sunny). Thus, depending on the
season and latitude when detached, floating seaweeds but also their associated
hitchhikers might respond differently (e.g. growth, physiological acclimation and
reproduction) (Rothäusler et al. 2012; Macaya et al. 2016 and references therein).
At high latitudes (54°S), floating rafts of M. pyrifera and D. antarctica displayed
different short-term physiological adjustments to floating conditions depending on
the season, which are apparently associated to their biogeographic affinity and
growth strategies (Tala et al. 2016). During winter, M. pyrifera lost biomass although
seaweeds maintained their maximum quantum yield (Fv/Fm) and increased their pig-
ment levels, presumably because of light limitation and to support some biomass
production. Opposite responses such as positive biomass changes, photoregulation,
decreasing Fv/Fm and pigment levels were found during summer (Tala et al. 2016).
Durvillaea antarctica might support better the winter conditions that prevail at high
latitudes because positive biomass changes were found during the first three months
afloat and only small variations in Fv/Fm, pigment, and phlorotannin levels. However,
in summer, tissue deterioration and antioxidant activity increased, which were
reflected in biomass loss (Tala et al. 2016, 2019). Therefore, at high latitudes,
D. antarctica can stay longer afloat (>200 days) during winter than during summer
(90 days).
4.5.1 Out of Antarctic: Is it Physiologically Feasible?
Even though there is no specific information about the physiological and reproduc-
tive responses of floating seaweed in and out Antarctica, important transoceanic
routes have been identified through phylogeographic studies at high latitudes (Fraser
et al. 2010; Coyer et al. 2011; Fraser et al. 2013; Boo et al. 2014; Moon et al. 2017),
confirming the capacities of floating and non-buoyant seaweeds to acclimate during
long journeys (see also Chap. 3 by Fraser et al.). The successful dispersal of floating
seaweeds over short or long distances requires an efficient physiological acclima-
tion (e.g. photosynthetic efficiency adjust, high antioxidant activity, production of
defensive metabolites) not only to maintain growth and reproductive capacity, but
also to deal with the herbivore pressure and epibiont load. When rafting is success-
ful, seaweeds can extend their distributional ranges according to their physiologi-
cal and/or reproductive tolerances and/or abiotic and biotic interactions (Thiel and
Gutow 2005b; Nikula et al. 2010; Coyer et al. 2011; Waters et al. 2013; Batista et al.
2018; López et al. 2018).
Performance and tolerance of benthic seaweed populations can give us an indica-
tion of how they may respond under floating or drifting conditions. The optimum
temperatures for photosynthesis in Antarctic seaweeds range between 5 and 15 °C
(Wiencke et al. 1993; Eggert and Wiencke 2000), thus floating seaweeds entering
Antarctic from Tierra del Fuego or sub-Antarctic sources might be able to sur-
vive. Temperature requirements for growth and survival of 15 Antarctic red seaweed
species were studied by Bischoff-Bäsmann and Wiencke (1996). Consequently,

if eurythermal species (with a broad performance breadth) become pushed through
the APF they can acclimate more easily to more temperate temperatures more easily
and can support large distance dispersal. Hence an “out of Antarctic” scenario,
could be supported at least by the high environmental tolerance showed by some
cold-adapted Antarctic seaweeds. In fact, various species display different mecha-
nisms to support elevated temperatures and high UVR /PAR conditions (Huovinen
and Gómez 2013; Rautenberger et al. 2015). In experimental conditions, UVR tol-
erance is improved in sensitive species modulated by temperature via an efficient
damage repair of the photosynthetic apparatus instead of increasing photo-protective
metabolites or antioxidant activity (Rautenberger et al. 2015). Therefore, chemi-
cally based tolerance mechanisms are not inducible as has been reported for some
Desmarestiales (Flores-Molina et al. 2016). In fact, high constitutive concentrations
of soluble and insoluble phlorotannins (a type of phenolics found mainly in brown
seaweeds) have been determined irrespective of the UV levels at which these sea-
weeds are exposed in their habitat (Rautenberger et al. 2015). In brown sea-
weeds, phlorotannins have different biological functions such as UV shielding,
ROS scavenging, herbivore deterrence, and cell wall formation. Therefore, species
that maintain high phlorotannin concentrations are better prepared to face vari-
able environmental conditions (see also Chap. 18 by Gómez and Huovinen).
However, due to an extended period of low light during the polar winter, and turbid
seawater during summer and autumn following sea-ice melting and phytoplankton
blooms, Antarctic seaweeds are strongly shade adapted, which could impair their
physiological performance during rafting and limiting the migration to lower
latitudes.
The endemic floating species Cystosphaera jacquinotii is commonly found
between 5 to 30 m depth, usually in more exposed areas and disappear south of 66°S
(Neushul 1963; Wulff et al. 2009). Adenocystis utricularis with its vesicle saccate-
like morphology are abundant in the intertidal (Valdivia et al. 2014) and have also
been recorded floating (see above). Photosynthetic characteristics showed that
C. jacquinotti has a low saturating irradiance (Ek = 37 μmol photons m−2 s−1) and
stress tolerance to UVR and enhanced temperature, while A. utricularis showed
high saturating irradiance (Ek = 137 μmol photons m−2 s−1) and stress tolerance
(Gómez et al. 2019). Both saturating irradiance levels match with the subtidal and
intertidal prevailing light conditions. Similar patterns were detected in seaweeds
from King George Island, with saturation irradiances of 55 μmol m−2 s−1 in subtidal
and 120 μmol m−2 s−1 in eulittoral species (Huovinen and Gómez 2013). For
instance, photosynthesis of Desmarestia antarctica, D. anceps and Gymnogongrus
antarcticus was sensitive when exposed to higher light conditions, especially to
UVB (Bischof et al. 1998). In this context, seaweeds from subtidal environments
that form drifting patches can deteriorate quickly, thus contributing to an important
carbon source for higher trophic levels.
High concentrations of soluble phlorotannins are found in C. jacquinotii (>5% of
DW in both vegetative and reproductive tissues), acting as UVR shield and herbi-
vore deterrent (Iken et al. 2007; Huovinen and Gómez 2015; see also Chap. 17 by
Amsler et al. and Chap. 18 by Gómez and Huovinen), thereby contributing to a
higher floating persistence.
Environmental factors that affect seaweed physiology and growth under benthic
and floating conditions, can also modify the reproductive capacity. Considering the
short-life and dispersal distances of seaweed propagules (Santelices 1990), the abil-
ity to remain reproductively competent during rafting and when arriving on a new
site is crucial for a successful dispersal and colonization. Long floating times
together with high temperature and radiation conditions decreas the availability of
propagules and can increas the disintegration of reproductive tissues such as shown
for D. antarctica (Tala et al. 2016, 2019), M. pyrifera (Macaya et al. 2005;
Hernández-Carmona et al. 2006; Rothäusler et al. 2011b) and Hormosira banksii
(McKenzie and Bellgrove 2008). Rafting and long distance dispersal might be facil-
itated in monoecious species or in dioecious species (e.g. D. antarctica and C. jac-
quinotti) when male and female individuals are traveling together and arriving to a
new suitable habitat (Lizée-Prynne et al. 2016).
Presumably the establishment of non-native species within the Antarctic shores is
prevented by the physiological and reproductive tolerance ability to extreme envi-
ronmental conditions rather than transport. Low temperatures, tides and wave
action, ice-scouring, salinity changes, sediment and detritus accumulation may limit
the establishment of foreign taxa on hard substrates (Campana et al. 2009). Biotic
interactions associated to local herbivores and competition can also determine the
colonization success of the colonization. However, under a warming climate sce-
nario, more sub-Antarctic and temperate species might be able to grow and survive
at higher latitudes. However, if the substrate availability is low at the new site of
arrival or the the habitat is highly diverse, only strong competitors may have the
chance to establish (Stachowicz et al. 2002). The density-dependent blocking mech-
anism of conspecifics has been described to prevent the colonization of floating
D. antarctica, due to low space for new recruits and the low contribution of new
gametes in relation to those produced by local individuals (Waters et al. 2013).
Future warming scenarios might facilitate colonization by floating seaweeds, reduc-
ing competition with local species and increasing substrate availability.
Acknowledgements We thank the editors for inviting us to contribute to this review. Financial
support was received through Fondap-IDEAL grant 15150003 to ECM and FONDECYT grant
1131023 to FT and ECM, CONICYT PAI (Chile) 79160069 to FT.
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Chapter 5
Biogeography of Antarctic Seaweeds
Facing Climate Changes
Franciane Pellizzari, Luiz Henrique Rosa, and Nair S. Yokoya
Abstract The seaweed biogeography and diversity in remote areas, such as

Antarctica, should be reassessed considering the population shifts induced by global
changes. This chapter addresses the hypothesis that ecological isolation can be dis-
rupted and that biogeographical distribution of some species could be altered by
thermohaline changes, which in turn would alter the dispersal patterns of macroal-
gae driven by severe meteorological and oceanographic events. Algal growth and
distribution are limited by physical and biological processes, acting as sensitive
bioindicators of changes or abrupt oscillations in the environmental regimes. In
addition, Antarctica represents a natural laboratory highly susceptible to the climate
changes, and the monitoring of their ecosystems may help to predict their potential
effects beyond the Southern Ocean. Another fundamental issue is to understand the
increase in species richness due to the cryptic and alien species, considering shifts
in their biogeographic distribution. The large-scale patterns of some of these species
reported for Antarctica may provide clues to reevaluate aspects of endemism, bio-
logical corridors, ecotone, and expansion of geographical distribution of algal
assemblages facing climate changes, reinforcing the hypothesis that these isolated
ecosystems will become gradually more connected.
Keywords Alien species · Biogeographic processes · Deception Island ·

Endemism · Seaweed diversity
F. Pellizzari (*)
Universidade Estadual do Paraná, Campus Paranaguá, Laboratório de Ficologia e Qualidade
de Água Marinha, Paranaguá, Brazil
e-mail: franciane.pellizzari@unespar.edu.br
L. H. Rosa
Universidade Federal de Minas Gerais, Departamento de Microbiologia,
Belo Horizonte, Brazil
e-mail: ihrosa@icb.ufmg.br
N. S. Yokoya
Instituto de Botânica, Núcleo de Pesquisa em Ficologia, São Paulo, Brazil
e-mail: nyokoya@hotmail.com

https://doi.org/10.1007/978-3-030-39448-6_5
84 F. Pellizzari et al.
5.1 The Abiotic Setting of the Southern Ocean
The Southern Ocean (SO) biota distribution is the result of major geological, ocean-
ographic, and climate changes during the last 50 Ma, and there is a paradox between
the broad distributions of some species and their inherently poor dispersal capacity,
although marine biogeographic studies supported by molecular studies are increas-
ingly revealing examples of this paradox and indicating that long-distance dispersal
of macroalgae is possible (Fraser et al. 2013).
The seaweed processes in the Antarctic and sub-Antarctic regions are strongly
limited and correlated with environmental parameters (Wiencke and Amsler 2012).
In contrast with the Arctic Ocean, the Southern Ocean has no land bridge to temper-
ate regions since the late Mesozoic and has been further separated from the southern
continents by the Antarctic Circumpolar Current (ACC) since ca. 26 Ma (Kirst and
Wiencke 1995). The eastward movement of the ACC or the West Wind Drift (WWD)
had strongly defined the oceanography in the Southern Hemisphere and conse-
quently the diversity, biogeography, and ecology of seaweeds in all the adjacent
coastal regions (Orsi et al. 1995; Huovinen and Gómez 2012). Thus, biogeographic
barriers and ecological corridors are fundamental concepts to understand macroeco-
logical and evolutionary processes, since that ocean circulation, considering present
and past patterns of continental drift, may isolate or connect groups of marine
organisms, including seaweeds.
The Southern Ocean encircling Antarctica, whose natural boundary is the
Antarctic Convergence, is known as the most extreme environment on the Earth.
Considering ocean circulation in the SO, the ACC is permeated by the Southern
Antarctic Circumpolar Front, located between the Polar Front (50°–60°S) and sur-
roundings of the Antarctic coastline, representing the disjunction of Antarctic waters
and resulting in distinct thermal stratifications for each zone (Orsi et al. 1995;
Sanches et al. 2016). In the southern hemisphere, two circumpolar fronts define the
boundaries of the cold-temperate region (Fig. 5.1a): (1) the Antarctic Polar Front
(APF or Antarctic Convergence), the southern limit, characterized by cold surface
waters (ranging 3–5°C), and (2) the Subtropical Front (STF or Subtropical
Convergence), the northern limit that separates subtropical water in the north from
sub-Antarctic water, showing ca. of the 10°C and 15°C surface temperature, during
winter and summer, respectively (Huovinen and Gómez 2012). Thus the ACC,
being the largest and deepest current in the world, was considered in several past
studies as a physical barrier that could limit passive dispersal of new species to
Antarctica (Wells et al. 2011; Pritchard et al. 2012; Sanches et al. 2016).
In a macroscale, Longhurst (2007) identified four “biogeochemical” provinces in
the Southern Ocean considering physical and hydrological properties of these cur-
rents: South Subtropical Convergence, sub-Antarctic water ring, Antarctic, and
Polar Southern provinces. On a regional scale, the dynamics of ice formation and/or
its presence as drifting sheets or icebergs, substrate type, and current regime are the
main factors that set biogeographical boundaries for biota.
5 Biogeography of Antarctic Seaweeds Facing Climate Changes 85
Fig. 5.1 (a) Antarctica contextualized in the Southern Ocean, showing continental proximities
and major oceanographic fronts: subtropical front (STF), Antarctic Polar Front (APF), and
Antarctic Circumpolar Current (ACC). (b) Detailed map indicating the geographical position of
the SSI South Shetland Islands, including Deception, WAP Western Antarctic Peninsula, and EAP
Eastern Antarctic Peninsula. (Photo by Franciane Pellizzari)
5.2 Biogeographic Patterns
Due to the isolation, the SO presents higher endemism of seaweeds, although

lower richness than some sub-Antarctic islands and continental areas from the
Southern Atlantic and Pacific. The Eastern Antarctic Peninsula (EAP) and south-
ern regions from the Western Antarctic Peninsula (WAP) present low species rich-
ness when compared to the South Shetland Islands (SSI – Fig. 5.1b) (Pellizzari
et al. 2017) (see also Chap. 2 by Oliveira et al.). However, Wulff et al. (2009),
comparing the biodiversity, biogeography, and zonation of seaweeds from the
Arctic and Antarctic regions, reported that the diversity and number of endemic
species are higher in Antarctica than in the Arctic. Wiencke and Clayton (2002)
mentioned that about a third of the 120 species recorded to the Antarctic region
are endemic (Phaeophyceae 44%, Rhodophyta 32%, and Chlorophyta 18%).
These differences are explained by the biogeographical histories of both regions
(Wiencke and Clayton 2002).
Temperature is the most important factor controlling biogeographic distribution

of macroalgae, and then shifts in their distribution are inevitable during periods of
global changes. However, other factors must be considered. For example, rafting of
floating organisms and objects appears to have a critical role in facilitating long-
distance dispersal and structuring intertidal ecosystems in Antarctica (Fraser et al.
2013). Many species that lack obvious transoceanic dispersal ability (e.g., brood-
ing invertebrates, small non-buoyant macroalgae, and terrestrial vertebrates) are
nonetheless evidently able to disperse long distances attached in floating wood or
detached kelp (see also Chap. 3 by Fraser et al.). Also, aiming to avoid generalized
biogeography of the SO benthos, Griffiths et al. (2009) studied distributional data
of mollusks, cheilostome, cyclostome, and bryozoans (species richness, rates of
endemism, patterns of radiation) in 29 provinces in the South American, South
African, Tasmanian, New Zealand, sub-Antarctic, and Antarctic regions. The
authors reported high species numbers in New Zealand, Tasmania, and South
Africa and low species richness in South America. In contrast, no difference was
found in richness between the east and west parts of the Southern Ocean (called
“single functional unit”). Besides evidence of strong faunal links between the
Antarctica and South America, biogeographical regions in the SO differ depending
upon the class of organism, which is being considered. Linse et al. (2006) indicated
that patterns of diversity and endemism were very different between the bivalves
and gastropods. Moreover, Pierrat et al. (2013), in a comparative study among
echinoids, bivalves, and gastropods from the Antarctic, sub-Antarctic, and cold-
temperate areas, reported a significant advantage of the BSN (bootstrapped span-
ning network) procedure in the identification of faunal similarities among
biogeographical regions and transitional areas, considering the following faunal
provinces: (1) New Zealand, (2) southern South America, (3) east sub-Antarctic
islands, (4) West Antarctica, and (5) East Antarctica. Strong faunal relationships
perfectly match the flows of the ACC and Antarctic Coastal currents, suggesting
strong connections and groupings between bioregions. However, Antarctic and
sub-Antarctic regions are regarded as distinct biogeographical regions, with pat-
terns driven by a small number of widely distributed species (Griffiths and Waller
2016). Gutt et al. (2016) studied macroepibenthic communities in Weddell Sea,
Bransfield Strait, and Drake Passage and suggested that large-scale patterns in
pelagic organisms segregate three eco-regions possibly correlated with ice pres-
ence and depth. Keith et al. (2011), using a geographically weighted regression
(GWR) model, determined that some environmental conditions could predict
genus richness in macroalgae and confirmed the hypothesis that environmental
tolerances influence species distributions more strongly at higher latitudes, whereas
biotic interactions play a more prominent role in the tropics. This chapter discusses
in that extent shifts in seaweed diversity and distribution in the SO may be also
associated to the rapid climatic changes, resulting in higher connections or disrup-
tion of these previously established provinces.
5.3 S
eaweed Assemblages: Are Antarctic Seaweed Diversity
and Richness Changing?
Shifts in seaweed distribution were important during periods of changing tempera-

tures as demonstrated in the geological past during the last glaciation (Crame 1994).
Similar changes may be expected during the current period of global warming with
a significant impact on marine communities. In addition, Antarctic macroalgal com-
munities will presumably expand north and also southward due to less strong ice
abrasion and improved light conditions, and the new ice-free areas appearing due to
glacier retreat will be probably colonized by seaweeds (Quartino et al. 2013;
Wiencke et al. 2014 and studies summarized in Pellizzari et al. 2017) (see also
Chap. 8 by Quartino et al.).
Climate changes in Antarctic Peninsula are resulting in shifts of marine popula-
tions (summarized in Ducklow et al. 2013). These authors suggested that macroal-
gal assemblages show lower biomass and diversity in the southern region of WAP
when compared to the northern assemblages. Additionally, they mentioned that the
assemblages of the northern WAP seem to be expanding to the south as the annual
sea ice declines.
Physico-chemical changes, mainly due to increased surface seawater tempera-
tures (SST) in the SO, result in a potential driver to shifts in seaweed assemblages
(Müller et al. 2009; Sangil et al. 2012; Wernberg et al. 2016; Pellizzari et al. 2017).
Based on a multivariate analysis of Antarctic and sub-Antarctic seaweed distribu-
tion focusing in an evaluation of the role of the ACC, Sanches et al. (2016) found
differences in the distributional patterns of species and genera in relation to the
zones and sections connected with South America (1: north), influenced by the Ross
Sea Gyre (2: Western Antarctica Peninsula) and by the Weddell Sea Gyre (3: Eastern
Antarctica Peninsula). The predicted latitudinal gradient of species richness was
confirmed, and two main biogeographical clusters were defined: (1) subtropical and
sub-Antarctica and (2) Antarctic Peninsula and surroundings of continental
Antarctic. These differences in diversity patterns between both regions suggest the
existence of a species distributional flux. This may result either from natural disper-
sion or due to global changes, suggesting that Antarctica may not be as isolated and
as suggested in Chap 3 of this book and by Fraser et al. (2019).
Recently, high seaweed richness among the South Shetland Islands (SSI), high-
lighted by six new records for the area, four cryptogenic species and two putative
new species, was reported (Pellizzari et al. 2017). It is noteworthy that the 104 spe-
cies of benthic marine algae listed by these authors represent ~82% of all seaweeds
described to Antarctica. The majority of these new records are cryptic species, rep-
resented by small specimens and inconspicuous forms, and their occurrence may
easily pass unnoticed until a large-scale sampling and a seasonal program have been
implemented (Fig. 5.2) (see also Chap. 2 by Oliveira et al.). Dubrasquet et al. (2018)
studied the diversity of red algae and their distribution along the WAP and SSI
through a molecular-assisted revision, identifying significant differences among
assemblages of SSI and northern part of the WAP (at ≈63°S), central part of the
Fig. 5.2 Activities carried out within the frame of the Antarctic Program supported by the
Brazilian Navy. (Photos by Franciane Pellizzari)
WAP (at ≈64°S), and central-southern part of the WAP (at ≈67°S). Apparently,
these subregions do not correspond to the classical bioregions reported in previous
studies, suggesting that the Bransfield Strait cannot be regarded as a strong barrier
for red macroalgae.
The South Shetland Islands and interface islands between Antarctic and sub-
Antarctic regions were previously reported to have transitional biota features, which
are most likely related with the composition and distribution of benthic marine com-
munities (Pellizzari et al. 2017). The seaweed richness found in the SSI (ca. 60°S)
was higher than in Adelaide Island and Terra Nova Bay (Ross Sea, above latitude
70°S), according to Cormaci et al. (1992) and Mystikou et al. (2014). In addition,
Pellizzari et al. (2017) considered Livingston and King George islands as hotspots
among the SSI.
Recent changes in the composition and structure of algal assemblages from
Antarctica are featured by new records, including green algae and cyanobacteria
identified unprecedentedly for the area, followed by detection of cryptogenic spe-
cies and reduction of endemism (Pellizzari et al. 2017; see also Chap. 2 by Oliveira
et al.). Cyanobacteria are opportunistic organisms that can inhabit diversified and
extreme environments, and they have been regarded as indicators of changes in
seawater pH and temperature (Sangil et al. 2012). Antarctic cyanobacteria are con-
spicuous and well studied in lake assemblages (Taton et al. 2006). However, incipi-
ent information in marine ecosystems is available. Pellizzari et al. (2017) identified
six species of filamentous Cyanobacteria as epiphytes on large seaweeds, occurring

along the intertidal mats of Deception Island. They also reported new record of
opportunistic Chlorophyta, including a cryptogenic species. It has been suggested
that general diversity may be decreasing due to the effects of climate changes (sum-
mary in Pibernat et al. 2007; Wiencke and Amsler 2012). However, this pattern is
not reported in some studies (synopsis in Pellizzari et al. 2017), considering that
seaweed communities seem to be in “transit” for a higher connectivity and distribu-
tion expansion. Further taxonomical studies supported by molecular analyses and
biogeographical models are needed to infer more consistent information regarding
effects of global changes in seaweed diversity.
5.4 The Physiological Bases of Macroalgal Shifts
Antarctic seaweed species are adapted to extreme environmental conditions; how-

ever, they can be highly sensitive to abrupt changes in meteorological and oceano-
graphical settings, suggesting that the distribution, diversity, and richness of these
organisms can be used as suitable sentinels of the effects of the climate change.
In general, Antarctic macroalgae are very well adapted to low seawater tempera-
tures. Kirst and Wiencke (1995) suggested that changes in lipid composition of
membranes are related to genetic adaptation to extreme conditions. Moreover,
endemic Antarctic species show high photosynthetic efficiency and high P:R ratios
at low temperatures (0–5°C), which allow them to exhibit high growth rates and
positive carbon balance at depths close to 30–40-m locations (Gómez et al. 1997;
Wiencke et al. 2007) (see also Chap. 9 by Deregibus et al.). Additionally, endemic
species exhibit upper survival temperatures (USTs) between 9°C and 13°C. The red
alga Georgiella confluens exhibits even lower temperature demands, growing only
at 0°C, but not at 5°C, and exhibits an UST of 11°C (Wiencke et al. 2014). In con-
trast, few endemic Antarctic species have higher temperature demands. For exam-
ple, the brown alga Ascoseira mirabilis grows up to 10°C but exhibits a low UST
similar to the above-mentioned species. The red algae Gymnogongrus antarcticus
and Phyllophora ahnfeltioides grow up to temperatures of 10°C or even 15°C, but
exhibit considerably higher USTs of 19°C or 22°C, respectively. So, the latter three
species could theoretically occur even at temperate sites (Bischoff-Bäsmann and
Wiencke 1996). The highest temperature demands of Antarctic species were dem-
onstrated in Antarctic cold-temperate green algae. These species grow up to 10°C,
15°C, or 20°C and exhibit USTs between 19 and 26 (28)°C (Wiencke et al. 2014).
These temperature requirements reflect the preferential occurrence of these species
along supra- and eulittoral zones, where temperatures may vary considerably.
Responses to climate changes are particularly rapid and strong in marine habitats
especially in high latitudes and in the intertidal and shallow subtidal zones, where
species are often growing at their upper temperature tolerance limits (Hoegh-
Guldberg and Bruno 2010; Sorte et al. 2010). In this context, temperature require-
ments for growth and survival of endemic Antarctic species and species distributed
in the Antarctic cold-temperate region have been extensively tested in laboratory.

However, results from laboratory experiments should be interpreted with caution
since growth and survival of seaweeds in their natural habitat depend on a complex
interaction of physical, chemical, and biological factors. In fact, warming at coastal
Antarctic waters can alter light regime due to increased turbidity and shortening in
the ice cover period, with consequences not well understood for algae adapted to
short periods of favorable light conditions and extended periods of darkness
(Wiencke et al. 2007) (see also Chap. 7 by Huovinen and Gómez). On the other
hand, the inflow of melt water in summer, due to enhanced glacier melting or
increased terrestrial runoff, has also considerable effects on the salinity and tem-
perature regime in inshore waters down to 20-m depth (Klöser et al. 1993; Zacher
et al. 2009). In other instance, inorganic nutrient concentrations may be high and in
general not limiting for seaweeds at any time of the year in the Antarctica (Sanches
et al. 2016).
It is well known that species that fails to acclimatize physiologically or evolve
genetically to increasing temperature will probably move into another habitats or
become extinct (Parmesan 2006; Thomas 2010; Jueterbock et al. 2013). According
to Guo et al. (2005), the most effective and informative method of predicting
declines or disappearances and/or expansion of nonnative species is by monitoring
boundary conditions of very isolated populations, as is the case in Antarctic sea-
weed assemblages. In all, large-scale climate-driven changes have recently been
observed in maritime Antarctic (Macaya et al. 2016; Pellizzari et al. 2017; López
et al. 2018; Fraser et al. 2019; Diaz Tapia et al. 2018), which can favor the prolifera-
tion and extend the growing season of warm affinity species, inducing local domi-
nance of introduced species and causing adverse effect on cold-adapted species
(López et al. 2018).
5.5 D
eception Island: A Case Study of Opportunistic, Alien,
Cryptic and Cryptogenic Species
Deception Island (62°57’S; 60°38’W), South Shetland Islands (SSI – Fig. 5.1b),
affords unique ecosystems essential to understanding the impacts of global warm-
ing due to conditions of a highly temperature-sensitive environment. This island is
also an excellent model to work in a semi-enclosed environment that can be moni-
tored with long-term instrumentation while being free from the blocking effects of
the prevalence of ice and icebergs even during the winter (Smith et al. 2003). The
ATCM XXXV (2012) defines Deception Island as an ecosystem of high relevance
associated to a unique terrestrial flora, including at least 18 species that have not
been recorded elsewhere in Antarctica (e.g., the communities associated with geo-
thermal areas of the Antarctic flowering plant, pearlwort, Colobanthus quitensis).
All these areas are under conservation strategies (classified in ASPAs and ASMAs).
Due to its scientific importance, the area offers a rare opportunity to study the effects
Fig. 5.3 (a) Deception Island (SSI) aerial view. (Photo: DAE, Brazilian Navy); (b) hydrothermal
vents; (c) volcanic fumaroles; (d) Spongomorpha arcta (Chlorophyta); (e) filamentous
Cyanobacteria epiphytized by diatoms, opportunistic taxa dominating the benthic algae assem-
blages in the area; (f) lake along the island cone. (Photos by Franciane Pellizzari)
of environmental changes, in order to contrast them with the dynamics and recovery
from natural disturbance. On the other side, the long history of human activity
(since c.1820), including exploration sailing, whaling, war aviation, and scientific
research (e.g., the Norwegian whaling station; the British secret base of the World
War II, “Base B”), makes this island a site of high historical value. The island was
previously a whaling station, and the presence of research stations (Argentina and
Spain) is also since decades ago. About 11 localities were designated as Antarctic
Specially Protected Area (ASPA).
Deception Island is a circular-shaped volcano, with a linear glaciated coastline,
forming semi-enclosed environments showing intense geothermal activity. Black
sand beaches and outcrops of volcanic rock form the hard substrate (Fig. 5.3a–c, f).
Deception Island exhibits widely varying microclimates with a diameter of ca.
12 km; the center of the island was formed by a huge eruption that flooded the sea
to form a large bay (Port Foster). The bay has a narrow entrance (Neptune’s
Bellows), and shortly after the pass, there is a cove (Whalers Bay).
The fumarolic emissions and thermal springs generally occur along a principal
fracture encompassing Fumarole Bay, Telefon Bay, and Pendulum Cove.
Temperatures of fumarolic discharges as high as 110°C have been recorded depend-
ing on tidal cycle. These fumarolic emissions and thermal springs along the main
fracture result in temperature and pH anomalies (Fig. 5.3a–c), and the bottom water
temperatures in shallow areas could rise to 8°C (Pellizzari et al. 2017).
Thus, mainly due to the unique physical and chemical features besides long
human presence history, including current tourism, Deception Island (Antarctic
Specially Managed Area No. 4) is exceptionally vulnerable to the impacts of intro-
duced nonnative species. The human visitation, the mild climate (compared to other
polar areas), protected and safest natural harbor, and the presence of geothermal
heated sites may catalyze more introduced marine and terrestrial species than any
other Antarctic locations.
The diversity of macroalgae from Deception was early described by Clayton
et al. (1997), Gallardo et al. (1999), and Pellizzari et al. (2017). Two putative new
species, Prasiola sp. and Callophyllis sp., occur in Deception Island and deserve
elucidation due to their cryptic features (Pellizzari et al. 2017). Besides, the widely
distributed species Ulvella viridis, Spongomorpha arcta, and Rhizoclonium ambig-
uum are also conspicuous in the island. Pellizzari et al. (2017) also reported the
predominance of filamentous, opportunistic, and widely distributed or cosmopoli-
tan cyanobacteria and green algae, high diatom epiphytism, and it was one of the
locations where the bipolar and cryptogenic species were reported (Fig. 5.3d, e).
Monostroma grevillei, whose introduction possibilities lie in the anthropic activity
(whaling and/or tourism), is also a bipolar species, although with some degree of
latitudinal disruption. Clayton (1994) reported the first occurrence of Petalonia fas-
cia for Deception Island and suggested that ships could introduce the species, men-
tioning also that the intertidal and subtidal seaweeds from Port Foster belong
probably to widely distributed cold-adapted species. At least 20 seaweed species in
Antarctica are broadly distributed, e.g., the red alga Plocamium cartilagineum, the
brown alga Petalonia fascia, and the green alga Ulothrix flacca (Wiencke and
Clayton 2002). It is possible that such species may be recent invaders from temper-
ate regions (Clayton 1994). Two decades later, Pellizzari et al. (2017) observed the
intertidal diversity permeated by filamentous algae belonging mainly to
Cyanobacteria and typical eurythermal Chlorophyta such as Cladophora albida and
Rhizoclonium riparium. Following McCarthy et al. (2019), many Northern
Hemisphere species have become invasive in southern temperate sites, such as Port
Phillip Bay (Melbourne, Australia). Pathways to the Southern Hemisphere are
clearly viable for some species of algae, polychaetes, and sponges that can inhabit
polar waters. Besides, several bipolar species have been reported, including micro-
organisms, macrofauna, and macroalgae, for example, M. grevillei (Pellizzari et al.
2017). Other studies have demonstrated the presence of cryptic species in Antarctica
(Billard et al. 2015 and synopsis in Dubrasquet et al. 2018), and Deception Island is
one of the target places where cryptic and hidden species must be investigated.
Crustose calcareous algae belonging to Corallinaceae (Pseudolithophyllum sp.
and Lithophyllum subantarcticum) and Hapalidiaceae (Clathromorphum obtectu-
lum, Lithothamnion granuliferum, Synarthrophyton patena, and two unidentified
species of the Phymatolithon/Mesophyllum complex) have been reported along the
Shetland Islands (listed in Pellizzari et al. 2017) (Fig. 5.4a, f). However, in Deception
Island, these calcareous algae are absent, probably due to lower pH values, confirm-
ing the island as a natural laboratory to study responses in species facing extreme
abiotic changes. Moreover, the macroalgae from Deception Island host a rich
Fig. 5.4 Some species sampled along the SSI. (a) Clathromorphum (calcareous Rhodophyta), (b)
fertile Iridaea cordata, (c) transverse section of I. cordata, (d) Delesseriaceae, (e) cystocarp of
Myriogramme mangini, (f) Nacella concinna (the Antarctic limpet) grazing over benthic algae.
(Photos by Franciane Pellizzari)
associated fungal diversity composed of endemic, cold-adapted, or cosmopolitan

taxa. Fungal species of the genera Aspergillus, Cryptococcus, Debaryomyces,
Meyerozyma, Penicillium, and Pseudogymnoascus have been isolated from algae
such as Adenocystis utricularis, Monostroma hariotii, and Adenocystis sp. and
Pyropia endiviifolia (Godinho et al. 2013; Furbino et al. 2014). The studies also
emphasize that the fate of endemic or cold-adapted macroalgal species under chang-
ing Antarctic environment will affect also their associated microbiota.
5.6 R
eevaluating Eco-Regions, Isolation, and Endemism
in the Southern Ocean
According to Wiencke and Tom Dieck (1990), many endemic Antarctic species
show a lower range of thermal tolerance compared to Arctic species. Arctic species
have been isolated for a much less time than Antarctic species. However, some of
these species were also listed in Falkland Islands (Clayton 2003), South Georgia
(Wells et al. 2011), and Macquarie Island (Ricker 1987), e.g., Desmarestia menzie-
sii, G. confluens, and Myriogramme manginii. Ramírez and Santelices (1991)
reported D. anceps for Chile. Monostroma hariotii Gain was registered in
Argentinean Patagonia (Boraso de Zaixso 2003, 2013), South Georgia (Wells et al.
2011), and the Falkland Islands (Clayton 2003). Iridaea cordata (Fig. 5.4b, c) and
Geminocarpus geminatus also occurs in the sub-Antarctic islands and Tierra del
Fuego. Ballia callitricha and Adenocystis utricularis also occur in New Zealand and
Australia, suggesting higher connectivity among the assemblages and as already
discussed in this chapter.
Studies using molecular markers (Hommersand et al. 2009; Medeiros 2013;
Billard et al. 2015; Ocaranza-Barrera et al. 2018; Dubrasquet et al. 2018) have
revealed that cryptic species previously listed in both maritime Antarctica and South
America, e.g., Plocamium, Ulothrix, Gigartina, and Iridaea, are in fact distinct
taxonomic entities. John et al. (1994) reported 127 species of benthic algal flora
from South Georgia (54°S). Comparing the results of this sub-Antarctic island with
the list from the SSI (Pellizzari et al. 2017, Fig. 5.5a–d), 40% of the species co-
occurred in both locations, suggesting high similarity between marine flora of dis-
tinct eco-regions or provinces (Sanches et al. 2016). Wells et al. (2011) described
the intertidal and subtidal benthic seaweed diversity of South Georgia revealing that
63% of these species list co-occur in the SSI. Palmaria decipiens and Iridaea cor-
data (Fig. 5.4), conspicuous Antarctic red algae, occur from the Ross Sea to sub-
Antarctic islands (Wiencke and Clayton 2002). However, I. cordata was also
Fig. 5.5 (a) King George Island (SSI) threatened by global changes. (b) Weddell seal in a drifted
bed of conspicuous Palmaria decipiens, (c) Iridaea cordata, Adenocystis utricularis, Ascoseira
mirabilis, (d) Monostroma hariotii. (Photos by Franciane Pellizzari)
reported in Chile and recently in Argentinean Patagonia (Ramírez and Santelices

1991; Boraso de Zaixso 2013), and P. decipiens was also recorded in New Zealand
(Nelson 2012), Macquarie Island (Ricker 1987), and South Georgia (Wells
et al. 2011).
Advances in molecular techniques have allowed estimating more precisely phy-
logenetic relationships, levels of differentiation, and divergence time between popu-
lations from these continents (Ocaranza-Barrera et al. 2018). According to Papenfuss
(1964), the seaweed flora of the sub-Antarctic islands and the Antarctic region
totaled 550 species. Approximately 75% of these species were distributed in the
sub-Antarctic islands (Clayton 1994). Wulff et al. (2009) suggested that, after the
endemics, the second largest seaweed group in Antarctic includes those occurring
both in the Antarctic region and on sub-Antarctic islands and Tierra del Fuego (see
also Chap. 2 by Oliveira et al.). Some of these species may be examples of distribu-
tional extension northward; besides few studies are supported by molecular data
(Hommersand et al. 2009; Fraser et al. 2013; Medeiros 2013; Billard et al. 2015;
Pellizzari et al. 2017; Ocaranza-Barrera et al. 2018). Fraser et al. (2013) studied the
genetic affinities between transoceanic populations of Adenocystis utricularis and
Bostrychia intricata in southern Chile, New Zealand, and several sub-Antarctic
islands (disjoint regions connected oceanographically by the ACC). The authors
observed divergent clades for both species, but close phylogenetic relationships –
even shared haplotypes – among populations separated by large oceanic distances.
Despite not being particularly buoyant, A. utricularis and B. intricata showed
genetic signatures of recent dispersal across vast oceanic distances, presumably by
attachment to floating substrata (e.g., wood, buoyant large macroalgae, or still, hull
fouling, or ballast water), although the genetic data indicate the possibility of cryp-
tic species within both taxa (see also Chap. 4 by Macaya et al.).
For algae present on both sides of the ACC, e.g., Gigartina skottsbergii, two
hypotheses have been discussed: (1) they correspond to recent immigrants from
adjacent continents, or (2) they have evolved in situ surviving the effects of the last
glaciations. The haplotype networks of G. skottsbergii suggested that there is some
evolutionary divergence between populations and a disjoint distribution, a pattern
that exceeds its dispersal capacity (Billard et al. 2015; see also Chap 6 by Guillemin
et al.). In accordance to Hommersand et al. (2009), the monophyletic clades of
G. skottsbergii may correspond to two cryptic species: (1) G. skottsbergii distrib-
uted in the sub-Antarctic islands and in the southern coast of Chile and (2) a new
species, still to be formally described and named, that occurs in the Antarctic
Peninsula, South Shetland, and South Orkney Islands. The divergence time between
these two cryptic species suggested that algae with limited dispersal capabilities
were able to cross the Scotia Sea after separation of the continents, potentially via a
stepping stone process through the volcanic arc of islands. This strongly supports
the idea that the last Quaternary glaciations induced marked bottlenecks that were
followed by rapid colonization events (Billard et al. 2015; see also Chap. 6 by
Guillemin et al.).
Regarding other connections in the SO, the seaweed assemblage of Southern
Australia (Victoria-Tasmania Region) has been featured by high species richness
(Kerswell 2006) – endemic (40–77%) and temperate (17–45%) species – whereas

species with tropical (4.5– 9.7%) and polar (1.5–5.1%) affinities are much less rep-
resented. Wernberg et al. (2011a) used a seaweed database from herbarium records,
sampled in Australia since the 1940s, and documented changes in communities’
distribution in Indian and Pacific Oceans, related with rapid warming over the past
five decades. For the coasts of New Zealand, regarded as areas of high seaweed
diversity (Kerswell 2006), a recent list suggested that among the 770 currently
known seaweed recorded, 265 are endemic (34%) and 22 alien (2.9%). Rhodophyta
accounts around 60% of the total taxa. Overall, a reduction in endemism (see also
Chap. 2 by Oliveira et al.) and higher species “transit” among assemblages from
Antarctica, sub-Antarctic, and Southern America have been suggested, probably
requiring increasing seawater temperatures over a longer period of time (Sjøtun
et al. 2015).
Although temperature increases may not directly affect the latitudinal distribu-
tion of Antarctic key structural seaweeds in the short term (Müller et al. 2009), they
may modify the presence of these species indirectly via changes in sea ice dynam-
ics, which enhances the hard substrate availability, besides changes on thermoha-
line and circulation patterns. Stammerjohn et al. (2008) reported that the sea ice
cover along the southern portion of the Western Antarctic Peninsula (WAP)
advances nearly 2 months later in the winter and retreats approximately 1 month
earlier in the spring. In this context, the duration of the sea ice season around the
Antarctic Peninsula decreased by 4 days per year from 1979/1980 to 2011/2012
(Hughes and Ashton 2017). However, the sea ice surrounding Antarctica has
increased in extent and concentration from the late 1970s, when satellite-based
measurements began, until 2015. While this increased ice cover trend is modest, it
is surprising given the general warming of the global climate (Fig. 5.6a, b) and
despite some climate models – that incorporate a better understanding of the pro-
cesses affecting the region – usually simulating a tendency of sea ice decrease in
the mid and long term. In contrast, in the Artic, the sea ice cover has exhibited
pronounced declines over the same period, consistent with global climate model
simulations. However, and due to the oscillating patterns of the sea ice cover
recently in the Antarctic shelves, this random behavior in distinct Antarctic areas
has presented an enigma for global climate change science. In addition, significant
differences between the Southern and Arctic Oceans resulted from SST opposite
anomalies (Fig. 5.6c).
Recent data suggest that the SO seems to be barely sensitive to greenhouse
gases (GHG), resulting in a current lower warming levels of SST than observed
in other areas (NASEM 2017). However, changes in the deep ocean can have
important effects due to significant upwelling (NASEM 2017). Other factors that
may play a role in this conundrum include tropical Pacific and Atlantic telecon-
nections, variability in the wind, and ocean circulation that circumnavigate
Antarctica. However, an understanding of the mechanisms and processes driving
sea ice variability, as well SST trends, is limited by the lack of long and homog-
enous records.
Fig. 5.6 (a) Antarctic sea ice extent: line is the median of ice edge between 1981 and 2010 and the
white contour, in 2019. A decrease has been observed since January 2016. (Image Source: National
Snow & Ice Data Center http://nsidc.org/data/seaice_index). (b) Southern Ocean sea ice extends
anomalies. (Between 2010 and 2016 the trend line is slightly positive http://nsidc.org/data/seaice_
index). (c) SST anomalies of the Arctic and Southern Oceans. (Source: NOAA NOMADS http://
nomad1.ncep.noaa.gov/cgi-bin/pdisp_sst.sh)
5.7 C
oncluding Remarks: Prospects for the Future Marine
Flora of the Southern Ocean
Shifts in species distribution are being reported worldwide as a result of changes in

connectivity patterns, mediated by anthropic activity, climate changes, and increased
species “transit” even towards remote areas. Dispersal refugia for Antarctic and sub-
Antarctic seaweeds (see Billard et al. 2015) are also concepts that contribute to the
better understanding of the dispersal mechanisms and recolonization processes dur-
ing biogeographic expansion in the Southern Ocean and connections (see also Chap.
6 by Guillemin et al.). Thus, seaweed assemblages in Antarctica, and in the Southern
Hemisphere, will be modified not only by large-scale geological and paleoclimatic
processes, but also by long-distance dispersal events (see also Chap. 3 by Fraser
et al.).
Changes in meteorological and oceanographic patterns are rearranging the bio-

geography of ecologically important species (Wernberg et al. 2010, 2011a, b). The
impacts on Antarctic seaweed assemblages probably will include (i) shifts in disper-
sal patterns and invasive potential with impacts on local richness and diversity, (ii)
changes in primary productivity and biogeochemical fluxes, (iii) changes in the
genetic pool with consequences for phenotypic plasticity and adaptive responses
due thermohaline shift and habitat losses, and (iv) changes in the intensity and
direction of biological interactions. Considering these projections, the threat to
polar unique lineages, regarded as climatic relics, will increase.
One major issue to accurately interpret the effects of abiotic and biotic changes
on the Southern Ocean marine flora is the scarce basic knowledge of seaweed dis-
tribution over large areas. Although some advances have been made, the studies are
spatially fragmented due mostly to difficulties to sample in polar/extreme sites,
impairing suitable estimations on their potential genetic loss due to environmental
shifts. Thus, in a macroscale, changes in the distributional patterns of the Antarctic
seaweed assemblages highlight the essential importance of long-term monitoring
programs along the West Antarctic Peninsula, probably the area experiencing the
most rapid regional warming. These initiatives will improve the knowledge of these
natural laboratories and models for further comparative biogeographic studies in the
Southern Ocean.
Finally, Antarctic macroalgae can be regarded as suitable bioindicators of global
changes in virtue not only of their specialized physiological mechanisms to cope
with low temperatures and limited light conditions, but also by their high adaptabil-
ity to extreme conditions in their habitat. These remote assemblages can provide
essential clues to understand the resilience potential of organisms living in the edge
of their adaptive windows and are fundamental to reinforce the need for maintaining
global database aiming to integrate and normalize abiotic/biotic metadata (see also
Chap. 2 by Oliveira et al.).
Acknowledgements The authors thank PROANTAR (Brazilian Antarctic Program

557030/2009-9, 407588/2013-2 and 442258/2018-2), INCT Criosfera 2, Brazilian Navy (Polar
Ship Almirante Maximiano–H41), Brazilian Air Force, MMA (Ministry of Environment), MCTIC
(Ministry of Science, Technology and Innovation), CNPq (National Council of Research and
Development), Fundação Araucária–Government of Paraná, CAPES, FAPEMIG, and FNDC.
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Chapter 6
Comparative Phylogeography of Antarctic
Seaweeds: Genetic Consequences
of Historical Climatic Variations
Marie-Laure Guillemin, Claudio González-Wevar, Leyla Cárdenas,

Hélène Dubrasquet, Ignacio Garrido, Alejandro Montecinos,
Paula Ocaranza-Barrera, and Kamilla Flores Robles
Abstract In the Southern Ocean, rapid climatic fluctuations during the Quaternary
are thought to have induced range contractions and bottlenecks, which drastically
impacted marine communities. For photosynthetic macroalgae that are restricted to
very shallow waters, survival in deepwater refugia is not possible. Comparing pat-
tern of distribution of genetic diversity using sequences of mitochondrial and chlo-
roplast markers in distinct species of green, brown and red macroalgae, we sought
to detect common responses to the effect of these glacial cycles. All the Antarctic
macroalgae were characterized by very low genetic diversity, absence of genetic
structure and significant signatures of recent population expansion. The eight stud-
ied species seem to have barely survived glacial events in situ, in a unique refugium
from which they recolonized their current distribution area. We propose that polyn-
yas or areas showing long-term geothermal activity along Antarctic continental
M.-L. Guillemin (*)

Instituto de Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Campus Isla
Teja, Valdivia, Chile
CNRS, UMI 3614 Evolutionary Biology and Ecology of Algae, Sorbonne Universités,
Roscoff, France
e-mail: marie-laure.guillemin@uach.cl
C. González-Wevar
Instituto de Ciencias Marinas y Limnológicas, Facultad de Ciencias, Universidad Austral de
Chile, Campus Isla Teja, Valdivia, Chile
e-mail: claudio.gonzalez@uach.cl
L. Cárdenas

https://doi.org/10.1007/978-3-030-39448-6_6
104 M.-L. Guillemin et al.
margins or peri-Antarctic islands could be good candidate as glacial refugium, but

more variable genetic markers will be needed to precisely pinpoint its location.
Common haplotypes, scattered over hundreds or even thousands of kilometres of
coastline, point out to long-distance dispersal of fronds drifting on the strong oce-
anic currents in the region as the main mechanism of postglacial expansion.
Keywords Glacial refugia · Genetic diversity · Last glacial maximum · Population

bottleneck · Quaternary · Southern ocean
6.1 Historical Isolation of Antarctic Marine Macroalgae
Antarctic marine macroalgae diversity, described as less diverse than other areas of
the Southern Ocean, is still characterized by high levels of endemism reaching up to
35% (Wiencke and Clayton 2002; Wiencke et al. 2014; also see chapter by Oliveira
et al. 2020 in this volume). As recorded for much of the Antarctic flora and fauna
(Clarke et al. 2005; Allcock and Strugnell 2012), the presence of various endemic
Antarctic macroalgal species has been linked to the major tectonic, oceanographic
and climatic changes that have affected the region during the last 50 million years
(Ma) (Dell 1972; Crame 1999, 2018; Mackensen 2004; Aronson et al. 2007; Moon
et al. 2017; Halanych and Mahon 2018). Indeed, the fragmentation of the continen-
tal landmasses and the initiation of the Antarctic Circumpolar Current (ACC)
(Fig. 6.1) gradually isolated the Antarctic waters from the rest of the Southern
Ocean (Crame 1999; Scher and Martin 2006; Aronson et al. 2007; Dalziel et al.
2013; Sijp et al. 2014; Scher et al. 2015). Currently, the Antarctic Polar Front (APF)
(Fig. 6.1) is considered as an effective barrier for many near-shore marine benthic
H. Dubrasquet · K. Flores Robles
I. Garrido
Chile, Campus Isla Teja, Valdivia, Chile
Département de Biologie et Quebec Océan– Ocean Institute, Université Laval,
Quebec City, QC, Canada
A. Montecinos
CNRS, UMI 3614 Evolutionary Biology and Ecology of Algae, Sorbonne Universités,
Roscoff, France
P. Ocaranza-Barrera
Laboratorio de Ecosistemas Marinos Antárticos y Subantárticos, Universidad de Magallanes
(LEMAS), Punta Arenas, Chile
6 Comparative Phylogeography of Antarctic Seaweeds: Genetic Consequences… 105
Fig. 6.1 Reconstruction of the Antarctic and sub-Antarctic ice coverage during the Last Glacial
Maximum (LGM; ~20,000 ka) and in the present day. Putative LGM ice extension is based on vari-
ous recent glaciological studies published for the tip of South America (McCulloch et al. 2000), the
Antarctic Peninsula and the South Shetland Islands (Simms et al. 2011; Larter et al. 2014;
O’Cofaigh et al. 2014) and South Georgia (White et al. 2018). Current ice extension is drawn based
on ®GoogleEarth satelital images. Arrow: Antarctic Circumpolar Current (ACC); thickness repre-
sent the strength of the ACC (Roberts et al. 2017). Dotted blue lines: Antarctic Polar Front (APF;
mean position of the Polar Front is represented) and sub-Antarctic Front (SAF) (Roberts et al.
2017). The five sampling areas where Antarctic seaweeds were sampled are noted with back points
(more details are given in the text and in Figs. 6.3 and 6.4)
taxa (but see chapter by Oliveira et al. 2020 in this volume), especially between
Antarctic and sub-Antarctic provinces (Clarke et al. 2005; González-Wevar et al.
2012, 2017; Poulin et al. 2014; Billard et al. 2015; Crame 2018; Halanych and
Mahon 2018). Non-endemic Antarctic seaweeds have classically included (1) cos-
mopolitan species reported on most Antarctic and sub-Antarctic/temperate coasts of
the Southern Ocean (e.g. Plocamium cartilagineum), (2) cold-water species with
disjoint amphiequatorial distribution (e.g. Acrosiphonia arcta and Desmarestia viri-
dis/confervoides) and (3) more broadly distributed species also occurring in peri-
and sub-Antarctic areas of the Southern Ocean as South Georgia, South Sandwich
Islands or even the southern tip of South America (e.g. Iridaea cordata, Gigartina
skottsbergii and Adenocystis utricularis) (Wiencke and Clayton 2002; Wiencke
et al. 2014).
Nevertheless, reconstruction of these Southern Ocean macroalgae species geo-
graphic distribution maps relies solely on classical taxonomy. Macroalgal anatomy
and high degree of phenotypic plasticity could lead to incorrect taxonomic classifi-
cation of specimens and molecular tools are now recognized as essential for species
determination in these organisms (Saunders 2005, 2008). Inaccurate morphological
identification and existence of cryptic species have been commonly reported in

green, red and brown macroalgae, including in Antarctica (Hommersand et al. 2009;
Moniz et al. 2012; Billard et al. 2015; Pellizzari et al. 2017; Dubrasquet et al. 2018;
Ocaranza-Barrera et al. 2019).
If few molecular studies have indeed confirmed the existence of macroalgal spe-
cies characterized by vast disjoint distributions that include Antarctica (i.e.
Acrosiphonia and Desmarestia; Olsen et al. 1993), most genetic data available sup-
port the existence of endemic Antarctic cryptic species. For example, two cryptic
species, one Antarctic and one sub-Antarctic, were detected in G. skottsbergii and
I. cordata (Hommersand et al. 2009; Billard et al. 2015; Ocaranza-Barrera et al.
2019). In the same way, even if exhaustive phylogenetic studies have yet to be under-
taken for P. cartilagineum, Hommersand et al. (2009) noted that ‘unpublished rbcL
sequence analyses by S. Fredericq show that P. “cartilagineum” from Antarctica is
distinct from all other species of Plocamium investigated so far’. In G. skottsbergii,
the two cryptic species are clearly separated by the APF (Fig. 6.1) with the sub-
Antarctic species distributed in South America along the coasts of Chile and
Argentina and the Falkland Islands, while the Antarctic species is found in the
Antarctic Peninsula, the South Shetland Islands and the South Orkney Islands
(Billard et al. 2015). Divergence time estimations between Antarctic and sub-
Antarctic cryptic macroalgal species indicate a split between two lineages occurring
at the end of the Miocene, some 10–5 Ma ago (Hommersand et al. 2009; Billard et al.
2015; Ocaranza-Barrera et al. 2019), long after the physical fragmentation of the
Southern Ocean continental landmasses or even to the formation of the ACC (Crame
1999; Mackensen 2004). However, the time of divergence between Antarctic and
sub-Antarctic lineages of macroalgae predates the Quaternary glacial cycles (~2 Ma).
The existence of macroalgal species (both nominal species and cryptic species
detected only when using molecular tools), entirely restricted to the Antarctic shelf,
or at most including some adjacent islands of the maritime Antarctic (i.e., South
Shetland Islands, South Orkney Islands and Balleny Islands) and offshore peri-
Antarctic islands located south of the APF (i.e., South Georgia and Sandwich
Islands), evidenced the long evolutionary history of these organisms within the
Antarctic waters. In contrast to the hypothesis that most of the Antarctic biota could
be recent colonists, arrived after the deglaciation of the Last Glacial Maximum
(LGM) ice sheets (Clarke and Crame 1992), various Antarctic marine species,
including macroalgae, have withstood Quaternary glacial cycles in situ (Convey
et al. 2008, 2009; Allcock and Strugnell 2012).
6.2 A
ntarctic Marine Macroalgae: Surviving Quaternary
Glacial Cycles in Situ
The onset of glaciations in Antarctica began during the Eocene-Oligocene bound-

ary, and after a slightly warmer stage (27–15 Ma) that seemed to have reduced the
extent of Antarctic ice, gradual cooling during the Miocene-Pliocene transition led
to the re-establishment of major ice sheets covering Antarctica (Kennett 1977;

Zachos et al. 2001). Later on, the Quaternary (2 Ma to 20 Ka) was characterized by
the alternation between glacial and interglacial periods that greatly affected the sea-
sonality and intensity of sea ice formation in the region (Clarke and Crame 1992;
Barker and Thomas 2004; Gersonde et al. 2005; Kemp et al. 2010). During the
LGM, ice sheet expansions were accompanied by eustatic drop in sea level (~120 m
lower than at present), as well as important latitudinal changes in the position of the
ACC (Fig. 6.1; McCulloch et al. 2000; Simms et al. 2011; Larter et al. 2014;
O’Cofaigh et al. 2014; Roberts et al. 2017; White et al. 2018).
The development of large ice sheets generated major landscape and seascape
changes in Antarctica (Zachos et al. 2001; Thatje et al. 2005; Davies et al. 2012).
For instance, glacial reconstructions of the Antarctic Peninsula during the LGM
(20 Ka) showed stable grounding ice sheets advancing up to the continental shelf
edge (Larter et al. 2014; O’Cofaigh et al. 2014) (Fig. 6.1). Major glacial events in
Antarctica are thought to have led to mass extinctions, with ice scouring pushing
near-shore marine communities down the steep shelf slopes surrounding the
Antarctic continent (Clarke and Crame 1992; Thatje et al. 2005). Antarctic benthic
communities, especially sessile organisms with narrow depth distribution range, as
macroalgae, would have been remarkably vulnerable to continental sea ice advances
and retreats (Thatje et al. 2005; Dambach et al. 2012). Nevertheless, it seems that
grounded ice did not completely cover the Antarctic continental shelf, not even dur-
ing the glacial maxima (Klages et al. 2017), and some isolated areas could have
acted as in situ glacial refugia. A wealth of evidences support this view, including
genetic data obtained for various terrestrial and marine organisms (Convey et al.
2008, 2009; Allcock and Strugnell 2012), fossil evidences (Hiller et al. 1988) and
glaciological and oceanographic reconstructions (Paillard and Parrenin 2004;
Bentley et al. 2014; Larter et al. 2014; O’Cofaigh et al. 2014; Klages et al. 2017).
Several mechanisms could have sustained Antarctic shelf areas uncovered by ice
during the Quaternary glacial events. First, areas of open water (polynyas) formed
along Antarctic continental margins could have acted as in situ marine refugia
(Thatje et al. 2008). The possible existence of much more saline waters surrounding
Antarctica during glacial periods could have produced more stable and widespread
polynyas than previously postulated (Paillard and Parrenin 2004; Thatje et al. 2008).
Alternatively, in situ refugia could also be associated to volcanoes or areas of geo-
thermal activities (Fraser et al. 2014). Such geothermal refugia could be very impor-
tant in areas where clusters of long-lived volcanoes are recorded such as the tip of
the Antarctic Peninsula, the South Shetland Islands or the Ross Sea (Fraser et al.
2012, 2014) (see Chaps. 3 and 4 in this volume). Moreover, geological evidence
supports the diachrony of ice sheet extensions around Antarctica (Anderson et al.
2002) and near-shore marine organisms could ultimately have survived, hopping
from one open ice-free continental shelf area to another during glacial periods
(Thatje et al. 2008; Allcock and Strugnell 2012; Hughes et al. 2013).
At last, Antarctic near-shore macroalgae could also have endured the Quaternary
glacial events south of the APF but beyond the Antarctic continental shelf margins.
The coasts of peri-Antarctic islands have been postulated as potential glacial refugia
for some species since their distribution generally includes islands of the Scotia Arc
such as South Georgia and the South Sandwich Islands and Balleny Islands
(Wiencke and Clayton 2002; Wiencke et al. 2014). South Georgia represents the
northern limit of distribution for many species of the Antarctic benthos (Barnes
et al. 2006), and this area was reported as glacial refugium for some Antarctic
marine invertebrates (e.g. the Antarctic limpet Nacella concinna: González-Wevar
et al. 2013).
6.3 P
ersistence in Multiple Isolated Glacial Refugia Versus
a Single Antarctic Refugium
Quaternary climatic oscillations dramatically affected species geographic range and

demography, especially at high latitude (Hewitt 2000, 2004; Maggs et al. 2008;
Provan and Bennett 2008; Allcock and Strugnell 2012; Fraser et al. 2012). The
expansion-contraction model (Provan and Bennett 2008) proposed an alternation
between the contraction of species distribution ranges during glacial advances and
subsequent rapid expansions during interglacial periods. These expansion/contrac-
tion cycles had a strong impact on the distribution of genetic variation of high lati-
tude organisms and can be detected, nowadays, using molecular tools and
phylogeographic analyses (Hewitt 2000, 2004; Provan and Bennett 2008; Allcock
and Strugnell 2012). Depending on the number and localization of glacial refugia,
different evolutionary scenarios can arise (Fig. 6.2).
For species that have survived glacial events in a unique refugium from which
they recolonized their current distribution area, a very low level of genetic diversity
and a high spatial genetic homogeneity are expected (see scenario 1 in Fig. 6.2). In
this case, the effect of genetic drift during glacial bottlenecks could be amplified by
gene surfing at expanding frontiers leading to extreme erosion of genetic diversity
and even complete fixation of pioneer alleles over huge areas (Excoffier and Ray
2008; Excoffier et al. 2009; Hallatschek and Nelson 2010). Supporting this idea,
complete genetic fixation has been recorded over distance of hundreds or even thou-
sands of kilometres for some temperate Southern Hemisphere macroalgae, with the
same mitochondrial haplotype covering all regions of the species distribution previ-
ously scoured by ice during glacial maxima (e.g. along the southern coast of Chile:
Fraser et al. 2009; Montecinos et al. 2012).
In contrast, population fragmentation in multiple disjoint glacial refugia (see sce-
nario 2 in Fig. 6.2) could lead to repeated events of divergence and diversification
(Clarke and Crame 1992; Allcock and Strugnell 2012). Indeed, small populations
could rapidly diverge due to strong genetic drift and, in addition, divergence could be
enhanced due to selection if environmental differences exist between refugia.
Divergence during isolation could be sufficient to generate reproductive barrier and
lead to speciation (Wilson et al. 2009; Allcock and Strugnell 2012; Lecointre et al.
2013). This phenomenon, classically known as the climate ‘diversity pump’ (Haffer
1969), has been proposed to be at the origin of recent evolutionary radiation events
Fig. 6.2 Putative effects of genetic bottleneck due to intense ice scouring during glacial periods
(i.e. the LGM) and postglacial range expansion following ice retreat yielding to the species current
distribution. Two distinct scenarios have been considered: (1) the existence of only one in situ
glacial refugium and (2) the existence of multiple (here three) in situ glacial refugia. Species dis-
tribution area is drawn in grey; each circle represents one individual; distinct colours represent
genetic variants (e.g. distinct haplotypes). Effects of bottleneck and postglacial expansion on the
current genetic diversity and phylogeographic structure potentially observed nowadays in species
affected by the glacial cycles are given on the right
in Antarctica (Clarke and Crame 1989; Near et al. 2012; Crame 2018). Such process
is expected to be more effective for species having limited dispersal capabilities such
as those with non-pelagic development or very short free-living larval stage (Pearse
et al. 2009). Indeed, highly differentiated genetic lineages/sister species have been
detected in various Antarctic marine organisms characterized by low dispersal capac-
ity and related to a scenario of isolation in multiple refugia during glacial events
(Wilson et al. 2009; Allcock and Strugnell 2012; Hemery et al. 2012). In macroalgae,
population fragmentation in multiple refugia has been commonly reported in the
North East Atlantic where genetic distinctiveness characterizes patchy populations
located at low latitude and inhabiting former refugial areas (Neiva et al. 2016).
6.4 A
ntarctic Macroalgae Genetic Diversity: COI and TufA
Sequences Data Sets
Little is known about Antarctic macroalgae genetic diversity and most of the studies
have used molecular markers primarily for species identification (Hommersand
et al. 2009; Moniz et al. 2012; Mystikou et al. 2014; Pellizzari et al. 2017; Dubrasquet
et al. 2018; Ocaranza-Barrera et al. 2019) or phylogenetic inferences among taxa

including Antarctic species (Olsen et al. 1993; Peters et al. 2000). However, infor-
mation about intraspecific genetic diversity, mostly based on the acquisition of
mitochondrial sequences (coding sequences of the cytochrome c oxidase I gene,
noted COI, Guillemin et al. 2018; Ocaranza-Barrera et al. 2019; non-coding
sequences of the intergenic region Cox2–3, Billard et al. 2015), is building up for
some red macroalgae in the South Shetland Islands and the Antarctic Peninsula:
Curdiea racovitzae, Georgiella confluens, Gigartina skottsbergii, Iridaea cordata,
Palmaria decipiens and Plocamium cartilagineum.
Here we used the published COI data set obtained for six species of Rhodophyta
(Guillemin et al. 2018) to which we added new COI sequences for one species of
Ochrophyta (Himantothallus grandifolius) and sequences of the plastid gene tufA,
encoding for protein synthesis elongation factor Tu (EF-Tu), for one species of
Clorophyta (Monostroma hariotii) in order to compare genetic signature among
macroalgae phylum. Monostroma hariotii and H. grandifolius DNA extractions
were performed with an E.Z.N.A tissue DNA kit (Omega Bio-tek, Inc. Georgia,
USA) following the manufacturer’s instructions. Primers TufAgf4 and TufAR and
PCR reactions and programme described in Famà et al. (2002) were used to amplify
tufA fragments in M. hariotii, while a fragment of the COI gene was amplified in
H. grandifolius using the primers GazF2 and GazR2 and methodology described in
Lane et al. (2007). PCR products were purified using the commercial kit
UltraCleanTM (MO BIO Laboratories, Carlsbad, USA) and sequenced in both
directions at the AUSTRAL-omics Core-Facility (Universidad Austral de
Chile, Chile).
Sequences of all macroalgae except H. grandifolius were obtained from five
sampling localities: two located in the South Shetland Islands (in Greenwich and
King George Island), two along the Northern part of the West Antarctic Peninsula
(WAP) near the Chilean O’Higgins Antarctic base and in Paradise Bay and one
along the central part of the WAP (Marguerite Bay) (Figs. 6.1, 6.3, and 6.4).
Himantothallus grandifolius COI data set includes 17 new sequences obtained from
Greenwich Island, King George Island, O’Higgins and Paradise Bay (GENBANK
N° MK503231–MK503247) and two sequences available in GENBANK
(HE866784, King George Island, Yang et al. 2014; GQ368262, Terre Adelie,
Silberfeld et al. 2010). Monostroma hariotii tufA sequences correspond to
GENBANK N° MK507414–MK507450. For each species-specific data set, we cal-
culated five diversity indices, Tajima’s D (Tajima 1989) and Fu’s Fs (Fu 1997) sta-
tistics and estimated the observed distributions of pairwise differences between
sequences using Arlequin v 3.5 (Excoffier and Lisher 2010). For Tajima’s D and
Fu’s Fs, significant departure from mutation drift equilibrium was tested using 1000
bootstrap replicates in Arlequin (Excoffier and Lisher 2010). Observed distributions
of pairwise differences between sequences were compared to estimated values
under a model of sudden demographic expansion through a generalized least squares
approach and goodness of fit was tested using 1000 permutations in Arlequin
(Excoffier and Lisher 2010). Haplotype networks were reconstructed using
NETWORK v 4.510 (Bandelt et al. 1999).
Curdiea Palmaria
racovitzae decipiens
(2) (5)
GEO GEO
(6) PRA (10) PRA
OHI OHI
Network: 42 COI (10) Network: 35 COI (4)
sequences sequences
100 km
PAR Land PAR
(14) (13)
Ice shelf
(10) (3)
MAR MAR
Fig. 6.3 Haplotype networks and pie charts showing the geographical distribution of haplotypes
for the mitochondrial genetic marker COI (632 bp) in Curdiea racovitzae and Palmaria decipiens.
In the networks, each circle represents a haplotype and its size is proportional to the frequency in
which the haplotype was encountered, and black lines correspond to one mutational step. The five
localities correspond, from north to south, to King George Island (GEO), Greenwich Island (PRA),
O’Higgins (OHI), Paradise Bay (PAR) and Marguerite Bay (MAR). The number of sequenced
individuals is given between brackets. From the six species of red algae studied (Guillemin et al.
2018), only results obtained for C. racovitzae and P. decipiens are illustrated since these two spe-
cies represent the less and the most diverse Rhodophyta sampled along the coasts of the Antarctic
Peninsula and the South Shetland Islands, respectively. Underwater photographs of specimen’s
characteristic of both species were taken by I. Garrido; please note the impact of ice scour on
nearby sea bed P. decipiens populations. (King George Island)
6.5 B
rown, Red and Green Macroalgae: Sharing a Common
Pattern of Glacial Impact and Postglacial
Populations Recovery?
All the analysed macroalgae are non-buoyant and commonly found in the Antarctic
waters. Nevertheless, they present some noticeable ecological differences. While
I. cordata, G. skottsbergii, C. racovitzae and P. decipiens are mostly found in the
intertidal down to the shallow subtidal, G. confluens and P. cartilagineum are gener-
ally found deeper in the subtidal, as understory of large brown macroalgae.
Monostroma hariotii presents very thin, delicate thalli, is very common in both the
intertidal and subtidal zones and is considered a pioneer species able to colonize
Fig. 6.4 Haplotype network and pie charts showing the geographical distribution of haplotypes
for the plastid genetic marker tufA (772 bp) in Monostroma hariotii and distribution of the unique
haplotype detected in the 19 COI sequences (mitochondrial marker, 619 bp, include HE866784
from King George Island and GQ368262 from Terre Adelie already published in GENBANK) in
Himantothallus grandifolius. In the network, each circle represents a haplotype and its size is
proportional to the frequency in which the haplotype was encountered; black line corresponds to
one mutational step. The five localities correspond, from north to south, to King George Island
(GEO), Greenwich Island (PRA), O’Higgins (OHI), Paradise Bay (PAR) and Marguerite Bay
(MAR). The number of sequenced individuals is given between brackets. An underwater photo-
graph of a mixed high subtidal bed of M. hariotii (arrow) and H. grandifolius (arrow heads) is
given on the top. (King George Island) (Photo by Ignacio Garrido)
areas with freshwater influence from glacier run-off, presenting heavy ice scour or
recently available for colonization after glacier retreat (Quartino et al. 2013;
Wiencke et al. 2014). With thalli more than ten meters long, H. grandifolius is the
largest seaweed reported in Antarctica. The species, in combination with other
brown macroalgae of the genus Desmarestia, form dense beds of canopy-forming
algae, dominating the subtidal rocky shores.
6.5.1 S
ignature of a Drastic Impact of the Last
Glacial Maximum
Regardless of their ecological differences or classification into distinct taxonomic

divisions, molecular data show that all eight macroalgae have been strongly
impacted by glacial events (Table 6.1, Figs. 6.3 and 6.4). Extremely low genetic
diversity was observed at the intraspecific level with a number of haplotypes vary-
ing between one in H. grandifolius up to only seven in the case of I. cordata and
P. decipiens (Table 6.1). These results could be related to historical changes in mac-
roalgal population size in the study area. The complete lack of diversity observed
for H. grandifolius does not allow to further test this hypothesis; however, the seven
other species presented additional results that support this idea: a starlike topology
was observed in haplotype networks (Figs. 6.3 and 6.4), mismatch distributions
were unimodal (hypothesis of sudden expansion could not be rejected when calcu-
lated for the sum of squared deviation, SSD, or Harpending’s raggedness index,
Rag, except for M. hariotii Rag for which a p < 0.05 was obtained; Table 6.1; see
also Guillemin et al. 2008 for more details on red algae species) and all but the green
alga M. hariotii presented negative values of Tajima’s D and Fu’s Fs statistics
(Table 6.1).
None to very few mutations have been accumulated in the populations since
expansion from their glacial refugium, strengthening the idea that the demographic
expansion occurred recently. We proposed (as in Billard et al. 2015; Guillemin et al.
2018; estimations based on the calculation of the parameter Tau from models of
sudden expansion and previously published mutation rate per sequence per genera-
tion for mitochondrial genes in macroalgae) that the demographic bottleneck cor-
responds to population contraction of macroalgae in refugium during the LGM and
that recolonization of the coast begun some 18,000 years ago, at most, a date con-
gruent with time of deglaciation in the area (Simms et al. 2011; O’Cofaigh et al.
2014). Similarly, other studies have related the recent expansion detected in the
southern most populations of sub-Antarctic macroalgae to population recolonizing
areas previously covered by ice after the LGM (Fraser et al. 2009, 2012, 2013;
Montecinos et al. 2012; Billard et al. 2015).
The level of genetic diversity estimated for Antarctic macroalgae is within the
lowest reported for Antarctic marine species with broad distribution, with values of
haplotype diversity (H) ranging between 0.000 and 0.398 and nucleotide diversity
Table 6.1 Genetic diversity indices and neutrality test in six red algae, one brown alga and one
green alga sampled along the Antarctic Peninsula and South Shetland Islands. Sequences used for
analyses of all six species of Rhodophyta and Himantothallus grandifolius correspond to the
mitochondrial gene COI, while the plastid gene tufA was used for analyses of Monostroma hariotii
π Mismatch
Species N k S H Π (×102) Tajima’s D Fu’s FS distribution
Rhodophyta
Curdiea 42 2 1 0.048 0.048 0.008 −1.120∗ −1.491 ns Unimodala
racovitzae
Georgiella 20 4 4 0.363 0.489 0.077 −1.638∗ −1.613 ns Unimodala
confluens
Gigartina 28 2 1 0.071 0.071 0.011 −1.151 ns −1.155 ns Unimodala
skottsbergii
Iridaea cordata 90 7 5 0.398 0.623 0.102 −0.797 ns −2.882 ns Unimodala
Palmaria 35 7 6 0.318 0.343 0.054 −2.103∗∗∗ −7.041∗∗∗ Unimodala
decipiens
Plocamium 64 4 4 0.122 0.155 0.025 −1.759∗∗∗ −3.466∗∗ Unimodala
cartilagineum
Ochrophyta
Himantothallus 19b 1 0 0.000 0.000 0.000
grandifolius
Clorophyta
Monostroma 37c 2 1 0.378 0.378 0.049 0.846ns 1.223ns Unimodald
hariotii
N, number of sampled specimens; k, number of haplotypes; S, polymorphic sites; H, haplotype
diversity; Π, average number of nucleotide difference; π, nucleotide diversity; ns, non-significant.
All results obtained for Rhodophyta were taken from Guillemin et al. (2018). COI sequences are
of 632 base pair (bp)
∗p < 0.05
∗∗p < 0.01
∗∗∗p < 0.001
a
Hypothesis of sudden expansion could not be rejected when calculated for the sum of squared
deviation or Harpending’s raggedness index (i.e. 0.000 < SSD < 0.007; 0.179 < Rag < 0.821; all
p > 0.05). See Guillemin et al. (2018) for more detail
b
Include two sequences available in GENBANK: HE866784 from King George Island (Yang et al.
2014) and GQ368262 from Terre Adelie (Silberfeld et al. 2010). All COI sequences are of 619 bp
c
Sequences for the plastid gene tufA were all of 772 bp, except for the individual GGVMLG0575,
which was 52 bp shorter. Since the 3′ part of the tufA gene was not variable in our whole data set,
GGVMLG0575 was completed to 772 bp as in the other individuals before analyses
d
Goodness-of-fit tests for a model of sudden expansion calculated in ARLEQUIN v.3.5 for the sum
of squared deviation (SSD = 0.005, p = 0.0001) and for Harpending’s raggedness index
(Rag = 0.202, p = 0.459)
(π × 102) ranging between 0.000 and 0.102 (lowest values in H. grandifolius and
highest values in I. cordata; Table 6.1). Rather low level of diversity and complete
lack of genetic structure have also been reported in some widespread Antarctic
marine invertebrates as Sterechinus neumayeri (H = 0.257; π × 102 = 0.036; Díaz
et al. 2018), Chorismus antarcticus (H = 0.639; π × 102 = 0.209; Raupach et al.
2010), Parborlasia corrugatus (H = 0.762; π × 102 = 0.118; Thornhill et al. 2008),

Euphausia superba (H = 0.856; π × 102 = 1.394; Bortolotto et al. 2011),
Nematocarcinus lanceopes (H = 0.902; π × 102 = 0.568; Raupach et al. 2010) and
Nymphon australe (H = 0.918; π × 102 = 0.657; Soler-Membrives et al. 2017). The
lowest levels of genetic diversity have been observed in benthic marine inverte-
brates with distribution restricted to shallow waters of the Antarctic shelf and have
been related to the extreme effect of ice scouring in these organisms, not able to
migrate to deeper waters during glacial maxima (Raupach et al. 2010; Díaz et al.
2018). It is then not surprising to observe genetic diversity congruent with extreme
events of mortality due to LGM ice impact in photosynthetic macroalgae, these
organisms being characterized by one of the most restricted bathymetry in the
marine realm.
Indeed, Antarctic macroalgae are anchored to the sea bottom and cannot survive
under ice, without direct sunlight, for long periods of time. Glacial refugia for these
organisms should then be limited in depth (generally dense beds of Antarctic mac-
roalgae are reported growing down to 40–50 m) and to areas where the sea ice melt
during summer. However, periods of ice-free summer as short as 2 months allow
macroalgal bed growth (Norkko et al. 2004) and living specimens of various mac-
roalgae species were retrieved in Terre Adelie under ice sheets in an area that did not
melt during summer for 2 years in a row (S. Hourdez pers. com., specimens kept in
the Museum of Natural History, Paris, France). This time period could, however, be
considered as a maximum before severe population decline. Indeed, none of the
fleshy macroalgae were considered as healthy (but half the encrusting coralline
algae were still pigmented) after 3 years of permanent sea ice coverage in the
Commonwealth Bay, a polynya affected by the grounding of a huge drifting iceberg
in 2010 (Clark et al. 2015). Moreover, Antarctic macroalgae are extremely shade
adapted and have been observed to grow at depth of 90 m (Wiencke and Clayton
2002; Wiencke et al. 2007). In other regions of the world, the existence of kelp beds
reaching depth of 200 m was even predicted using oceanographic and ecophysio-
logical models (Graham et al. 2007; see also Spalding et al. 2019 for reports of
macroalgae growing down to 140 m). Additionally, long-term survival of Antarctic
macroalgae in areas highly impacted by ice could be facilitated by the synthesis and
accumulation of protective compounds (Wiencke et al. 2007). Some species, such
as the green algae Acrosiphonia arcta and Prasiola spp., have developed remark-
able adaptations to cope with ice disturbance characteristic of Antarctic habitats.
Indeed, both synthesize cryoprotectants that prevent damage by ice to membranes
or enzymes and Prasiola has been reported to photosynthesize at temperatures as
low as −15 °C (Jacob et al. 1991; Raymond and Fritsen 2001; Wiencke et al. 2007).
Antarctic macroalgae could then be tougher than expected and may have survived
in small areas highly impacted by ice during the LGM.
6.5.2 One Refugium to Rule Them all
Classically, locations of glacial refugia have been inferred by comparing genetic

diversity between populations located within areas potentially free of ice during the
LGM and the ones located in recently colonized areas, previously covered by ice
(Hewitt 2000, 2004; Maggs et al. 2008; Provan and Bennett 2008). Since population
effective size is more stable in glacial refugia than in recently colonized areas, a
much higher genetic diversity is expected to characterize the former than the later
(Hewitt 2000, 2004; Maggs et al. 2008; Provan and Bennett 2008). If the particu-
larly low genetic variability observed in our species lead to the idea of one unique
refugium in Antarctica, it frustratingly does not allow pinpointing its location.
Indeed, whatever the species under study, none of our sampled populations shows a
specifically high genetic diversity (Figs. 6.3 and 6.4; see also Guillemin et al. 2018
for more details on distribution of genetic diversity of I. cordata, G. confluens,
G. skottsbergii and P. cartilagineum).
Various areas could be proposed as in situ refugia along the coast of Antarctica
for our seaweeds and these include localities close to active volcanoes (as Deception
Island, Penguin Island and Bridgeman Island in the South Shetland Islands or the
coast of the Western Ross Sea; Fraser et al. 2014) or localities where the shelf sea-
floor was free of grounded ice during glacial maxima (i.e. Alexander Island, Eastern
Amundsen Sea Embayment, Western Ross Sea, George V Land and Prydz Bay;
Klages et al. 2017). Moreover, all eight macroalgal distributions include offshore
peri-Antarctic Islands located south of the APF, such as the South Orkney Islands,
South Sandwich Islands and South Georgia (Wiencke and Clayton 2002; Wiencke
et al. 2014; Griffiths and Waller 2016). We then cannot rule out a recolonization of
the Antarctic coasts from these more northern areas. Supporting this idea, a study
based on molecular markers allowed the recent discovery of one cryptic species of
the brown alga Adenocystis utricularis endemic to South Georgia (Fraser et al.
2013). The authors related this result to a persistence of Adenocystis in local refu-
gium along the island coasts during the LGM (Fraser et al. 2013). Antarctic samples
were not included in the study of Fraser et al. (2013) and the level of genetic diver-
gence between peri-Antarctic and Antarctic Adenocystis remains to be estimated in
order to test for a possible recolonization of the Antarctic shelf from a South Georgia
glacial refugium. However, ice coverage during the LGM strongly impacted South
Georgia (White et al. 2018) and coastal glacial refugia could have been as scarce in
the offshore peri-Antarctic Islands as at the margins of the Antarctic shelf itself
(Fig. 6.1). Indeed, the complete eradication of populations of another brown alga,
the intertidal/shallow subtidal Durvillaea antarctica, from the coasts of most peri-
Antarctic islands (in particular in Macquarie Island, Falkland Islands, South
Georgia, Marion Island and Kerguelen Islands) during the LGM has been estab-
lished (Fraser et al. 2009, 2012).
Unfortunately, in order to locate glacial refugia in the region, we will need more
variable genetic markers and a much better sampling of the coasts of the Antarctic
shelf (i.e. Alexander Island, Western Ross Sea, George V Land and Prydz Bay; see
Griffiths and Waller 2016), adjacent islands of the maritime Antarctic and offshore
peri-Antarctic Islands south of the APF where populations of macroalgae have been
reported (in particular, South Orkney Islands, South Sandwich Islands and South
Georgia, Bouvet Island, Heard Island and Balleny Islands). Sampling localities that
could have been less affected by ice scour during the Last Glacial Maximum should
be a priority.
The proposed scenario of one unique in situ refugium in Antarctica contrasts
with history of glacial perturbations in Arctic macroalgae. Indeed, based on patterns
of genetic diversity and distribution of private haplotypes, the existence of various
marine glacial refugia has been proposed in the Northern Hemisphere for these
organisms (Maggs et al. 2008; Provan and Bennett 2008; Neiva et al. 2016). Less
severe cooling in the Arctic than the Antarctic could explain, in part, these differ-
ences between hemispheres (Pointing et al. 2015). Moreover, Arctic macroalgae
distribution during glacial cycles could have shifted along continuous coastlines
spanning a huge latitudinal gradient (Fraser et al. 2012; Neiva et al. 2016), while no
such opportunity was available for Antarctic species, bounded by the deep water of
the Southern Ocean, leading to a more thorough extinction along the Antarctic
coastline during the LGM.
6.5.3 P
ostglacial Recolonization: Widespread Haplotypes
Drifting Around Antarctica?
Apart from their very low genetic diversity, all eight algae under study present a
common striking characteristic: one or a few haplotypes were encountered in all
localities even when situated hundreds or even thousands of kilometres apart
(Figs. 6.3 and 6.4). For all six red algae and for the green alga M. hariotii, the most
common haplotype was observed from King George Island in the South Shetland
Islands down to Marguerite Bay, a sampling point located along the central part of
the WAP (Figs. 6.3 and 6.4). These common haplotypes are spread over more than
450 km of coast and within two distinct biogeographic subregions (the South
Shetland Islands and the WAP; Linse et al. 2006; Spalding et al. 2007; Terauds et al.
2012). Shared haplotypes have been observed even between the WAP and South
Orkney Island, reaching distances greater than 1600 km, in the red alga G. skotts-
bergii (same Cox2–3 haplotype from Marguerite Bay to the South Orkney Islands;
Billard et al. 2015). The same pattern is observed in I. cordata for which the same
COI haplotype has also been sequenced along the WAP and South Orkney Island
(Guillemin M-L. unpublished data, no genetic differences detected between the
most common haplotype encountered along the WAP and three individuals from
South Orkney Island sequenced for 632 pb). For H. grandifolius, the distribution of
the unique COI haplotype encountered in our study zone could be extended to Terre
Adelie, in a sampling site located almost on the other side of the Antarctic continent
(sequence from Silberfeld et al. 2010). Himantothallus grandifolius is then the first
register of a non-buoyant species displaying a true Antarctic circumpolar distribu-

tion supported by genetic data. Complete circum-Antarctic distribution has been
described for other seaweeds, including common species of brown (Desmarestia
menziesii), green (M. hariotii and Urospora penicilliformis) and red (I. cordata,
P. cartilagineum, P. decipiens, Phyllophora antarctica and Phycodrys antarctica)
macroalgae (Wiencke et al. 2014). However, for these species, all sequences avail-
able to date have been obtained for specimens located in the South Shetland Islands
and/or the WAP (Olsen et al. 1993; Peters et al. 2000; Hommersand et al. 2009;
Dubrasquet et al. 2018; Ocaranza-Barrera et al. 2019). One could thus wonder if
other common Antarctic macroalgae species will present the same pattern as
H. grandifolius and samples should be gathered from the Western Ross Sea, Terre
Adelie and Prydz Bay and sequenced in order to test this hypothesis.
In contrast to what was reported for pelagic species or benthic species exhibiting
extensive dispersal by planktonic stage (Lange et al. 2002; Raupach et al. 2010;
Sromek et al. 2015; Soler-Membrives et al. 2017; Caccavo et al. 2018), we believe
that the presence of widespread haplotypes in our data sets clearly reflects Antarctic
macroalgae past glacial demographic histories but not necessarily contemporary
high gene flow. Benthic macroalgae free-living stages (i.e. for all species except
buoyant ones, Macaya et al. 2016, also see chapter by Macaya et al. 2020 in this
volume) are generally extremely restricted to short-lived gametes and spores that
quickly sink a few meters, at most, from thalli of origin (Valero et al. 2011).
However, in these organisms, large-scale spread of haplotypes was commonly
related to strong genetic drift and allelic surfing at species’ leading edges during
postglacial range expansions or after transoceanic colonization (Maggs et al. 2008;
Provan and Bennett 2008; Montecinos et al. 2012; Fraser et al. 2013; Guillemin
et al. 2014; Neiva et al. 2016). Non-buoyant macroalgal species, for which both
population genetic and phylogeographic data sets are available, show well this dis-
crepancy with, on the one hand, the presence of haplotypes distributed over thou-
sands of kilometres in area of recent colonization and, on the other hand, current
reproduction and recruitment occurring at a very local scale (in Agarophyton [for-
mer Gracilaria]: Guillemin et al. 2008, 2014, in Fucus: Neiva et al. 2016; Jueterbock
et al. 2018). Exceptional events of thalli rafting on strong oceanic currents and colo-
nizing new areas when depleted of abundant algal coverage (Waters et al. 2013)
have been advanced to explain these patterns (Montecinos et al. 2012; Fraser et al.
2013; Guillemin et al. 2014; Neiva et al. 2016). In order to test for actual gene flow
between studied populations of macroalgae, more variable genetic markers, such as
microsatellites or SNPs (i.e. single nucleotide polymorphism), will be needed.
Indeed, highly variable microsatellite loci revealed a clear regional substructure of
populations in Phaeocystis antarctica, a brown micro algal planktonic species for
which no clear phylogeographic patterns were described before around Antarctica
using nuclear and plastid sequences (Lange et al. 2002; Gäbler-Schwarz et al. 2015).
Even if none of the study models possess floating structures, large amounts of all
eight species can easily be found cast ashore after storm events, including huge
adult specimens of H. grandifolius (authors pers. obs.). Passive transport of detached
fronds could therefore play a major role in Antarctic non-buoyant macroalgae
long-distance dispersal, a mechanism most probably facilitated by the strong oce-

anic currents in the region (Loeb 2007). Classically, the circumpolar current (ACC,
see Fig. 6.1) was reported as a structuring force in the Southern Ocean and has been
proposed to be the main connecting current between populations of marine organ-
isms located around Antarctica (e.g. Fraser et al. 2009; Soler-Membrives et al.
2017). For the red algae G. skottsbergii and I. cordata, fronds rafting on the ACC
could easily explain the spread of the most common haplotypes between localities
of the South Shetland Islands, the Antarctic Peninsula and even South Orkney Island
(Billard et al. 2015; Guillemin et al. 2018; Ocaranza-Barrera et al. 2019). Indeed,
the ACC flows northeastward from the Bellingshausen Sea through the South
Shetland Islands and the South Orkney Islands, before entering the Scotia Sea (Loeb
2007). However, since it deflects from the Antarctic coasts during most of its jour-
ney around the continent (from the Weddell Sea to Prydz Bay and the Western Ross
Sea, see Loeb 2007), rafting on the ACC does not easily explain the presence of the
same COI haplotype in Terre Adelie and the Antarctic Peninsula for H. grandifolius.
It is highly probable that fronds transport between these two distant regions was
promoted by the Antarctic Costal Current (ACoC), a current that flows in a counter-
clockwise motion and located near the coast of the Antarctic shelf (Loeb 2007). The
importance of transport by the ACoC was also proposed to be at the origin of the
widespread haplotypes observed in marine species with distribution restricted to the
shallow waters of the shelf, as in the sea urchin S. neumayeri (Díaz et al. 2018).
Remarkably, a study following the track of icebergs around Antarctica shows that a
large majority do travel counterclockwise around the continental shelf and that the
ACoC can very easily connect Terre Adelie with the tip of the Antarctic Peninsula
(Stuart and Long 2011).
Macroalgae are very important primary producers and ecosystem engineers in

Antarctic coastal ecosystems, serving as food for herbivores and detritivores and
providing habitat for many associated organisms (see Chaps. 15 and 16 of this
book). Even if these species have developed remarkable adaptations to cope with
the high level of disturbances characteristic of Antarctic swallow depth (Wiencke
et al. 2007, 2014), they could be highly vulnerable to actual threats intensifying in
the region as global warming, pollution and introduction of invasive species. As
seawater temperature rise around Antarctica, a trend particularly noticeable along
the Antarctic Peninsula, extent and duration of sea ice coverage decline and glaciers
are in retreat (Cook et al. 2016). At first sight, this scenario seems highly favourable
for Antarctic macroalgae that can rapidly colonize these newly deglaciated areas
(Quartino et al. 2013; also see chapter by Quartino et al. 2020 in this volume).
Indeed, in the Arctic, the long-term study of Kortsch et al. (2012) shows that
decrease in sea ice cover can produce rapid shift in marine communities from ben-
thic habitats dominated by calcareous algae and sea anemones to dense beds of
fleshy, habitat-forming macroalgae. However, climatic changes are also associated

with higher probability of ice sheet collapse and iceberg calving. Scouring by these
drifting icebergs, which can even get stuck and ground in polynyas, may have a
highly detrimental effect on macroalgae beds (Clark et al. 2015). Climate changes
have also been related to possible alteration in large-scale ocean circulation and
gyre and eddy kinetic in the Southern Ocean, leading to breaches in the dispersal
barriers (APF and ACC) established since the Eocene/Oligocene in the region
(Barker and Thomas 2004; Fraser et al. 2018). When coupled with the intensifica-
tion of maritime transport (linked to both touristic and scientific activities) between
Antarctic and sub-Antarctic provinces, these oceanic changes could lead to an
increase in propagule pressure and introduction of sub-Antarctic macroalgae spe-
cies in the Antarctic waters. To the date, only one green alga (i.e. Ulva intestinalis)
has been reported as an established introduced alien species in the South Shetland
Islands, probably arriving as fouling on the hull of a visiting vessel (Clayton et al.
1997). However, macroalgae highly successful in recolonising sub-Antarctic coasts
after glacial retreat have recently been reported to recurrently reach the Antarctic
coasts as cast ashore living thalli (i.e. Durvillaea antarctica, Fraser et al. 2018; also
see chapter by Macaya et al. 2020 in this volume). The capacity of Antarctic mac-
roalgae to withstand competition from sub-Antarctic invaders has not been studied
yet. Nonetheless, Antarctic macroalgae are organisms highly adapted to the local
stenothermal environment. Studies report temperature optima between −2 °C and
10 °C for most Antarctic species with limitation or even failure in growth or game-
togenesis at temperature higher than 5 °C in G. confluens, G. skottsbergii, P. carti-
lagineum and Desmarestia antarctica (Wiencke et al. 2007; Wiencke et al. 2014). In
the actual context of rapid temperature increase, populations of sub-Antarctic or
even more temperate colonizers may then more easily settle along the Antarctic coasts.
Antarctic macroalgae were clearly able to cope with changes related to the cool-
ing and then freezing of the Southern Ocean waters and have survived Quaternary
glacial perturbations in situ. However, our study shows that maximal glacial events
have led to mass extinction in all eight model species, whatever their taxonomic
divisions. Will these species be able to keep pace with the current rapid environmen-
tal fluctuations? Genetic adaptation could be key in enhancing resistance and resil-
ience to climatic changes and a high level of genetic diversity has classically been
related to high population fitness, resilience and future adaptability (Reed and
Frankham 2003; Jump and Peñuelas 2005). Due to strong bottleneck during the
LGM, standing genetic diversity in Antarctic macroalgae populations seems to be
extremely depleted and an adaptive response of Antarctic algae populations to
future changes could be limited. Nevertheless, recent studies on the brown seaweed
Sargassum muticum show a complete absence of genetic diversity in all populations
of the invaded range when tested using mitochondrial sequences or even nuclear
microsatellites and only a very low level of diversity when using more than 8000
SNPs (Cheang et al. 2010; Le Cam et al. 2019). Rapid and successful invasion of
Europe and the USA was clearly not impaired by the extremely low genetic diver-
sity in S. muticum. In order to predict the possible outcome of future climatic
changes on macroalgae populations, it is now essential to use more variable genetic
markers in order to detect a subtle genetic structure along the Antarctic coasts and
point out restricted regional or local genotypes that could be of interest (see results
using SNPs in Le Cam et al. 2019) and to experimentally test for existence and
extent of phenotypic plasticity/acclimatization potential (a mechanism that can
potentially buffer negative effects of climate change long enough to allow for popu-
lation adaptation; Jump and Peñuelas 2005) and potential for an in situ adaptive
response to climate change of these organisms.
Acknowledgments Funding by Instituto Antártico Chileno (INACH) T_16-11 and RG_15-16

and the Centro FONDAP IDEAL no. 15150003 is gratefully acknowledged. At King George
Island, sampling of Monostroma hariotii and Himantothallus grandifolius was done with the help
of the Project Anillo ART1101 from Conicyt-Chile. The authors thank P. Brunning, J. L. Kappes,
T. Heran, Y. Henriquez and L. Vallejos for their help in the field. The authors would also like to
thank the Chilean Navy (especially the captain and crew of the ships Almirante Oscar Viel and
Lautaro), the staff from the Chilean Army in the O’Higgins base and the Air Force of Chile (FACh)
for the logistic support of our fieldwork in Subantarctica and Antarctica.
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Part III
Physiology, Productivity and
Environmental Reponses
Chapter 7
Underwater Light Environment
of Antarctic Seaweeds
Pirjo Huovinen and Iván Gómez
Abstract Antarctic seaweeds are highly shade-adapted organisms, which can pho-
tosynthesize under very dim light. This remarkable characteristic allows them colo-
nizing over 30 m depths and surviving extended dark periods during the polar
winter. On the other hand, they are well equipped to cope with high light stress,
which points to a trade-off between shade adaptation and efficient UV stress toler-
ance. Optical properties of water determine both the underwater light climate for
photosynthesis and the risk of seaweeds for UV exposure in their habitats. Thus,
understanding the natural (spatial, temporal) and anthropogenic-driven changes in
spectral transparency of water and factors governing it is fundamental in evaluating
the state of seaweeds under current and future environmental scenarios. In the pres-
ent chapter the aspects related to the optical properties determining the underwater
habitat of Antarctic seaweeds are summarized, along with the potential changes in
water optics as a result of climate change, ozone depletion and other environmental
and emerging threats, and their interactions.
Keywords Antarctic costal waters · Light climate · Ozone depletion ·

Photosynthesis · Pollution · UV radiation · Water column optics
7.1 Introduction
Aquatic organisms in the polar regions have adapted to survive wide seasonal
changes in the light field of their habitats (McMinn and Martin 2013). The polar
winter accompanied by ice cover leads to extended periods of dim light conditions
or even darkness (Berge et al. 2015), while in spring-summer, water column receives
increasing levels of solar radiation, which is furthermore enhanced after icebreak
P. Huovinen (*) · I. Gómez

Instituto de Ciencias Marinas y Limnológicas, Facutad de Ciencias, Universidad Austral de
Chile, Valdivia, Chile
e-mail: pirjo.huovinen@uach.cl; igomezo@uach.cl

https://doi.org/10.1007/978-3-030-39448-6_7
132 P. Huovinen and I. Gómez
and also during episodes of ozone depletion leading to higher risk of UV exposure
during austral spring (Frederick et al. 1989; Neale et al. 1998). In order to withstand
such widely changing conditions, Antarctic seaweeds are characterized by remark-
able photobiological adaptations to grow and photosynthesize at irradiances as low
as 10 μmol m−2 s−1, allowing them surviving extended dark periods during winter
and colonizing over 30 m depths. On the other hand, they present efficient mecha-
nisms to tolerate high UV stress (Gómez et al. 2009; Karsten et al. 2009; Gómez and
Huovinen 2015).
Underwater light climate is governed by the optical properties that define the
depth limits for photosynthesis and hence the vertical distribution of seaweeds as
well as the risk for exposure to detrimental UV levels in Antarctic coastal waters
(see Chap. 11 by Gómez and Huovinen). Thus, understanding the natural (temporal,
spatial) and anthropogenic-driven changes in water optics and factors controlling it
is essential, not only in evaluating aquatic primary production and UV risk in
aquatic habitats (Holm-Hansen et al. 1993; Cullen and Neale 1994) but also for
predictions of the status of these ecosystems under current and future scenarios of
global climate change (Vincent and Belzile 2003). The knowledge on light attenua-
tion and the potential impact, e.g., of glacier-derived freshwater input, are also
needed in order to explain the spatial variation in primary production and carbon
fluxes with far-reaching implications for the benthic communities with a potential
to modify the biogeochemical gradients in the whole Antarctic coastal system (see
review by Sulzberger et al., 2019, and Chap. 8 by Quartino et al.). In the present
chapter, we summarize the aspects related to the optical characteristics determining
the underwater habitat of Antarctic seaweeds with implications for their photobiol-
ogy, along with the potential changes in water optics as a result of interactions with
climate change factors and other environmental and emerging threats.
7.2 Optics of Antarctic Coastal Waters
7.2.1 Light in Aquatic Environment
In natural waters, sunlight may be either absorbed or scattered. Principles of under-

water optics have been described and reviewed by Hargreaves (2003), Kirk (2011),
and Mobley (2015). In summary, the main components responsible for light absorp-
tion have been described: (1) water itself, (2) colored dissolved organic matter
(CDOM), (3) living photosynthetic organisms (phytoplankton), and (4) nonliving
organic and inorganic particulate material. Pure water absorbs and thus attenuates
light increasingly in red (>550 nm) and infrared (IR) bands, while absorption by
CDOM (mainly yellow dissolved humic substances with diverse intrinsic proper-
ties, e.g., molecular weight, origin, age; see Hessen and Tranvik, 1998) increases
strongly towards blue and UV bands. Phytoplankton attenuates photosynthetically
active radiation (PAR) through their light-absorbing photosynthetic pigments and
7 Underwater Light Environment of Antarctic Seaweeds 133
also by causing scattering of light as a result of their particulate form. Nonliving

particulate matter attenuates light strongly through scattering, whereas their light
absorption (increasing towards blue and UV wavelengths) is weaker (for details, see
Hargreaves 2003, Kirk 2011 and Mobley 2015).
Underwater light climate varies strongly in different types of water bodies
according to their inherent optical properties (IOPs), i.e., those describing aquatic
medium (such as absorption coefficient and volume scattering function) indepen-
dent of the light field (thus measurable in a water sample). Together with IOPs,
environmental conditions (e.g., radiance, solar angle, waves) partially influence
apparent optical properties (AOPs, such as reflectance and diffuse attenuation coef-
ficient), which can be used to describe water optics through in situ measurements
(see Kirk 2011; Mobley 2015). In an optically homogeneous water column, the
downward irradiance (Ed) diminishes in an exponential manner with depth (z); thus
diffuse attenuation coefficient for downward irradiance (Kd) can be calculated
according to Kirk (2011) as:
K d = −dln Ed ( z,λ ) / dz

Consequently, a depth where 1% or 10% of the subsurface irradiance is available
can be estimated from Kd as:
=zz1 4=
.6 / K d and zz10 2.3 / K d

The upper water column down to a depth where 1% of PAR remains is generally
defined as the euphotic zone, which can range from the upmost water layer to hun-
dred meters. For example, in saline-alkaline lakes and turbid estuaries, z1% can reach
less than half and one meter, respectively (Oduor and Schagerl 2007; Coljin et al.
1987), while in some oceanic areas (e.g., Sargasso Sea in the Atlantic and the coast
of Hawaii in the Pacific), light can penetrate more than hundred of meters (Tyler
1975; Bienfang et al. 1984). Penetration of UV wavelengths in the water column
can also range widely, from few centimeters (e.g., in small humic lakes; Scully and
Lean 1994; Huovinen et al. 2003) to dozens of meters in highly transparent oligo-
trophic waters (e.g., z1% around 40 m in Sargasso Sea; Smith and Baker 1979).
7.2.2 Light Climate in Antarctic Waters
An extensive study around the Antarctic Peninsula in mid-1980s by Mitchell and

Holm-Hansen (1991) revealed euphotic zone of approximately 75 m in the offshore
waters in Drake Passage, while in coastal areas PAR attenuated to 1% within the
upper 15 m. The clear open water areas were characterized by negligible sediment
load and terrigenous material, which can be explained by the scarcity of terrestrial
vegetation (the ice-free landscape is largely dominated by tundra-type vegetation
like moss and lichen; Convey 2010) and hence a low contribution of allochtonous
organic matter from the catchment. In contrast, shallow near-shore waters around
the South Shetland Islands with glaciers showed high turbidity due to meltwater
runoff and related increase of organic matter decreasing transparency (Mitchell and
Holm-Hansen 1991). In fact, long-term measurements from Potter Cove (King
George Island, South Shetland Islands) indicate that increased light attenuation due
to strong sedimentation in areas impacted by glacier retreat is modifying the growth
conditions for seaweeds and their upper distribution limits (Deregibus et al. 2016;
see also Chap. 9 by Deregibus et al.). Also in Fildes Bay, another well-studied area
in King George Island, biomass of subtidal seaweeds displays a glacier-related gra-
dient (Valdivia et al. 2015). In Bransfield and Gerlache Straits, seasonal variation in
light penetration was observed: in January, light was strongly attenuated (z1% around
4.6 m based on Kd (488 nm)) in coastal areas due to massive phytoplankton blooms,
which disappeared by February–March leading to deeper (over 30 m) light penetra-
tion, reducing also the spatial (onshore-offshore) gradient in water transparency
(Mitchell and Holm-Hansen 1991). Strong spatial heterogeneity was also observed
by Figueroa (2002) with euphotic zone ranging 9–58 m in open waters of Gerlache
and Bransfield Straits. On the other hand, in Drake Passage where no blooms
occurred, the waters remained clear (z1% 46–76 m based on Kd (488 nm)) from
December to March (Mitchell and Holm-Hansen 1991). In coastal waters of Fildes
Bay, z1% PAR ranging 19–34 m has been reported (Huovinen et al. 2016) (Figs. 7.1
and 7.2). In Potter Cove, higher water transparency in November–December (z1%
PAR over 25 m) has been shown to decrease in January–February, light attenuating
already in the upper meters in areas influenced by meltwater (Klöser et al. 1993).
Here, in winter and early spring, light attenuation is mainly regulated by phyto-
plankton, while towards summer, particulate matter from increasing meltwater con-
tributes strongly (up to 47%) (Schloss and Ferreyra 2001).
During the open water season, relatively high UV transparency has been mea-
sured in Fildes Bay (Huovinen et al. 2016), although spatial variation between sites
and with depth is observed (Fig. 7.1). UV (z10%) penetration has been shown to range
here from approximately 3 to 6 m for UV-B305nm to 8 to 19 m for UV-A395nm (Huovinen
et al. 2016). Based on theoretical estimations (tropospheric ultraviolet and visible
(TUV) model) for summer solstice and mean Kd of the bay area, sunlight levels at
z10% could reach 0.13 W m−2 for UV-B (at 5 m), 4.4 W m−2 for UV-A (at 10 m), and
170 μmol m−2 s−1 for PAR (at 15 m) (Fig. 7.2). In Potter Cove, penetration depth
(z10%) of up to 8 m has been reported for UV-B radiation. Subsurface (10 cm) levels
of up to 1.5 and 26 W m−2 of UV-B (280–320 nm) and UV-A (320–400 nm), respec-
tively, were measured. Corresponding levels at 2 m depth were decreased to 0.26
and 8.6 W m−2. PAR levels at corresponding depths were 1178 and 515 μmol m−2 s−1
(Quartino et al. 2005; Zacher et al. 2007a). It should be noted that these authors
considered 320 nm as the limit between UV-B and UV-A bands, resulting in mark-
edly higher UV-B levels than when limiting the band to 315 nm (see Huovinen et al.
2006). Maximal penetration depths (z10%) for UV-B (305 nm) and UV-A (340 nm)
of 8 m and 11 m, respectively, have been reported for Bransfield and Gerlache
Straits and Palmer Station (Helbling et al. 1995; Figueroa 2002). In Bellinghausen
Fig. 7.1 Fildes Bay (King George Island, Maritime Antarctica (a). Variation of spectral irradiance
with depth in Fildes Bay based on measurement with the hyperspectral radiometer RAMSES-
ACC2-UV–vis (Trios Optical Sensors, Oldenburg, Germany) (b). Spatial (with depth and dis-
tance) variation of Kd at 395 nm (m−1) determined at 1 m intervals from measurements with the
radiometer PUV-2500 (Biospherical Instruments Inc., USA) in six areas of Fildes Bay and visual-
ized with Ocean Data View software (Schlitzer R., Ocean Data View, odv. Awi.de, 2015) (Adpated
from Huovinen et al. 2016) (c)
Sea, even higher penetration depths for UV-B (z10% 310 nm around 12 m) and UV-A
(340 nm around 17 m) have been measured. Here, UV-B radiation could be detected
down to 60–70 m (Smith et al. 1992).
Potential for DNA damage at depths ranging 3.5–16 m (based on z10% DNA
weighted irradiance) have been reported for Antarctic waters (Huot et al. 2000;
Buma et al. 2001). Under ozone hole the effective UV-B penetration depth was
found to increase by 7 m (Smith et al. 1992). For the estimations on net UV impact
on aquatic organisms, knowledge on spectral attenuation is needed as it varies with
depth (see Figs. 7.1b and 7.2), and shifts in underwater irradiance spectra have
implications for repair and other processes that depend on spectral light composi-
tion (Neale 2000; Williamson et al. 2001). For example, a higher ratio (mean around
1.0) between z10% 305 and 340 nm has been reported in Antarctic waters under
Fig. 7.2 Estimation of irradiance levels at different water depths, based on irradiance levels during
summer solstice in Fildes Peninsula (62°S, 50°W) derived from Tropospheric Ultraviolet and
Visible (TUV 5.3; Madronich and Flocke (1999)) model (https://www2.acom.ucar.edu/modeling/
tropospheric-ultraviolet-and-visible-tuv-radiation-model) and on Kd values (mean of 305 and
313 nm for UV-B; mean of 320, 340, 380, and 395 nm for UVA) of the bay area (data from
Huovinen et al. 2016). Penetration depths z1% (solid arrows) and z10% (open arrows) are indicated.
Representative seaweeds for different depths are shown. (Photos by Ignacio Garrido except
Urospora by Iván Gómez)
ozone hole conditions than in other oceanic areas (without ozone depletion) (mean
0.54) (Tedetti and Sempéré 2006).
In polar regions, seasonal ice cover plays an important role in governing the
underwater light climate (Lesser et al. 2004; Fritsen et al. 2011; Taskjelle et al.
2016). In McMurdo Sound (Ross Sea), 0.16% of incident irradiance (mainly blue-
green band) was transmitted through a 2-m-thick ice (Schwarz et al. 2003) and
0.05% (0.2–0.6 μmol m−2 s−1) reached bottom (23 m) (Robinson et al. 1995). Under
ice cover, water was highly transparent with Kd for PAR 0.09 m−1 (Schwarz et al.
2003). In scenarios of global climate change, the importance of sea-ice duration has
been highlighted and is regarded, together with light penetration and sedimentation,
a major driver structuring the shallow Antarctic benthos (Clark et al. 2017). Thinner
ice cover and its shorter duration results in enhanced exposure to solar radiation for
extended periods, which can bring consequences for photosynthesis (Runcie and
Riddle 2007)‚ zonation patterns of seaweeds (Campana et al. 2009; Clark et al.
2017) and increase UV damage (Fountoulakis et al. 2014). Timing of ice breakup
may be crucial for the establishment of canopy-forming seaweed communities in
spring (Johnston et al. 2007). When large brown algae are established, their cano-
pies can markedly reduce light levels reaching their understory species, and it can
be also altered by tidal fluctuations (Huovinen and Gómez 2011). In Antarctic
coastal waters, the presence of large brown algae growing at depths as shallow as
5 m can affect considerably the incident irradiance at deeper locations where sea-
weeds coexist with abundant populations of understory species, especially red algae
(Klöser et al. 1996; Gómez et al. 2019; see also Chap. 11 by Gómez and Huovinen).
7.3 A
daptations of Antarctic Seaweeds to Extreme
Light Conditions
7.3.1 Photosynthetic Shade Adaptation of Antarctic Seaweeds
The strong seasonality and turbidity of coastal waters (Zacher et al. 2009) imply
severe constraints for photosynthesis of Antarctic seaweeds (see Wiencke et al.
2009). They can overall be characterized by very low requirements of light and
constitutively high efficiency of photosynthesis, allowing them colonizing deep
habitats with low light availability and coping with periods of darkness (reviewed
by Gómez et al. 2009). For example, some Antarctic crustose red algae (corallines)
in the Ross Sea live permanently under ice cover and remain in darkness for several
months in winter (Schwarz et al. 2005). In fact, shade adaptation is considered a
metabolic prerequisite that allows survival under wide gradient of light (Weykam
et al. 1996; Huovinen and Gómez 2013; Gómez and Huovinen 2015).
Photosynthetic adaptations to cope with low light availability allow Antarctic
seaweeds supplying their light requirements over a broad depth distribution (Gómez
et al. 1997). The growth and photosynthesis especially of the endemic brown sea-
weeds has been shown not to be limited even at deep locations close to 30–40 m
(Drew 1977; Weykam et al. 1996; Schwarz et al. 2003). Although some species
from King George Islands collected at shallow waters displayed higher saturated net
photosynthesis (Pmax) than species from deeper sites, their photosynthetic efficiency
(α) and light demands for photosynthesis (Ek) did not vary with depth (Weykam
et al. 1996). These photosynthetic characteristics have been confirmed more recently
with chlorophyll fluorescence techniques (Huovinen and Gómez 2013). Also photo-
synthetic efficiency (αETR) has been found to be high along the depth gradient
(0–30 m) (Gómez and Huovinen 2015) in spite of relatively high water transparency
(PAR at 20 m depth around 50 μmol m−2 s−1) (Huovinen et al. 2016; Fig. 7.2).
Despite their wide vertical distribution (from 5 m downwards), lower distribution
limit (close to 30 m) of Antarctic seaweeds such as Desmarestia mensiezii, D. anceps,
Palmaria decipiens, and Gigartina skottsbergii coincides with the depth of
compensation irradiance level (Klöser et al. 1996; Gómez et al. 1997; Deregibus
et al. 2016). Also, although it can be found at depths close to 5–10 m, Himantothallus
grandifolious starts to dominate only at depth below 30 m when substrate and com-
petitive balance with other large Desmarestiales, e.g., D. anceps, are favorable
(Zielinski 1990; Klöser et al. 1996). Thus, the vertical distribution patterns of
Antarctic seaweeds cannot be explained by light limitation alone, but rather in com-
bination with other biotic (e.g., herbivory, competition) and abiotic (e.g., substrate
characteristics, ice-induced perturbations, water movement) factors (Klöser et al.
1996; Iken et al. 1998; Amsler et al. 2011; see Chap. 13 by Valdivia and Chap. 17
by Amsler et al.).
7.3.2 Tolerance of Antarctic Seaweeds to High PAR and UV
Antarctic coastal waters are often characterized by high water transparency with
light (PAR) penetration (z1%) ranging 19–34 m (Huovinen et al. 2016; Figs. 7.1 and
7.2). In coastal waters of King George Island, PAR has been found to penetrate
down to 40 m depth (Klöser et al. 1993), and levels around 50 μmol m−2 s−1 have
been measured at 30 m (Gómez et al. 1997). This contrasts with the light conditions
in some Arctic near-shore waters, e.g., in the Beaufort Sea with muddy bottoms and
estuarine characteristics where PAR penetration is markedly lower (z1% 3–11 m; in
offshore waters >4.6 m) (Dunton et al. 2009). After Antarctic icebreak in spring-
summer, seaweeds experience sudden increase of underwater light; however, water
optics may present strong variation due to turbidity, e.g., from glacier melting or
freshwater runoff (Klöser et al. 1993; Deregibus et al. 2016; see Chap. 9 by
Deregibus et al.). Under these conditions, seaweeds exhibit a suite of physiological
mechanisms to cope with high levels of solar radiation. One of them is dynamic
photoinhibition, downregulation of photosynthesis under high solar radiation, dis-
sipating excess absorbed energy as heat in photosystem II (PSII) (Adams III et al.
2006). This protective mechanism has been reported in Antarctic seaweeds exposed
to natural solar irradiation, showing decreased photosynthetic activity around solar
noon followed by recovery towards evening (Hanelt et al. 1994). Thus, the capacity
to withstand high solar radiation allows these shade-adapted organisms thriving also
at environments where light levels exceed their requirements for saturation of pho-
tosynthesis, such as in intertidal and shallow waters (Huovinen and Gómez 2013;
Gómez et al. 2019).
Together with high PAR levels, seaweeds can also be exposed to harmful levels
of UV radiation in their habitats (Huovinen and Gómez 2013, Huovinen et al. 2016;
Figs. 7.1 and 7.2). Deleterious effects of UV-B radiation on aquatic organisms,
including seaweeds, are widely recognized (reviewed by Holm-Hansen et al. 1993;
Vincent and Neale 2000; Karsten et al. 2009; Burritt and Lamare 2016). UV-B radi-
ation can directly affect cellular components (e.g., nucleus, chloroplast), their ultra-
structure and processes, as well as target important biomolecules, such as DNA
(leading, e.g., to formation of cyclobutane dimers (CPDs) and 6–4 photoproducts
that interfere with replication) (Mitchell and Karentz 1993), proteins (e.g., D1 pro-
tein in PSII), and photosynthetic pigments (Gerber and Häder 1992). It can also
interfere with uptake of nutrients (Döhler et al. 1991) and metabolism of fatty and
amino acids (Goes et al. 1994, 1995). It may cause oxidative stress by inducing
production of reactive oxygen species (ROS, such as singlet-oxygen, hydroxyl, and
superoxide radicals) that are damaging to biomolecules and can cause, e.g., peroxi-
dation of lipids (Bischof and Rautenberger 2012). ROS may also be formed in
aquatic environment when UV interacts with DOM (Kieber et al. 2003) (see also
Sect. 7.4.1). Disturbance or damage to important cellular components and biomol-
ecules can impair biochemical and physiological processes, such as photosynthesis
(through effect on pigments, enzymes, photosynthetic apparatus, etc.), growth, and
reproduction (reviewed in Bischof et al. 2006).
The magnitude of final harmful impact depends on the balance between pro-
duced damage and the efficiency of protective, e.g., UV-shielding compounds such
as mycosporine-like amino acids (MAAs) in red algae and phlorotannins in brown
algae (see Chap. 18 by Gómez and Huovinen) and repair (e.g., light-induced repair
of DNA damage involving photolyase enzyme) mechanisms to mitigate it (Karentz
et al. 1991; Mitchell and Karentz 1993; Vincent and Roy 1993; Nuñez-Pons et al.
2018). Antioxidants (e.g., carotenoids, phlorotannins, enzymes such as superoxide
dismutase and glutathione peroxidase) furthermore serve as defense mechanism
through ROS scavenging (Bischof and Rautenberger 2012). Also, downregulation
of PSII (dynamic photoinhibition) has been proposed as a protective mechanism,
not only against high PAR, but also against UV radiation, contributing to the physi-
ological tolerance of seaweeds (Bischof et al. 2006).
Early life stages of seaweeds with a thinner wall are more vulnerable to UV dam-
age than multicellular adult stages. Marked DNA damage and physiological stress
has been reported in propagules of Antarctic seaweeds upon UV exposure (Roleda
et al. 2006; Zacher et al. 2007b), although they also show capacity for recovery
(Navarro et al. 2019) and UV-screening compounds (Roleda et al. 2006; see also
Chap. 10 by Navarro et al.). Furthermore, adult thalli of intertidal species display
high tolerance to light stress as they have to cope with high levels of solar radiation,
especially during low tidal levels (Cruces et al. 2013). Here, dynamic photoinhibi-
tion seems to play a key role as a protective mechanism (Hanelt et al. 1994).
Interestingly, high photosynthetic tolerance has also been reported for subtidal spe-
cies that are not exposed to high UV levels in their habitat (deeper than 20 m)
(Huovinen and Gómez 2013). Especially large endemic brown algae have shown
marked UV stress tolerance over their broad vertical distribution (5–30 m), which
has been related to efficient morph-functional mechanisms and constitutively high
levels of phlorotannins (Gómez and Huovinen 2015; Flores-Molina et al. 2016;
Gómez et al. 2019; see also Chaps. 11 and 18 by Gómez and Huovinen). Overall,
UV sensitivity of seaweeds at their different life stages is considered one of the
ecologically important factors defining their vertical zonation and distribution limits
(Bischof et al. 1998; Wiencke et al. 2000, 2006; see Chap. 10 by Navarro et al.). In
contrast to short-term laboratory experiments, organisms in their natural habitats are
influenced by complex interactions of multiples environmental factors, which may
mitigate or potentiate the adverse impact of UV radiation (see Sect. 7.4). For exam-
ple, a global field study examining UV impact on marine benthic community level
found that any effect disappeared after few months during succession (Wahl et al.
2004). However, recent reports based on meta-analyses point to overall negative UV
impact at all trophic levels (summarized by Williamson et al. 2019).
7.4 C
onsequences for Light Field Under Current
and Future Threats
7.4.1 Ozone Depletion
The deleterious effects of solar radiation are mainly associated with the UV wave-
bands, i.e., UV-C (100–280 nm), UV-B (280–315 nm), and UV-A (315–400 nm)
radiation, with greater effectiveness for biological damage occurring towards
shorter wavelengths (Setlow 1974; Cullen et al. 1992). The most damaging UV-C
waveband is absorbed by oxygen and ozone in the atmosphere thus not reaching the
earth’s surface. On the other hand, UV-A waveband is not absorbed by atmospheric
ozone, while UV-B waveband is partially absorbed and its levels are affected by
changes in the thickness of the ozone layer (Frederick et al. 1989; Madronich et al.
1998). Based on radiation amplification factors (RAF), it has been estimated that
1% ozone depletion leads to approximately 2–3% increase in DNA-damaging UV-B
dose, i.e., weighted with DNA action spectra (Madronich 1994). More than four
decades ago, Molina and Rowland (1974) discovered the destructing effect of chlo-
rofluorocarbons (CFCs) for ozone layer. A decade later, Farman et al. (1985)
reported for the first time the “ozone hole” over the Antarctic. Although the biologi-
cal risk from UV radiation also in aquatic environments had already been recog-
nized (Smith and Baker 1979; Calkins and Thordardottir 1980), stratospheric ozone
depletion and consequently enhanced levels solar UV-B radiation started to gain
importance as one of the major anthropogenic-driven threats for Antarctic biota
thereafter (Holm-Hansen et al. 1993; Weiler and Penhale 1994). After several
decades of alarming trends, recent reports indicate that the ozone layer over the
Antarctic is showing recovery (Solomon et al. 2016, 2017; summarized by Bais
et al. 2018, 2019). Since 2000, the observed recovery seems to be in agreement with
a decreasing amount of ozone-depleting substances. Although global trend over all
latitudes is masked due to strong variability (Chipperfield et al. 2017), recovering
trend has been reported for some areas, including Antarctica (Kuttippurath and Nair
2017). However, the complex interactions of stratospheric ozone with climate
change effects in the atmosphere and ocean lead to uncertainties in estimating the
timescale for recovery, and changes (either increase or decrease) in UV levels are
estimated to vary in different regions (summarized by Bais et al. 2018, 2019).
Together with greenhouse gases, ozone depletion has led to latitudinal shifts of cli-
mate (by moving the Southern Annular Mode (SAM) towards a more positive
Fig. 7.3 Overview of the major components related to underwater optics and processes occurring
under changing environmental context in Antarctic coastal waters, with implications for photobiol-
ogy of Antarctic seaweeds. See text for details and references
phase), which results in the strengthing of the westerly winds over Antarctic, with
impact on aquatic ecosystems, e.g., their mixed layer depth (Bais et al. 2019;
Williamson et al. 2019). Because climate change also modifies surface reflectivity
(through changes in snow and ice cover), clouds, and aerosols, it together with
ozone layer plays key role in defining the UV exposure of Antarctic ecosystems in
future (Bais et al. 2019).
Under episodes of ozone depletion during austral spring, band ratios can be mod-
ified resulting in enhanced UV-B exposure in proportion to UV-A/PAR, i.e., affect-
ing the balance between UV damage and photorepair (Mitchell and Karentz 1993),
thus leading to a higher risk for Antarctic ecosystems. In addition to direct adverse
effects on organisms (see Sect. 7.3.2 in the present chap), enhanced UV levels imply
elevated potential for photochemical reactions between UV radiation and CDOM,
leading to photodegradation of CDOM and hence increasing water transparency
(Morris and Hargreaves 1997), bioavailability of complexed contaminants (e.g.,
heavy metals), and nutrients (reviewed by Zepp 2003), formation of biologically
damaging products (e.g., singlet oxygen) (reviewed by Kieber et al. 2003), and
stimulating bacterial growth (Kieber et al. 1989). Overall, in recent years increasing
attention has been paid to the role of UV radiation in a variety of biogeochemical
processes (e.g., carbon cycling, enhanced photodegradation) and how global change
is altering them (summarized by Sulzberger et al. 2019; Williamson et al. 2019)
(Fig. 7.3).
7.4.2 Regional Warming
Among the major consequences of warming are the retreat of glaciers and reduction
of ice cover (Vaughan and Doake 1996; Cook et al. 2005; see also Chap. 1 by
Gómez and Huovinen). Ice sheets play an important role in global carbon cycle
(Wadham et al. 2019), and in the Antarctic where marine biota was evolved in
response to a massive glaciation since 30 Ma (Crame 1992; Clayton 1994), the
enhanced melting will have far-reaching consequences for the biogeochemical pro-
cesses in vast coastal areas (Constable et al. 2014; Sulzberger et al. 2019). Under the
strongest forcing scenario of IPCC, climate change-driven expansion of ice-free
areas is estimated to be around 25% by the end of the century in the Antarctic,
mainly in the WAP (Amesbury et al. 2017; Lee et al. 2017), where summer snow
melting has currently reached its highest intensity over last 1000 years (Abram et al.
2013). New ice-free areas provide habitats that can be colonized by seaweeds
(Quartino et al. 2013; see also Chap. 8 by Quartino et al.). On the other hand, these
areas are often characterized by high turbidity (low light penetration) as a result of
sediment runoff (see Fig. 7.3), which can modify the zonation patterns of some spe-
cies towards shallower waters (Deregibus et al. 2016) and cause reduction of sea-
weed productivity (Jerosch et al. 2019; see Chap. 9 by Deregibus et al.). In the
Arctic, the growth of kelp Laminaria solidungula has been found to depend directly
on the water transparency, which is strongly governed by resuspension of sediments
especially during increased frequency of storm events (Dunton et al. 2009).
Increased turbidity can furthermore interfere with disinfection of pathogens and
other microbiomes by UV radiation in surface waters with consequences hitherto
not well understood (Williamson et al. 2017, 2019; see Chap. 14 by Gaitan and
Schmid).
In polar regions, high permafrost temperatures have been registered, with poten-
tial impact on global climate through emissions of CO2 and release of methane. In
the Antarctic, temperature increased by 0.37 °C in zones with continuos permafrost
during 2007–2016 (IPCC 2019). Increased input of organic matter from catchment
as a result of glacier melting can also lead to enhanced nutrient (e.g., nitrates, iron)
transfer to coastal areas (Hodson et al. 2017; Ducklow et al. 2018), potentially
increasing phytoplankton biomass and thus decreasing light penetration. Increased
nutrient availability can also modify the responses of seaweeds to environmental
stress, e.g., mitigating adverse effects of UV radiation and metals as observed in
sub-Antarctic kelps (Huovinen et al. 2010). Elevated temperature is also known to
improve the efficiency of repair processes, leading to higher UV tolerance of
Antarctic seaweeds (Rautenberger et al. 2015). Increase of Fe from runoff may
cause oxidative stress in Antarctic seaweeds (González et al. 2017).
7.4.3 Feedback with Other Emergent Threats
Growing evidence on the presence of anthropogenic pollution in the Antarctic,

especially in the WAP region, is changing our vision of a pristine environment
(reviewed by Bargagli 2008). In spite of natural barriers (Antarctic Circumpolar
Current and atmospheric circulation) and remoteness, these ecosystems receive pol-
lution, e.g., persistent organic pollutants (POPs), from other regions through long-
range atmospheric transport (LRAT), in addition to local sources (Bengtson Nash
2011; Vecchiato et al. 2015; Khairy et al. 2016). In fact, growing human activities
(e.g., waste incineration, sewage effluents, fuel combustion) within this region are
leaving their marks in the environment (reviewed by Bargagli 2008). Emerging con-
taminants, such as microplastics, have also already been reported in the Antarctic
environment (Waller et al. 2017; Lacerda et al. 2019). In this context, more acces-
sible areas such as the Antarctic Peninsula are increasingly threatened by human
impact (e.g., from scientific stations and visitors), which is evidenced by chemical
contamination including heavy metals (de Moreno et al. 1997; Farías et al. 2002;
Amaro et al. 2015; Padeiro et al. 2016; Chu et al. 2019) and polycyclic aromatic
hydrocarbons (PAHs) (Na et al. 2011; Préndez et al. 2011) in the sediments, water,
and snow in these ecosystems. The fate of environmental contaminants can be dras-
tically modified under changing climate and ozone depletion scenarios implying
multiple and complex consequences (Wrona et al. 2006; Schiedek et al. 2007;
Noyes et al. 2009; Grannas et al. 2013; Galic et al. 2017; Sulzberger et al. 2019)
(Fig. 7.3). For instance, increased melting of cryospheric environments can release
chemical contaminants that have been stored in ice and snow for prolonged periods
(Wania and Westgate 2008; Grannas et al. 2013; Hauptmann et al. 2017). The risk
of enhanced levels and availability of contaminants like POPs and mercury due to
climate change is receiving increased attention (IPCC 2019; Sulzberger et al. 2019).
Certain light-absorbing impurities (LAIs) deposited on snow and ice surfaces can
induce complex feedback processes that further accelerate melting (Lutz et al. 2014;
Tedesco et al. 2016; Huovinen et al. 2018), potentially leading to unpredicted pollu-
tion levels in the surrounding environments. The fate of LAIs reaching aquatic envi-
ronment and their potential for underwater light attenuation is still largely unknown.
On the other hand, interaction of certain environmental contaminants (such as
PAHs) with UV radiation can lead directly or via ROS to their photomodification
(photooxidation, photolysis) resulting in photodegradation or formation of photo-
products with different characteristics and effects (including lower toxicity) as the
original compound. They can also achieve higher toxicity (phototoxicity) through
photosensitization reactions when they interact with UV radiation (reviewed by
Björn and Huovinen 2015; Sulzberger et al. 2019) (Fig. 7.3). Therefore, even when
PAH levels in the environment are low, such as those reported for King George
Island (Na et al. 2011; Préndez et al. 2011), their potential for UV-induced or
UV-enhanced toxicity under ozone depletion implies an unpredicted risk. UV radia-
tion can also contribute to generation of microplastics (summarized by Andrady and
Pandey 2019) and interact with other emerging contaminants (e.g., pharmaceutical
and personal care products such as sunscreens) (see Björn and Huovinen 2015; Bais
et al. 2019; Williamson et al. 2019).
Since 1980s, the oceans as carbon sink have removed 20–30% of CO2 from
anthropogenic emissions, leading to increased ocean acidification (summarized in
Gattuso and Hansson 2011). Such conditions are corrosive to marine organisms,
causing a decline (3.9% during 1998–2014 in the Southern Ocean) in calcification
rates in skeleton- and shell-forming species (IPCC 2019). Ocean systems at high
latitudes are especially vulnerable to experience changes of pH due to their lower
buffering capacity (McNeil and Matear 2008; Jewett and Romanou 2017). Decreased
pH can increase UV transparency of water through photodegradation of CDOM
(Schindler et al. 1996; Yan et al. 1996) (Fig. 7.3). In systems affected by freshening
due to local glacier melt, acidification can be exacerbated increasing calcium car-
bonate corrosivity (Evans et al. 2014). To date, studies carried out in calcareous and
non-calcareous seaweeds indicate that responses to acidification depend on the
taxonomic status, biogeographic location, prevailing metabolism of species (e.g.,
algae with carbon concentrating mechanisms versus those that rely on CO2 trans-
port), the type of experimental approach and time of responses, etc. (Hurd et al.
2009; Roleda and Hurd 2012; Hofmann and Bischof 2014). Overall, interaction of
acidification, climate change, and UV radiation has been found to impact negatively
some calcifying seaweed species (e.g., by reducing structural UV protection)
(Russell et al. 2011) or affecting photosynthesis (Gao and Häder 2017). In the
Antarctic seaweeds Desmarestia anceps and D. menziesii, changes in protein and
lipid contents were observed when the algae were exposed to combined treatments
of pH and temperatures (Schram et al. 2017); however, these conditions did not
affect markedly other physiological parameters such as photosynthesis and phloro-
tannin content (Schoenrock et al. 2015).
Global change together with increasing anthropogenic impact lead to complex sce-
narios for Antarctic coastal waters: enhanced turbidity from glacier and ice melt
impedes the light penetration, but earlier ice breakup in late winter-spring increases
underwater light levels during extended open-water period, whereas UV radiation
and acidification can lead to degradation of organic matter and hence increase light
penetration. Under favorable light conditions in the water column, increased nutri-
ent load from terrestrial and glacier runoff can stimulate phytoplankton growth
causing blooms with negative impact on water clarity and light availability for ben-
thic productivity. Therefore, complex implications for seaweeds are to be expected,
ranging from beneficial to harmful, depending on local processes as well as the
structure and function of the seaweed communities. How other feedbacks related,
e.g., with transient and persistent contaminants, ocean acidification and local fresh-
ening will impact the underwater light climate in the Antarctic and their conse-
quences for the biota are difficult to predict. Overall, the scarcity of long-term data
that connects the changes in climate and habitat with ecosystem responses has been
identified among the major gaps when predicting the climate change impact on
Antarctic cryosphere and its associated marine realm (Fountain et al. 2012).
Similarly, susceptibility of seaweeds to the predicted changes in the Antarctic habi-
tat and their photobiological adaptations need to be addressed from molecular to
systemic scales. In fact, the novel molecular approaches are likely to improve our
understanding of the mechanisms that cold-adapted organisms display to cope with
the projected environmental variability (Lyon and Mock 2014).
Acknowledgments The funding provided by CONICYT (through Projects Anillo ART1101,

FONDECYT 1161129 and FONDAP 15150003) and by Instituto Antártico Chileno (INACH;
Grant T-20-09) to carry out our research in the Antarctic is greatly acknowledged. We are also
grateful to the members of our research group in Universidad Austral de Chile and the staff of the
Instituto Antártico Chileno for their invaluable cooperation.
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Chapter 8
Production and Biomass of Seaweeds
in Newly Ice-Free Areas: Implications
for Coastal Processes in a Changing
Antarctic Environment
María L. Quartino, Leonardo A. Saravia, Gabriela L. Campana,

Dolores Deregibus, Carolina V. Matula, Alicia L. Boraso,
and Fernando R. Momo
Abstract The Antarctic rocky coasts are mainly colonized by extensive seaweed
communities, which play key roles as food resource, habitat, and refuge for many
benthic and pelagic organisms. Due to climate warming, Antarctic marine ecosys-
tems are being affected by glacier retreat opening new habitats, e.g., newly ice-free
areas that can be colonized by macroalgae. As a consequence, primary production
and fate of macroalgae are changing in these new polar environments. In these eco-
systems, the carbon production, especially from large brown algae, is an important
food source to the benthic invertebrate communities mainly when other resources
are scarce. Thus, in new areas colonized by seaweeds, the trophic structure and
biogeochemical fluxes can vary considerably. Moreover, when seaweeds die or are
removed by water movement, ice scouring, or storms, they are detached, frag-
mented, and degraded, incorporating and releasing particulate and dissolved organic
matter to the coastal food webs, i.e., they support a large fraction of the secondary
production of the benthos. The present chapter is a review of the knowledge on
seaweed biomass and production in the coastal Antarctic ecosystem opening a dis-
cussion on the role of these organisms as main energy sources in, e.g., small fjords
and glacier-influenced sites, impacted by recent climatic change.
Keywords Carbon flux · Glacier retreat · Ice-free areas · Potter Cove · Seaweed
production
M. L. Quartino (*)
Departamento de Biología Costera, Instituto Antártico Argentino (IAA),
Buenos Aires, Argentina
Museo Argentino de Ciencias Naturales B Rivadavia (MACN), Buenos Aires, Argentina
e-mail: lquartino@dna.gov.ar

https://doi.org/10.1007/978-3-030-39448-6_8
156 M. L. Quartino et al.
8.1 Introduction: Seaweeds in Coastal Marine Ecosystems
Worldwide, macroalgae are essential components of coastal waters providing habi-

tat‚ nursery and refuge for fish and numerous mobile and sessile invertebrates (Hurd
et al. 2014) and can potentially also play a role in providing refuge from climate
change driven stressors, e.g., ocean acidification (Hurd 2015; Krause-Jensen et al.
2016; Wahl et al. 2018; see also Chap. 11 by Gómez and Huovinen). Furthermore,
large brown algae, e.g., species of order Laminariales (known as “kelps”), are
regarded as ecosystem engineers that could significantly modify the habitat charac-
teristics such as water velocity, light penetration, and physic-chemical properties of
seawater (Jones et al. 1994; Dawson et al. 2010), while creating an understory con-
dition favorable for species adapted to, e.g., low light intensity (Steneck et al. 2002).
The macroalgal biomass is an important component of the functioning of the
marine ecosystem; a large portion of seaweeds is not consumed by herbivores but
returns to the environment as decaying organic matter (Cebrián 2004). These large
L. A. Saravia
Instituto de Ciencias, Universidad de General Sarmiento (UNGS),
Los Polvorines, Buenos Aires, Argentina
e-mail: lsaravia@campus.ungs.edu.ar
G. L. Campana
Departamento de Ciencias Básicas, Universidad Nacional de Luján (UNLu),
Luján, Buenos Aires, Argentina
e-mail: gcampana@dna.gov.ar
D. Deregibus
Consejo Nacional de Investigaciones Científicas y Técnicas, (CONICET),
e-mail: dderegibus@dna.gov.ar
C. V. Matula
e-mail: ucv@mrecic.gov.ar
A. L. Boraso
Instituto de Desarrollo Costero, Universidad Nacional de la Patagonia San Juan Bosco
(UNPSJB), Comodoro Rivadavia, Argentina
F. R. Momo
Instituto de Ciencias, Universidad de General Sarmiento (UNGS),
e-mail: fmomo@campus.ungs.edu.ar
8 Production and Biomass of Seaweeds in Newly Ice-Free Areas: Implications… 157
quantities of seaweed biomass can follow different paths: they can be detached from
the hard bottom and drift by the water movements (Baring et al. 2018). Also the
whole thalli can drift and slowly be fragmented and be thrown by the waves to the
coastline. On the beach they can be accumulated and, once degraded, enter again to
the system by the tides sinking to the bottom of the seabed where they decompose
(Krause-Jensen and Duarte 2016). Thus, this algal debris can supply important
amounts of organic matter to benthic ecosystems and provide food, directly for
detritivores or indirectly, by stimulating bacterial metabolism (Rossi et al. 2013).
Primary production is the formation of organic matter (carbon) in a photosyn-
thetic organism per time unit (Israel 1995). In general, ecological studies of primary
production refer to “net primary production” (NPP), which is that portion of gross
primary production from photosynthesis that remains after consumption via respira-
tion. This may represent different processes depending on the methodology used to
measure it. In most studies, net primary production represents the dry mass of plant
matter produced per unit area per unit time (Reed et al. 2008).
Seaweed biomass can be measured using destructive and nondestructive sam-
pling. The first one corresponds to the collection of algal biomass in terms of grams
by unit area (g m−2). The nondestructive sampling implies the use of underwater
images or video, which mainly permit to gain information on algal cover. Coverage
data must be converted into biomass, usually through linear regression to estimate
finally biomass (Allison 2004). Several improvements have been proposed to this
method, taking into account the species-specific and nonlinear nature of the rela-
tionship between cover and biomass due to the different algal architectures. Thus, a
better prediction of biomass would be obtained by fitting a multivariate generalized
additive model (GAM) considering all species present in each quadrat (Pedersen
et al. 2019). Various studies have focused on quantifying the macrophyte production
to assess its contribution to the marine ecosystem worldwide. For example, mac-
roalgae and seagrasses store about 0.4% and 16% of their net primary production in
the sediments, respectively (Duarte and Cebrián 1996), and some of the excess
organic matter can be exported to adjacent water column (Barrón and Duarte 2009;
Wada and Hama 2013). Duarte and Cebrián (1996) reported that the export of
organic matter accounts, on average, for 25% of the net primary production of mac-
roalgae. Thus, macroalgae can be regarded as the most extensive and productive
primary producers in coastal zones around the world. It was estimated that they
cover about 3.5 million km2 and can account for a global net primary production of
about 1.5 Tg Cyr−1 (Krause-Jensen and Duarte 2016).
8.2 M
acroalgae and Carbon Fluxes in Antarctic
Coastal Areas
In contrast to the global algal production, there is not enough information on mac-
roalgal production in Antarctica. In Antarctic marine ecosystems, macroalgae are
one of the major primary producers that grow and develop associated to rocky
substrates of different slope and size (Klöser et al. 1996; Wiencke and Amsler
2012). In general, Antarctic benthic macroalgae are distributed from the intertidal
down to the lower subtidal zone at 40 m depths and present a clear zonation: an
intertidal fringe is usually abraded by winter ice floes, it is mainly colonized by
opportunistic species, and it is devoid of large perennial macroalgae. The upper
subtidal is dominated by the brown seaweeds Desmarestia menziesii J.Agardh and
Ascoseira mirabilis Skottsberg under strong turbulence. The central subtidal (above
15 m) is mainly dominated by Desmarestia anceps Montagne under moderate tur-
bulence, and it is gradually replaced by Himantothallus grandifolius (Gepp and
Gepp) Zinova. This latter species becomes dominant at deeper waters, where turbu-
lence is usually negligible (Klöser et al. 1996; Quartino et al. 2005; Wulff et al.
2009; see Chap 11 by Gómez and Huovinen).
Antarctic macroalgae are thought to deliver huge amounts of organic matter to
the Antarctic coastal food webs (Fischer and Wiencke 1992; Gómez et al. 2009,
Marina et al. 2018). Furthermore, they are a food source for numerous mobile con-
sumers, including invertebrates and some nototheniid fish (Iken et al. 1998; Amsler
et al. 2005; Barrera Oro et al. 2019). Sublittoral rocky shores dominated by mac-
roalgae have been regarded as important areas hosting high values of abundance and
biomass of organisms (Amsler et al. 1995; Brouwer et al. 1995; Quartino and
Boraso de Zaixso 2008; Wulff et al. 2009).
One of the main macroalgal carbon contributions to the ecosystem is probably
the great amounts of biomass scattered on the coasts, an accumulation of allochtho-
nous organic debris known as “wrack” that is commonly observed in the intertidal
zone. In the maritime Antarctic zone, this type of organic matter has been recog-
nized as an important source of carbon for diverse consumers (Zenteno et al. 2019).
Grange and Smith (2013) reported drifting macroalgae as very abundant in some
fjord basins compared to the open shelf. These authors observed substantial abun-
dances of drifting algae ranging from ~8 to 130 cm m−2.
Once on the coast, the stranded algae can also be used by seals and sea elephants
as resting places. Westermeier et al. (1992) recorded a mean value of 22 kg m−2 cor-
responding to the highest abundance of drifting macroalgae along the coastline of
Maxwell Bay. In Admiralty Bay, the amount of macroalgae deposited on the beach
was estimated to be 104 kg m−2 dry weight (Rakusa-Suszczewski 1995). The organic
matter of the decomposed algae mixed with excrement of seabirds (guano) reenters
the marine ecosystem by the waves, winds, and tide action. Leaching of nutrients to
the environment and subsequently to the coastal waters, are the final stages of mac-
roalgal decomposition, after which the dissolved nutrients fertilize the shore through
the tidal beach runoff with nitrate, nitrite, ammonia, and phosphorous (Nedzarek
and Rakusa-Suszczewski 2004). Thus, the volumes of algal debris can reflect the
high productivity normally assigned to Antarctic seaweeds populating different
regions across the Antarctic Peninsula.
8.3 Macroalgal Biomass Studies in Antarctica
In the decade 1980–1990s and early the 2000s, several studies described the bio-
mass (standing crop) of macroalgae at the Antarctic benthos, particularly around the
West Antarctic Peninsula (Table 8.1). These early works implied frequently the use
of “destructive sampling,” which allowed a more accurate assessment of the identity
and biomass of each taxa (DeLaca and Lipps 1976; Miller and Pearse 1991; Amsler
et al. 1995; Brouwer et al. 1995; Quartino et al. 2001, 2005). These studies showed
that in the northern portion of the Western Antarctic Peninsula and adjacent islands,
seaweeds dominate shallow benthic communities on hard substrates, covering over
80% of the seafloor, with standing biomass levels in the range of 5–10 kg m−2 wet
weight (Wiencke and Amsler 2012, Gómez et al. 2009), a number comparable to
temperate kelp forests (Mann 1972; Duggins 1988).
During the following decades, many benthic community studies were conducted
using underwater photo and/or video (nondestructive sampling) (Quartino et al.
2013; Sahade et al. 2015; Valdivia et al. 2015; Lagger et al. 2018; Jerosch et al.
2019). These methodologies facilitate fast sampling and are a great advantage in
Table 8.1 Maximum biomass (g m−2, wet or dry weight) determined for four species of macroalgae
reported by different surveys (depths between brackets when provided by the authors)
Desmarestia Desmarestia Himantothallus Iridaea
Locality anceps menziesii grandifolius cordata Reference
Wet weight
(1) – 2050 – – Richardson (1979)
(2) 5660 (11 m) 1850 (11 m) 1250 (11 m) – Brouwer et al. (1995)
(3) – 3440 Cormaci et al. (1996)
(4–5 m)
(4) a 6044 (20 m) 6737 (5 m) 10,336 (20 m) 2554.60 Quartino and Boraso
(0 m) de Zaixso (2008)
(4) b 3900 (5 m) 3470 (3 m) 923.8 C. Matula, personal
(3 m) communication
4198 (10 m) 3975 (5 m) 575 (5 m)
Dry weight
(5) – 800 (4 m) 600 (12 m) – DeLaca and Lipps
(1976)
(2) 1000 (11 m) 460 (11 m) 240 (11 m) – Brouwer et al. (1995)
3300 (5 m)
(4) a 671 (20 m) 749 (5 m) 1152 (20 m) 255.36 Quartino and Boraso
(0 m) de Zaixso (2008)
(4) b 821 (5 m) 730.5 (3 m) 194.5 C. Matula, personal
(3 m) communication
883.8 (10 m) 836.85 (5 m) 121 (5 m)
Localities: (1) Borge Bay; South Orkney Islands (60° 43′S, 45° 36′W); (2) Signy Island, South
Orkney Islands (60° 42′S 45° 36′W); (3) Ross Sea (74° 30′S, 165° 30′E); (4) Potter Cove, South
Shetland Islands (62° 14′S, 58° 38′W), a, sampling done in 1994–1996, and b, sampling done in
2015–2016; (5) Ansvers Island (62° 46′S, 64° 04′W)
this extreme and rough environment. Values recorded by these methods are mainly
percent coverage of macroalgae by unit area. Although cover data are valuable, it is
always convenient to transform it into biomass in order to calculate and quantify the
algal production as mentioned previously.
8.4 T
he Ecosystem of Potter Cove: An Outstanding
Case Study
Potter Cove (62° 14′S, 58° 40′W), a small fjord at the Isla 25 de Mayo/King Gorge
Island, South Shetland Islands, has become an ideal place to carry out biological,
geological, and oceanographic studies. This cove is divided into two characteristic
areas, the mouth (or outer part) and an inner part separated by a shallow sill (Klöser
et al. 1996). Both areas are biologically distinctive: the rocky shores of the outer
part of Potter Cove host a high biomass of macroalgae (Klöser et al. 1996; Quartino
et al. 2005), whereas the inner cove has one of the largest concentrations of benthic
filter feeders found in Antarctica (Tatián et al. 2004).
In fact, the first surveys on macroalgae had identified an important benthic algal
community associated with the presence of hard bottom substrate and light avail-
ability (Quartino et al. 2001, 2005). In most of the studied sites, abundance of large
Desmarestiales was observed from 5 down to 30 m depth, in a continuous vertical
zonation. This high algal biomass was detected on rocky coastal areas close to the
mouth of the cove, where the more transparent, oceanic water prevailed (Quartino
et al. 2001, 2005).
Macroalgal production of the most abundant species decreased during summer
months (Quartino and Boraso de Zaixso 2008) following the seasonal strategy
exhibited normally by “season anticipators,” which start their growth under short-
day conditions in late winter/spring, often under the sea-ice, reaching their maxi-
mum biomass in summer months (Wiencke et al. 2009; Wiencke et al. 2014).
Quartino and Boraso de Zaixso (2008) calculated an average standing stock of 792,
84 ton and an algal production of 1401 ton during summer season for the whole
Potter Cove. This study provided the first estimation of seaweed production in
Antarctica, combining field biomass data with experimental growth rates calculated
by Wiencke (1990a, b) and Gómez and Wiencke (1997). Additionally, an estimation
of their decomposition was included to describe the macroalgal mass balance in this
Antarctic fjord (Fig. 8.1). Due to the usually low pelagic primary productivity in
Potter Cove (Schloss and Ferreyra 2002), the study suggested that macroalgae were
the main carbon source, supporting a large fraction of the secondary production of
the benthic system (Tatián et al. 2004; Sahade et al. 2004; Quartino et al. 2008).
The continuous monitoring of this marine ecosystem has permitted to survey the
changes in the physiognomy of the cove along the last three decades. One of the
most singular observations was the progressive melting of the Fourcade Glacier
(Rückamp et al. 2011), which surrounds Potter Cove. The retreat of this glacier has
Fig. 8.1 Pathways of macroalgae production in Potter Cove. The average macroalgal standing
stock (792 ton) was calculated for the summer season considering the entire cove area (Quartino
and Boraso de Zaixso 2008). The production (1401 ton) and the flux of biomass to the ecosystem
(1370 ton) were calculated using only the dominant macroalgal species (Quartino et al. 2008).
Detached macroalgae are expected to enter the inner cove via the prevailing cyclonic water circula-
tion (Schloss and Ferreyra 2002). The decomposed fraction was calculated using a rate of
0.0016 day−1, estimated by Brouwer (1996) for Desmarestia anceps
been uncovering new hard bottom ice-free areas available for benthic colonization,
especially macroalgae (Quartino et al. 2013). These newly ice-free areas are
extremely disturbed, presenting a considerable alteration of the water column (due
to the increase of sediment input and salinity changes particularly during the sum-
mer melting season) and on the ice disturbance patterns (Eraso and Domínguez
2007; Quartino et al. 2013). In fact, the photographs and video records revealed a
well-developed macroalgal community even in close proximity to the retreating
glacier where the sediment load was high. In these sites, the increase in the sediment
runoff reduces the light penetration and can constitute a constraint for photosynthe-
sis (Schloss et al. 2012; Wiencke and Amsler 2012; Quartino et al. 2013). Particularly,
this can result in a change in the vertical distribution of those species adapted to
dark conditions, which probably will move to shallower depths adjusting their light
requirements in this new environment with higher sediment load (Deregibus et al.
2016; see also Chap. 9 by Deregibus et al.).
Thus, under these optical conditions, development and vertical distribution of the
macroalgae can be strongly affected by the high turbidity (Deregibus et al. 2016; see
also Chap. 7 by Huovinen and Gómez). Additionally macroalgal colonization was

negatively impacted by the ice disturbance caused by ice blocks originated from the
glacier (Quartino et al. 2013). Nevertheless some species such as the red alga
Palmaria decipiens (Reinsch) Ricker and the green alga Monostroma hariotii Gain
thrive in the most disturbed sites. It was also shown that Gigartina skottsbergii
Setchell and Gardner and Himantothallus grandifolius were adapted to harsh abi-
otic conditions, but the red alga G. skottsbergii seemed to be more sensitive to the
external stress (González et al. 2017). The vertical distribution of the subtidal spe-
cies in the inner part of the cove did not fit with the typical macroalgal zonation
reported for other sites around King George Island (Huovinen and Gómez 2013 and
Chap 11 by Gómez and Huovinen); in Potter Cove algal species usually found at
greater depth were observed growing at shallow waters. The main results showed
that (1) the complexity of the macroalgal community was positively correlated to
the elapsed time from the ice retreat: newly ice-free areas closer to the outer side of
the cove presented mature macroalgal communities dominated by perennial and
large brown algae of the genus Desmarestia, (2) algal development depended on the
optical conditions and the sediment input with some species being limited by light
availability, (3) macroalgal colonization was negatively affected by ice disturbance,
and (4) the colonization was determined by the size and type of substrate and by the
slope of the seafloor (Fig. 8.2).
In this new warming scenario, ice melting is probably the primary cause of
changes in the macroalgal communities in the inner Cove, and it could be mediated
by different associated phenomena (Fig. 8.3). Glacier retreat originates newly ice-
free areas providing hard substrate available for benthic colonization, which can be
positively related to increased diversity, richness, and macroalgal cover at different
spatial scales (Valdivia et al. 2014). In addition, glacier melting increases ice scour-
ing, sediment runoff in the water column and enhances turbidity having a negative
effect on these ecological parameters because algae do not have enough light avail-
able for photosynthesis. Consequently, macroalgae may shift their vertical distribu-
tion increasing overlapping and competition, resulting in a negative effect (Fig. 8.3).
Additionally a complementary PAR model was performed with the variables affect-
ing the annual PAR availability in this climate change context (see Chap 9 by
Deregibus et al.).
8.5 A
Dynamic Growth Model for Antarctic Macroalgae
Under a Fast-Changing Environment
Dynamic growth models have been developed mainly for farmed macroalgae
(Hadley et al. 2015; Zhang et al. 2016; Broch and Slagstad 2012; Duarte and Ferreira
1997) and also to determine the growth of species in eutrophicated sites and under
algal blooms at mid latitudes (Ren et al. 2014; Perrot et al. 2014). Despite their
recognized great importance as primary producers (Hurd et al. 2014), there are no
Fig. 8.2 Three different situations observed in the newly ice-free areas of Potter Cove. S1 corre-
sponded to sites unaffected by sedimentation and dominated by large brown algae. S2 corre-
sponded to a site dominated by the red algae Palmaria decipiens in close proximity to a retreating
glacier with high sediment inflow and high ice disturbance. S3 represented a newly ice-free area in
the inner side of the cove close to the glacier and with influence of sediment runoff from small
creeks. In this site the coexistence of macroalgae and macrofauna was observed. Macroalgae were
classified according to their life history as annuals, pseudo perennials and perennials. Symbols +
and – correspond to the grade of intensity. (Adapted from Quartino et al. (2013))
dynamic models for Antarctic macroalgae. In this line, we recently described a new
model adapted to the particular conditions of the Antarctic environment (Guillaumot
et al. 2018). The model describes the biomass dynamics of algal assemblages with-
out considering a particular species (Fig. 8.4) and can also be applied to dominant
species that do not experience interspecific competition. The outputs of this approach
can be integrated in carbon flux models of Antarctic coastal ecosystems. The
assumptions of the model are that the growth is not limited by nutrient availability
(Drew and Hastings 1992; Ducklow et al. 2007; Wiencke and Amsler 2012) and that
substrate availability, light, and ice scouring should be regarded as the main envi-
ronmental variables (Quartino et al. 2013). Considering that the levels of irradiance
that reach the bottom is mediated by depth, suspended sediments, and incident radi-
ation, the model takes into account the high variability in incident light and turbid-
ity, two factors with high seasonal fluctuations in Antarctic. The estimations use a
daily time sequence, assuming that the numbers of days available for growth are
Fig. 8.3 Conceptual model on the effects of glacier retreat on structural attributes of the macroal-
gal community. (Adapted from Quartino et al. (2013))
Fig. 8.4 Overview of the dynamic growth model of Antarctic macroalgae and the main variables
entered in the algorithm. (Adapted from Gómez and Huovinen (2015))
determined by the period when the zone considered is free of ice. Then the model
equations would be:
B ( t + 1) = B ( t ) + µmax Λ ( t ) Γ ( t ) B ( t ) − D ( t ) B ( t ) − M ( t )

where B(t) is the biomass; μmax is the maximum intrinsic growth rate; Λ(t) and Γ
represent the effects of light and temperature on growth, respectively; and D(t) and
M(t) are the biomass dependent mortality rates associated with herbivory and ice
scouring respectively.
Each of these terms is also dependent on other environmental characteristics
defined as:
 I 
I 1− I 
Λ = e 0 
I0

where I0 is the optimum irradiance and I is the light available at the seabed that will
have more dependencies:
I = I s e − Kd Z

where Is is the irradiance at the sea surface, Kd is the extinction coefficient (Kirk
1994), and Z is the depth. The incident light Is must be recorded in situ and averaged
over several years to represent the mean conditions, while Kd is also affected by the
turbidity produced by glacier melting (Deregibus et al. 2016; see also Chap. 9 by
Deregibus et al.).
The dependence of growth on temperature is modeled as a function of an optimal
temperature range (Duarte et al. 2003):
2.0 (1 + β ) XT
Γ=
X + 2.0 β XT + 1.0
2
T
where Tmax is the upper temperature above which growth ceases and β is an adjust-
ment parameter. XT is defined as:
T − Topt
XT =
Topt − Tmax

where Topt is the optimal temperature for growth and T is the average daily water
temperature which must be supplied from local measurements or estimated. Even
although this kind of mechanistic model requires experimental and field data to be
calibrated and validated, it can be a useful tool to provide predictions of macroalgal
biomass in different scenarios of climate change.
8.6 S
eaweed Production in Present and Future
Warming Scenarios
In recent decades, the ice shelves of the WAP have changed rapidly and conse-
quently a significant retreat was observed on both sides of the Peninsula (Cook et al.
2005). In response to relatively small environmental change, some ecosystems can
undergo abrupt transformation (Clarke et al. 2013). For example, decreases in the
spatial and temporal extent of sea ice will affect the underwater light environment
during winter and early spring altering photosynthesis of organisms adapted to spe-
cific light regimes (See Chap. 9 by Deregibus et al.). Moreover, a shorter perma-
nence of sea ice and enhanced sediment inflow from the glaciers will modify the
environment reducing light availability for algal photosynthesis and can also affect
survival and germination rates directly (Arakawa and Matsuike 1992; Chapman and
Fletcher 2002; Eriksson and Johansson 2005). A significant change in the annual
light budget is likely to have major consequences for benthic ecosystems in shallow
waters: the timing of annual sea ice breakup affects the composition of benthic com-
munities, primarily due to a change in the available light on an annual basis (Clarke
et al. 2013; see also Chap. 7 by Huovinen and Gómez). Thus, global warming is
expected to cause an earlier sea-ice melting, which will likely induce tipping points
for many areas at shallow depths, probably causing ecosystems to shift from pre-
dominantly heterotrophic to predominantly autotrophic, the later state dominated by
macroalgal production (Clarke et al. 2013; see also Chap. 15 by Momo et al. and
Chap. 16 by Ortiz et al.).
Linking macroalgal decomposition and the trophic network in the future coastal
scenarios, the colonization of macroalgae in the new areas probably will change the
structure and composition of the whole ecosystem. As it was mentioned before, this
situation is being detected in Potter Cove, where the increasingly higher coloniza-
tion of macroalgae in newly ice-free areas is providing carbon sources (food) for the
second fraction of the trophic web. In this system sediment retains the nitrogen and
carbon released from the macroalgae degradation process, whereas a relatively
small amount of macroalgal-derived nutrients is released back into the overlying
water, with a negative feedback on phytoplankton production in the water column
(Braeckman et al. 2019). These authors suggested that this “sink effect” or “food
bank” would also explain the prolonged food availability in the euphotic Antarctic
sedimentary benthos in the form of microphytobenthic biomass, at least as long as
the overlying waters are not too turbid or ice covered (Mincks et al. 2005).
A recent study in Potter Cove using an ensemble model predicted a reduction of
macroalgal summer production under increasing sedimentation (Jerosch et al.
2019). Thus, the projection of macroalgal distribution in a near future scenario
shows a dramatic reduction of summerly macroalgal productivity inside the cove,
while the glacier continues melting and increasing the discharge of sediments.
However, this process could be mitigated in part by an increased colonization and
productivity of macroalgae in shallow newly ice-free hard bottom areas inside the
cove (Quartino et al. 2013; Deregibus et al. 2016; Campana et al. 2018).
8.7 Future Prospects
Even though macroalgae are the most productive marine macrophytes worldwide,
they have been excluded from “blue carbon” assessments as they typically grow in
habitats that are not considered to accumulate large stocks of organic carbon
(Krause-Jensen and Duarte 2016). Recently, more studies have highlighted the
potential of marine vegetation as a sink for anthropogenic C emissions (known as
“Blue Carbon”) suggesting that marine macroalgae can sequestrate anthropogenic
CO2 (Chung et al. 2011; Queirós et al. 2019). So far, there are also some few reports
of the presence of macroalgal carbon in marine sediments, suggesting that the pres-
ence of macroalgal carbon may be widespread, extending from shallow to deep-sea
sediments and from polar to tropical regions. It has been also reported that this type
of carbon can be found across a broad range of depths into the sediment, from sur-
face and subsurface layers down to deeper than a hundred metres into the sediment
(Krause-Jensen et al. 2018).
Despite the evidence of macroalgae as carbon sinks, the rates and magnitude of
this process has not been estimated precisely. Some studies have delivered a first-
order estimate of the contribution of macroalgae to carbon sequestration from burial
in coastal sediments and its export to the deep sea (Duarte and Cebrián 1996;
Krause-Jensen and Duarte 2016). This last step of macroalgal C sequestration is
particularly important because the exchange of carbon with the atmosphere is pre-
cluded over extended time periods, even after being remineralized (Krause-Jensen
and Duarte 2016).
In all, meltwater influences coastal areas where macroalgae are the dominant
species covering most of the rocky bottoms of many coastal areas along the
WAP. However, there is still little knowledge on the macroalgal carbon production
in Antarctic shallow waters and its fate under changing environmental conditions.
Therefore, it would be necessary to implement monitoring programs to measure the
expansion of these organisms in other locations of the WAP to estimate at large
scale the fraction of macroalgae production sink in the sediment, the budget of mac-
roalgal production, their decomposition, and further export to other marine
ecosystems.
Acknowledgments Special thanks to Silvia Rodríguez for her valuable collaboration and techni-
cal assistance at the Coastal Biology Department of Instituto Antártico Argentino. We also thank
the support of the diving and logistic teams at Carlini Station. This study was performed with the
financial support of Instituto Antártico Argentino/Dirección Nacional del Antártico, ANPCyT-
DNA (PICTO 2010-116, PICT 2017-2691). This chapter also presents an outcome of the interna-
tional Research Network IMCONet funded by the Marie Curie Action IRSES IMCONet (FP7
IRSES, Action No. 318718) and of CoastCarb (Funding ID 872690, H2020-MSCA-RISE-2019 -
Research and Innovation Staff Exchange).
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Chapter 9
Carbon Balance Under a Changing Light
Environment
Dolores Deregibus, Katharina Zacher, Inka Bartsch, Gabriela L. Campana,

Fernando R. Momo, Christian Wiencke, Iván Gómez, and María L. Quartino
Abstract The natural environment of Antarctic seaweeds is characterized by

changing seasonal light conditions. The ability to adapt to this light regime is one of
the most important prerequisites for their ecological success. Thus, the persistence
of seaweeds depends on their capacity to maintain a positive carbon balance (CB)
D. Deregibus (*)
Departamento de Biología Costera, Instituto Antártico Argentino, Buenos Aires, Argentina
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires,
Argentina
K. Zacher · I. Bartsch · C. Wiencke
Alfred-Wegener-Institute, Helmholtz Centre for Polar and Marine Research,
Bremerhaven, Germany
e-mail: katharina.zacher@awi.de; inka.bartsch@awi.de; Christian.wiencke@awi.de
G. L. Campana
F. R. Momo
Instituto de Ciencias, Universidad de General Sarmiento, Los Polvorines, Buenos Aires, Argentina
I. Gómez
e-mail: igomezo@uach.cl
M. L. Quartino
Museo Argentino de Ciencias Naturales “B. Rivadavia”, Buenos Aires, Argentina

https://doi.org/10.1007/978-3-030-39448-6_9
174 D. Deregibus et al.
for buildup of biomass over the course of the year. A positive CB in Antarctica
occurs only during the ice-free period in spring and summer, when p hotosynthetically
active radiation (PAR, 400–700 nm) penetrates deeply into the water column. The
accumulated carbon compounds during this period are stored and remobilized to
support metabolism for the rest of the year.
Over the last decades climate warming has induced a severe glacial retreat in
Antarctica and has opened newly ice-free areas. Increased sediment runoff, and
reduced light penetration due to melting during the warmer months, may lead to a
negative CB with changes in the vertical distribution of seaweeds. Furthermore,
warmer winters and springs result in earlier sea-ice melt, causing an abrupt increase
in light, compensating the reduction in PAR in summer or increasing the annual
light budget. Studies performed in Potter Cove, Isla 25 de Mayo/King George
Island, reveal that algae growing in newly ice-free areas did not acclimate to the
changing light conditions. Lower or even negative CB values in areas close to the
glacier runoff seem to be primarily dependent on the incoming PAR that finally
determines the lower distribution limit of seaweeds. The present chapter discusses
how carbon balance respond to the changing Antarctic light environment and its
potential implications for the fate of benthic algal communities.
Keywords Metabolic carbon balance · Glacier runoff · Light requirements ·

Photosynthesis · Photosynthetic acclimation · Turbidity
9.1 Introduction
9.1.1 Climate Change in the Antarctic Coastal Zone
Rapid regional warming will continue to be one of the major forcing elements in
Antarctica during this century (Hendry et al. 2018; IPCC 2014, 2019). The Western
Antarctic Peninsula (WAP) is a hotspot of climate warming evidenced by a rapid
increase in air temperature and, as a consequence, strong sea-ice decline and fast
glacial retreat (Cook et al. 2005; Meredith and King 2005; Stammerjohn et al. 2008;
Turner et al. 2009). This region is also highly impacted by ice disturbance, and the
rates of iceberg scour have been shown to increase with consequences still not well
understood for the benthic life (Barnes and Souster 2011; Barnes et al. 2014). Due
to a high density of research stations, accessibility, and mild climate, the WAP
coastal areas are natural laboratories for studying how ecosystems respond to rapid
climate change (Constable et al. 2014; Deregibus et al. 2017; Lagger et al. 2018). In
fact, a high diversity of benthic assemblages concentrate in the upper 70 m zone,
which is subject to diverse physical perturbations.
9 Carbon Balance Under a Changing Light Environment 175
A notorious phenomenon in coastal zones of the WAP is the formation of “newly

ice-free areas” as a consequence of glacier retreat (Cook et al. 2005; Rückamp et al.
2011; Quartino et al. 2013). In these areas new substrates become available for ben-
thic colonization (Constable et al. 2014; Lagger et al. 2017, 2018). In parallel, the
enhanced glacier melting leads to increased turbidity and decreases salinity in the
water column (Barnes and Conlan 2007; Campana et al. 2009; Schloss et al. 2012;
Bers et al. 2013; Grange and Smith 2013). Moreover, ice-scouring events can be
intensified (Barnes and Souster 2011; Barnes et al. 2018). These climate-driven
rapid shifts and concomitant new stressors (e.g., sedimentation, ice disturbance) can
have complex consequences for the functioning of the coastal ecosystems (Gutt
et al. 2015). Thus, various hypotheses have arisen inspiring numerous studies on
their effects on coastal ecosystems (Smale and Barnes 2008; Gutt et al. 2011;
Schofield et al. 2010; Torre et al. 2012; Ducklow et al. 2013; Barnes et al. 2014;
Moon et al. 2015; Sahade et al. 2015; Valdivia et al. 2015). The question whether
rising air temperatures could cause changes in the light environment in Antarctic
coastal zones and their effect on primary producers is central to understand the
future benthic primary production in these coastal ecosystems (Zacher et al. 2009;
Clark et al. 2013, 2017). In this context, given that photosynthesis in coastal areas is
the most important biological process affected by light and due to its vital impor-
tance in neritic areas, seaweeds can be considered as sentinel taxa to evaluate these
changes.
9.1.2 A
ntarctic Seaweeds and the Changing Light
Environment
The availability of light for photosynthesis and growth is the major factor governing
depth distribution of seaweeds (Lüning 1990). At the southern distribution limit of
seaweeds in the Antarctic, the polar night lasts for about 4 months. Sea-ice cover
extends the period of hibernal darkness even more (reviewed in Zacher et al. 2009).
Besides phytoplankton blooms, circulation and wind have major importance in lim-
iting light penetration into the water column (Schloss et al. 2012). Thus, Antarctic
seaweeds are well adapted to cope with extended periods of darkness showing low
light requirements for photosynthesis (Ek) and high photosynthetic efficiencies (α).
In addition, a number of species have also the ability to cope with high light condi-
tions in summer (Wiencke 1990; Gómez et al. 1997, 2009; Wiencke and Amsler
2012; see also Chap. 7 by Gómez and Huovinen).
Seasonality strongly determines the fluctuations in abiotic factors, which affect
the physiological and ecological performance of seaweeds (Wiencke and Amsler
2012; Marcías et al. 2017). In Antarctica, adaptation to the seasonality of the light
regime is a fundamental prerequisite for the ecological success of seaweeds
(Wiencke et al. 2011). There are two different growth strategies, i.e., season antici-
pators and season responders sensu Kain (1989). The season anticipators start grow-
ing in late winter/spring. In contrast, the season responders start growth and
reproduction later in spring and summer when the light conditions are favorable
(Wiencke and Amsler 2012; see also Chap. 10 by Navarro et al.). However, both
groups are highly dependent on the light availability in spring and summer when
primary production mostly occurs as the solar angle is high and fast ice is absent
(Miller and Pearse 1991; Wiencke et al. 2006; Runcie and Riddle 2012; see also
Chap. 7 by Huovinen and Gómez).
Changes in light availability do not only have natural causes; besides the high
seasonal variability in Antarctica, changes in external variables that influence sea-
weeds are due to anthropogenic reasons (e.g., higher regional air temperatures due
to the CO2 emissions) (Vaughan et al. 2003; Turner et al. 2013). Especially in coastal
areas, climate change may significantly shrink the annual light budget available for
benthic primary producers due to an enhancement of sedimentation and a decrease
in the duration of the fast ice season (Clark et al. 2013; Quartino et al. 2013). Algae
growing in newly ice-free areas are subjected to a reduction of light penetration,
which constitutes a constraint for photosynthesis (Schloss et al. 2012; Wiencke and
Amsler 2012; Deregibus et al. 2016; González et al. 2017; see also Chap. 8 by
Quartino et al.). Furthermore, glacier melting also causes accumulation of sediment
on the seafloor, which could affect the attachment of benthic algae (Johnston et al.
2007). On the other hand, beneficial effects of sediment input could be considered
during spring and summer by attenuating high PAR, which may inhibit the recruit-
ment of macroalgal species (Graham 1996; Hanelt 1996; Hanelt et al. 1997) or may
protect against harmful UV radiation (Roleda et al. 2009). However, previous stud-
ies have shown a positive relationship between the degree of light penetration and
the complexity of the macroalgal community (in terms of diversity and the presence
of large perennial species) in the newly ice-free areas (Quartino et al. 2013). Thus,
the time of occurrence of the thawing is extremely relevant for seaweeds as favor-
able light conditions for algal growth are constrained to only a few months of the
year during the bright light season (Wiencke and Amsler 2012; see also Chap. 7 by
Huovinen and Gómez). Here, the maintenance of positive carbon balance is proba-
bly one of the most significant physiological adjustments of seaweeds to cope with
these changing light conditions (Gómez et al. 1997; Deregibus et al. 2016).
9.1.3 C
arbon Balance: Concepts and Methodological
Challenges
The production of organic matter via photosynthesis using carbon dioxide, water,
and sunlight is known as primary production, while primary productivity is the rate
at which energy is converted to organic substances by photosynthetic organisms
(Hurd et al. 2014). The rates of primary productivity refer to the efficiency at which
solar energy is used to fix inorganic carbon and create biomass, and hence it is an
essential parameter reflecting the ecosystem function (Falkowski and Raven 1997).
The carbon balance (CB) equalizes the assimilated carbon (C) during photosyn-
thesis in relation to the C that is lost due to respiration (Wiencke and Amsler 2012).
Photosynthesis versus irradiance (P-E) curves describes how the photosynthetic rate
(e.g., net O2 evolution) varies with increasing irradiance. Integrating data on daily
changes of in situ irradiance with the P-E-derived parameters, Ek, the photosynthetic
capacity (Pmax), and dark respiration (Deregibus et al. 2016), it is possible to calcu-
late the daily metabolic CB as an indicator of the physiological ability to live at a
certain depth (Hanelt and Figueroa 2012). In coastal areas not affected by glacial
melt, PAR can penetrate into the water column as deep as 30 m (1% depth) during
late winter-spring, still allowing a positive CB (Gómez et al. 1997; see also Chap. 7
by Huovinen and Gómez).
The lower distribution limit of algae is determined by their capacity to main-
tain a positive CB to build up biomass (Hanelt and Figueroa 2012). During this
period a positive CB replenishes the energy budget to be used to survive the long
periods of darkness during the rest of the year (Wiencke et al. 2011; Deregibus
et al. 2016). Several studies indicate that the daily exposure time to light is more
important than the intensity of light for macroalgal productivity in coastal areas
(Dennison and Alberte 1985; Matta and Chapman 1991; Gómez et al. 1997).
Direct associations between increases in turbidity and decreases in macroalgal
productivity have been reported from a variety of systems worldwide (Airoldi
2003; Anthony et al. 2004; Spurkland and Iken 2011; Pritchard et al. 2013).
Similarly, changes in the productivity of seaweeds in relation to sea ice variations
have been reported in Antarctic (Clark et al. 2013) and Arctic (Krause-Jensen and
Duarte 2014) assemblages. Apparently, direct and indirect effects of climate
change on light availability will have dramatic effects on the annual macroalgal
CB, which could result in changes in benthic primary productivity (Runcie and
Riddle 2012; Bartsch et al. 2016; Deregibus et al. 2016; Gómez et al. 2019; see
also Chap. 8 by Quartino et al.).
Various mathematical models have related irradiance to photosynthesis in order
to estimate primary productivity (Jassby and Platt 1976; Nelson and Siegrist 1987;
Henley 1993; Jones et al. 2014). However, the photosynthetic parameters α, Ek, and
Pmax derived from P-E curves may differ depending on the selected fitting model
(Smith 1936; Steele 1962; Webb et al. 1974; Jassby and Platt 1976; Cullen 1990;
Frenette et al. 1993; Henley 1993). Thus, productivity estimates using distinct mod-
els may not be comparable and even lead to erroneous conclusions (Frenette et al.
1993; Deregibus et al. 2016). Therefore, the use of best mathematical fit will
improve considerably the quality of our productivity estimations (Jassby and Platt
1976; Nelson and Siegrist 1987).
The primary productivity of seaweeds can be estimated in several ways, e.g.,
through changes in net weight, through growth, in situ productivity measurements,
or measurements of dissolved oxygen production (Gómez et al. 2009; Runcie et al.
2009; Runcie and Riddle 2011; Hanelt and Figueroa 2012). These different method-
ologies show constraints in their ability to accurately describe the primary produc-
tivity in marine environments (Runcie and Riddle 2012). In the WAP, Gómez et al.
(1997) did an initial effort to calculate the seaweed primary productivity through the
calculation of the daily metabolic CB using the amount of in situ daily hours when
algae are light saturated. Their findings could explain well the vertical zonation of
seaweeds according to the light regime at the WAP (Gómez et al. 1997).
9.2 Carbon Balance: A Case Study in Potter Cove
Over the last years, numerous studies have been performed in Potter Cove, Isla 25
de Mayo/King George Island, which is a distinctive example of an area with a spe-
cial focus on studies related to the impacts of climate-forced glacier retreat across
an entire shallow water ecosystem.
Adjacent to Carlini Station, Potter Cove is surrounded by the Fourcade Glacier.
Over the last decades, this glacier has been retracting and melt water inflow in the
cove increased (Eraso and Dominguez 2007; Rückamp et al. 2011) (Fig. 9.1). Newly
ice-free areas in costal shallow areas were formed and are still appearing (Quartino
et al. 2013; Lagger et al. 2017, per obs). In this cove, increase in sedimentation has
negatively affected species and changed benthic communities (Torre et al. 2012;
Quartino et al. 2013; Pasotti et al. 2014; Sahade et al. 2015; Campana et al. 2018;
Meredith et al. 2018; Jerosch et al. 2019; see Chap. 8 by Quartino et al.). As a con-
sequence of glacier melting, a spatial gradient developed along the cove, providing
the opportunity to analyze the primary productivity under a natural abiotic gradient
(Deregibus et al. 2016). For the first time, the primary productivity of seaweeds
growing in these new areas in a gradient of glacial influence was estimated. High
“glacier influence” was defined as a decrease in light penetration in the water col-
Fig. 9.1. Small creek originated by glacier melting during summer months causing a discharge of
turbid fresh water filled with terrigenous sediments into the inner zone of Potter Cove. (Adapted
from Deregibus (2017) with permission (photos by Dolores Deregibus))
umn (increased turbidity) due to sediment input. Improvements on the calculations

were proposed through a novel and more accurate approximation of seaweed CB
calculations with the inclusion of in situ continuous-light measurements (Deregibus
et al. 2016).
9.2.1 Light Availability
The major new achievement and challenge was to install and perform continuous
underwater PAR measurements along a depth gradient (5, 10, 20, and 30 m) in sev-
eral areas along the turbidity gradient in summer 2010, for the first time in an
Antarctic environment. Since then, daily continuous PAR measurements are
obtained at 10 m depth and are utilized in combination with the photosynthetic
parameters to estimate the CB of seaweeds over the seasons and along turbidity
gradients (Deregibus 2017).
The light loggers (for details see Deregibus et al. 2016) were installed in an
upright position, on a specially constructed concrete base and are periodically
secured by SCUBA divers at the respective sites (Fig. 9.2). The PAR data could then
be used to plot irradiance vs time with a time interval of 15 min (Fig. 9.3).
As an example, in Fig. 9.3, we present the mean PAR records of one selected
week in January 2010. At 5 m depth, seaweeds were exposed to PAR for 12 h (mean
daily irradiance of 22.2 μmol photons m−2 s−1). At 10 m depth, PAR values showed
an abrupt decrease indicating a very low daily light budget below 5 m in summer in
this area. Also, the daily exposure time to sunlight PAR decreased with increasing
depths shortening the photoperiod (Fig. 9.3).
Despite high solar angle, the question rises how the investigated seaweeds may
survive and grow under these conditions in Potter Cove. It became evident that it is
insufficient to consider not only summer periods to assess productivity but also
annual irradiance (Fig. 9.4), and carbon budgets need to be calculated. Accordingly,
Fig. 9.2 Underwater PAR measurements: (a) Odyssey Logger Sensor for continuous PAR mea-
surements. Setup (concrete base and adjustable arm) that holds the sensor. (b) Diver exchanging
the sensor. (Adapted from Deregibus (2017) (photos by Dolores Deregibus))
Fig. 9.3 Daily course of
Irradiance (µmol photons m-2 s-1)

100
irradiance in newly ice-free 5m
area in Potter Cove at 5 10 m
and 10 m depth between
Jan 15 and 22, 2010 (Data
were averaged over seven
50
continuous days). (Adapted
from Deregibus et al.
(2016))
0
0:00 4:00 8:00 12:00 16:00 20:00 0:00
Time of the day
Fig. 9.4. Annual course of incident irradiance measured at Potter Cove, Isla 25 de Mayo/King
George Island. Daily mean of PAR was integrated over single months in a newly ice-free area dur-
ing 2015
whole-year continuous PAR measurements are being performed to estimate the

light climate over an entire year – and between years in Potter Cove (e.g. Fig. 9.4).
During 2015, which serves as an example here, there was an evident presence of
fast ice in winter leading to very low mean values of daily PAR, followed by an
abrupt increase of the PAR intensity once the pack-ice broke up in spring (Fig. 9.4).
Whole-year underwater in situ irradiances show that the most productive season
may start as early as October with highest mean daily PAR values. This is in con-
trast to our expectations as during the warmer summer months (December to
March), the light intensity was lower than in spring, mainly due to the input of sedi-
ment of terrestrial origin into the water column. On an interannual scale, these val-
ues may differ considerably (Deregibus unpublished). Similar results were found
for the Arctic in Kongsfjorden (Spitsbergen), a fjord system highly affected by melt-
ing glaciers (Bartsch et al. 2016; Pavlov et al. 2019). Overall, our long-term, year-
round PAR measurements can be further used to estimate the annual primary
productivity of Antarctic seaweeds in coastal areas subjected to extreme changes in
light availability.
9.2.2 Photosynthetic Acclimation
The endemic brown alga Himantothallus grandifolius (A. Gepp and E. S. Gepp)
Zinova and the red alga Palmaria decipiens (Reinsch) Ricker, presented here as
examples, were sampled at 5 and 10 m in the vicinity of the light logger.
Photosynthetic oxygen evolution and dark respiration were measured under labora-
tory conditions, and photosynthesis versus irradiance curves (P-E curves) were
obtained and used to calculate photosynthetic parameters with the hyperbolic tan-
gent function of Jassby and Platt (1976). This function, which was proved to be the
best fitting model to the experimental data, is expressed as:
P = Pmax ∗ tanh (α E / Pmax ) + R

where P is the photosynthetic rate, Pmax is the maximum photosynthetic rate, tanh is
the hyperbolic tangent, α is the initial slope of the curve at low irradiance, E is the
incident irradiance, and R is the dark respiration rate (Fig. 9.5).
The hyperbolic tangent function (Jassby and Platt 1976) was found to be the best
fit for our data compared to other commonly used models (e.g., Webb et al. 1974).
Jassby and Platt (1976) found that their hyperbolic tangent equation proved to be
the best overall fit to 200 types of datasets in a comparison of various equations
(Jassby and Platt 1976; Jones et al. 2014).
In Potter Cove, photosynthetic parameters such as Pmax, α, and Ek of seaweeds
growing in newly ice-free areas with variable glacial influence and at different
depths were generally quite similar. This indicates a low acclimation potential of
photosynthesis to different irradiance regimes (Deregibus et al. 2016). The absence
of photoacclimation in Antarctic seaweeds living under different? light availability
has been reported previously (Gómez et al. 2009). Apparently, this is a characteristic
that forms part of suite of photobiological features conferring the extreme shade
adaptation of these organisms, developed primarily to cope with dim light in
autumn-winter (Gómez and Huovinen 2015). In fact, similar values of Pmax and α
were reported at different depths for H. grandifolius (Drew and Hastings 1992;
Fig. 9.5. Photosynthesis-irradiance (P-E) curves of Palmaria decipiens (a) and Himantothallus
grandifolius (b) in a newly ice-free area in Potter Cove, which represents a typical P-E curve for a
shade-adapted species. Generally, the oxygen production under light saturation is lower in H. gran-
difolius than in P. decipiens. Both species did not show any sign of photoinhibition even under
highest irradiances of 800 μmol photons m−2 s−1. (Adapted from Deregibus et al. (2016))
Gómez et al. 1997), and in P. decipiens, Gigartina skottsbergii Setchell and Gardner
Trematocarpus antarcticus (Hariot) Frederic and Moe, and Desmarestia anceps
Montagne (Gómez et al. 1997). Interestingly, other studies, carried out in the Ross
Sea, Antarctica (Schwarz et al. 2003), in Greenland (Kühl et al. 2001), and in the
Arctic (Krüger 2016) using chlorophyll fluorescence, suggest a greater acclimation
potential of seaweeds to low light at deeper depths as reflected in their lower Ec
(photosynthetic compensation point), Ek, and rETRmax values. Furthermore, a recent
study reports different photosynthetic response to low light between algae growing
in Antarctica and in the Subantarctic (Navarro et al. 2019).
9.2.3 Daily Carbon Balance of Seaweeds
Calculations of daily net CB (mg C g−1 FW day−1) integrated the photosynthetic

parameters derived from the P-E curves and the incident underwater irradiances
according to the following formula:
  E1 
  
E
P = Pmax ∗ tanh  α  average 2  + R
  Pmax 
  
  
Fig. 9.6 Example of the daily metabolic carbon balance of two selected Antarctic seaweeds grow-
ing at different depths in a highly turbid newly ice-free area in Potter Cove during summer 2010.
Values correspond to an overall net gain or loss of C during 24 h. (Adapted after Deregibus et al.
(2016))
where “average (E1:E2)” is the average of two incident irradiances between time 1
and time 2. This formula improved the calculation of the net oxygen production
along an entire day (Fig. 9.6) and shows that in an area with high turbidity due to
sedimentation, the CB was only positive for P. decipiens at 5 m depth with a mean
value of 0.2 (±0.4) mg C g−1 FW day−1, but negative at 10 m. In the case H. grandi-
folius, it was negative for both depths (Fig. 9.6). Negative values were mainly due
to the low light availability and a reduction of the time to which algae were exposed
to light (Deregibus et al. 2016). The results agree with the in situ distribution of both
species: they grow only to a maximum depth of 10 m in this highly disturbed area
(Deregibus et al. 2016; Deregibus 2017).
9.3 N
ew Scenarios and Their Implications for Algal
Photosynthesis
Carbon balance is the most conclusive parameter to understand and explain the
zonation patterns in Antarctic seaweeds (Gómez et al. 2009). This parameter is
directly related to light availability as it is lower or negative in more turbid areas
and/or at deeper depths compared to shallower depths and areas with low turbidity.
Isla 25 de Mayo/King George Island is characterized by a marked increase in the
atmospheric temperature in recent decades (Ferron et al. 2004; Schloss et al. 2012;
Bers et al. 2013). Falk and Sala (2016) indicated an anticipation of the thawing
period towards spring and an extension towards autumn in this area. The latter, and
the fact that turbidity has increased not only in summer but also in spring in Potter
Cove over the last years (Schloss et al. 2012; Deregibus et al. 2016), and that in
some cases negative CB have also been measured in spring (Deregibus 2017) raises
additional questions. For example: What would happen if the thawing season starts
earlier due to increased air temperatures, leading also to negative CB in spring?
Would the storage compounds produced in summer be enough to support the energy
requirements the rest of the year?
Conversely, it should also be considered that warmer winters and springs lead to
earlier fast ice melting (Schloss et al. 2012; Deregibus et al. 2017), which causes an
abrupt increase of light, probably compensating the reduction of PAR in summer or
even significantly increasing the annual light budget for seaweeds (Johnston et al.
2007; Clark et al. 2013). This last assumption leads to additional questions: Will the
total CB values become really lower under a future warming? Or will there be com-
pensation due to a higher light availability in late winter and early spring (less or no
fast ice cover)?
If the annual photon doses do not sustain growth and reproduction at a certain
area, seaweeds will not survive (Runcie and Riddle 2012). Furthermore, light not
only serves as a source of energy for seaweeds, but it is also an environmental signal
inducing changes in processes which are dependent on daylength as trigger signal
Climate Change and Underwater Light Variations
Fast ice
Temperature
duration and
increase
extension decrease
Glacier Turbidity Underwater Seaweed

retreat increase Irradiance
Community
Changes in wind
directions and
intensities
Fig. 9.7 Conceptual model on the impact of direct and indirect climate change factors on the
underwater irradiance in newly ice-free areas at the Western Antarctic Peninsula. (Adapted from
Quartino et al. (2013) and Deregibus (2017))
(Hanelt and Figueroa 2012). The seasonal development of seaweeds must be tuned
to the strong seasonality of the light conditions (Wiencke et al. 2011). This is very
important as variations in PAR would not only affect the primary energy source but
could also alter the information to modulate the morphogenetic development and
the other signals for growth and reproduction. It is key and maybe relevant to eluci-
date the growth seasons that are being more/most? affected by global warming
during the year, as higher temperatures in winter impact differently on the light
availability than in spring and summer (Wiencke and Amsler 2012).
The conceptual model in Fig 9.7 describes the ways through which these envi-
ronmental changes could be affecting the light availability for the benthic autotro-
phic organisms. Environmental conditions directly affect, and are reflected, in the
underwater annual PAR budget. Light changes are mediated by a series of factors:
firstly, glacier melting increases the amount of sediments in the water column and
enhances turbidity. This factor has most impact on benthic primary producers as it
directly and negatively reduces light availability, which is a constraint for photosyn-
thesis. Secondly, the decrease in fast ice duration may increase the open water
period and thereby the availability of underwater light in winter and spring. Thirdly,
wind, depending on its intensity and direction, has a significant impact on sediment
resuspension and distribution processes of the sediments limiting light penetration.
This model is complementary to the general conceptual model shown in Chap. 8 by
Quartino et al., on the environmental factors affecting the coastal macroalgal
community.
9.4 Concluding Remarks and Future Prospects
So far, glacial retreat has opened new space (hard substratum) in the inner Potter
Cove and seaweeds have colonized and persisted in newly ice-free areas (Quartino
et al. 2013; Campana et al. 2018). Although newly ice-free areas are highly affected
by the glacial influence, several seaweed species grow under high sedimentation
showing their exceptional ability to survive and successfully reproduce under such
conditions (Becker et al. 2011; Quartino et al. 2013; Deregibus et al. 2016).
The realization that seaweeds are the most productive marine macrophytes and
identified as very relevant contributors to global blue carbon sequestration (Hill
et al. 2011; Krause-Jensen and Duarte 2016) has consigned them in a key role at a
global scale. Considering that the spatial distribution of the seaweed community has
expanded to the inner side of Potter Cove, it is likely that the increase in seaweed
biomass leads to an enhanced production in this area (Quartino et al. 2013), with
cascading effects to the rest of the food web (Marina et al. 2018). This raises the
question of how changes in seaweed productivity could affect the rest of the coastal
ecosystem in Potter Cove. In this context, given that seaweeds in Potter Cove are in
a constant tradeoff between extending their distribution into newly ice-free areas
and being affected by climate change, an interest to reveal whether this expansion
will give way to a persistence and maturation of these communities in these new
areas exists.
Due to climate change in polar ecosystems, shifts from predominantly heterotro-
phic to autotrophic states of shallow polar seabeds have been predicted (Bartsch
et al. 2016; Clark et al. 2013, 2017). Kortsch et al. (2012) and Scherrer et al. (2018)
reported marked community shifts with abrupt and persistent increase in macroalgal
cover in the Arctic following the extension in the ice-free period. Krause-Jensen
et al. (2012) also reported substantial increases in the productivity and maximal
depth distribution of kelps in Greenland. Furthermore, in the Arctic it was also
stated that longer ice-free seasons have extended the growth season of seaweeds
favoring an increased diversity of algae and macrozoobenthos (Paar et al. 2016). In
this context, it is also expected that further glacier retreat will continue to favor
seaweed colonization in new coastal areas potentially resulting in higher productiv-
ity and carbon sequestration (Clark et al. 2013; Krause-Jensen and Duarte 2016).
The future projection in case study systems such as Potter Cove would be to
continue with the long-term monitoring of multiple abiotic factors and primary pro-
ductivity calculations. Knowledge on the minimum light requirements for seaweeds
and on their ecophysiological characteristics are needed to better understand and
predict macroalgal survival and possible changes in primary productivity, distribu-
tion, and depth zonation in areas affected by glacial melting due to climate change.
Continuous PAR measurements are currently being performed in the newly ice-free
areas of Potter Cove, which is a unique data set in terms of time span (more than five
years) and continuity in a gradient of glacial influence in Antarctica.
Finally, as a way to understanding the regional variability and its impacts on the
biota, these monitoring programs require international collaboration including inte-
grated actions among different Antarctic stations (Deregibus et al. 2017).
Acknowledgments The fieldwork described in this chapter has been performed at Carlini Station-
Dallmann Laboratory within the framework of the scientific collaboration existing between
Instituto Antártico Argentino/Dirección Nacional del Antártico and the Alfred-Wegener-Institute,
Helmholtz Centre for Polar and Marine Research (AWI). The research was supported by Grants
from DNA-IAA (PICTA 7/2008–2011) and ANPCyT-DNA (PICTO 0116/2012–2015, PICT
2017-
2691). These studies were also supported by MINCYT-BMBF Program (AL/17/06-
01DN18024) and Conicyt-Chile (Center FONDAP IDEAL 15150003). We are especially grateful
to the scientific, logistic, and diving groups of Carlini Station. We thank Carolina Matula for her
contribution to improve the annual light figure. We gratefully acknowledge financial support by the
AWI. We thank Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, for allow-
ing the reuse of material published in Deregibus 2017 Thesis. The present research also presents
an outcome of the EU project IMCONet (FP7 IRSES, Action No. 319718) and EU project
CoastCarb, Funding ID 872690, H2020-MSCA-RISE-2019 – Research and Innovation Staff
Exchange.
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Chapter 10
Life History Strategies, Photosynthesis,
and Stress Tolerance in Propagules
of Antarctic Seaweeds
Nelso Navarro, Pirjo Huovinen, and Iván Gómez
Abstract Reproduction is one of the most important processes to maintain sea-

weed populations. In general, growth and reproduction of seaweeds depend on envi-
ronmental cues, such as change in temperature, light, and nutrients. However, the
fact that Antarctic waters show a small variation in temperature and nutrient levels
over the year, these biological processes depend mainly on variables related to light
conditions, especially daylength. This seems to be more obvious in the eulittoral
and shallow sublittoral species, because the reproduction and growth coincides with
the spring season. However, in species inhabiting the deeper sublittoral zone, repro-
duction seems to be controlled by a free-running endogenous clock synchronized by
the seasonal variation of daylength or by photoperiodisms. Whatever the case, the
Antarctic environment imposes physiological constraints to reproductive output,
settlement and development of propagules, recruitment, and growth of seaweeds.
Early life stages (e.g., spores, gametes, propagules, and plantlets) are extremely
shade-adapted and susceptible to environmental stress, such as exposure to UV
radiation; however, they are thermally well adapted, at least for short periods of
time, allowing them to develop in a highly variable environment. In this chapter, we
review the main reproduction strategies that Antarctic seaweeds display to cope
with the extreme environment. Additionally, we review recent studies on stress tol-
erance of early developmental stages from selected species. In scenarios of the
changing Antarctic environment due to warming, UV radiation, freshening, and
N. Navarro (*)
Laboratorio de Ecofisiología y Biotecnología de Algas (LEBA), Universidad de Magallanes,
Punta Arenas, Chile
e-mail: nelso.navarro@umag.cl
P. Huovinen · I. Gómez
Research Center Dynamics of High Latitude Marine Ecosystems IDEAL, Valdivia, Chile
e-mail: pirjo.huovinen@uach.cl; igomezo@uach.cl

https://doi.org/10.1007/978-3-030-39448-6_10
194 N. Navarro et al.
other emergent stressors, the knowledge on adaptive life strategies of early develop-
mental phases can allow us better predicting the fate of seaweed communities.
Keywords Life history stages · Photosynthetic light requirements · Reproduction

· Seaweed propagules · Seasonal development
10.1 Seasonal Strategies and Life History Cycles
In their environment, seaweeds are exposed to a complex suite of abiotic variables,

whose interaction may affect reproduction synergistically or antagonistically. In the
case of Antarctic seaweeds, the life strategy of the individual species is regulated by
the strong seasonal variation in light conditions (Wiencke et al. 2009). Two different
growth (and reproduction) strategies have been identified: the season anticipator
and season responder strategy (sensu Kain 1989; Wiencke and Clayton 2002). These
strategies have been corroborated through long-term laboratory culture experiments
in which temperature and nutrient levels were kept constant and only light and day-
length were modified in order to simulate the seasonally fluctuating Antarctic irradi-
ances (Wiencke 1990a, b; Dummermuth and Wiencke 2003). Moreover, other
phenological events such as seasonal induction of propagules, their release, and the
growth of early developmental stages have been examined in the field (Roleda et al.
2007, 2008; Zacher et al. 2009; Navarro et al. 2016).
10.1.1 Season Anticipators
This group of algae grows and reproduces in winter under short-day and low-light
conditions (Fig. 10.1). Thus, physiological and reproduction processes seem to be
controlled by a free-running endogenous annual rhythm synchronized by the sea-
sonal changes of daylength or by photoperiodisms and not by environmental condi-
tions (such as levels of light or temperature) as demonstrated by Lüning and tom
Dieck (1989), tom Dieck (1989), and Lüning and Kadel (1993) in several species
from temperate regions. Likewise, the growth of Antarctic season anticipators has
been related to increasing daylength during the late winter and early spring (Wiencke
et al. 2007, 2009). Many endemic Antarctic seaweeds with sublittoral distribution
are regarded as season anticipators, e.g., the brown seaweeds Himantothallus gran-
difolius (A.Gepp and E.S.Gepp) Zinova, Desmarestia anceps Montagne, D. antarc-
tica Moe et Silva, Phaeurus antarcticus Skottsberg (Wiencke 1990a), Ascoseira
mirabilis Skottsberg (Gómez et al. 1995, 1996; Wiencke 1990a), and D. menziesii
J. Agardh (Gómez and Wiencke 1996) and the red seaweeds Palmaria decipiens
10 Life History Strategies, Photosynthesis, and Stress Tolerance in Propagules… 195
Fig. 10.1 Life history development of some conspicuous Antarctic seaweeds. The green line
shows the period when growth starts. In the case of season anticipators, growth take place in late
winter onwards, while in responders, growth occur during spring onwards
(Reinsch) Ricker (Wiencke 1990b), Paraglossum salicifolia (Reinsch) Schowe

M. Lin, Fredericq, and Hommersand (formerly Delesseria salicifolia Reinsch),
Gymnogongrus antarcticus Skottsberg; G. turquetii Hariot, Hymenocladiopsis pro-
lifera (Reinsch) M. J. Wynne (formerly H. crustigena R.L. Moe), Trematocarpus
antarcticus (Hariot) Fredericq and R. Moe (formerly Kallymenia antarctica Hariot),
and Phyllophora ahnfeltioides Skottsberg (Dummermuth and Wiencke 2003).
Reproductive responses to the environment are particularly evident in season
anticipators with strongly heteromorphic phase expression, such as in members of
the genus Desmarestia (Wiencke et al. 1991, 1995, 1996), Himantothallus grandi-
folius (Wiencke and Clayton 1990), and Phaeurus antarcticus (Clayton and Wiencke
1990). The heteromorphic life history of large brown algae is characterized by the
development of large perennial sporophytes and a marked reduction of the gameto-
phytic generation (Clayton 1988). In these species, microscopic gametophytes and
early stages of sporophytes grow under limited light conditions during winter,
whereas adult stages of macroscopic sporophytes grow in late winter–spring
(Fig. 10.1). In the case of Desmarestia anceps, one of the most important seaweeds
in terms of biomass in the Antarctic region, the microstage of male and female
gametophytes becomes fertile between July and September under a daylength of 5
and 7 h day−1 at photon fluence rates <3 μmol photon m−2 s−1 (Wiencke et al. 1996).
The induction of fertility is a photoperiodic short-day response as revealed by the
effect of a night-break regime (Wiencke 1990b; Wiencke et al. 1996), while in con-
tinuous darkness gamete formation was inhibited (Wiencke et al. 1996).
Gametogenesis under short daylengths was also demonstrated in other Desmarestiales
members, e.g., Himantothallus grandifolius (Wiencke and Clayton 1990) and
Desmarestia menziesii (Wiencke et al. 1995; Gómez and Wiencke 1997), whereas
no daylength dependence of gamete formation has been found in Desmarestia ant-
arctica (Wiencke et al. 1991). In this latter species and in Phaeurus antarcticus,
gametogenesis occurs both in short and long days. According to Wiencke et al.
(2009) the phenology in these species is controlled by the sporophytic stage, which
becomes fertile at daylengths between 6 and 8 h day−1, while gametophytes form
gametangia soon after germination (Clayton and Wiencke 1990; Wiencke 1990a;
Wiencke et al. 1991). A typical feature of Antarctic Desmarestiales is the fact that
they exhibit in situ fecundation, and the juvenile sporophytes remain attached to the
female gametophytes (Wiencke et al. 1995, 1996). This feature could have ecologi-
cal significance for the sporophytes recruitment and dominance of this group in
Antarctic environment (Wiencke et al. 2006).
The brown alga Ascoseira mirabilis, another season anticipator, exhibits maxi-
mum growth rates in late winter–spring, while the minimum growth rates were
recorded in May–June (Wiencke 1990a). However, a further, much smaller growth
optimum became evident between January and March. On the other hand, unlike
typical season anticipators, fertile fronds in A. mirabilis are present all year round,
and growing and reproducing when environmental conditions are favorable (see
below). A. mirabilis is the only member of the order Ascoseirales, and the Antarctic
environmental constraints might have exerted an evolutionary pressure to develop a
unique life history and reproductive biology when compared with other
Phaeophyceae (Roleda et al. 2007). The species is monoecious with sexual (iso-
gamia) reproduction. There is one, free-living diploid generation, and zygotes
develop into new individuals (Wiencke and Clayton 2002). Conceptacles are scat-
tered all over the blades and the extrusion of gametangial masses through the osti-
oles precedes the release of heterokont gametes (Müller et al. 1990). Zygote
formation follows immediately after fusion of gametes.
For red seaweeds, the phenology of six season anticipator species from the
Antarctic, Paraglossum salicifolium, Gymnogongrus antarcticus, Gymnogongrus
turquetii, Hymenocladiopsis prolifera, Trematocarpus antarcticus, and Phyllophora
ahnfeltioides were investigated by Dummermuth and Wiencke (2003) in a two-year
culture study under fluctuating daylengths simulating the Antarctic conditions. The
period of highest growth rate in these species was registered between September
and November (late winter–spring) and the formation of new blades occurred from
January/February onwards. Before the summer solstice, growth ceased. However, in
Hymenocladiopsis prolifera, the seasonal growth peak was observed in August
when the light conditions increased from 3 to 25 μmol photon m−2 s−1. This suggests
that the phenology of season anticipators could not only be controlled by daylength
but also by photon fluence rates. Thus, in species distributed along wide ranges of
depth (e.g., 5–30 m), the seasonal growth peak could be later in the season at deeper
water depths and earlier in shallower waters. Reproductive fronds were not observed,
except in Trematocarpus antarcticus, which completed its life cycle with carpo-
spore formation between June and August, but with the first cystocarps found in
March (Dummermuth and Wiencke 2003). These results agree with the findings
reported by Lamb and Zimmermann (1977), who reported cystocarps in thalli of
T. antarcticus in January. Similarly, in Gymnogongrus antarcticus, cystocarps are
formed in the summer (Skottsberg 1953; Cormaci et al. 1992). Cystocarps and tet-
rasporangia of Paraglossum salicifolium have been observed in late winter (Wynne
1982). Likewise, spermatangia, cystocarps, and tetrasporangia in Delesseria san-
guinea, a comparable species in the same family, are formed during winter
(Kornmann and Sahling 1977). In the case of G. turquetii (Kylin and Skottsberg
1919; Skottsberg 1953) and Phyllophora ahnfeltioides (Kylin and Skottsberg 1919),
cystocarpic fronds have been reported between May and June (autumn).
The red seaweed Palmaria decipiens, one of the dominating species in terms of
biomass, is considered as season anticipator (Wiencke 1990b; Weykam and Wiencke
1996) and displays a heteromorphic life history perfectly adapted to the Antarctic
conditions. In this species female gametophytes represent the microscopic phase,
while the male gametophyte develops into a macro-thallus similar in morphology to
the tetrasporophytes (Fig. 10.1). The male and tetrasporophytic blades are formed
in winter (Wiencke 1990b; Weykam et al. 1997) and the optimum growth period and
high rates of net photosynthesis and photosynthetic efficiency coincide with increas-
ing light intensities in spring (Wiencke 1990b; Weykam and Wiencke 1996).
Tetrasporophytes become fertile in February and tetraspores develop in May into
semiglobular to discoid gametophytes. The females become fertile only once from
May to June. After fertilization, the female gametophyte is overgrown by the devel-
oping sporophyte, which matures and releases tetraspores in the next summer.
Interestingly, it takes about a year until male gametophytes become fertile; thus
fertilization of females is only possible by mature males of the previous season,
indicating a life span of the species of several years (Wiencke 1990b).
10.1.2 Season Responders
In these organisms growth and reproduction coincide with favorable light condi-
tions in spring and summer. Thus, these species react directly to the primary factors
in their environment (such as light availability) and show an opportunistic life strat-
egy (Wiencke 1990a, b). Most of the season responder species are distributed in the
eulittoral and upper sublittoral zone, and they can have temperate or cold-temperate
affinities (Wiencke et al. 2007; Navarro et al. 2019; see Chap. 12 by Campana
et al.). Well-known members of this group are the red seaweeds Iridaea cordata
(Turner) Bory (Weykam et al. 1997) and Gigartina skottsbergii Setchell et
N.L. Gardner (Wiencke 1990b), the brown alga Adenocystis utricularis (Bory)
Skottsberg (Wiencke 1990a), and the green seaweeds Ulva hookeriana (Kützing)
H. S. Hayden, Blomster, Maggs, P. C. Silva, Stanhope, and Walland (formerly
Enteromorpha bulbosa (Suhr) Montagne and Acrosiphonia arcta (Dillwyn)
J. Agardh (Wiencke 1990b).
The pseudoperennial Gigartina skottsbergii and Iridaea cordata have a triphasic
life history with isomorphic haploid male and female gametophytes and a diploid
tetrasporophyte. They occur normally in eulittoral pools and in the upper sublittoral,
but also can be found down to 30 m (Wiencke and Clayton 2002; Navarro et al.
2016). Both species show the maximum growth rate during the spring-summer sea-
son (e.g., December), while the minimum growth rates were recorded from May to
July (Wiencke 1990b). Mature tetrasporophytes and gametophytes of Iridaea cor-
data were observed during spring-summer (Roleda et al. 2008; Navarro et al. 2016).
Tetraspores and carpospores of this species germinate normally forming a discoid
germling from which new plantlets arise from July onwards. The plantlets show a
growth optimum between September and November and large blades are formed in
summer (Wiencke 1990b). Regrowth from the perennial basal parts of the blades is
possible (Wiencke and Clayton 2002), which could explain its dominance at the
eulittoral (Marcías et al. 2017). In the case of G. skottsbergii, Wiencke (1990b)
reported the induction of sporangium formation in tetrasporophytes in the labora-
tory by the end of September, when irradiances were between 27 and 46 μmol pho-
ton m−2 s−1, but spores were not released before June. In contrast, in the field,
reproductive fronds with viable propagules have been collected in October (Roleda
et al. 2008) and January (Navarro et al. 2016). This discrepancy in reproductive
periods might be related to differences related to the experimental setup of labora-
tory cultures by Wiencke (1990b). As suggested for the season anticipator
Hymenocladiopsis prolifera, photon fluence rates might also control the seasonal
phenology of this species. Thus, these algae apparently have the capacity to repro-
duce during a prolonged time span under changing environmental conditions.
Adenocystis utricularis has a heteromorphic life cycle with a sporophytic macro-

thallus and gametophytic microthallus. Spores from the macrothalli develop into
microscopic filamentous, dioecious gametophytes (Wiencke and Clayton 2002), the
dominant life phase under winter conditions in laboratory culture (Wiencke 1990a).
Macrothalli start to develop asexually on crustose parts of the microthalli from June
onwards. Between October and December, growth rates of macrothalli are optimal.
Reproductive macrothalli are present in January–February, while release of spores
occurs in February, after which the thalli disintegrate.
As suggested for other species with heteromorphic phase expression, the micro-
thallus is probably an important over-wintering stage (Wiencke and Clayton 2002).
However, eventually all developmental stages can be present at the same time
depending where they occur. De Reviers and Délépine (1981) reported that macro-
thalli are present throughout the year with juveniles being most abundant in October
in the eulittoral zone, while in the sublittoral zone, small macrothalli are present
only from November to June. Laboratory experiments where the photon fluence
rates varied from 2 to 46 μmol photon m−2 s−1 confirmed this field observation
(Wiencke 1990a). Thus, in the eulittoral zone, A. utricularis occurs as an aseasonal
annual, while in upper sublittoral zone, the species probably occurs as a seasonal
annual due to less available light. The species has been reported to occur down to
20 m (Wiencke and Clayton 2002), and at these depths the alga possibly is biannual
as suggested by Wiencke (1990a).
10.2 Photosynthetic Light Requirements of Early Stages
Irrespective of the life history strategy, the Antarctic environment imposes physio-
logical constraints to the reproductive output (propagules), settlement, recruitment,
and growth of seaweeds. However, seaweeds have adapted their biological pro-
cesses by evolving different functional mechanisms to cope with the Antarctic light
and temperature conditions. In general, Antarctic seaweeds are very low light
adapted, adult phases being able to photosynthesize at irradiances as low as
10 μmol photon m−2 s−1, while propagules can photosynthesize at even lower irradi-
ances (Gómez et al. 2009). In Table 10.1 the saturating irradiances of photosynthe-
sis (Ek values) of different Antarctic seaweed propagules are summarized, and in
Fig. 10.2 mean values of Ek for propagules from eulittoral and sublittoral algae are
plotted. With the exception of some eulittoral species, most of the studied Antarctic
seaweeds exhibit Ek values lower than 60 (μmol photon m−2 s−1). Although differ-
ences in saturation irradiance between eulittoral (65 ± 20 μmol photon m−2 s−1) and
sublittoral (40 ± 15 μmol photon m−2 s−1) exist, propagules are able to adapt to dif-
ferent light conditions (quantity and quality) mainly during the winter–spring tran-
sition. This is particularly evident in propagules of species that colonize a wide
range of vertical distribution (e.g., Desmarestia anceps). After sea ice breakup in
King George Island (South Shetland Islands), light can penetrate down to 30 m
200
Table 10.1 Overview of light requirement for saturation (Ek), photosynthetic efficiency (αETR), inhibition by PAR and PAR + UV radiation, and subsequent
recovery in different life history stages of Antarctic seaweeds collected from different depths. Propagule size and date of collection are also indicated.
Irradiance values represent conditions during incubation in the laboratory. PAR and PAR + UV inhibition were calculated after 4 h of exposition according to
information provided in the papers)
Cell Irradiance
Date of diameter (μmol PAR PAR + UV
Species Depth collection (μm) m−2 s−1) Ek αETR Fv/Fm inhibition inhibition Recovery Reference
Urospora Upper Oct 2004 6 22 87 0.16 ~0.50 No ~37% (PA; 100% Roleda
penicilliformis eulittoral 4 h); ~39% (24 h) et al.
zoospores, (0 m) (PAB; 4 h) (2009)
gametes
Urospora Upper Oct 2004 22 252 0.18 ~0.51 No ~20% (PA; 94% Roleda
penicilliformis eulittoral 4 h); ~23% (1 h) et al.
gametophytes (0 m) (PAB; 4 h) (2009)
Pyropia Eulittoral Jan–Feb 12 ± 1 13 101 ± 19 0.14 ± 0.01 0.35 ± 0.01 No ~16% (PAB, 100% Navarro
endiviifolia (0 m) 2015 4 h) (4 h) et al. (2016,
carpospores 2019)
Pyropia Upper Jan–Mar 15 ± 2 23 33 0.12 0.49 ± 0.04 46% (4 h) ~56% (PA; 100% Zacher
endiviifolia eulittoral 2005 4 h); ~60% (48 h) et al.
monospores (0 m) (PAB; 4 h); (2007)
Adenocystis Eulittoral Jan–Feb 6 ± 1 13 59 ± 6 0.45 ± 0.01 0.64 ± 0.02 No ~2% (PAB, 100% Navarro
utricularis (0–1 m) 2015 4 h) (4 h) et al.
zoospores (2016)
Adenocystis Eulittoral Jan–Mar 4 23 64 0.14 0.46 ± 0.11 No ~20% (PA; 100% Zacher
utricularis (0–1 m) 2005 4 h); ~57% (48 h) et al.
zoospores (PAB; 4 h); (2007)
N. Navarro et al.
Cell Irradiance
Monostroma Eulittoral Jan–Feb 5 ± 0.5 13 295 ± 84 0.09 ± 0.01 0.26 ± 0.01 23% (4 h) ~28% (PAB; 100% Navarro
hariotii gametes (0–1 m) 2015 4 h) (4 h) et al. (2016,
2019)
Monostroma Eulittoral Jan–Mar 7 23 83 0.065 0.29 ± 0.04 50% (4 h) ~66% (PA; 100% Zacher
hariotii gametes (0 m) 2005 4 h); ~71% (48 h) et al.
(PAB; 4 h); (2007)
Iridaea cordata Eulittoral Jan–Feb 18 ± 2 13 46 ± 6 0.17 ± 0.03 0.39 ± 0.06 No ~20% (PAB; 100% Navarro
tetraspores (0–1 m) 2015 4 h) (4 h) et al. (2016,
2019)
Iridaea cordata Upper Oct 2004 20 ± 2 22 57 0.12 0.47 ± 0.04 53% (4 h) ~78% (PA; 100% (2 Zacher
tetraspores sublittoral 4 h); ~82% d) et al.
(0 m) (PAB; 4 h) (2009)
Gigartina Sublittoral Jan–Feb 25 ± 2 13 27 ± 9 0.27 ± 0.05 0.42 ± 0.32 52% (4 h) ~80% (PAB, 35–60% Navarro
skottsbergii (5–8 m) 2015 4 h) (4 h) et al.
carpospores (2016)
Gigartina Sublittoral Oct 2004 27 ± 2 22 54 ± 2 0.14 0.40 ± 0.03 73% ~87% (PA; 100% (2 Roleda
skottsbergii (3 m) 4 h);89% d) et al.
carpospores (PAB; 4 h) (2008)
Gigartina Sublittoral Oct 2004 23 ± 1.5 22 44 ± 21 0.14 0.31 ± 0.07 69% (4 h) ~86% (PA; 100% (2 Roleda
skottsbergii (3 m) 4 h);90% d) et al.
tetraspores (PAB; 4 h) (2008)
Ascoseira Deep Jan–Feb 22 ± 4 13 17 ± 5 0.21 ± 0.03 0.48 ± 0.02 16% (4 h) ~30% (PAB; 85% Navarro
mirabilis sublittoral 2015 4 h) (4 h) et al.
gametangia (17–30 m) (2016)
(continued)
10 Life History Strategies, Photosynthesis, and Stress Tolerance in Propagules…
201
202
Cell Irradiance
Ascoseira Upper Oct 2004 8–10 22 52 0.09 0.40 ± 0.06 85% (4 h) ~91% (PA; 100% (2 Roleda
mirabilis sublittoral 4 h); 95% d) et al.
gametangia (2 m) (PAB; 4 h) (2007)
Ascoseira Shallow Jan 2014 13 52 ± 14 0.20 ± 0.04 ~0.6 ~0% (6 h) 100% Huovinen
mirabilis sublittoral (14 h) and Gómez
conceptacles (1 m) (2015)
Cystosphaera Deep Jan–Feb 13 13 ± 6 0.28 ± 0.01 ~15–21% ~ 90% Huovinen
jacquinotii sublittoral 2015 (2 h) (4 h) and Gómez
receptacles (2015)
N. Navarro et al.
Fig. 10.2 Summary of light requirement for saturation (Ek) and inhibition by PAR and PAR + UV
radiation in propagules of eulittoral and sublittoral Antarctic seaweeds. PAR and PAR + UV inhibi-
tion were calculated after 4-h exposure according to the information provided in each of the studies
consulted. For references, see Table 10.1
depth reaching an average of photon fluence rates of 70 μmol photon m−2 s−1 (Gómez

et al. 1997). This level of irradiance can also be strongly attenuated in terms of
spectral characteristics under the canopy of large brown algae (Huovinen et al.
2016; Gómez et al. 2019). Below the canopy the spectrum is enriched in green and
in far red light, probably affecting photosynthesis as well as the photomorphoge-
netic development of the understory species (Salles et al. 1996) (see Chap. 7 by
Huovinen and Gómez).
Fig. 10.3 Rapid light curves (PAR vs rETR) and rETR/ rETRmax ratio of Antarctic and sub-
Antarctic populations of Adenocystis utricularis and Iridaea cordata measured using chlorophyll
fluorescence. rETRmax represents the maximum value for each curve. (Modified from Navarro
et al. 2019)
10.2.1 E
stimating Photosynthetic Parameters
from Chlorophyll Fluorescence
Photosynthetic characteristics of propagules of Antarctic seaweeds are normally

determined estimating photosynthetic parameters (ETRmax, alpha and saturation
irradiance, Ek) calculated from P-E curves (summarized in Gómez et al. 2009).
When P-E curves are based on chlorophyll fluorescence measurements, the electron
transport rates (ETR) are commonly used as a parameter (Fig. 10.3). Considering
the limitations of the fluorescence method, as well as various factors that can affect
light requirements, e.g., form, season, size, number of cells, chlorophyll concentra-
tion, etc., the P-E curve-derived light requirements for photosynthesis (Ek) represent
the best measures to estimate shade adaptation in adult (Huovinen and Gómez
2013) and early stages (Zacher et al. 2007; Roleda et al. 2008, 2009; Navarro et al.
2016, 2019). However, two important aspects for calculation of electron transport
rates are sometimes not considered: (1) the proportional rates of chlorophyll a at
each photosystem (FII factor), which is different between red, green, and brown
algae (Grzymski et al. 1997), and (2) the amount of light absorbed by the algal
samples (absorptance). Due to the difficulty of measuring absorptance in a propa-
gule suspension, the use of the relative ETR has been proposed (Beer et al. 2001).
This parameter provides useful information for the description of relative changes
in photosynthetic activity if the experimental approach uses standardized

measurements.
Thus, the comparison of photosynthetic parameters of propagules using the
ETR-based P-E curves must be made with caution. Alternatively, the rETR can be
normalized to rETRmax (with rETRmax as the maximum value for each curve) express-
ing the rETR curve between 0 and 1 (relative units), which allows comparing propa-
gules from species with very different ETR values. For example, Navarro et al.
(2019) showed differences in photosynthetic performance of propagules from con-
generic and conspecific Antarctic/sub-Antarctic seaweeds using the rETR and
rETR/rETRmax ratio curves. While the rETR curve demonstrates that tetraspores of
I. cordata from Antarctic populations exhibit very low rETR values when compared
to the sub-Antarctic population, the rETR/rETRmax ratio allows detecting differ-
ences in the shape of the curves (Fig. 10.3).
10.3 E
ffects of Environmental Factors on the Biology
of Propagules
10.3.1 High Solar Radiation
Environmental shifts will affect recruitment, and consequently, the whole fate of the
seaweed population and their maintenance through time. Once Antarctic seaweed
spores or gametes are released, they face a completely different physical environ-
ment than what existed when they were housed in the parental reproductive struc-
tures (Amsler et al. 1992; Zacher 2014). During the last decade, various studies
have examined the effects of stress factors (e.g., temperature and UV radiation) on
microscopic stages, e.g., propagules and plantlets, of some selected Antarctic sea-
weeds (Gómez et al. 2009; Roleda et al. 2009; Zacher et al. 2009; Navarro et al.
2016). There is a consensus that propagules are the most susceptible life stage of
seaweeds in terms of their responses to environmental perturbations. However, the
effect of a given factor on the propagule physiology is highly variable, depending on
a suite of environmental and endogenous factors, which can act synergistically or
antagonistically.
It is well known that UV wavelengths cause direct and indirect effects on algal
cells (e.g., Karsten et al. 2009). The direct effects are normally mediated by absorp-
tion of UV by important biomolecules, in particular the DNA, enzymes, and mem-
brane components (Vass 1997). In the case of propagules, which attain small size,
translucent cytosol and an incipient development of the cell wall, UV radiation can
easily reach the DNA where diverse injuries are produced, e.g., formation of
cyclobutane pyrimidine dimers (CPDs) (Wiencke et al. 2000). This results in the
inability of RNA and DNA polymerases to recognize the damaged sectors, causing
the interruption of gene transcription and DNA replication (Britt 1995).
Consequently, modifications in the metabolism, cellular division, and germination

of unicellular propagules can occur (Huovinen et al. 2000).
DNA damage has been reported in propagules of eulittoral Antarctic seaweeds
Adenocystis utricularis, Monostroma hariotii, and Iridaea cordata after exposure to
different doses of UV radiation (Roleda et al. 2007, 2008; Zacher et al. 2007, 2009).
In general, the amount of CPDs increases with increasing UV-B dose; however,
lesions can be effectively repaired after 48 h under photoreactivation processes
(Zacher et al. 2007, 2009). Besides, contrasting patterns have been detected in spe-
cies from different depths: propagules of Pyropia endiviifolia from upper eulittoral
did not exhibit CPDs under different UV-B doses (Zacher et al. 2007), while propa-
gules of Gigartina skottsbergii and Ascoseira mirabilis from the deep sublittoral
were more affected and not able to repair their damaged DNA completely after 8-h
UV-B exposure (0.4 Wm−2) (Roleda et al. 2007, 2008). Interestingly, in the case of
Gigartina skottsbergii, the accumulation of DNA damage was related to the ploidy
level of the propagules: DNA damage was lower in diploid carpospores (2n) com-
pared to haploid tetraspores (n) suggesting that diploid carpospores are more toler-
ant to UV radiation in terms of UV-B-induced DNA damage (Roleda et al. 2008).
These authors suggested that higher UV-stress tolerance of diploid carpospores than
haploid tetraspores could be related to the genetic buffering hypothesis, which says
that diploid organisms are more vigorous and tolerant to stress than haploid ones,
i.e., the two copies of every gen confer them advantages to withstand the effects of
deleterious recessive mutations (Raper and Flexer 1970; Gerstein et al. 2010).
However, diverse studies have stated many important genetic advantages of hap-
loidy such as lower mutation load and more rapid spread of beneficial alleles and of
diploidy, e.g., protection from somatic mutation and heterozygote advantage (Otto
and Gerstein 2008). In fact, in spite of the higher DNA damage, tetraspores of
G. skottsbergii exhibited a higher DNA damage repair rate than carpospores when
the UVR was excluded. It must be noted that DNA damage in spores exposed to
high UV-B dose was not repaired completely after 2 days of post-cultivation, and
the remaining DNA damage was lower in carpospores than in tetraspores (Roleda
et al. 2008).
UV radiation affects also photochemical processes, especially inhibiting the
energy transfer within the PSII reaction center by blocking the electron flow. UV-B
radiation affects the D1/D2 protein complex (Richter et al. 1990) mainly by frag-
menting the D1 protein (Vass 1997; Bischof et al. 2006) through UV-active chromo-
phores on both the donor and acceptor side of this protein (Bouchard et al. 2006).
On the oxidizing side, the oxygen evolving system (water splitting complex) is
another sensitive target of UV-B (Renger et al. 1986). Moreover, it has been sug-
gested that UV-B can affect the antenna complex through the functional shutdown
of the photosystem, resulting in a failure in the transfer of energy to the reaction
center (Renger et al. 1986; Lorenz et al. 1997; Bischof et al. 2006). In propagules of
Antarctic seaweeds, UV radiation has also been pointed out as responsible for the
decrease in photosynthetic activity, measured as decreases in optimum quantum
yield-Fv/Fm. For example, Navarro et al. (2016) reported that propagules of species
from the eulittoral (e.g., Iridaea cordata, Pyropia endiviifolia, Adenocystis
utricularis) showed <20% inhibition in Fv/Fm from UV (1.5 and 0.26 Wm−2 of
UV-A and UV-B, respectively) after 4 h of exposure, while propagules of the red
alga G. skottsbergii collected in the sublittoral were more sensitive exceeding 30%
inhibition in Fv/Fm in the same condition. It is important to emphasize, however, that
photochemical reactions of propagules from Antarctic seaweeds can also be strongly
photoinhibited by PAR (Fig. 10.2). For example, 1-h exposure under 22 μmol pho-
tons m−2 s−1 of PAR decreased Fv/Fm in propagules of the sublittoral G. skottsbergii
(53–58%) (Roleda et al. 2008) and A. mirabilis (62%) (Roleda et al. 2007) and in
the eulittoral M. hariotii (62%), P. endiviifolia (81%) (Zacher et al. 2007), and
I. cordata (~25%) (Zacher et al. 2009). Increasing exposure time further reduced
Fv/Fm in all these species, with exception of M. hariotii (Zacher et al. 2007). In
contrast, in the case of propagules of the eulittoral Adenocystis utricularis (Zacher
et al. 2007) and Urospora penicilliformis (Roleda et al. 2009), the photosynthetic
activity was not affected by PAR. PAR supplemented with UV-A (~4.3 Wm−2)
decreased photosynthetic efficiency significantly compared to only PAR treatment
in all mentioned species during 1-h exposure. However, additional UV-B
(~0.35 Wm−2) revealed a further decrease of Fv/Fm only in sublittoral Ascoseira
mirabilis (25%) and G. skottsbergii (3–7%) (Roleda et al. 2007, 2008). Although
UV radiation further decreased photosynthetic efficiency in these species, all propa-
gules recovered completely after 48 h (Table 10.1).
Additionally, the UV susceptibility has been related to propagule size as cell path
length affects various bio-optical processes such as scattering and spectral extinc-
tion (Swanson and Druehl 2000; Roleda et al. 2008; Navarro et al. 2016). However,
at the cellular level, UV tolerance does not seem to respond to complex biochemical
and bio-optical processes. For example, tetraspores of I. cordata from Antarctica
exhibit a smaller size but very high UV tolerance compared to tetraspores of the
same species from sub-Antarctic region (Navarro et al. 2019). UV tolerance can
also be related to the presence and/or the capacity to induce formation of
UV-absorbing compounds, what could result in a more effective UV photoprotec-
tion, still in small propagules (Roleda et al. 2008). To our knowledge, only few
studies have described absorption of UV in Antarctic seaweed propagules under UV
stress. Higher concentration of palythine (λmax = 320 nm) than shinorine
(λmax = 334 nm) has been reported in freshly released tetraspores of G. skottsbergii
(Roleda et al. 2008) and I. cordata (Zacher et al. 2009). However, contrasting pat-
terns in MAA content were observed after 8 h under PAR or PAR + UV treatments,
while the total content of MAAs in tetraspores of G. skottsbergii was not signifi-
cantly different between control (freshly released spores) and treatment. In contrast,
MAA concentration in spores of I. cordata decreased in treated compared to freshly
released spores. Based on these findings, it could be suggested that (1) freshly
released propagules could have a basal level of UV-absorbing substances due to the
higher in situ incident solar radiation in the field and (2) the level of UV-absorbing
substances can acclimate depending on environmental conditions. In the first case,
the synthesis of UV-absorbing substances would take place when the spores are still
protected by the thick tissue of the parental thalli (tetrasporangial tissue in the case
of tetraspores of G. skottsbergii and I. cordata). For I. cordata, Karsten et al. (2000)

reported a higher amount of MAAs in tetrasporangial tissue than in vegetative parts
of the thalli. Similarly, Huovinen and Gómez (2015) reported that reproductive tis-
sue of Ascoseira mirabilis and Cystosphaera jacquinotii contain higher amounts of
soluble phlorotannins, a type of UV-absorbing phenols found in brown algae. The
presence of these compounds in reproductive tissues could ensure the maturation,
survival, and germination of released propagules when they are exposed to UV
radiation in the water column. Although photoprotection was only partial in labora-
tory experiments, propagules of I. cordata and G. skottsbergii tetraspores exposed
to UV-B radiation showed the higher total MAAs in comparison with those incu-
bated under only PAR (Roleda et al. 2008; Zacher et al. 2009).
10.3.2 Temperature
Antarctic seaweed propagules are adapted to low temperature. Cold adaptation was
confirmed by the high photosynthetic efficiency (in terms of maximum quantum
yield of fluorescence – Fv/Fm) at 0 °C in six Antarctic distributed species (Navarro
et al. 2016). This low temperature requirement for photosynthesis is certainly the
result of the long Antarctic cold-water history of at least 14 Ma (Crame 1993).
However, it is well known that photosynthesis increases progressively with increas-
ing temperature and then rapidly declines near upper critical temperature (Davison
1991). In the case of Antarctic species, the optimum temperature for photosynthesis
is between 10 and 20 °C (Eggert and Wiencke 2000; Eggert 2012), lower than that
reported for algae from other geographic regions (reviewed in Gómez et al. 2009).
In propagules of eulittoral species such as Adenocystis utricularis, Monostroma
hariotii, and Pyropia endiviifolia and shallow sublittoral Ascoseira mirabilis, the
highest photosynthetic efficiency was observed at 25 °C (Navarro et al. 2016). This
suggests that propagules of these species are thermally well adapted (eurythermal
species), allowing them to develop in a highly variable environment or in different
biogeographic regions. For example, A. utricularis and M. hariotii are widely dis-
tributed in sub-Antarctic and temperate coasts of South America (Huovinen and
Gómez 2012, see Chap. 2 by Oliveira et al. and Chap. 4 Macaya et al.). In contrast,
the high photosynthetic efficiency exhibited by propagules of Antarctic endemic
Ascoseira mirabilis at 25 °C could be explained by the upper vertical distribution of
the parental sporophytes or could be a conserved trait related to the fact that the spe-
cies is probably a relic of Mesozoic (Gondwana) marine flora, which was highly
diverse when the average water temperatures were close to 12 °C (Clayton 1994).
Temperature is a factor modifying the susceptibility/tolerance to UV radiation.
The influence of this factor apparently depends on the position of parental thalli on
the shore. In this context, a recent study provided evidence that propagules of
Antarctic seaweeds are relatively tolerant to enhanced temperature, which can fur-
thermore modulate UV tolerance at least under laboratory conditions (Navarro et al.
2016). These authors observed that the exposure of propagules to a combination of

UV radiation and temperature stress inhibits the photosynthetic capacity of propa-
gules of six Antarctic seaweed species from the eulittoral (Pyropia endiviifolia,
Iridaea cordata, Adenocystis utricularis, and Monostroma hariotii) and the sublit-
toral (Ascoseira mirabilis, and Gigartina skottsbergii), the former group being more
tolerant to UV and enhanced temperature than the sublittoral group. Additionally,
propagules of eulittoral species P. endiviifolia, I. cordata, and A. utricularis exhibit
negative UV effects at 2 °C compared to 7 and 12 °C, suggesting that enhanced
temperature improves UV tolerance. On the contrary, this positive interaction was
not observed in propagules of the shallow sublittoral A. mirabilis, where an increase
in temperature exacerbates the reduction of photosynthetic efficiency (Navarro et al.
2016). It is known that various processes related to photoprotection, e.g., D1 protein
turnover, enzyme repair mechanisms, and dissipative quenching, operate more effi-
ciently at higher temperatures (Wünschmann and Brand 1992; Becker et al. 2010).
Thus, the lower inhibition of photosynthesis observed at 12 °C compared to 2 and
7 °C can be regarded as an efficient acclimation of photosynthesis in these cells.
Even though photosynthesis was inhibited by UV radiation, propagules from eulit-
toral species recover completely after 4 h under dim visible light, whereas sublitto-
ral ones do not. A fast turnover of D1 protein may be responsible for the fast
reversible photoinhibition of photosynthesis in eulittoral macroalgae as suggested
for Urospora penicilliformis propagules (Roleda et al. 2009). However, the recovery
is not influenced by a temperature increase in the studied species (Navarro
et al. 2019).
Antarctic propagules can retain their capacity to tolerate elevated temperatures,
which is evident when they are compared with their sub-Antarctic counterparts. For
example, Fv/Fm measured in I. cordata tetraspores from Antarctica was not inhibited
by UV radiation at 2 °C or 8 °C, while propagules from sub-Antarctic populations
exhibited a decrease after a 4-h exposure, mainly at 2 °C in PAR (30%) and
PAR + UV (67%). Considering only the effects of temperature, Fv/Fm decreased by
14% in tetraspores from sub-Antarctic population exposed at 2 °C when compared
to the control (8 °C). Surprisingly, photosynthetic activity in tetraspores from
Antarctic increased by 2% relative to control. These results suggest that low tem-
peratures may exacerbate UV stress to photosynthesis in spores from the sub-
Antarctic population, whereas Antarctic spores would be adapted to low temperature
and UV. The results also confirm previous evidence obtained in adult thalli of Ulva
spp. from Antarctic and sub-Antarctic region by Rautenberger and Bischof (2006).
At 10 °C the inhibition of Ulva hookeriana (known as Enteromorpha bulbosa (Suhr)
Montagne) from Antarctica was comparable to its sub-Antarctic counterpart Ulva
clathrata (10% of control). However, at 0 °C, inhibition was of 50% in the sub-
Antarctic Ulva clathrata and 37% in U. hookeriana (Rautenberger and Bischof
2006). Overall, the results indicate that in cold-adapted species, stress tolerance can
be efficient, which allow many shallow sublittoral, and especially eulittoral species,
to thrive under extremely changing thermal conditions.
10.3.3 Other Environmental Stressors
In the Antarctic environment, seaweeds are also facing fluctuations of other envi-
ronmental factors such as salinity, influenced by local meltwater influx and calving
glaciers as well as desiccation when algae are exposed to air during low tides.
Although the effects of salinity on seaweeds are relatively well known (reviewed in
Kirst 1990 and Karsten 2012), few studies have been conducted on Antarctic sea-
weeds (e.g., Jacob et al. 1991, 1992a, b; Karsten et al. 1991a, b). In general, it has
been reported that seaweeds respond to external salinity changes with osmotic accli-
mation processes involving the control of internal organic (e.g., proline, sucrose,
β-dimethylsulphoniopropionate) and inorganic (K+, Na+, Mg2+, Cl−, SO42−, and
PO43−) ions (Karsten et al. 1991a, b; Kirst 1990). Antarctic seaweeds inhabiting the
eulittoral and supralittoral zone can be characterized as euryhaline organisms,
which can survive salinities between 7 and 102 PSU with a low rate of mortality.
Most taxa grow, photosynthesize, and respire optimally under normal seawater con-
ditions with rather broad tolerances between 7 and 68 PSU. Hitherto, there is no
information of the effect of salinity on Antarctic seaweed propagules. On the other
hand, emergent stressors in Antarctic environment, e.g., ocean acidification (Hurd
et al. 2009) and marine pollution (Goutte et al. 2013), can pose risks to adult and
early phases of Antarctic seaweeds. Ocean acidification can affect the physiology of
seaweeds; however, practically no data exist on their effects on early phases of mac-
roalgae. In the giant kelp Macrocystis pyrifera, pH between 7.59 and 7.60 reduced
meiospore germination, which was ameliorated when CO2 was added (Roleda et al.
2011). Hitherto there is no information on the effects of these compounds on the
biology of Antarctic propagules.
It has been suggested that metals may inhibit reproduction in brown algae by
interfering with the ability of sperm to find eggs, perhaps via interference of the
pheromone attractant (Maier 1993). However, the effect of trace metals is expected
to be detrimental to propagules (spores, gametes, and zygotes) due to poor develop-
ment of the protective cell wall. Moreover, cell walls of brown seaweeds composed
of alginate and fucoidan can bind cations and have a high affinity for copper (Lignell
et al. 1982), affecting the settlement and germination of propagules. For example, in
Lessonia, copper drastically affected spore release by mature sporophytes as well as
spore settlement. The highest copper concentration applied interrupted the develop-
ment of the spores totally after settlement (Contreras et al. 2007). In all, the impor-
tance of studying the effects of metals and other pollutants (hydrocarbons, pesticides,
other persistent pollutants, and so on) on Antarctic algae propagules lies in the
recent increase of contaminant concentration in Antarctic due to human activities
(Bargagli 2008). On the other hand, although the harmful effects of metals, e.g.,
copper toxicity, have been analyzed in brown species (reviewed by Coelho et al.
2000; Contreras et al. 2007), the effects of these new, emergent stressors on the biol-
ogy of Antarctic seaweeds have to be examined in a context of the combined action
of multiple factors (see Chap. 7 by Huovinen and Gómez).
10.4 C
oncluding Remarks: Biology of Propagules under
Climate Change
Despite having a crucial importance in the biology of seaweeds, propagules have

not been sufficiently studied in relation to their physiological requisites to respond
to climate change. The importance of understanding the effects of global climate
change on reproductive stages lies in the fact that early stages of development are
essential for recruitment, especially for those species that rely their dominance
entirely on reproductive abilities.
The predicted increase of temperature and the prevalence of episodes of depleted
ozone around the Antarctic Peninsula region and adjacent islands will impose phys-
iological constraints to reproductive output, settlement, and recruitment of different
species of seaweeds. Increase in seawater temperature could also influence the phe-
nology and the formation of propagules (spores and/or gametes) and consequently,
the timing and formation of juvenile thalli, especially in species inhabiting the eulit-
toral and shallow sublittoral zone (Zacher et al. 2007; Campana et al. 2009; see
Chap. 12 by Campana et al.). Furthermore, as a consequence of temperature
increase, glaciers can retreat opening new free space for recruitment of benthic
organisms, including macroalgae (Quartino et al. 2013; see Chap. 8 by Quartino
et al.). In these new open areas, however, alteration in light, salinity, sedimentation,
and disturbance processes can occur, limiting settlement of established communi-
ties and even favoring the arrival of cold-temperate species (see also Chap. 9 by
Deregibus et al.). Increased turbidity can have, however, contrasting implications
for the biology of reproductive cells, which can become favored by a minimized
impact of UV radiation, but decreasing available irradiance for photosynthesis.
Undoubtedly, Antarctic seaweeds have developed life strategies to colonize and
form a complex structure in the coastal ecosystems. In scenarios of climate change
and warming in the Antarctic, dispersal and colonization of Antarctic coastal zones
via efficient adaptations of early developmental phases of seaweeds are central to
envision the future seaweed diversity in Antarctica (see Chap. 2 by Oliveira et al.
and Chap. 5 by Pellizzari et al.).
Acknowledgments This work was supported by CONICYT-Chile: Fondecyt Iniciación

N°11160520, Anillo ART1101, and Centro Fondap-IDEAL 15150003.
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Chapter 11
Form and Function in Antarctic Seaweeds:
Photobiological Adaptations, Zonation
Patterns, and Ecosystem Feedbacks
Abstract Morpho-functional traits of Antarctic seaweeds are modeled by different

physical and biological factors. Due to the extreme seasonality, which imposes light
limitation for extended periods, Antarctic seaweeds are shade-adapted organisms
that are physiologically able to thrive at considerable depths down to 40 m. This
vertical distribution is defined by a suite of bio-optical and morphological features
that allow algae occupying habitats with different environmental conditions in the
water column. However, various species can also colonize the highly perturbed
intertidal zone where environmental setting, e.g. ice scouring, high solar radiation,
extremely variable temperature, limit growth, and reproduction. In the maritime
Antarctic region, large endemic brown algae attaining a massive (leathery) mor-
phology and perennial life history dominate at depths below 10 m or less. Here, they
coexist with perennial highly shade-adapted coarsely branched rhodophytes, which
show understory characteristics. At shallower locations, various annual species with
very rapid growth can be found. The intertidal zone, characterized by a depauperate
diversity, is populated mostly by ephemeral and delicate green algae. In the present
chapter, form and function of seaweeds is revisited in the context of a changing
Antarctic environment. Here, the functional groups display different acclimation
mechanisms, which can operate at different temporal scales and consequently with
variable impact on the biogeochemical coastal processes. The role of canopy-
forming algae, whose “bioengineering” processes alleviate the impact of environ-
mental variability, is fundamental in determining the fate of the benthic communities
in the coastal system.
Keywords Canopy-forming algae · Life strategy · Light absorption ·

Morpho-functional traits · Vertical zonation


https://doi.org/10.1007/978-3-030-39448-6_11
11.1 Brief Overview of Form and Function in Seaweeds
In contrast to unicellular algae, organisms bearing multiple cells (from simple plu-
ricellular colonies to more advanced forms attaining, e.g. parenchyma) have to syn-
chronize a more complex structural organization, characterized by different
function-specific elements that follow a morpho-genetic-based program. Thus, mul-
ticellular algae adjust form and function through an intricate molecular network that
allows them to interact with their physical, chemical, and biotic environment
(Grosberg and Strathmann 2007). A suite of morphological models found in benthic
organisms (e.g. seaweeds, sponges, corals, bryozoa) coexist in a physical environ-
ment, which raises a question of how similar convergent forms have evolved even in
species phylogenetically very distant or, alternatively, how related organisms dis-
play completely different growth patterns and shape (Kaandorp and Kübler 2001).
A striking characteristic of almost all seaweeds is their morphological plasticity,
i.e. although the basic thallus plan is based on a determined morphogenetic design,
body shape can change through the life span of an organism or within the life his-
tory sequence. These variations in the morphological traits within a genotype can be
subtle or drastic depending on the intensity of the endogenous and environmentally
driven shifts (Innes 1984; Taylor and Hay 1984). Especially in sites where the phys-
ical perturbations are extreme, seaweeds display complex mechanisms to adjust
form and function to the prevailing environmental condition (Hay 1986). Phenotypic
plasticity, one of the most well-known types of intrinsic morphological variability,
is normally prompted by environmental conditions and thereby complicates efforts
to identify the routes of morpho-functional responses within a multi-specific assem-
blage: intrinsic properties at an organismal level mask the morpho-functional differ-
ences at community scale (Steneck and Dethier 1994). Changes in morphology due
to ontogenetic development and heteromorphic phase expression within of life
cycle are also important to characterize form and function in seaweeds. For exam-
ple, in the brown alga Himantothallus grandifolius, the largest Antarctic seaweed,
the thallus undergoes considerable changes with development: while juvenile indi-
viduals are characterized by partial cortication and coarsely branched morphology,
adult plants are characterized by a thick leathery strap-like anatomical structure,
where lateral branches are absent (Moe and Silva 1981; Wiencke and Clayton 1990).
Traditionally, functional groups of seaweeds (which could also be applied to
other groups of benthic marine organisms) are defined by their thallus architecture
(also called life form). This concept implies intuitively a series of intrinsic proper-
ties of an organism, which can or not be shared by other unrelated organisms.
Clearly this gives a high value to the anatomical features (form) and less emphasis
on the function. Such conceptual framework represented the basis on, which Littler
and Littler (1980) and Steneck and Watling (1982) developed their general func-
tional form models, where functionality of algae, e.g. resistance to biotic distur-
bance, was inferred from gross morphology. Although the general applicability of
these models has been questioned since similar morphologies often show different
functional responses to, e.g. disturbance gradients (Phillips et al. 1997; Ingólfsson
11 Form and Function in Antarctic Seaweeds: Photobiological Adaptations, Zonati… 219
2005; Padilla and Allen 2000), functionality, which depends on extrinsic factors
(e.g. resource utilization, disturbance, biotic interactions, etc.), has an unavoidable
expression in the morphology. The rationale to understand in what ways form and
function is modeled by the environment, known as “the holy grail framework”,
considers necessarily different areas of knowledge, e.g. genomics, physiology, ecol-
ogy, demography, etc., and has been used with different emphasis to explain the
structure of different types of vegetation, both in terrestrial and aquatic realms
(Littler and Littler 1980; Grime 1981; Steneck and Dethier 1994; Lavorel and
Garnier 2002). Thus, if one assumes that different habitats have a different environ-
mental setting, it is possible to argue that they host assemblages of organisms with
similar morphology but different functional attributes. For example, in littoral
stress, tolerance of macroalgae depends strongly on fine photochemical adjust-
ments, which are related to their position on the shore and less with functional form
groups (Aguilera et al. 1999; Gómez and Huovinen 2011; Balata et al. 2011). This
has been commonly found in different types of terrestrial vegetation where environ-
mental tolerance, and not gross morphology, defines functional groups (Grime
1981; Ackerly and Reich 1999; Poorter and Bongers 2006).
11.2 Functional Groups of Seaweeds in the Antarctic
The coastal systems around Antarctica may be regarded as highly inhospitable for
life, where physical disturbance associated with ice scouring, extreme light limita-
tion, and low temperatures imposes severe restrictions for marine organisms.
However, benthic algae thrive in these habitats displaying different functional strat-
egies and morphologies (Fig. 11.1). Based on various surveys, 131 species of sea-
weeds (Fig. 11.2) are distributed among different types of functional groups:
filamentous and finely branched (45); foliose (9); coarsely branched, including cor-
ticated species (48); thick leathery, including terete forms (11); and postrate species
(18) (Fig. 11.2). However, when the different functional forms are grouped accord-
ing to the major phylogenetic categories, it is possible to observe that 64% of green
algae are filamentous, while practically the totality of thick leathery forms belong to
brown algae. In red algae, 58% of the known species can be recognized as finely and
coarsely branched morphs. In the case of Chlorophyta, most of the species attain del-
icate filamentous or sheet-like morphs, and with the exception of the endemic
Lambia antarctica and Monostoma hariotii (Wiencke and Clayton 2002; see also
Chap. 2 by Oliveira et al. and Chap. 5 by Pellizzari et al.), all are restricted to inter-
tidal zones. However, it should be emphasized that many species cannot be easily
assigned to these major functional categories. For example, the brown algae
Adenocystis utricularis and Utriculidium durvillaei are the only species with a sac-
cate morphology (and thus were not included in this analysis). Moreover, the num-
ber of postrate species, which may include crustose, calcareous, and endophytic life
forms, is largely underrepresented. In fact, these algae have been very little studied,
Fig. 11.1 Diversity of gross morphologies in Antarctic seaweeds. (a) Crustose Rhodophyta; (b)
Saccate morphology (Adenocystis utricularis); (c) Filamentous tubular (Ulva intestinalis); (d)
finely branched Plocamium cartilagineum; (e) coarsely branched (Trematocarpus antarcticus); (f)
Thick leathery (Ascoseira mirabilis). (Photos a, d, e and f by Ignacio Garrido; b and c by
Iván Gómez)
due to mostly that they are not ubiquitous (e.g. encrusting morphs) or can inhabit
deeper locations (e.g. calcified coralline algae) (Alongi et al. 2002).
The absence of a marked dominance of a given seaweed gross morphology in the
Antarctic can only be explained in terms of the distribution of these different func-
tional forms in the mosaic of benthic habitats. In fact, the arrangement of species
across different environmental gradients implies also an ordination of organismal
traits that can be classified in different functional entities (e.g. gross morphology,
size, life forms, physiological responses). Thus, it is possible to understand why
similar morpho-functional “solutions” are exploited by different taxa, many of them
phylogenetically unrelated. For example, of the 25 species of green algae recorded
in the Antarctic, 56% correspond to widely distributed taxa, which normally display
Fig. 11.2 Major functional-form groups in different divisions of Antarctic seaweeds based on dif-
ferent surveys (Clayton et al. 1997; Wiencke and Clayton 2002; Hommersand et al. 2009; Ramírez
2010; Charles Amsler, personal communication)
Fig. 11.3 Antarctic seaweeds and their organization in relation to form and function, size, geo-
graphic affinity, and taxonomy. Number of taxa extracted from Fig. 11.2
filamentous or sheet-like forms (Fig. 11.3). According to Gómez et al. (2019), form

and function and biogeographic affinity are highly correlated in Antarctic green
algae. In contrast, only 12% of Rhodophyta can be regarded as widely distributed,
contrasting with the high prevalence of endemic (42%) and Antarctic/sub-Antarctic
taxa (46%). Similar pattern can be observed in brown algae where endemic and
Antarctic/sub-Antarctic species (characterized by thick leathery and saccate
morphs) account by 88% of the total numbers of recorded taxa (Fig. 11.2).
11.3 T
he Vertical Zonation of Antarctic Seaweeds:
A Paradigm of Spatial Distribution of Different
Morpho-functional Traits
Knowledge on zonation and in general the structure of the submarine landscape in

the shallow sublittoral in the Antarctic began to increase in the 1960s and 1970s,
along with scuba diving–based surveys (Neushul 1965; Delépine et al. 1966;
Zaneveld 1966; DeLaca and Lipps 1976; Lamb and Zimmerman 1977). These stud-
ies across different geographical zones demonstrated that the vertical distribution of
macroalgae could be defined in terms of functional groups, which apparently do not
follow uniform patterns, principally due to differences in latitude, substrate, influ-
ence of ice, associated fauna, etc. The vertical distribution of Antarctic seaweeds
has been much more studied in the Western Antarctic Peninsula and adjacent
islands, an eco-region known as the Maritime Antarctic. Due to the relatively milder
climatic conditions, seaweed assemblages reach their maximal development in
terms of abundance and diversity in the north-western part of the Antarctic Peninsula,
decreasing the macroalgal biodiversity towards the southern regions (Wiencke et al.
2014; Mystikou et al. 2014). The zonation in the Maritime Antarctic can be charac-
terized by a dominance of large canopy-forming endemic species of the order
Desmarestiales (Desmarestia menziesii, D. anceps, and Himantothallus grandifo-
lius) between 10 and 40 m or greater depth (Fig. 11.4a). These three species have
thick leathery and terete gross morphology and can alternate their dominance
depending on the substrate characteristics, whose consolidation can vary consider-
ably depending on closeness to glaciers, slope of the vertical profile, terrestrial run-
off, etc. (Klöser et al. 1994). Coexisting at this level, it is possible to found delicate
understory red algae, e.g. Myriogramme, Gymnogongrus, and Georgiella (Amsler
et al. 1995). Between 0 and 5 m depth, a zone marked by ice abrasion and waves,
the substrate is colonized by fast-growing species, algae with an ability for re-sprout
from basal shoots and crustose forms. In contrast, the intertidal rocky shores are
dominated by ephemeral, turf species, mainly filamentous Chlorophyceans (e.g.
Urospora, Ulva, Ulothrix) and the saccate brown alga Adenocystis utricularis
(Huovinen and Gómez 2013; Marcías et al. 2017).
In areas outside the Western Antarctic Peninsula, e.g. around the Ross Sea and
some sites along the East Antarctica, the diversity and abundance of seaweeds
decreases and their vertical distribution is much more constrained by available sub-
strata and the longer permanence of sea ice cover (Zaneveld 1966; Miller and Pearse
1991; Gambi et al. 1994; Johnston et al. 2007; Clark et al. 2011). In these sites,
although some large Desmarestiales (e.g. H. grandifolius and D. menziesii) can be
found at deeper locations, in general the coarsely branched red algae Iridaea cor-
data and Phyllophora antarctica are the dominant assemblages, especially at inter-
mediate depths (between 2 and 20 m) (Cormaci et al. 2000) (Fig. 11.4b). Another
particular feature of these ecosystems is the massive presence of crustose coralline
red algae at deeper locations, especially of Phymatolithon foecundum (Hommersand
et al. 2009), which can cover >70% of the available substrate under the canopy of
red and brown algae (Irving et al. 2005). Remarkably, algae have to adapt to very
low light conditions for primary productivity, irrespective of their functional form
architecture. In fact, due to their extreme shade adaptation, these species can reach
considerable depths and live with <2% of surface irradiances (Schwarz et al. 2003,
2005; see also Chap. 7 by Huovinen and Gómez).
Fig. 11.4 Patterns of vertical distribution of seaweeds in Western Antarctic Peninsula (a) and
Eastern Antarctica (b) indicating major functional groups and photobiological processes. Synthetic
schemes from observations reported in Gambi et al. (1994), Johnston et al. (2007), and Huovinen
and Gómez (2013)
11.4 L
ight Use Characteristics as a Major Factor
Delineating Physiological Thallus Anatomy of Seaweeds
The arrangement of different functional forms along the depth gradient is strongly
determined by different physico-chemical and biological factors. However, spatial
and temporal availability of light is probably the most relevant factor by which
zonation of Antarctic seaweeds can be explained. Because light governs the primary
processes of photosynthesis, and, hence, primary productivity and biomass forma-
tion, Antarctic seaweeds, irrespective of their morphological organization, display
efficient mechanisms of light harvesting. In fact, in the Antarctic, the marked sea-
sonality in light availability defines strongly an intrinsic shade adaptation of mac-
roalgae. Here the whole phenology of algae is closely tuned with the Antarctic light
regime, which exposes organisms to darkness in winter (Wiencke et al. 2009).
However, although in summer algae can be exposed to very high doses of solar
radiation due to extended daylengths of up to 24 h at the highest latitudes, they do
not acclimate and retain the capacity for very low light requirements for metabolism
(Gómez and Huovinen 2015). This ability to use very low irradiances for photosyn-
thesis and an intrinsic positive metabolic carbon balance (an indicator of compensa-
tion of carbon losses due to respiration) (Gómez et al. 1997; Deregibus et al. 2016)
has important implications for the spatial dimension of the algal zonation: it allows
Antarctic algae to colonize shaded locations, especially deeper sites. As a conse-
quence, many Antarctic species can occupy extended ranges of depth and hence
different light fields (Gómez et al. 1997). This situation contrasts with zonation pat-
terns of various cold and temperate coasts, where the different algal groups are
arranged in well-defined “belts” (Lüning 1990). Light trapping, especially under
very limited conditions of irradiance, requires not only a specific pigment configu-
ration but also morphological features such as thickness and thallus translucency,
which are important in terms of absorptance of the different wavelengths (Gómez
and Huovinen 2011). Algae increase light trapping through their thallus architec-
ture, which can result in different in vivo spectral absorptance (Lüning and Dring
1985; Gómez et al. 2019). In Fig. 11.5, the spectral characteristics of several
Antarctic macroalgae with different functional form and thickness are exemplified.
In the case of thick leathery and coarsely branched morphs (e.g. Himantothallus,
Desmarestia, Iridaea), attaining thallus thickness >500 μm, show high absorptance
practically along the whole spectrum. In contrast, delicate morphs with thick-
ness <100 μm, mostly foliose and finely branched such as Monostroma, Pantoneura,
Myriogramme, and Pyropia, show decreased absorptance between 550 and 650 nm.
Interestingly, some thin filamentous algae, e.g. Ulva intestinalis, Acrosiphonia, and
Urospora, can exhibit high absorptance at these wavelengths, which is related to
their turf arrangement, i.e. the overlapping of different filaments equals the several
cell layers of thicker algae. Overall, these patterns are related to algal taxonomy and
distribution in the zonation profile. In fact, thick leathery forms commonly belong
to the brown algae, and their efficient light absorption over an extended range of
wavelengths allows using the impoverished light field at higher depths (Gómez and
Fig. 11.5 Patterns of spectral in vivo absorptance of several Antarctic seaweeds with different
morpho-functional organization. Examples of thallus gross morphology, cross section, and thick-
ness are indicated for selected species. Cross-sectional microphotographs courtesy of Nelso Navarro
Huovinen 2015). Similarly, understory coarsely branched and finely branched red
algae, inhabiting deep sites with high absorption between 400 and 500 nm, are well
suited to live at these depths (Gómez et al. 2019). Considering that, irrespective of
their thallus shape and taxonomical affinity, Antarctic seaweeds are shade-adapted
organisms, whose morphological and optical traits (e.g. thickness), pigment compo-
sition, and intrinsic photochemical capacities are superimposed in their vertical dis-
tribution (Huovinen and Gómez 2013; Gómez et al. 2019).
11.5 F
orm and Function in the Context of Life Strategies
and Stress Tolerance
Since the publication of MacArthur and Wilson in 1967 on r and k selection, which
put into a context the evolutionary divergences of organisms in relation to the pro-
duction and care of offsprings, many studies have tried to expand these concepts to
other adaptive traits (concept discussed in Pianka 1970). Because r and k strategies
involve normally differences in energy allocation and, hence, body size, the form
and function concept could be easily integrated in the theory (Grime 1981). For the
case of marine macroalgae, in the 1980s, Joanna Kain used the terms “season
responder” and “season anticipator” to describe the different phenological responses
of seaweeds to seasonal changes in the environment (Kain 1987). Accordingly,
“season responders” correspond to organisms that grow and reproduce under
favourable environmental conditions, which could be analogous to r strategists,
while “season anticipators” are organisms whose development is triggered by envi-
ronmental factors at which they anticipate. The latter classification resembles
k-selection strategy. Although not a strict rule, most of the season responders identi-
fied in the literature seem to correspond to delicate, small-sized forms, which nor-
mally exhibit an opportunistic strategy. In contrast a number of season anticipators
can be associated with long-lived (perennial) seaweeds attaining normally large
thalli (Kain 1989). However, although intuitively one may argue that differences in
thallus complexity (including size) are correlated with differential responses to sea-
son, in general they are complex and depend on different environmental factors,
type of biological indicator (growth, photosynthesis, reproduction, etc.), age and
life history phase, and endogenous rhythms, all which can show complementary or
divergent patterns (Kain 1986; Lüning and Kadel 1993; see also Chap. 10 by
Navarro et al.).
In the Antarctic benthos, seaweeds are exposed to a marked seasonality, and thus,
the concepts of “responders” and “anticipators” could explain well the different
phenological patterns found in Antarctic seaweeds. In fact, various Antarctic spe-
cies, e.g. Iridaea cordata, Ulva intestinalis, Acrosiphonia arcta, and Adenocystis
utricularis, have been regarded as “season anticipators”, while Antarctic
Desmarestiales, Ascoseira mirabilis and Palmaria decipiens, can be considered as
“season anticipators” (Wiencke 1990a, b). Although these classifications were
based mostly on growth responses to the Antarctic light regime, it has been shown
that photosynthetic light use characteristics can respond in the same seasonal man-
ner. For example, the brown alga Adenocystis utricularis and the red alga Iridaea
cordata, two species regarded as responders, maintain high photosynthetic func-
tionality still in winter, when light is very limited (Gutkowski and Maleszewski
1989; Weykam et al. 1997). This strategy is completely different in large
Desmarestiales and Ascoseira mirabilis, as well as the red alga Palmaria decipiens,
which activate their photosynthetic apparatus during early spring to optimize the
available irradiance after the ice break-up (Gómez et al. 1995a, b; Wiencke et al.
2009). For large brown algae whose thalli can have length of various meters, these
responses have important morpho-functional implications: Firstly, photosynthesis
and growth during early spring are strongly synchronized to potentiate the use of
newly fixed and stored carbon. Secondly, there is spatial separation between carbon
production and sink zones with different metabolic activity, which can also be
exposed to very contrasting light fields. Because these massive thick leathery spe-
cies require compensation for the enhanced carbon burning due to high rates of dark
respiration during the rapid biomass formation, the lamina elongation is powered by
carbon stored in the previous season (Gómez and Wiencke 1998), similarly as in
high-latitude kelps (e.g. Laminaria, Saccharina) (Dunton and Schell 1986). A well-
studied case is Ascoseira mirabilis, which grows through the action of an intercalary
meristem and presents “conducting channels” in medullary cell regions (Clayton
and Ashburner 1990; Gómez et al. 1995b). In this species, during the growth phase,
carbon stored as laminarin in distal parts is remobilized through the conducting
cells (normally as mannitol and some amino acids) towards the meristem to replen-
ish carbon substrates in the so-called light-independent carbon fixation (LICF) reac-
tions (Kremer 1981; Gómez and Huovinen 2012). Such morpho-functional strategies
have not only been demonstrated in large brown algae: in the perennial, coarsely
branched red alga Palmaria decipiens, LICF reactions accounting 9% of the total
fixed carbon have been reported (Weykam et al. 1997), suggesting that this type of
mechanisms are operating in algae with complex thallus anatomy and season antici-
pation phenology, which allow them thriving at high depths and under extreme sea-
sonality in the Antarctic.
Form and function in the context of stress tolerance have been revisited in the last
years. Interestingly, several anatomical traits related to resistance to physical distur-
bance, e.g. multilayered architecture, thickness, and large size, are also functional to
increase light trapping, e.g. efficient absorptance (Gómez and Huovinen 2011).
Recently it was claimed that populations of three species of Desmarestiales
(D. anceps, D. menziesii, and H. grandifolius) and Ascoseira mirabilis extending
between 5 and 30 m depth show similar photosynthetic characteristics along the
depth profile (Gómez and Huovinen 2015). However, not only the efficient and
highly conserved light use across different irradiances but also an intrinsic capacity
for UV stress tolerance was shown in these algae (see Chap. 7 by Huovinen and
Gómez). Although all these traits conferring UV shielding show a strong overlap-
ping with other factors, e.g. competence for space and overgrowth, scape from her-
bivores, there appears to exist a trade-off between photoprotection against enhanced
solar UV radiation, mostly due to an increased thallus cross section (low area/
weight ratio) and ultrastructural compounds, and highly efficient shade adaptation
(Gómez and Huovinen 2015). A key element explaining this feature in algae rarely
exposed to UV radiation is their constitutively high levels of phenolics (phlorotan-
nins) (Flores-Molina et al. 2016). These secondary metabolites in Antarctic brown
algae represent multifunctional compounds with putative roles in, e.g. resistance to
grazing, temperature, and UV radiation (Amsler et al. 2005; Iken et al. 2009;
Huovinen and Gómez 2013; Rautenberger et al. 2015) (for a description of func-
tional roles of phlorotannins in Antarctic seaweeds, see Chap. 17 by Amsler et al.
and Chap. 18 by Gómez and Huovinen).
In the case of delicate morphs, mostly filamentous and finely branched green
algae, the opportunistic life strategy of these organisms allows them to respond
rapidly to environmental stressors and, in virtue of their high metabolic rates per
weight, to restore the homeostasis at short term (Holzinger and Karsten 2013).
Albeit stress tolerance of seaweeds living in the intertidal zone would rely on highly
efficient metabolic adjustments (Holzinger and Lutz 2006; Karsten et al. 2009;
Gómez and Huovinen 2011), some structural adaptations have been described. For
example, in Urospora penicilliformis a dense cell wall, presence of mucilage and
external mineral deposition provide efficient shielding from high solar radiation and
desiccation (Roleda et al. 2010). In many cases, filamentous green algae can form
mats or turf-like structures that are effective to minimize the harmful effects of
changing environment (Bischof et al. 2006). In all, in terms of photosynthetic char-
acteristics and physiological responses to stress, form and function of some Antarctic
seaweed assemblages have been related to biogeographic affinity and depth. Based
on 31 species from King George Island, three major groups of species were defined:
(a) coarsely branched Rhodophyta are mostly found at shallow subtidal sites and
have an Antarctic-sub-Antarctic origin; (b) endemic Antarctic brown algae are dom-
inant at depths between 10 and 30 m and practically all attain thick leathery mor-
phology; and (c) filamentous and sheet-like green algae, mostly intertidal species,
normally can be categorized as algae with wide geographic distribution (Gómez
et al. 2019).
11.6 F
unctional Traits of Seaweeds and Properties
of Benthic Communities
Seaweeds in practically all cold-temperate and polar coastal ecosystems represent

foundational organisms, whose processes and fate determine key community indi-
cators, such as structure and functional and taxonomic richness (Chapman 1987;
Lüning 1990). In King George Island, the distribution and composition of different
functional groups in both intertidal and subtidal sites are regulated by different fac-
tors, which are defined by some species that account by 90% of the dissimilarities
between depth strata (Valdivia et al. 2014). When representative taxa are analysed,
effects are scale dependent: variance components increase at the finer scale of varia-
tion (from centimeters to meters) compared to shore level (hundreds of meters)
(Valdivia et al. 2014). In the intertidal system dominated by filamentous and finely
branched morphs, the grazing by the limpet Nacella concinna is probably one of the
most important biological interactions (Kim 2001; Segovia-Rivera and Valdivia
2016). Apart from green algae, N. concinna exerts control on periphyton, thus deter-
mining far-reaching ecological processes, e.g. the fate of re-colonization and suc-
cession in these systems (Campana et al. 2009; Valdivia et al. 2019; see also Chap.
12 by Campana et al. and Chap. 13 by Valdivia).
At the subtidal zone, facilitative interactions held by large brown algae through
bioengineering seem relevant for the structure and maintenance of the benthic com-
munities (Valdivia et al. 2015). These canopy-forming seaweeds are important as
they shelter other species of algae and invertebrates from harmful environmental
conditions and thus have an important effect on the community biomass of the
whole ecosystem (Valdivia et al. 2015; Ortiz et al. 2016; see also Chap. 15 by Momo
et al. and Chap. 16 by Ortiz et al.). However, in locations exposed to severe impact
of physical disturbance, small organisms can be favoured while canopy-forming
algae would be more sensitive (Smale 2007). For example, in eastern Antarctica
where ice cover can be considerably extended through spring, canopy-forming mac-
roalgae were only abundant at sites where sea-ice cover break-up occurs during
spring, but absent at sites that retained ice cover until summer (Johnston et al. 2007).
Thus, these organisms appear to respond slowly to the changing environment due,
for example, to enhanced warming. For example, in new ice-free areas originated
from glacier retreat where enhanced sediment input limits light penetration, estab-
lishment of large brown algae is highly constrained (Quartino et al. 2013). In these
highly perturbed sites, ice scouring and unconsolidated substrate affect consider-
ably the presence of canopy-forming algae and hence the taxonomic richness
(Klöser et al. 1994; Smale 2007; Smale et al. 2008; Valdivia et al. 2015). On the
other hand, environmental shifts driven by climate change can affect the morpho-
functional responses of Antarctic species. For example, physiology of canopy-
forming algae (e.g. Desmarestia spp.) may have consequences for the whole benthic
community (Schoenrock et al. 2015). In the case of crustose species, fleshy encrust-
ing forms (Hildenbrandia) could be favoured in scenarios of changing pH and tem-
perature compared to calcified Coralline species (Clathromorphum) (Schoenrock
et al. 2016). In general, morpho-functional and anti-stress mechanisms of macroal-
gae to cope with sharp physical gradients percolate towards upper hierarchies
through insurance of functional richness in the community, which set high degree of
resilience to physical perturbation (Ortiz et al. 2016, 2017) or to minimize the
impact of alien species (Arenas et al. 2006; see Chap. 16 by Ortiz et al.).
Considering some functional form models for marine seaweeds, similitudes and
analogies with terrestrial vegetation strategies can be identified. For example,
according to the functional groups described by Grime (1981) for terrestrial vegeta-
tion, opportunistic green algae growing at the intertidal zone could correspond to
the “ruderal” species, permanently subjected to strongly physical perturbation. In
contrast, large endemic brown algae, which thrive in sites with lower physical
Fig. 11.6 CSR Grime’s triangle describing the main strategies and environmental trade-off of the
major functional groups of Antarctic seaweeds. (Photos Myriogramme and Desmarestia by Ignacio
Garrido; Urospora by Iván Gómez)
perturbation, can be analogue to “competitive species” in virtue of their exuberant

canopy and perennial characteristics. For many temperate ecosystems, the life his-
tory traits conferring advantages under high levels of disturbance are convergent in
different types of algal assemblages, suggesting that some patterns could be gener-
alized (Steneck and Dethier 1994). However, in Antarctic communities some fac-
tors associated with disturbance and stress require adjustment to the extreme
Antarctic conditions. In the conceptual framework in Fig. 11.6, three major func-
tional groups of Antarctic seaweeds (turf algae, dominated by intertidal green algae;
canopy-forming algae, especially large brown algae; and corticated red algae,
grouping many understory species) can be oriented through the three axes following
a Grime’s CSR triangle schema. Here, the extreme action of ice (perturbation), light
limitation (stress), and biomass (competition) dimensions determine the separation
among algal groups. Corticate red algae in virtue of their extreme shade adaptation
represent the stress tolerant group. Here, many crustose species growing at very low
light conditions in the eastern Antarctic can also be added to this group. In the per-
turbation axis, filamentous and finely branched green algae and some little saccate
brown algae (Adenocystis utricularis) exemplify the colonizers, well adapted to
occupy sites highly perturbed by ice, terrestrial run-off, and high solar radiation.
Under these conditions abundance and species richness are less influenced by bio-
logical interactions (Valdivia et al. 2014; Segovia-Rivera and Valdivia 2016).
Finally, the canopy-forming algae, represented by species of the order Desmarestiales,

and Ascoseira and Cystosphaera that exhibit high biomass production, are dominat-
ing at sites with lower physical perturbation. However, they show competitive abili-
ties for light and substrate (Gómez et al. 1997; Valdivia et al. 2015).
The main ecological expression of the morpho-functional adaptation of Antarctic

seaweeds is the macroalgal zonation, which is not only a vertical arrangement of
species but also represents an ordination of organismal traits that can be classified
in different functional entities (e.g. gross morphology, life forms, physiological
responses). These attributes can be scaled up to community structure and ecosystem
functioning. The concept, well studied in plants, has been revitalized in the last
decade in the context of the contemporary climate change.
Due to the seasonally changing light conditions, characterized in the highest lati-
tudes by several months of very dim light, Antarctic seaweeds are adapted to very
low light levels. In contrast, after the ice break-up in spring, they suddenly can be
exposed to strong solar radiation. Thus the adaptations of Antarctic algae are finely
tuned with the daylength, changes in water turbidity, and ice perturbations. This
environmental variability is fully exploited by seaweeds in virtue of their efficient
morpho-functional adaptations. However, due to climate change, the environmental
settings in which Antarctic seaweeds have evolved for millions of years are chang-
ing. In these new scenarios, the adaptive capacities of these organisms as well as the
ecosystem functions they provide will be challenged (Constable et al. 2014; Gutt
et al. 2015). Although one can recognize that polar seaweeds are particularly sus-
ceptible to these changes with unpredictable consequences for the whole coastal
ecosystem, we have still a limited understanding on how physiological and morpho-
logical traits respond and how they will be integrated in, for example, molecular
mechanisms of environmental tolerance and stress resilience.
Acknowledgements The authors acknowledge the financial support from Conicyt Chile

(FONDAP 15150003, Anillo-PIA ART1101, Fondecyt 1161129) and INACH T-20-09 from the
Instituto Antártico Chileno. The helpful assistance and collaboration of the members of our labo-
ratories at Universidad Austral de Chile as well as the staff of the Instituto Antártico Chileno for
during various Antarctic expeditions are acknowledged.
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Part IV
Biological Interactions and Ecosystem
Processes
Chapter 12
Successional Processes in Antarctic
Benthic Algae
Gabriela L. Campana, Katharina Zacher, Fernando R. Momo,

Dolores Deregibus, Juan Ignacio Debandi, Gustavo A. Ferreyra,
Martha E. Ferrario, Christian Wiencke, and María L. Quartino
Abstract Despite the importance of benthic algal communities to Antarctic coastal

ecosystems, much information about their dynamics is still needed. Primary succes-
sion processes in the Antarctic benthos are frequently initiated by ice-mediated dis-
turbance and by the creation of denuded substrate following glacier retreat, both
expected to increase in the future. Primary succession of benthic algae starts with
rapid colonization by diatoms, ephemeral green algal filaments and propagules of
annual and pseudoperennial macroalgae. Early stages of macroalgae can be particu-
larly vulnerable to environmental stress factors, being critical for the structure of
mature communities. The Antarctic environment is severely affected by global
change, and successional patterns can change due to species-specific susceptibilities
to abiotic and biotic drivers, introducing changes in the matter and energy flow in
the coastal food webs.
This chapter summarizes new advances in our knowledge on the successional
dynamics of benthic primary producers in the Antarctic hard-bottom benthos.
Manipulative experiments on the effects of grazing and ultraviolet (UV) radiation as
drivers of the succession at early stages and long-term experiments carried out at
sites with different environmental conditions are compiled. The gathered informa-
tion can contribute to achieve a deeper knowledge of these key communities and
their structure and functioning in a changing environment.
G. L. Campana (*)
Departamento de Biología Costera, Instituto Antártico Argentino (IAA) - Dirección Nacional
del Antártico (DNA), Buenos Aires, Argentina
K. Zacher · C. Wiencke
Alfred-Wegener-Institute, Helmholtz Centre for Polar and Marine Research (AWI),
Bremerhaven, Germany
e-mail: katharina.zacher@awi.de; christian.wiencke@awi.de

https://doi.org/10.1007/978-3-030-39448-6_12
242 G. L. Campana et al.
Keywords Early colonizers · Ecological succession · Grazing ·

Microphytobenthos · Rocky substrate · UV radiation
12.1 Introduction
The Antarctic benthos is frequently exposed to ice-mediated disturbance leading to

successional processes and to the coexistence of patches of different developmental
stages (Gutt 2001; Quartino et al. 2005; Barnes and Conlan 2007; Teixidó et al.
2007). Furthermore, climate change-related phenomena have accelerated the retreat
of glaciers opening newly available substrate formerly covered by ice and, hence,
initiating primary succession processes (Quartino et al. 2013; Sahade et al. 2015;
Lagger et al. 2017, 2018). Even though the successional process in marine rocky
coasts has been subject to a great number of studies worldwide, they were con-
ceived mainly on temperate habitats (Noël et al. 2009; Benincà et al. 2015), whereas
successional processes in polar regions are still less known.
Studies on the successional patterns on the Antarctic benthos have mainly been
focussed on sessile faunal assemblages (Barnes and Conlan 2007; Dayton et al.
2016; Lagger et al. 2017, 2018, and references therein). These studies showed a
F. R. Momo
Instituto de Ciencias, Universidad Nacional de General Sarmiento (UNGS),
Los Polvorines, Argentina
D. Deregibus
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET),
J. I. Debandi
G. A. Ferreyra
Centro Austral de Investigaciones Científicas (CADIC-CONICET), Ushuaia, Argentina
e-mail: gferreyra@cadic-conicet.gob.ar
M. E. Ferrario
Facultad de Ciencias Naturales y Museo (FCNyM), Universidad Nacional de La Plata
(UNLP), La Plata, Argentina
e-mail: meferra@fcnym.unlp.edu.ar
M. L. Quartino
12 Successional Processes in Antarctic Benthic Algae 243
general low cover of the substrate even after several years, postulating predictable
successional processes as a result of slow growth and high seasonality (Bowden
2005; Bowden et al. 2006). However, the occurrence of high interannual changes as
a result of episodic events of massive colonization was also reported (Dayton 1989;
Dayton et al. 2016). More recent studies revealed a rapid colonization by a few spe-
cies after ice shelves collapse (Raes et al. 2010; Gutt et al. 2011; Fillinger et al.
2013) and the discovery of complex communities in newly ice-free areas (Lagger
et al. 2017, 2018).
For Antarctic hard-bottom coasts dominated by macroalgae, the successional
stages of the assemblages were frequently indirectly assessed, by relating it to the
identity and relative abundance of the dominant taxa and to the disturbance regime
of the site (Klöser et al. 1996; Quartino et al. 2005; Valdivia et al. 2014). For
instance, the presence of the green seaweed Monostroma hariotii Gain and colonial
diatoms in habitats severely affected by ice scouring was signalled as indicators of
early stages of succession (Klöser et al. 1996). In the study carried out by Quartino
et al. (2005), the cause of higher macroalgal diversity recorded at intermediate depth
ranges (5–10 m) was attributed to the coexistence of patches in different succes-
sional stages. More recent studies performed in newly ice-free hard-bottom areas
demonstrated the capability of macroalgae to colonize them rapidly (Quartino et al.
2013). The complexity of these communities, in terms of cover and richness, was
positively correlated to the elapsed time since the generation of the space and the
lower level of stress and disturbance imposed by a retreating glacier (Quartino et al.
2013; see also Chap. 8 by Quartino et al.).
In Potter Cove, a small fjord at the western Antarctic Peninsula (South Shetland
Islands), quite a number of studies were focussed to unravel the successional pat-
terns of benthic algal communities at the inter- and subtidal and over different time
spans (months to years) (Fig. 12.1). This chapter summarizes these works and the
advances in our knowledge on the successional process of primary producers in the
hard-bottom Antarctic benthos. We review in situ primary succession studies that
have been performed at this site and that have allowed for the description of the
structure of benthic primary producer communities during succession. Early stages
of succession are characterized through studies performed over the first 2–3 months
of colonization in the rocky substrate in the intertidal (Zacher et al. 2007a, b) and
the upper subtidal, at approximately 2 m depth (Campana et al. 2008a, b; Zacher
and Campana 2008; Campana 2018) (Fig. 12.1). These studies included a multifac-
torial design to test the effects of ultraviolet radiation and grazing on the developing
communities. Furthermore, experiments performed over a 4-year period with
monthly surveys at the subtidal (3–5 m depth) allowed for the characterization of
communities over a longer time span, at a site with no glacial influence, located at
the outer part of the cove and at an inner cove site, in close proximity to a retreating
glacier (Campana et al. 2018) (Fig. 12.1). We also discuss the importance of abiotic
and biotic drivers on community succession, the importance of their interactions
and the experimental approaches applied so far, with an emphasis on the effects of
global change-related phenomena.
Fig. 12.1 Map of Potter Cove (South Shetland Islands, western Antarctic Peninsula), showing the
location of successional experiments performed at the upper subtidal (at Peñón de Pesca, situated
in the outer part of the cove and at a site located in the inner cove, in close proximity to a retreating
glacier) and at an intertidal platform (Peñón Uno, located on Potter Peninsula). The effects of
ultraviolet radiation and grazing on developing communities were studied at the subtidal of Peñón
de Pesca and the intertidal of Peñón Uno (yellow square); long-term successional studies were
performed at Peñón de Pesca and at the inner cove over 4 years (green square). (Satellite image of
Potter Cove: Google Earth 2016). (Photos: left by Gabriela L. Campana; right by Katharina
Zacher)
12.2 S
tructural Patterns and Changes in Algal Community
Composition during Succession
Along the Antarctic hard-bottom coastlines studied in Potter Cove, the primary suc-
cession of benthic algae begins with a rapid colonization by diatoms, filamentous
green algae and propagules of annual and pseudoperennial macroalgae (Zacher
et al. 2007a, b; Campana et al. 2011; Campana 2018) (Fig. 12.2). This general taxo-
nomic composition is similar to studies carried out at the Arctic for early stages of
succession (Fricke et al. 2008, 2011).
As early colonizers in the marine benthos, diatoms may enhance or inhibit mac-
roalgal recruitment and growth (Huang and Boney 1985; Noël et al. 2009). As an
example, it was shown for the Arctic that diatoms apparently facilitate the establish-
ment of macroalgal propagules (Fricke et al. 2008). In the Antarctic benthos, few
investigations have focussed on the simultaneous study of microalgae and macroal-
gae in the successional process, particularly including detailed taxonomic analyses
(Wahl et al. 2004; Zacher et al. 2007a, b; Zacher and Campana 2008; Campana et al.
2008a, b; Campana 2018). Furthermore, the ecology and taxonomy of Antarctic
benthic diatoms are generally scarce when compared to macroalgae studies (Wulff
et al. 2011).
Over the first months of colonization, diatom assemblages were mainly domi-
nated by pennate, typically benthic diatom species (Zacher et al. 2007b; Campana
0 - 2,5 months 1 year 2 years 3 years 4 years
colonial diatoms annual and pseudoperennial macroalgae

green algal filaments
red algal propagules
Colonial diatoms Palmaria decipiens Phaeurus antarcticus
Green algal filaments Monostroma hariotii Iridaea cordata
Red algal propagules Adenocystis utricularis Corallinaceae
Fig. 12.2 The composition of the community of benthic primary producers over succession in an
Antarctic upper subtidal rocky coast. The scheme compiles the information obtained by in situ
studies focussed on the effects of ultraviolet radiation and grazing at early succession (0–2.5 months)
and long-term successional studies carried out from 1 to 4 years (Campana et al. 2008a, b, 2018;
Campana 2018). Both studies were performed at the same subtidal site (Peñón de Pesca, Fig. 12.1),
at low depths (less than 3 m), and were started during summer (December and February, respec-
tively). The succession of the bacterial community during biofilm development is not described
(see Lee et al. 2016). The new substrate is initially colonized by pioneer groups that occupy rapidly
the space; the colonization starts with dominance of diatoms, and a gradual higher space occupa-
tion by green algal filaments occurs. Propagules of red algae are established since the beginning of
the colonization, P. decipiens being the more abundant. These young sporelings probably develop
the sporophyte during the following spring, which coincides with the appearance of individuals in
communities of 1 year of colonization, during summer. At longer time scales, annual and pseudo-
perennial macroalgae dominate the substrate. Monostroma hariotii and P. decipiens are identified
in these stages, after 1 and 2 years of colonization, whereas P. antarcticus and I. cordata were more
abundant after 3 and 4 years, respectively. The dominance of A. utricularis was evident since the
first year, and a higher space occupation by red crustose algae occurs over time. The 4-year-old
communities were similar to the surrounding communities at low depths (less than 5 m), with
absence of large thalli of Desmarestiales that usually form dense forests at deeper depths
et al. 2008b; Campana 2018). The small naviculoid Navicula perminuta Grunow
was conspicuous in the intertidal and the subtidal assemblage (Zacher et al. 2007b;
Campana 2018). The assemblages further included colonial forms, some of which
reached macroscopic dimensions in the subtidal, such as Fragilaria striatula
Lyngbye and Fragilaria islandica Grunow var. adeliae Manguin; pedunculated
forms, such as Pseudogomphonema kamtschaticum (Grunow) Medlin and the spe-
cies of the genus Licmophora; and adnate forms, which have a firm adhesion to the
substrate through most of the valvar surface, such as the species of the genus
Cocconeis (Zacher et al. 2007b; Campana et al. 2008b; Campana 2018).
These benthic diatoms are probably more relevant to the early stages of succes-
sion and were shown to contribute less to the differences between years over longer
time scales, when macroalgae dominate the substrate (Campana et al. 2018)
(Fig. 12.2). During these early stages, diatom abundance can differ drastically when
comparing intertidal and subtidal assemblages, being much higher in the subtidal
(Zacher and Campana 2008). This pattern could be related to the more stable
prevailing conditions in the subtidal, with lower influence of stress and disturbance
factors and/or lower grazing pressure when compared to the intertidal (Zacher and
Campana 2008; Zacher et al. 2011).
Regarding seaweeds, within the first 2–3 months of development, no adult thalli
were observed in the intertidal, whereas only filamentous chlorophytes can be mac-
roscopically visible in the subtidal (Zacher et al. 2007a; Zacher and Campana 2008;
Campana 2018). Even though they gradually increased in space occupation in the
subtidal, they were never dominant (Campana 2018). In contrast, seaweeds can
dominate the space on artificial tiles within 2–3 months in temperate and tropical
habitats, a fact that may support the idea that succession proceeds more rapidly than
in the polar benthos (Wahl et al. 2004).
During early stages of succession (less than 10 months of development), young
algal recruits of M. hariotii and Palmaria decipiens (Reinsch) Ricker were regis-
tered in intertidal (Zacher et al. 2007a) and subtidal assemblages (Campana et al.
2011; Debandi et al. 2015) (Fig. 12.2). Both species were the only macroalgae
inhabiting a newly ice-free area severely affected by a retreating glacier, showing
their ability not only to colonize newly open space but also to grow in areas sub-
jected to high sedimentation, low light penetration and high ice disturbance
(Quartino et al. 2013). Monostroma hariotii is an annual species that can be very
abundant in intertidal habitats, which are subject to high stress and disturbance
intensity (Wiencke and Clayton 2002; Kim 2001; Marcías et al. 2017).
It has also been proposed as a pioneer species in the subtidal, as it has been
recorded in sites repeatedly affected by ice scouring (Klöser et al. 1996). Similarly,
P. decipiens can cope with marked changes in salinity and light availability and can
grow rapidly in intertidal sites subjected to ice scouring (Becker et al. 2011;
Deregibus et al. 2016; Marcías et al. 2017). For these reasons, it was signalled as
having a high competitive capacity and considered to be an opportunistic species in
the colonization process (Becker et al. 2011). The recruits of this species probably
develop the sporophyte during the next spring, which coincides with their appear-
ance in the communities after 1 year of colonization (Campana et al. 2018)
(Fig. 12.2).
The brown seaweed Adenocystis utricularis (Bory) Skottsberg is another species
that can also be present at early stages of succession, as small recruits were recorded
after only 1 month of colonization in the intertidal (Zacher et al. 2007a) and
10 months in the subtidal (Debandi et al. 2015). However, it was dominant over the
whole experimental exposure at a four-year successional study performed at the
upper subtidal, at 3 m depth (Campana et al. 2018) (Fig. 12.2). Adenocystis utricu-
laris is an aseasonal annual species in Antarctic intertidal habitats that can be very
abundant (de Reviers and Délépine 1981; Wiencke and Clayton 2002). It has a crus-
tose phase that can survive winter, and it is biannual in deeper subtidal habitats
(Wiencke 1990). The studies performed so far revealed that this species tends to
monopolize the substrate and, thus, may impede the recruitment—or resist the inva-
sion—by other species (Sousa 1979).
The brown seaweed Phaeurus antarcticus Skottsberg and the red Iridaea cordata
(Turner) Bory de Saint-Vincent were found to reach their maximum cover after 3
and 4 years of colonization, respectively (Fig. 12.2). A dense canopy of P. antarcti-

cus was found after 3 years of colonization, when the highest macroalgal cover and
space occupation were attained (Campana et al. 2018). The branched thalli of this
species generated several layers and a general more complex three-dimensional
structure of the communities (Campana et al. 2018). Between the third and the
fourth year, competitive interactions may result in the liberation of space, and the
red alga I. cordata reached its maximum cover, during the following summer. These
four-year-old communities were also composed of the crustose phase of A. utricu-
laris and red coralline algae, which showed a higher space occupation over time
(Campana et al. 2018). The same study has also shown that coralline algae have the
potential to establish and grow on the crusts of A. utricularis (Campana 2018;
Campana et al. 2018).
A great space occupation by crustose red algae can be a characteristic trait of
mature communities at the same study site, at these low depths (Klöser et al. 1994).
Besides, they can be indicators of low disturbance in the Antarctic subtidal (Barnes
et al. 1996), where they are frequently found under the canopies of Desmarestiales
(Irving et al. 2005; Clark et al. 2011). Long-term studies could reveal the role of
these algae in successional processes (Barner et al. 2016) as they have been pro-
posed to favour the recruitment of late colonizers by providing structurally simple
habitats, with higher rugosity than the natural substrate (Maggi et al. 2011).
It has been suggested that communities in the upper subtidal of polar regions are
permanently in early successional stages, with low species diversity (Witman and
Dayton 2001). In the long-term experiment carried out at Potter Cove, the experi-
mental tiles were colonized by fast-growing macroalgae, with absence of large thalli
of perennial species, and after 4 years of colonization, these communities resembled
the surrounding community at low depths (Quartino et al. 2005). Even though
recruits of perennial species were found in the colonization tiles, they did not grow
until maturity and reached only a few centimetres (Campana et al. 2018). Repeated
ice abrasion, interspecific competition with fast-growing species and/or high irradi-
ance conditions in spring if no canopies are present were signalled as possible driv-
ers of these communities that deflect the successional trajectory and maintain the
communities in early stages of succession at these low depths (less than 5 m)
(Campana et al. 2018).
In macroalgal dominated Antarctic subtidal sites, climax communities can be
identified by the abundance of large Desmarestiales that form extensive and persis-
tent patches that seem to be stable over time (Campana et al. 2011). Among these
species, some representatives can be the season anticipators Desmarestia menziesii
J. Agardh, D. anceps Montagne and Himantothallus grandifolius (A. Gepp and
E.S. Gepp) Zinova, as they are terete to leathery, perennial macroalgae with high
biomass and a complex three-dimensional structure and are habitat providers and
chemically defended (Wiencke and Clayton 2002; Amsler et al. 2005; Quartino
et al. 2005, 2008; Huang et al. 2006, 2007; see also Chap. 11 by Gomez and
Huovinen for a description of form and function in Antarctic seaweeds). These spe-
cies gather many of the attributes of species recorded in mature communities in
other environments (sensu Littler and Littler 1980; Noël et al. 2009; Wiencke and
Amsler 2012; Gómez et al. 2019). They can also be considered as foundation spe-
cies (sensu Dayton 1972) that provide structurally complex habitats favouring the
presence of smaller organisms that live associated to them, such as amphipods and
gastropods (Huang et al. 2007; Amsler et al. 2015). Whereas certain macroalgal
species are found as epiphytes on these species, it is noteworthy the low abundance
of epiphytic algae in this Antarctic subtidal forests (Wiencke and Clayton 2002;
Peters 2003). In contrast, there is a high occurrence of filamentous endophytes
(Peters 2003) that were shown to be highly palatable to sympatric amphipods
(Amsler et al. 2009; see also Chap. 17 by Amsler et al.).
12.3 E
cological Factors Influencing Antarctic
Algal Succession
12.3.1 Ultraviolet Radiation
Ultraviolet-B (UV-B) is an environmental stress factor that can limit the develop-
ment of benthic primary producers causing inhibition of photosynthesis and damage
to biomolecules such as DNA, proteins and lipids, among other damaging effects
(Villafañe et al. 2003; Bischof et al. 2006; Häder et al. 2011; Karsten et al. 2011). In
fact, it has been well established that Antarctic seaweed assemblages show species-
specific sensitivity towards UV, which determine major aspects of the ecology of
these organisms (Bischof et al. 1998, 2006; Wiencke et al. 2007). Thus, coloniza-
tion, establishment and further development of the benthic algae are affected by UV
radiation. As an example, green algae that inhabit the intertidal have a rapid and
high acclimation potential to UV, whereas some red algae that are found under the
canopy provided by other species are very UV-sensitive (Bischof et al. 2006).
Besides, certain species can show high phenotypic plasticity revealing a correspon-
dence between UV-B tolerance to their vertical distribution or growth sites
(Rautenberger et al. 2013; see Chap. 7 by Huovinen and Gómez).
The experiments carried out in the intertidal and the subtidal of Potter Cove
revealed that UV is an important structuring driver of the benthic primary producers
community in Antarctica at early stages of succession (Zacher et al. 2007a, b;
Campana et al. 2008a, b; Zacher and Campana 2008; Campana 2018). Ultraviolet
radiation was shown to affect algal groups differently: whereas diatoms were mostly
unaffected, the establishment and/or growth of green and red algal germlings was
limited by ambient UV radiation (Zacher et al. 2007a, b; Campana et al. 2008b;
Campana 2018). Antarctic benthic diatoms from soft-bottom habitats have shown a
high resistance to UV, with low levels of photoinhibition and efficient repair mecha-
nisms (Wulff et al. 2008). In these habitats, vertical migration can be a mechanism
of UV avoidance (Karsten et al. 2011). However, as revealed by experiments per-
formed in rocky coasts, a high resistance of these algae was also shown where this
mechanism of avoidance is not possible (Zacher et al. 2007b; Campana et al. 2008b).
Particularly for the subtidal, this group dominates the substrate at early stages of
succession, and when grazers were excluded (Fig. 12.3a), they provided a
UV-resistant canopy that could positively influence macroalgal recruitment and/or
growth (Molis and Wahl 2004).
Early life stages of macroalgae in polar environments can be more vulnerable to
UV radiation than their adult thalli (Bischof et al. 2006; Wiencke et al. 2007; Roleda
et al. 2009; Karsten et al. 2011). For instance, filaments of Antarctic specimens of
Urospora penicilliformis (Roth) Areschoug have high light requirements, but their
spores are more UV-B sensitive than adult stages (Roleda et al. 2009), being their
settlement possibly limited by UV-B radiation (Campana 2018). Besides, the nega-
tive UV-B effects on the photosynthesis and DNA of propagules can be correlated
to the depth collection of the adult thalli (Wiencke et al. 2000). In Antarctica, propa-
gules of macroalgae dwelling in the intertidal have a high resistance to UV, with
high recovery capacity and scarce or even null DNA damage (Zacher et al. 2007c).
In contrast, the germination of spores of species that inhabit the subtidal can be
severely affected by ambient UV, an effect that can be potentiated by UV-B in labo-
ratory conditions (Zacher 2014). Besides, UV was also shown to cause higher pho-
tosynthesis inhibition in spores of subtidal species compared to intertidal ones
(Navarro et al. 2016; see also Chap. 10 by Navarro et al.).
The available information suggest that at the beginning of the successional pro-
cess, during the colonization of the substrate, the differential sensitivity to UV radi-
ation among different groups of benthic algae (viz. diatoms and macroalgae), among
different seaweed species and/or different developmental stages of a species, can
shape the structure and functioning of the communities (Lotze et al. 2002; Villafañe
et al. 2003; Zacher et al. 2007a, b; Campana et al. 2008a; Zacher 2014), which seem
to be more UV-resistant over time (Lotze et al. 2002; Wahl et al. 2004; Molis and
Wahl 2004, 2009).
12.3.2 Grazing
According to the available information, grazing effects in the Antarctic benthos are
expected to be intense in early stages of algal succession, when communities are
composed of more vulnerable life forms such as diatoms and certain early life stages
of macroalgae (Brêthes et al. 1994; Kim 2001; Zacher et al. 2007a, b), a pattern that
has been recorded in other environments as well (Sousa 1979; Farrell 1991;
Lubchenco 1983; Sousa and Connell 1992). For instance, the conspicuous limpet
Nacella concinna Strebel exerts a high influence in structuring the assemblages of
primary producers in the intertidal, particularly at low shore levels (Kim 2001;
Segovia-Rivera and Valdivia 2016; Valdivia et al. 2019; see also Chap. 13 by
Valdivia). On their upwards migration from the subtidal to the intertidal, N. con-
cinna feeds on microphytobenthos and green filamentous algae at low shore levels
(Brêthes et al. 1994; Kim 2001), more severely affecting the early life stages of
macroalgae compared to adults (Kim 2001). In fact, grazing was identified as a
Fig. 12.3 (a) Experimental unit used to determine the effects of UV and grazing on developing
algal communities; the same experiment was performed at the subtidal of Peñón de Pesca and the
intertidal site Peñón Uno. Note tiles (100 cm2) obtained from a (i) caged (grazer-excluded treat-
ment) and (ii) an uncaged treatment, at the subtidal. (b) Underwater view of a set-up used to allow
colonization over 10 months; tiles (25 cm2) were subsequently transported to the laboratory to
perform further experiments. Note a detail of the obtained communities, composed of young germ-
lings of the red seaweed P. decipiens of different age (i and ii), brown A. utricularis (iii) and green
M. hariotii (iv). (c) Underwater view of a long-term successional study performed in Peñón de
Pesca and at an inner cove site exposed to the influence of a retreating glacier (Fig. 12.1); note
bigger-sized colonization tiles (500 cm2) applied to perform the study over 4 years. (Photos: (a) left
panel by Katharina Zacher, (b) left panel by Argentine Army diving crew, (c) left panel by Marcelo
Mammana; (a) and (c) right panel by Gabriela L. Campana, (b) right panel by Gabriela L. Campana
and Juan I. Debandi)
Fig. 12.3 (continued)
strong driver of the structure of developing algal communities in the studies per-
formed in Potter Cove. Biomass reduction was mainly caused by the gastropods
N. concinna and Laevilacunaria antarctica Martens (Zacher et al. 2007a, b;
Campana et al. 2008a, b; Campana 2018). At both depth ranges (intertidal and sub-
tidal), grazers significantly consumed diatoms, and particularly for the subtidal site,
feeding on colonial diatoms exerted a drastic change in the physiognomy of the
assemblages (Campana 2018) (Fig. 12.3a). This is a trait that was also observed for
freshwater (Steinman 1996) and other marine habitats (Nicotri 1977; Sommer
1999a, b; Hillebrand et al. 2000), where the consumption of canopy algae results in
an increase in the relative abundance of smaller taxa and prostrate forms (Nicotri
1977; Hillebrand et al. 2000).
A differential susceptibility towards grazing was detected among different mac-
roalgal species, which resulted in changes in species composition (Zacher et al.
2007a; Campana 2018). Among green algae, Urospora penicilliformis (Roth)
Areschoug was not affected by grazing, but early stages of M. hariotii could be
severely affected (Zacher et al. 2007a, Campana 2018). Besides, the reduction of the
abundance of the dominant taxa (diatoms) was shown to be beneficial for the estab-
lishment of certain red algal species whose early stages are firmly attached to the
substrate, such as P. decipiens (Zacher et al. 2007a; Campana 2018). The diminish-
ing space pre-emption and/or the reduction of shading may result in a higher abun-
dance of red algae, causing increased evenness and, thus, diversity of the community
(Campana et al. 2011; Campana 2018). A similar effect was observed at the intertidal
site at Potter Cove where a higher macroalgal diversity was attributed to the increased
spatial heterogeneity (Sommer 2000) caused by the simultaneous presence of
untouched biofilms and areas visibly consumed by gastropods (Zacher et al. 2007a).
In contrast to vulnerable early successional stages, chemically defended mac-
roalgae can be characteristic at later successional stages. Dominant brown
macroalgae (except for Desmarestia antarctica R.L. Moe and P.C. Silva) are chemi-
cally defended against the three most common sympatric consumers: the sea star
Odontaster validus Koehler, the fish Notothenia coriiceps J. Richardson and the
amphipod Gondogeneia antarctica Chevreux (Amsler et al. 2005). Macroalgal pal-
atability on the sea urchin Sterechinus neumayeri Meissner was not tested due to its
unsuitability for feeding bioassays (Amsler et al. 2005), but studies in McMurdo
revealed that both dominant macroalgae in that area are chemically protected against
this consumer (Amsler et al. 1998, 1999). These authors propose that macroalgae
are commonly unpalatable to sympatric consumers mainly as a result of chemical
defences, as nor physical properties such as the toughness of the thallus or the nutri-
tional content appeared to be related to the algal palatability (Amsler et al. 2005;
Peters et al. 2005; see also Chap. 17 by Amsler et al.). In this sense, several works
have stressed that there is a high macroalgal contribution to the food webs through
the detrital pathway (Fischer and Wiencke 1992; Amsler et al. 2005; Seefeldt et al.
2017; Braeckman et al. 2019). However, amphipod grazing can probably be consid-
ered a biological force that also shapes more mature seaweed communities (see
Huang et al. 2006; Amsler et al. 2009; Aumack et al. 2011; Bucolo et al. 2011).
Indeed, amphipod grazing is presumably responsible for the exclusion of subtidal
filamentous algae in the western Antarctic Peninsula (Peters 2003), and it is hypoth-
esized that they live in a mutualistic relationship with macroalgae, cleaning poten-
tially harmful epiphytes in a chemically defended habitat (Amsler et al. 2014; see
Chap. 13 by Valdivia and Chap. 17 by Amsler et al.).
It is important to point out that grazing effects are not unidirectional and interac-
tions with other biotic and abiotic stressors are expected to occur (e.g. Bothwell
et al. 1994). For instance, grazing by a limpet had a positive effect on Arctic mac-
roalgae germlings under intermediate levels of sedimentation (Zacher et al. 2016a).
In the subtidal experiment carried out at Potter Cove, some of the grazing effects
were more intense in UV or UV-B shielded communities: a direct effect on algae
causing lower palatability or a negative effect on grazers that reduce their activity or
density when this radiation is present was postulated as explanations for the observed
tendencies (Campana et al. 2008a).
12.3.3 Glacier Retreat
Climate change has already shown to have a strong influence on Antarctic benthic
communities (Smale and Barnes 2008; Pasotti et al. 2015; Sahade et al. 2015; Moon
et al. 2015). Antarctic macroalgae are cold-water-adapted organisms, and tempera-
ture stress may limit their development (Wiencke et al. 2007). Furthermore, the
rapid glacier retreat observed over the western Antarctic Peninsula has opened
newly ice-free areas where reduced light penetration caused by increased sedimen-
tation are the prevailing conditions (Rückamp et al. 2011; Quartino et al. 2013;
Deregibus et al. 2016). Primary succession patterns may be affected by high sedi-
mentation rates, which may reduce macroalgal propagules survival or even prevent
the spore settlement on the rocky substrate (Airoldi 2003; Zacher et al. 2016a). In
fact, in Potter Cove, the cover and diversity of the assemblages of macroalgae colo-
nizing newly ice-free areas were inversely correlated to the level of stress and dis-
turbance imposed by the retreating glacier, being the lowest in sites close to the
glacier with high sedimentation rates, lowest light penetration and high ice distur-
bance (Quartino et al. 2013; see Chap. 8 by Quartino et al. and Chap. 9 by Deregibus
et al.).
Long-term successional patterns were also evaluated by performing a coloniza-
tion experiment in close proximity to this retreating glacier in Potter Cove (Campana
et al. 2018). On one hand, this study showed convergent patterns to the observed for
the site not affected by glacier influence (Campana et al. 2018). The assemblages
were also dominated by algae, in particular a few opportunistic species, with
A. utricularis reaching a similar cover—approximately of 70%—after 2 years.
Besides, there were significant interannual changes in the assemblages and an
increase in cover over time until the third year, followed by a significant decline
between the third and fourth year. As both experiments were carried out with a year
of difference in their starting points, these convergent patterns can point to a predict-
able successional process for subtidal macroalgal communities in the Antarctic ben-
thos (Campana et al. 2018).
On the other hand, the communities located close to the retreating glacier showed
lower macroalgal richness and a decreased diversity trend over time, which was
attributed to (i) a lower spore availability in more simple communities established
in newly ice-free areas, (ii) a higher sedimentation causing direct abrasion or burial
of propagules and reduced light penetration and/or (iii) a higher ice disturbance
caused by ice block landslides from the glacier (Quartino et al. 2013; Deregibus
et al. 2016; Campana et al. 2018). More recent colonization studies performed in
newly ice-free areas with different glacial influence showed similar patterns, with
an inverse relationship between the algal cover and diversity, and the degree of sedi-
mentation (Deregibus 2017; see Chap. 9 by Deregibus et al.).
The combined effects of increased temperature, sedimentation and grazing on
the early succession of benthic algae were also studied for subtidal communities
developed over 10 months in Potter Cove (Debandi et al. 2015). These studies
revealed that increased sedimentation might favour the growth of P. decipiens and
M. hariottii and have neutral effects on brown algal early colonizers (Debandi 2019).
12.4 E
xperimental Approaches to Study In Situ Succession
of Antarctic Benthic Algae
Different experimental approaches have been applied so far in order to study pri-
mary succession at the polar benthos (Barnes and Conlan 2007; Campana et al.
2011; Dayton et al. 2016). In most of the cases, artificial substrates were used to
allow the colonization by benthic algae (Zacher et al. 2007a, b; Zacher and Campana
2008; Campana et al. 2008a, b; Campana 2018) (Fig. 12.3). The use of settlement
tiles was shown to be a useful tool to tackle these studies, particularly for polar
regions, where relatively easy installation and retrieval are very much needed
(Stanwell-Smith and Barnes 1997; Campana et al. 2011). This experimental
approach allows uniform settlement conditions and standardized replicates so that
several-factor designs and the possibility of deploying the same experiment simul-
taneously at different sites can be achieved (e.g. Wahl et al. 2004; Zacher and
Campana 2008).
In order to assess the effects of abiotic and biotic drivers of communities at the
very early stages of succession in Antarctica, artificial substrates of relatively small
dimensions (25 to 100 cm2) were shown to be adequate (e.g. Zacher et al. 2007a, b;
Campana et al. 2008a, b; Debandi et al. 2015) (Fig 12.3a), as they were in other
polar regions (Fricke et al. 2008, 2011). Besides the mentioned advantages of their
use, these tiles can be transferred to the laboratory, where detailed analyses of dia-
toms and early stages of seaweeds, as well as quantifications of biomass, cell densi-
ties and percentage of cover of algae on known areas, can be assessed (Foster and
Sousa 1985; Stanwell-Smith and Barnes 1997; Campana et al. 2011). Moreover,
these assemblages can be applied to physiological studies and further experimenta-
tion (Fig. 12.3b).
When studying successional patterns over a longer time scale (> a year), bigger
tiles, directly fixed to rocky substrate, were chosen (500 cm2) (Campana et al. 2018)
(Fig. 12.3c). These bigger dimensions still permitted an easy manipulation and rep-
lication of a somehow simpler design, and importantly, they allowed an adequate
assessment of community structure as organisms grew. For instance, the dense can-
opy formed by P. antarcticus included organisms reaching a maximum length of
1.2 m (Campana et al. 2018). In this experiment, tiles were monitored by two meth-
ods, as photographic samplings were performed on a monthly basis and detailed
laboratory analyses were done in spring and summer. Both methods revealed the
same patterns of succession and gave complementary information (Campana 2018).
Laboratory analyses applied the “point quadrat” method, which resulted to be the
most adequate to determine ecological indexes and community cover particularly at
later stages of succession, when several layers occur (Foster et al. 1991). This sam-
pling method gave information about the canopy and the understory algae and, thus,
about the three-dimensional characteristics of the analysed communities. On the
other hand, photographic samplings allowed for the detection of faster seasonal
changes that occurred over winter and autumn, achieving a higher time resolution of
the sampling.
12.5 Concluding Remarks and Perspectives
Even though preforming in situ experimental studies in the marine Antarctic ben-
thos can involve logistic constraints and difficulties, they are fundamental to eluci-
date mechanisms and to evaluate the influence of specific factors on biological
processes such as succession (Benedetti-Cecchi 2000; Meiners et al. 2015; Barner

et al. 2016). The studies performed so far reveal that continuous monitoring of envi-
ronmental conditions is essential to better explain the successional patterns of algae
in the Antarctic benthos. Light availability—including UV radiation—can be an
important driver of successional changes and is modified by season, ice cover, phy-
toplankton blooms and sediment input during the warmer seasons (Campana et al.
2011; Gómez et al. 2011). Furthermore, biological drivers such as grazers should
also be monitored; for instance, the increasing grazing pressure by N. concinna at
the end of winter can be signalled as an important factor in the control of the dynam-
ics of these communities in the rocky bottoms (Brêthes et al. 1994; Kim 2001).
Non-selective grazing by this gastropod could be seasonal, exerting a higher pres-
sure during its migration from the deep subtidal to the intertidal at the end of winter
and early spring (Brêthes et al. 1994; Kim 2001; Zacher et al. 2007b; Campana 2018).
Early stages of succession were shown to be particularly vulnerable to UV radia-
tion and grazing and are probably controlled by complex interactions among abiotic
factors and biological interactions. Considering that UV radiation is an environmen-
tal stress factor for Antarctic ecosystems, it is important to explore the effects of
these wavelengths on algae-grazers interactions, such as the effects of UV on algal
palatability (e.g. Pavia et al. 1997; Macaya et al. 2005; Fairhead et al. 2006) and on
the physiology and behaviour of consumers (Sommaruga 2003; Obermüller et al.
2007). Furthermore, the interactions with climate change processes such as
increased temperature and acidification should also be considered (Rautenberger
et al. 2015; Flores-Molina et al. 2016; Häder 2018).
Antarctica, and particularly the Antarctic Peninsula, is one of the regions most
seriously affected by climate change (Turner et al. 2009), where a number of associ-
ated phenomena can exert a strong influence on the structure and functioning of
benthic communities (Quartino et al. 2013; Sahade et al. 2015; Moon et al. 2015;
Torre et al. 2017; Häder 2018; see Chap. 8 by Quartino et al.). Some of these phe-
nomena are bound to initiate colonization processes and affect the following stages
of succession. On one hand, glacier retreat on the western Antarctic Peninsula has
originated newly ice-free areas that were colonized by macroalgae (Quartino et al.
2013) and invertebrates (Sahade et al. 2015; Lagger et al. 2017, 2018). Furthermore,
recent blooms of benthic diatoms have been registered on the soft substrate at sites
exposed to glacier melting (Ahn et al. 2016), pointing to a substantial change in
benthic communities. On the other hand, ice abrasion is postulated to increase due
to a lower formation of fast ice that allows higher movement of existing icebergs
and by the existence of new ice blocks and icebergs originated from retreating gla-
ciers (Barnes 2017; Deregibus et al. 2017).
Besides, the temporal and spatial reduction in fast ice formation may result in
higher light availability in the water column during winter and early spring, leading
to a higher primary production (Johnston et al. 2007; McClintock et al. 2008; Clark
et al. 2013; Deregibus et al. 2016) and favouring the colonization of deeper areas
(Miller and Pearse 1991; Gómez and Huovinen 2015). However, this will imply a
higher penetration and time exposure to damaging UV radiation (Gómez and
Huovinen 2015; see also Chap. 7 by Huovinen and Gómez). Besides, increased
sedimentation during warm months may counteract negative UV effects but simul-
taneously reduce photosynthetically active radiation (PAR, 400–700 nm) availabil-
ity, leading to changes in community structure and affecting the carbon balance of
macroalgae (Quartino et al. 2013; Deregibus et al. 2016; see Chap. 9 by Deregibus
et al.). As already mentioned, higher sedimentation can also affect the survival or
interfere with the establishment of macroalgal propagules (Zacher et al. 2016a),
benefitting the settlement of early space occupiers such as P. decipiens and M. hari-
otii (Quartino et al. 2013)
Overall, in this Antarctic environment seriously affected by global change phe-
nomena, it is important to assess the patterns of community development during
succession and how they can be modified due to a differential sensitivity of algae to
abiotic changes (i.e. a higher space availability but, simultaneously, higher tempera-
tures, changes in PAR availability, higher ice disturbance, higher sedimentation,
acidification) that may lead to changes in biological interactions, such as grazing
and competition (Schoenrock et al. 2015; Navarro et al. 2016; Zacher et al. 2016a,
b; Schram et al. 2017). Besides, studies using natural substrata, at greater depths,
and larger temporal and spatial scales are necessary to reveal the underlying mecha-
nisms and interactions (Campana et al. 2011). The gathered information can con-
tribute to achieve a deeper knowledge of these communities, whose structure and
functioning are key to the changing Antarctic coastal systems.
Acknowledgements A significant part of the work reviewed here was performed within the
framework of the scientific collaboration between Instituto Antártico Argentino (IAA)/Dirección
Nacional del Antártico (DNA) and the Alfred Wegener Institute Helmholtz Centre for Polar and
Marine Research (AWI). We thank the support of Carlini Station and Dallmann Laboratory crews
over the several expeditions involved. Field assistance of Oscar González and Alejandro Ulrich
was always invaluable, as was the work of summer and overwinter expedition scientists and of the
Argentine Army and German diving crews. We acknowledge the financial support by grants from
CONICET, DNA-IAA, ANPCyT-DNA (PICTO 0116/2012–2015, PICT 2017-2691), AWI,
Deutsche Forschungsgemeinschaft (DFG, grant Za735/1-1) and MINCyT-BMBF Program
(AL/17/06-01DN18024). This chapter also presents an outcome of the International Research
Network IMCONet funded by the Marie Curie Action IRSES IMCONet (FP7 IRSES, Action No.
318718) and CoastCarb (Funding ID 872690, H2020-MSCA-RISE-2019-Research and Innovation
Staff Exchange).
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Chapter 13
Seaweed-Herbivore Interactions: Grazing
as Biotic Filtering in Intertidal Antarctic
Ecosystems
Nelson Valdivia
Abstract Consumers constitute a key component of the environmental filters that

restrict the establishment of colonists into local assemblages. Thus, the trophic
activity of consumers, particularly grazers, can be pivotal to control the develop-
ment of potential algal invaders in Antarctic coasts. Here, the consumptive effects of
coastal macrobenthic grazers on algal communities are reviewed to assess the
degree to which these consumers can mediate the introduction of seaweeds in inter-
tidal Antarctic communities. Gastropods and amphipods have strong consumptive
effects on algal communities. Yet, amphipods are sensitive to climate change factors
such as warming and acidification, which could hamper their ability to control
native and alien macroalgae. Alien macroalgae that modify the abiotic environment,
such as the gutweed Ulva intestinalis in tidepools, represent potential superior com-
petitors in Antarctic ecosystems. In this line, simulations based on a simple proba-
bilistic model showed that intermediate to high levels of frequency-dependent
consumption seem to be fundamental to allow for stable coexistence when the alien
species is competitively superior. With this work, I hope to stimulate further manip-
ulative research to assess the role of benthic consumers in mediating the coexistence
(or lack thereof) between alien and native seaweeds under multiple climate change
scenarios.
Keywords Competition · Environmental filters · Grazing · Alien macroalgae
N. Valdivia (*)
Instituto de Ciencias Marinas y Limnológicas, Facultad de Ciencias, Universidad Austral
de Chile, Valdivia, Chile
e-mail: nelson.valdivia@uach.cl

https://doi.org/10.1007/978-3-030-39448-6_13
266 N. Valdivia
13.1 B
iological Invasions and Their Impact on the Ecology
of Antarctic Coastal Systems
Biological invasions are one of the major anthropogenic threats to biodiversity

across multiple spatiotemporal scales (Simberloff et al. 2013). The negative conse-
quences of invasions range from local extinction of native species to the impairment
of ecosystem functioning and from alterations of interaction webs to the loss of
ecosystem services (Vitousek et al. 1997; Bulleri et al. 2010; White and Shurin
2011; Silva et al. 2019). In marine communities, for example, the introduction of
consumers into a bottom-up-controlled ecosystem can lead to severe compositional
shifts and significant declines in diversity (Kotta et al. 2018). Invasive macroalgae,
in addition, have been shown to reduce local diversity through interference competi-
tion that involves drastic environmental changes (Björk et al. 2005). The effects of
invasive species can be particularly severe on ecologically isolated ecosystems,
because of low functional redundancy and restricted niche coverage (Hughes and
Convey 2014). Antarctica is an iconic example for ecologically isolated ecosys-
tems—this isolation has influenced the evolution of a high proportion of endemic
species, which makes the Antarctic ecosystems a highly ranked scientific priority
(Kennicutt et al. 2014). Accordingly, the study of biological invasions, especially in
ecologically isolated ecosystems like Antarctica, is of widespread relevance for
conservation ecology.
Due to its well-described biological isolation and adverse abiotic conditions,
Antarctica provides a unique opportunity to improve our mechanistic understanding
of biological invasions (Chown et al. 2015; McCarthy et al. 2019). This is particu-
larly accurate for Antarctic coastal marine rocky communities, because of the mul-
tiple biotic and abiotic environmental changes that are currently increasing the risk
of non-native marine species in these ecosystems (McCarthy et al. 2019). For
instance, increasing ship activity and high transportability have been suggested as
critical factors during the first stages of the invasion process of marine macroalgae
and invertebrates (Blackburn et al. 2011; McCarthy et al. 2019). Associated to the
transport of marine invaders, recent evidence indicates that rafting macroalgae are
able to cross the Antarctic Circumpolar Current and arrive to Antarctica (King
George Island) from Subantarctic and cold-temperate source populations (Fraser
et al. 2017; Fraser et al. 2018). In addition, the establishment of alien species in
Antarctic marine rocky communities could well be facilitated by the current sce-
nario of increasing water temperature and decreasing ice cover (Blunden et al. 2013;
Clark et al. 2013; Quartino et al. 2013; McCarthy et al. 2019). These alterations
represent the weakening of dispersal limitations and also of abiotic filtering that
would benefit aliens over Antarctic natives (Duffy et al. 2017; Griffiths et al. 2017;
see also Chap. 3 by Fraser et al. and Chap. 4 by Macaya et al.).
In addition to dispersal and abiotic environmental filtering, local community
assembly also depends upon chance (particularly when population numbers are
low) and biotic filters that restrict the establishment of some taxa (HilleRisLambers
13 Seaweed-Herbivore Interactions: Grazing as Biotic Filtering in Intertidal Antarctic… 267
et al. 2012; Briski et al. 2018). As such, both factors are relevant during the
establishment of aliens. Once settlers have passed through the abiotic filtering (e.g.
environmental extremes in Antarctica), negative biotic interactions, such as compe-
tition, predation and herbivory, encompass local biotic filters that finally determine
the success of settled organisms (e.g. Guisan and Thuiller 2005; HilleRisLambers
et al. 2012; King and Howeth 2019). Although invasion theory predicts that general-
ist enemies (e.g. herbivores) have stronger impacts on native than alien competitors,
the analysis of local adaptation of consumers to native resources provides limited
evidence that generalist enemies are better adapted to attacking natives than exotics
(Keane and Crawley 2002). In addition, there are several examples of marine
Antarctic macroalgae that have developed chemical defences to local herbivores
(e.g. Amsler et al. 2005, 2009b; Aumack et al. 2010), which may allow them to have
fitness advantages over alien macroalgae (see Chap. 17 by Amsler et al.). Thus,
negative biotic interactions in Antarctic coastal marine communities can have an
important role as local filters mediating the process of invasion in these ecosystems.
13.2 R
ecent Introductions of Exotic Macroalgae
in Antarctica
Examples of alien macroalgae in Antarctica include green algae such as the gutweed
Ulva intestinalis, which was described as Enteromorpha intestinalis together with
the brown alga Petalonia fascia and the red alga Rhodymenia subantarctica in South
Shetland Islands (Clayton et al. 1997; see also Frenot et al. 2005; Campana et al.
2009). In addition, other green macroalgae have been suggested to be recent intro-
ductions to South Shetland Island shores, namely, the filamentous algae Urospora
penicilliformis and Ulothrix sp. (Gómez 2015). Considering the growing human
activity and ship traffic to South Shetland Islands (Frenot et al. 2005; Bender et al.
2016), the occurrence of exotic and potentially invasive species in these locations is
not surprising. Recent multivariate analyses suggest, moreover, a trend of biotic
homogenisation among seaweed assemblages of South Patagonia and both West
and East Antarctic Peninsula (Sanches et al. 2016). In this line, but not necessarily
related to recent biological invasions, a small subset of widely distributed macroal-
gae dominate the biogeographic structure of intertidal rocky shores in the Southern
Ocean, likely as a result of rafting across in the Antarctic Circumpolar Current
(Griffiths and Waller 2016; see also Pellizzari et al. 2017). Although the recent
increases of Antarctic seaweed diversity could well be the result of improved and
more efficient techniques of sampling and molecular taxonomical methods (e.g.
Dubrasquet et al. 2018), the role of human-mediated transport and climate change
in modifying the biogeography of macroalgae in the Southern Ocean should not be
ruled out (Pellizzari et al. 2017; McCarthy et al. 2019; see Chap. 5 by Pellizzari
et al.).
268 N. Valdivia
13.3 Can Grazers Control Alien Macroalgae in Antarctica?
Worldwide, marine herbivores have profound and chiefly negative effects on the
abundance of primary producers—in particular, these effects are strongest in rocky
intertidal habitats (Lubchenco 1978; Hawkins and Hartnoll 1983; Poore et al. 2012).
In this line, manipulative and observational studies suggest that grazers can exert a
significant effect on the structure of algal communities in Antarctica. For example,
field-based manipulative experiments show a strong control of intertidal grazers,
namely, the limpet Nacella concinna (Fig. 13.1), on intertidal periphyton assem-
blages in Fildes Bay, King George Island (Segovia-Rivera and Valdivia 2016). An
important outcome of this work is that the overall negative effects of N. concinna on
the abundance of periphyton taxa were consistent across intertidal microhabitats
(i.e. emergent rocks and tidepools). Similarly, Zacher et al. (2007b) demonstrate
that N. concinna’s effects on early-succession algal communities are consistent
across multiple levels of ultraviolet radiation (UVR) exposure. Moreover, the mag-
nitude and sign of the effects of this grazer on benthic periphyton in King George
Island can be similar to those of congeneric limpets in Chilean South Patagonia
(CSP), albeit channelled through different ecological mechanisms—while the
effects of Antarctic limpets appear to be frequency-dependent, the effects of
Magellan limpets seem to be related to niche complementarity in a rich community
of grazers (Aldea and Rosenfeld 2011; Valdivia et al. 2019). Generally speaking,
these results may indicate that the effects of N. concinna on algal abundance and
diversity may be consistent across abiotic environmental conditions related to emer-
sion time, desiccation, and photobiotic and osmotic stress. This conclusion is well
in line with a major meta-analysis that shows only a little influence of environmen-
tal conditions (i.e. latitude or mean annual water temperature) on the effects of graz-
ers on the abundance of primary producers (Poore et al. 2012).
Mesograzers, on the other hand, have also been suggested as strong top-down
controllers of Antarctic seaweed communities. Field experiments demonstrate that
Fig. 13.1 Aggregations of

individuals of Nacella
concinna in Antarctic
rocky tidepools. (Photo by
Nelson Valdivia, Proyecto
Anillo ART1101)
the abundant amphipod fauna rapidly consumes intertidal filamentous algae trans-
planted to the subtidal in West Antarctic Peninsula (WAP; Amsler et al. 2012). The
remarkable abundance of amphipods (e.g. up to 20 ind/g algal wet weight; Huang
et al. 2007) suggests that amphipod assemblages do have a significant population-
level control on benthic algal communities. Indeed, amphipods and subtidal mac-
roalgae have developed mutualist interactions in which the former benefit from
predator-sheltered habitats and the latter from reduced fouling (Amsler et al. 2014).
In this line, amphipods and other mesograzers are proposed to control the occur-
rence of filamentous macroalgae, which can explain the absence of these species in
Antarctic subtidal habitats (Peters 2003; Amsler et al. 2009a). Albeit less abundant
than amphipods, small-sized Antarctic gastropods can also play an important role as
top-down controls of epiphytic microalgae on large pseudo-kelps, as shown in
mesocosm experiments (Amsler et al. 2015, 2019). Thus, it is highly likely that
mesograzers, through their consumptive activities, can be relevant for the assembly
of local macrobenthic communities in WAP (see Chap. 17 by Amsler et al.).
The results of the experiments described above are supported by early and recent
observational evidence. Kim (2001), for example, found a strong association
between the seasonal variation in the abundance of N. concinna and that of intertidal
filamentous algae in King George Island—although the role of ice scouring in medi-
ating this association cannot be ruled out. In addition, the analysis of stomach con-
tents and stable isotopes strongly supports the idea that amphipods are central in
WAP coastal food webs (Aumack et al. 2017; Zenteno et al. 2019). On the other
hand, observational evidence shows that notothenioid fish, like Notothenia rossi and
N. coriiceps, actively select for macroalgae as food (Casaux et al. 1990; Barrera-
Oro et al. 2019). Despite correlation does not imply causality, the results of these
observational studies agree with field- and lab-based manipulative evidence of the
central role of herbivores in coastal Antarctic food webs.
Could these grazers prevent the establishment, or at least control the abundance,
of exotic seaweeds? As introduced above, theory predicts that parasites and general-
ist predators and herbivores (i.e. ‘enemies’) can have stronger impacts on native
than alien competitors, allowing the latter to expand their spatial distribution and
adopt an invasive behaviour (i.e. the Enemy Release Hypothesis, reviewed in Keane
and Crawley 2002). In addition, the current trend of seawater warming would also
reduce the physiological constrains imposed by Antarctic environmental extremes
to temperate seaweeds. This may picture a scenario of improving biotic and abiotic
environmental conditions for the establishment and spread of invasive seaweeds in
Antarctica. Yet, sophisticated anti-herbivory defences have evolved in several
Antarctic seaweeds (Amsler et al. 1998, 2009b, 2019; Aumack et al. 2010), and
today it is proposed that small-sized herbivores have actually positive effects on
macroalgae owing their antifouling consumptive activity (Amsler et al. 2014, 2019).
This could provide native seaweeds with consumer-mediated competitive advan-
tages over exotic seaweeds, provided that the latter are not equipped with anti-
herbivory defences. Indeed, grazing has been shown to mediate the competitive
interaction between native and alien seaweeds elsewhere (Noè et al. 2018). For
270 N. Valdivia
Antarctic communities, however, further empirical research is needed to assess the

role of consumers on competitive seaweed interactions.
How can climate change influence the potential effects of grazers on an invasion
process in Antarctica? The answer to this question seems to depend on the species
or functional type analysed. For instance, Antarctic grazing gastropods, including
N. concinna and Margarella antarctica, have been shown to resist the combined
effects of decreased pH and seawater warming (Schram et al. 2014), hinting for
certain level of resistance of the grazing function to this stressor. However, the
authors warn that the slow growth rates and longevity of the analysed gastropods
could mask long-term sublethal effects of warming and acidification. On the other
hand, ocean acidification can significantly increase the mortality rates of amphi-
pods, while warming can have sublethal effects in terms of increased whole-body
protein content of those organisms (Schram et al. 2016). Acute warming, moreover,
is shown to modify the feeding preferences of amphipods (Schram et al. 2015). As
changes in consumer abundances and prey shift have been proposed as major causes
of food web variations (e.g. Lopez et al. 2017), ocean acidification and warming can
have profound indirect effects on the structure of coastal Antarctic communities. In
addition, recent evidence hints for indirect effects of climate change on grazer popu-
lations, as seawater warming and freshening can have significant and independent
effects on consumption rates of predatory fish (Navarro et al. 2019). Sedimentation,
which relates to warming-associated glacier melting, has been shown to mediate the
effects of grazers on the germination and development of young sporophytes of
Arctic kelps (Zacher et al. 2016). Finally, ocean warming and increased pCO2 could
mediate macroalgal competitive interactions, as it is demonstrated that both factors
in combination favour fleshy over crustose forms (Schoenrock et al. 2016). In this
way, the role of grazing and competition as biotic filtering in the assembly of local
Antarctic communities should be assessed in combination to climate change
stressors.
13.4 U
lva intestinalis as a Case Study in a Simple,
Two-Species Assembly Model
The gutweed Ulva intestinalis was described inhabiting Antarctic shores in 1997
(Clayton et al. 1997). Elsewhere, this species is able to generate adverse abiotic
conditions for potential competitors in tidepools, which involve conditions of high
pH and low inorganic carbon concentrations—at the same time, U. intestinalis is
able to capture HCO3− under these conditions (Larsson et al. 1997). This ability is
suggested to provide U. intestinalis with competitive advantages over other mac-
roalgae in high-intertidal tidepools, explaining the dominance of this species
observed in Swedish Atlantic tidepools (Björk et al. 2004, 2005). In Antarctica,
however, U. intestinalis is not a dominant species like in Sweden, and its spatial
distribution is usually confined to high-intertidal tidepools (Clayton et al. 1997;
Gómez 2015). A first explanation for the restricted distribution of U. intestinalis

would be the climatic environmental conditions that prevail in WAP, particularly
average seawater temperatures that are below its optimum for somatic growth
(Bischoff and Wiencke 1993). According to the high consumption rates demon-
strated for Antarctic intertidal benthic grazers, including abundant populations of
amphipods (Huang et al. 2006) and the limpet N. concinna (e.g. Zacher et al. 2007a;
Segovia-Rivera and Valdivia 2016), a possible, non-exclusive explanation could be
that grazer activity defines the lower intertidal limit of this species. Intertidal herbi-
vores have been shown to control the abundance of fast-growing macroalgae in
tidepools of WAP (Segovia-Rivera and Valdivia 2016) and elsewhere (e.g. Noël
et al. 2009).
To improve our understanding of an invasion process in Antarctica, I used
U. intestinalis introduction into high-intertidal tidepools as a model system. The
scenario, therefore, includes two sites connected by dispersal (WAP and Chilean
South Patagonia, CSP), tidepools as local habitats, U. intestinalis as a competitively
superior alien (see previous paragraph) and the corticated red seaweed Iridaea cor-
data as a native competitor that is frequent in tidepools (Valdivia et al. 2014); for
simplicity, both species will be referred to as Ulva and Iridaea, respectively. To this
aim, I used a simple probabilistic model known as Moran model, which was origi-
nally generated to understand the temporal changes in allele frequencies in popula-
tions (Moran 1958). This model has been lately used and extended to simulate the
temporal dynamics of two-species communities (Hubbell 2001; Vellend 2016). The
basic structure of the model assumes a neutral, closed assemblage without specia-
tion, in which there are J individuals that belong to one of two species, either spe-
cies A or species B (either Ulva or Iridaea in this case). Since J is assumed to be
fixed (i.e. a zero-sum dynamic), there are j individuals of species A and J – j indi-
viduals of B. At each time, one individual of the community is selected at random to
die. At the next time, an individual is selected at random to produce one offspring
that replaces the dead individual. Each individual is chosen to be A or B with
probabilities
p j = jJ −1 , and

q j = ( J − j ) J −1 ,

for species A and B, respectively (Moran 1958). The community is then described
as a Markov chain in which the state (community structure at a given time) is defined
by the abundance of species (j) and a transition probabilities pjk from state j to k:
J 
p jk =   p kj q Jj − k .
k
In this work, and as previously done by Hubbell (2001) and Vellend (2016), I took
advantage of the simplicity of the Moran model to describe how differences in
272 N. Valdivia
c ompetitive abilities, reflected in differences between probabilities pj and qj, can

lead to differing community patterns. These differences were expressed as average
fitness ratios, in which larger ratios will indicate that species A (Ulva) generates a
larger offspring than species B (Iridaea); i.e. the former is competitively superior
than the latter (Vellend 2016). In addition, the simulations of this work were done in
a metacommunity context, in which the reproducing individual of the Moran model
was chosen at random from the entire set of habitat patches.
The rationale of these simulations was to resemble an invasion process in which
Ulva (species A) is an invasive and competitively superior species that already colo-
nised high-intertidal tidepools in the WAP from the nearest continental shore, i.e.
CSP. Iridaea, on the other hand, represents a native competitor in tidepools. The
simulations, thus, considered a simple metacommunity of two local sites that are
linked by dispersal (m in Fig. 13.2). Previous unpublished data was used to estimate
the initial abundances (in terms of frequency) of Ulva. Thus, the simulation included
empirical data only to set the initial abundances of Ulva. In addition, I assumed that
Ulva would be competitively dominant in high-intertidal tidepools in WAP but not
in CSP, because of the lower seaweed diversity observed in Antarctica that would
provide more niche opportunities to alien species. These differences were expressed
as fitness ratios >1 (1.3) in WAP and <1 (1/1.1) in CSP.
A central aspect of these simulations is the incorporation of negative density (or
frequency) dependence of competitive advantages as the result of grazing on the
abundance and fitness of competitors. If fitness ratio always is >1, that is, if species
A has consistently greater fitness than species B, then the former species will tend to
competitively exclude the latter, and no stable coexistence will take place (Chesson
2000; Letten et al. 2017). However, if the fitness advantages of species A over spe-
cies B are greater when species A is rare, and vice versa, then each species will have
relative advantage when rare, and there should be a stable coexistence (equilibrium)
point (Chesson 2000). This negative frequency dependence of growth rates can be
generated by, for instance, negative effects of consumers (predators and prey) that
become harsher with increasing prey abundances (i.e. enemy-mediated coexistence;
Holt et al. 1994). Therefore, the simulations in this work were done across a range
of strengths of negative frequency dependence (b in Fig. 13.2) to resemble potential
effects of grazers on the abundance of macroalgal competitors in Antarctic high-
intertidal tidepools. These values were set to 0, −0.1, and −0.5, representing absence
and intermediate and high negative density dependence. All simulations were con-
ducted in R programming environment (R Core Team 2019).
The simulations showed that the complete absence of dispersal in the metacom-
munity resulted in extinction in both regions, even at intermediate levels of negative
frequency dependence (Fig. 13.2a,b). Stronger negative density dependence would
allow for coexistence at low abundances of Ulva only in CPS (segmented line in
Fig. 13.2c). Interestingly, dominance, but not competitive exclusion, in Antarctica
would be apparent even in the absence of significant negative frequency dependence
(i.e. grazing) and when dispersal is intermediate (Fig. 13.2d). As expected, high
levels of dispersal would lead to biotic homogenisation of the region (Fig. 13.2g–i).
Intermediate dispersal and increasing negative density dependence led to reduced
(A) m = 0, b = 0 (B) m = 0, b = −0.1 (C) m = 0, b = −0.5

1.0 1.0 1.0
Frequency of species A
0.8 0.8 0.8
0.6 0.6 0.6
0.4 0.4 0.4
0.2 0.2 0.2
0.0 0.0 0.0
0 200 400 600 800 0 200 400 600 800 0 200 400 600 800
Time Time Time
(D) m = 0.1, b = 0 (E) m = 0.1, b = −0.1 (F) m = 0.1, b = −0.5

1.0 1.0 1.0
0.8 0.8 0.8
0.6 0.6 0.6
0.4 0.4 0.4
0.2 0.2 0.2
0.0 0.0 0.0
0 200 400 600 800 0 200 400 600 800 0 20 40 60 80 100
Time Time Time
(G) m = 0.5, b = 0 (H) m = 0.5, b = −0.1 (I) m = 0.5, b = −0.5

1.0 1.0 1.0
0.8 0.8 0.8

0.6 0.6 0.6
0.4 0.4 0.4
0.2 0.2 0.2
0.0 0.0 0.0
0 200 400 600 800 0 200 400 600 800 0 20 40 60 80 100
Time Time Time
Fig. 13.2 Simulations of two-species communities in two sites connected by dispersal. The lines
represent the frequency of one of the species (species A) in each site. The solid and segmented lines
represent WAP and CSP, respectively. Since the number of individuals in each site is fixed (J), then
the frequency of species B is equal to 1 – freq. species A. The parameters m and b represent the
dispersal parameter and negative frequency dependency, respectively. Competitive exclusion is
evident when species A reaches a frequency of 1 or 0. It was assumed that Ulva is competitively
dominant in high-intertidal tidepools in WAP but not in CSP, which was expressed as fitness ratios
>1 (1.3) and <1 (1/1.1), respectively. The b parameter resembles the effects of grazers on the fre-
quency of competitors and was set to 0, −0.1, and −0.5, representing absence and intermediate and
high negative density dependence
dominance (Fig. 13.2d–f). Competitive exclusion by Ulva was expected under the

scenario of high dispersal and no or intermediate negative density dependence
(Fig. 13.2g, h). An important outcome of the simulation is that stable coexistence
can be reached when both dispersal between CPS and WAP and negative frequency
dependence are high (Fig. 13.2i). This could be caused by, on the one hand, ‘rescue
effect’ of immigrants in both sites (e.g. Altermatt et al. 2011) and, on the other hand,
by the controlling effect of consumers on the numerically dominant competitor.
274 N. Valdivia
Benthic Antarctic grazers appear to have strong and deterministic effects on algal
communities across local environmental conditions, which can encompass a firm
biotic filter during the establishment stage of an alien seaweed. In addition, the evo-
lution of chemical anti-herbivory defences in Antarctic seaweed may provide them
with enemy-mediated competitive advantages over alien species. However, pro-
jected environmental conditions of warming and acidification can impair the ability
of amphipod grazers to control potential introductions in these ecosystems. The
results of a simple mathematical simulation, based on the introduction history of the
gutweed Ulva intestinalis, predict that intermediate to high levels of frequency-
dependent consumption seem to be fundamental to allow for stable coexistence
when the alien species is competitively superior. This brief literature review and
simulations provide a benchmark to develop an experimental research agenda in the
WAP, in which competitive interactions between alien and native seaweeds could be
assessed as functions of consumption and abiotic climate change-related factors.
With this review, I hope to stimulate further empirical research on seaweed invasion
processes in Antarctica.
Acknowledgements NV was financially supported by FONDAP 15150003 (IDEAL) and

FONDECYT 1190529 grants. Discussions with Viviana Segovia, Eliseo Fica, and Luis Miguel
Pardo contributed insightful ideas to the review. Gabriela Campana and Katharina Zacher provided
constructive criticism that greatly improved an early version of this manuscript.
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Chapter 14
Diversity and Functioning of Antarctic
Seaweed Microbiomes
Juan Diego Gaitan-Espitia and Matthias Schmid
Abstract Antarctic macroalgae are important primary producers and habitat-

forming species that play fundamental roles in Antarctic coastal habitats and sustain
important communities of benthic organisms, including a not well-known microbi-
ota. Anthropogenic pressures, e.g., increasing ocean temperatures and extreme
events, have threatened the ecological integrity of several seaweed species and also
can modify the range shifts (e.g., introduction of Durvillaea antarctica in King
George Island), cause local extinctions, and alter the structure of these associations
in their natural habitats. However, understanding and prediction of the responses of
seaweeds to changing environment and rapid anthropogenic-driven change cannot
be done without considering the associated microbiome. These complex microbial
communities are intricately involved in the host health, defense, growth, and devel-
opment of seaweeds, thus with far-reaching implications for the ecology of the
whole coastal ecosystem. For most Antarctic seaweeds, the microbiome comprises
a stable core as well as microbes whose presence depends on local conditions and
transient microbial associates that are responsive to biotic and abiotic processes
across spatial and temporal scales. In this chapter, we will explore the ecological
and genetic diversity of microbiomes in Antarctic seaweeds and their functional
connections.
Keywords Bacteria · Microbial communities · Genetic diversity · Holobionts ·

Microbiota
J. D. Gaitan-Espitia (*)
The Swire Institute of Marine Science and The School of Biological Sciences, The University
of Hong Kong, Hong Kong, SAR, China
e-mail: jdgaitan@hku.hk
M. Schmid
Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, TAS, Australia
e-mail: matthias.schmid@utas.edu.au

https://doi.org/10.1007/978-3-030-39448-6_14
280 J. D. Gaitan-Espitia and M. Schmid
14.1 I ntroduction: Environment and Antarctic Seaweed

Host-Microbiome
From very abundant and complex microbial communities to larger eukaryotes such
as seaweeds and marine mammals, Antarctic organisms have evolve a variety of
physiological, life history, and molecular adaptations that allow them to cope with
this challenging environment (Hoyer et al. 2002; Clark et al. 2004; Marx et al. 2007;
Rogers 2007). In Antarctic waters, the marine benthic flora is expected to be highly
susceptible to global changes (i.e., invasive species, ocean warming, ocean acidifi-
cation) due to its high degree of niche conservatism, reduced phenotypic plasticity,
and the low species richness (Clayton 1994; see also Chap. 11 by Gómez and
Huovinen). In order to survive in this harsh environment, Antarctic seaweeds have
evolved structural and functional adaptations such as high synthesis of photoprotec-
tive substances and antioxidant activity for mitigation of photodamage, molecular
adaptations of enzymes in order to maintain sufficient rates of enzyme-catalyzed
reactions of key metabolic processes, the evolution of cold shock and antifreeze
proteins, and different effective strategies for inorganic C acquisition and assimila-
tion (Morgan-Kiss et al. 2006; Karsten et al. 2009; Gómez et al. 2009, 2019;
Huovinen and Gómez 2013; Hurd et al. 2014). While there has been a lot of interest
in documenting and understanding these functional adaptations, only scattered
information is available about other potential adaptive mechanisms that influence
functional regulation of Antarctic seaweeds. In fact, we know that seaweeds are not
independent biological units. They rely on tight relationships with their associated
microbiota for basic functions such as morphological development, growth, health,
defense, nutrient supply, and adaptation/acclimation to environmental stress (Egan
et al. 2013; Wichard 2015; Dittami et al. 2016; Singh and Reddy 2016). This sug-
gests that seaweeds and their microbiome interact as a unified functional entity or
holobiont (Egan et al. 2013). Therefore, it is essential to gain better understanding
of the adaptive role of seaweed host-microbiome interactions in changing/extreme
oceans and the mechanisms underlying their eco-evolutionary dynamics in
Antarctica.
The complex microbial communities (mutualistic symbionts and hazardous
pathogens) are intricately involved in health, defense, growth, and development of
seaweeds (Friedrich 2012; Egan et al. 2013; Martin et al. 2014; Egan and Gardiner
2016; Singh and Reddy 2016). For most eukaryotic hosts, the microbiome com-
prises a stable core as well as microbes whose presence depends on local conditions
and transient microbial associates that are responsive to biotic and abiotic processes
across spatial and temporal scales (Vandenkoornhuyse et al. 2015; Hernandez-
Agreda et al. 2016). Nevertheless, for seaweeds, the notion of host-specific micro-
bial taxa in the core microbiome is not a rule of thumb: some species have specific
microbial functional genes rather than taxonomic affiliations of microbial popula-
tions (Burke et al. 2011a, b). On the contrary, in other seaweeds, microbial taxo-
nomic diversity can be unique to each type of seaweed host but with high degree of
functional redundancy (Roth-Schulze et al. 2016). Whether or not these patterns
14 Diversity and Functioning of Antarctic Seaweed Microbiomes 281
(i.e., host-specific vs variable microbial diversity, functional redundancy) apply

more broadly to species from other seaweed phyla in extreme polar regions, and
considering temporal and spatial scales, is unknown.
14.2 F
unctional Interactions of Antarctic Seaweeds
and Their Associated Microbiota
The seaweed microbiome represents a remarkably diverse array of microorganisms

that includes bacteria, archaea, fungi, and other eukaryotic unicellular organisms
and even viruses (Singh and Reddy 2016). Evidence suggests that the composition
of the seaweed microbiome is likely to be modulated, at least in part, by the host
because it is significantly different to the microbial community that is found in the
surrounding environment (Brodie et al. 2016). These microorganisms exhibit strong
seasonal and spatial changes in diversity and abundance (Tujula et al. 2010; Lachnit
et al. 2011; Campbell et al. 2015) that are also influenced by day length, nutrient
availability, and temperature (Gilbert et al. 2012; Moran 2015). Seaweeds can con-
trol and maintain communication with their associated microbes by producing sec-
ondary metabolites and exudates such as sugars and amino acids that serve as an
energy source, as well as for a variety of functions including antimicrobials, allo-
pathic molecules, and pathogen defenses (Friedrich 2012; Egan et al. 2013; Hollants
et al. 2013; Rout 2014). The seaweed microbiome, in turn, can exert influence on
trait expression by controlling growth and morphogenesis (Wichard 2015), acclima-
tion and physiological responses of the host to environmental gradients (Dittami
et al. 2016), survival and settlement of propagules (Morris et al. 2016), competition
among seaweeds by inhibiting the germination of algal spores (Egan et al. 2001),
and rapid defense adaptation (chemical controls) to the new bacterial epibionts and
pathogens during range shifts (Saha et al. 2016; Arnaud-Haond et al. 2017). All of
these effects influenced by associated microbial communities have important impli-
cations in the ecosystem services provided by the seaweed host (Rout 2014).
Although bacteria are by far the most abundant members of the seaweed microbi-
ome, our knowledge about epiphytic and endophytic bacterial communities living
in Antarctic seaweeds is quite limited. Very few studies have explored this compo-
nent of the seaweed microbiome. To date, a broad diversity of pigmented, Gram-
positive epiphytic bacteria has been reported (mainly affiliated to Actinobacteria)
(Leiva et al. 2015), some of them with antibiotic activity that may influence micro-
bial dynamics (i.e., competition and colonization) of bacterial epibionts (Alvarado
et al. 2018). On the contrary, other components of the seaweed microbiome such as
fungi are very well documented. This group is characterized by the presence of
symbiont, saprobe, and parasitic species that form fungal assemblages on the sea-
weed host. The structure and dynamics of these assemblages are controlled by envi-
ronmental factors (e.g., availability of dissolved oxygen and organic matter), the
seaweed host, and the capacity of the fungi to tolerate or detoxify the array of
antifungal metabolites produced by the seaweed (Ogaki et al. 2019). The typical
fungal community structure in Antarctic seaweeds is based on filamentous fungi
and yeasts belonging to the genera Geomyces, Antarctomyces, Oidiodendron,
Penicillium, Phaeosphaeria, Aureobasidium, Cryptococcus, Leucosporidium,
Metschnikowia, and Rhodotorula (Loque et al. 2010). These assemblages are domi-
nated by very few species (e.g., the filamentous fungus Pseudogymnoascus panno-
rum and the yeast Metschnikowia australis) (Loque et al. 2010; Godinho et al. 2013;
Furbino et al. 2014; Ogaki et al. 2019), some of which have the potential to degrade
algal biomass through agarolytic and carrageenolytic activities (Furbino et al. 2017).
14.3 D
eciphering the Structure and Diversity
of Seaweed Microbiomes
Pioneering studies of microbial communities in Antarctic marine environments

employed cultivation-based methods, which are based on techniques aiming to
grow microorganisms under controlled laboratory conditions (Pham and Kim 2012).
This approach has several limitations as it only provides a reduced representation of
the microbial community diversity because most of the species in environmental
samples do not grow on standard media under laboratory conditions (Stewart 2012).
However, in the last few years, a major progress in microbial research has been
achieved, thanks to the development of several culture-independent molecular tech-
niques (e.g., polymerase chain reaction (PCR), hybridization, fingerprinting, Sanger
sequencing). These approaches have been routinely applied to study microbial com-
munities in Antarctic soils, water, ice, and biota (Loque et al. 2010; Godinho et al.
2013; Furbino et al. 2014; Leiva et al. 2015; Moreno-Pino et al. 2016; Alvarado
et al. 2018; Castro-Sowinski 2019; Chua et al. 2018; Ogaki et al. 2019). From these,
the most powerful molecular approach to assess the structure and diversity of micro-
bial communities relies in the use of high-throughput sequencing (HTS) of house-
keeping genetic markers (amplicon sequencing) such as the internal transcribed
spacer region (ITS; fungi), the 18S gene (fungi and other eukaryotes), viral RNA
(viruses), and the 16 ribosomal RNA gene (16S rRNA; bacteria and archaea;
Fig. 14.1). The main drawback of microbial community profiling using these uni-
versal markers is that they cannot directly identify metabolic or other functional
capabilities of the microorganisms under study (Janda and Abbott 2007; Rausch
et al. 2019). This can be done using shotgun metagenomic sequencing (Fig. 14.1).
However, amplicon sequencing still offers many other advantages such as cost-
efficiency, high precision, and fast speed characterization of taxonomic composition
and phylogenetic diversity of microbial communities (Langille et al. 2013; Rausch
et al. 2019). Although amplicon/targeted sequencing and shotgun sequencing strate-
gies differ in the type of information produced, phylogeny and biomolecular func-
tion are strongly correlated. For instance, phylogenetic trees based on 16S rRNA
closely resemble clusters obtained based on shared gene content, and researchers
Shotgun sequencing
Community DNA Bacteria genomes
Primers
Variable regions Constant regions

27F 357F 928F
V1 V2 V3 V4 V5 V6 V7 V8 V9
Targeted sequencing
518R 805R 926R 1492R
V1-V3
V3-V4
V3-V5
V6-V9
Fig. 14.1 Schematic representation of the workflow for bacterial community assessment. First,
epiphytes are collected from the seaweed host for posterior total DNA extraction. The DNA from
the microbiome is then used for targeted, amplicon sequencing (16S; down arrow) and/or shotgun
metagenome sequencing (right arrow). For the targeted approach, different combinations (red
lines) of variable (white boxes) and conserved (cyan boxes) 16S regions are sequenced via PCR
with traditional primers (blue, green, and pink arrows). For the shotgun sequencing approach,
DNA is fragmented and then sequenced using Illumina platforms, and the reads are finally sorted
and assembled into contigs and into circular genomes
often infer properties of uncultured organisms from cultured relatives (Langille

et al. 2013). Here, we will focus on targeted sequencing of bacterial 16S ribosomal
RNA gene (Fig. 14.1), as this approach has been frequently used to characterize
dynamics of microbial communities in Antarctic marine areas. Molecular approaches
used for characterizing other groups, such as fungi, are well described in Ogaki
et al. (2019).
The 16S rRNA gene is the most popular target gene in many molecular methods
(e.g., fluorescence in situ hybridization, FISH; quantitative PCR; terminal restric-
tion fragment length polymorphism, T-RFLP; denaturing-gradient gel electrophore-
sis, DGGE) of microbial studies (Bukin et al. 2019; Fuks et al. 2018; Janda and
Abbott 2007; Sambo et al. 2018). This gene offers several advantages for the study
of bacterial phylogeny and taxonomy. Such advantages are as follows:
(i) 16S rRNA is present in all prokaryotes.
(ii) Its function over time has not changed, suggesting that random sequence
changes are a more accurate measure of time (evolution).
(iii) It is approximately 1600 base pairs long and includes nine hypervariable, fast-
evolving regions (V1–V9; Fig. 14.1), which can be used to classify organisms
at different taxonomic levels (genus or species).
(iv) The conserved, slow-evolving regions of this gene, which can be used for
determining higher-ranking taxa (Janda and Abbott 2007; Bukin et al. 2019).
These conserved regions have structural characteristics that allow to design broad-
spectrum, degenerated primers for polymerase chain reaction (PCR) amplification,
which in turn can be used to isolate species-specific fast-evolving regions (Fig. 14.1)
(Sambo et al. 2018). The accuracy of 16S rRNA gene sequencing as a tool in micro-
bial identification (taxonomic assignment and phylogenetic placement) depends, in
a great extent, on the selection of the 16S region (Pootakham et al. 2017; Fuks et al.
2018; Sambo et al. 2018; Bukin et al. 2019). Nowadays, the majority of microbial
profiling studies utilizes the short-read V3–V4, V4–V5, or V5–V6 amplicons
instead of the full-length 16S rRNA sequences in environmental community sur-
veys (Pootakham et al. 2017). The advance in throughput has, however, come at the
cost of read length, and this trade-off has inevitably resulted in less accurate classi-
fication of partial 16S sequences, especially at the genus or species level (Bukin
et al. 2019; Pootakham et al. 2017). For seaweeds, there is currently no consensus
on the most appropriate hypervariable region(s) for profiling associated microbial
communities. Some of the studies using amplicon sequencing have targeted the 16S
hypervariable regions V1–V3 (Campbell et al. 2015), whereas others have used the
V3 (Lachnit et al. 2009), V4 (Lemay et al. 2018; Marzinelli et al. 2015), V3–V4
(Martin et al. 2015; Parrot et al. 2019), V6 (Brodie et al. 2016), or the full-length
16S (Leiva et al. 2015; Kumar et al. 2016; Alvarado et al. 2018; Serebryakova et al.
2018; Morrissey et al. 2019). Overall, and considering the percentage of sequences
that retrieve hits from public databases (e.g., Greengenes, NCBI, RDP, and SILVA),
it seems that hypervariable regions targeting V3–V4 (90%), V4 (91%), V4–V5
(88%), and V1–V9 (full-length; >99%) produce more reproducible results than V1–
V2 (30%) or V1–V3 (40%). These findings have been also documented in microbial
communities associated to other environmental and biological systems (Pootakham
et al. 2017; Almeida et al. 2018; Pollock et al. 2018).
14.4 V
ariation of Bacterial Community Diversity
in Antarctic Seaweeds
In Antarctica, the diversity of marine prokaryotic (bacteria) communities in seawa-

ter correlates to both physical (Wilkins et al. 2013) and chemical oceanographic
conditions (Giudice and Azzaro 2019). These factors can be highly variable in space
and time, shaping life in this polar region. As a result, prokaryotes have evolved a
wide range of pro-survival mechanisms such as habitat selection, life cycle strate-
gies, changes in cellular composition and enzyme activity, and the production of
extracellular polymeric substances (De Maayer et al. 2014). These adaptations
might provide some functional benefits for the seaweed hosts. However, microbial
communities in seawater and sediments can differ in diversity and structure (as well
as in their functional properties) from those associated to seaweeds (Egan et al.
2013). In coastal and marine sediments along the west part of the Antarctic Peninsula
and Antarctic islands, the predominant bacteria include representatives of the phyla
Proteobacteria, Actinobacteria, Chloroflexi, Bacteroidetes, Verrucomicrobia, and
Firmicutes, followed by Acidobacteria and Cyanobacteria (Chua et al. 2018; Flocco
et al. 2019). In seawater, on the other hand, the dominant phyla are Proteobacteria
(mainly Alphaproteobacteria and Gammaproteobacteria) and Bacteroidetes (Gentile
et al. 2006; Moreno-Pino et al. 2016). Although there are some similarities at the
higher taxonomic level, major differences in bacterial community diversity can be
found between sediments and seawater at the at genus level. In sediments, for exam-
ple, the most predominant genera is Sphingomonas, while in seawater the more
abundant bacteria belong to the family Rhodobacteraceae and the genera
Psychromonas, Pseudoalteromonas, and Balneatrix (Gentile et al. 2006; Moreno-
Pino et al. 2016; Chua et al. 2018; Flocco et al. 2019; Giudice and Azzaro 2019; Lo
Giudice et al. 2019). This is also evidenced in bacterial communities associated to
Antarctic seaweeds (Fig. 14.2) (Leiva et al. 2015; Alvarado et al. 2018; Gaitan-
Espitia et al. unpublished). For instance, in a recent work, Gaitan-Espitia et al.
(unpublished data) used the full-length 16S rRNA gene and PacBio SMRT sequenc-
ing in order to assess the diversity of microbiomes associated to some of the most
abundant seaweeds in the north of the Antarctic Peninsula. This study included rep-
resentative of the phylum Ochrophyta (Adenocystis utricularis, Geminocarpus
geminatus, Ascoseira mirabilis, Desmarestia antarctica, D. menziesii,
a b
i
rgi
be
amsleri
tts
ko
Seawater Sediments
as
Palm
ta
Paraglossum
da
rtin
r
co
aria
ga
ea
Po
da
Gi
Iri
rp
dec
ta
dicula
hy
appen
ra
phora
ipie
Phyllo
en
di
ns
Ulv
vi
a in
ifo
tes
tina
liu
lis
m
Lin
nae
us
Brown Red
Monostroma hariotii Seaweeds Seaweeds
Antarc
tosac
cion a
pplan
atum
-proteobacteria
-proteobacteria
Hi
s m -proteobacteria
lari an
icu -proteobacteria
ilis
to
utr
us
th -proteobacteria
tis all
irab
Green
at
ys us Bacteroidetes
De
noc
in
Desmarestia
gr Seaweeds
de Cyanobacteria
m
ira m
sm
A an
ge
Actinobacteria
di
are
fo
us
Verrucomicrobia
liu
ose
rp
sti
s Firmicutes
ca
Chlorobacteria
am
Asc
o
in
Acidobacteria
em
en
antarctica
Other bacteria
zie
G
sii
Fig. 14.2 (a) Phylogenetic relationships of Antarctic seaweeds; and (b) taxonomic distribution of
their associated microbiomes at the phylum level (Gaitan-Espitia unpublished)
Himantothallus grandifolius, Antarctosaccion applanatum), Chlorophyta

(Monostroma hariotii, Ulva intestinalis Linnaeus), and Rhodophyta (Porphyra
endiviifolium, Paraglossum amsleri, Phyllophora appendiculata, Iridaea cordata,
Gigartina skottsbergii, Palmaria decipiens) (Fig. 14.2). These species are character-
ized by different evolutionary histories, physiological and genomic architectures,
and distribution along the vertical zonation of Antarctic shores (Klöser et al. 1996;
Wiencke et al. 2007; Valdivia et al. 2014; Pellizzari et al. 2017). Overall, the find-
ings indicate that microbial community composition (at the family and genera level)
differs among species of seaweeds despite shared distribution in the vertical zona-
tion (Fig. 14.2). This suggests that for Antarctic seaweeds, the composition of epi-
phytic bacteria is, at least in part, likely regulated by the host (Gaitan-Espitia et al.
unpublished).
Studies analyzing the epiphytic and endophytic bacterial communities of tem-
perate and tropical seaweeds have shown different phylogenetic patterns across eco-
logical (e.g., temporal, spatial) and evolutionary (e.g., host) scales (Burke et al.
2011b; Lachnit et al. 2011; Egan et al. 2013, 2017; Hollants et al. 2013; Campbell
et al. 2015; Marzinelli et al. 2015; Singh and Reddy 2016; Alvarado et al. 2018;
Serebryakova et al. 2018; Morrissey et al. 2019). This is consistent with findings
reported for Antarctic seaweed microbiomes (Alvarado et al. 2018; Leiva et al.
2015; Gaitan-Espitia et al. unpublished). However, in tropical and temperate sea-
weeds, Proteobacteria and Firmicutes are generally the most abundant bacteria
associated with seaweed hosts (Burke et al. 2011b; Lachnit et al. 2011; Egan et al.
2013, 2017; Hollants et al. 2013; Campbell et al. 2015; Marzinelli et al. 2015; Singh
and Reddy 2016; Serebryakova et al. 2018; Morrissey et al. 2019). In Antarctica, on
the other hand, members of phylum Actinobacteria are the most diverse and persis-
tent among different seaweed species, with a very low proportion of Firmicutes
(Leiva et al. 2015; Alvarado et al. 2018; Gaitan-Espitia et al. unpublished). The
predominance of Actinobacteria is probably related to their essential roles in eco-
logical functions such as degradation of organic matter and maintenance of environ-
mental stability (Castro-Sowinski 2019). Within Actinobacteria, the most dominant
members belong to the family Micrococcaceae followed by Microbacteriaceae,
Dermabacteriaceae, Sanguibacteriaceae, and Nocardiaceae (Leiva et al. 2015;
Gaitan-Espitia et al. unpublished). Some of the genera related to these families
(Amycolatopsis, Arthrobacter, Agrococcus, Brevibacterium, Kocuria, Leucobacter,
Leifsonia, Microbacterium, Micrococcus, Micromonospora, Nocardiopsis,
Pseudarthrobacter, Pseudonocardia, Salinibacterium, and Streptomyces) are
known to possess antimicrobial activity (Hollants et al. 2013; Leiva et al. 2015),
likely controlling bacteria colonization and competition in the seaweed host (Leiva
et al. 2015; Busetti et al. 2017; Alvarado et al. 2018). Additionally, the high propor-
tion of some Actinobacteria, such as the pigmented, Gram-positive epiphytic bacte-
ria (Leiva et al. 2015), may confer some direct benefits to the seaweed host. These
non-photosynthetic bacteria have high concentration of carotenoids that protect the
cells against solar radiation and freeze–thaw cycles (Dieser et al. 2010), as well as
against oxidative damage (Glaeser and Klug 2005). Therefore, the regulation of
biofilm formation of these epiphytic bacteria may represent an adaptive mechanism

to enhance tolerances and survival of Antarctic seaweeds.
14.5 Conclusions and Future Perspectives
Species diversity is widely recognized as an essential adaptive ecological property

that increases the robustness and evolvability of biological systems (Kahilainen
et al. 2014). This applies to the framework of the seaweed holobiont, because the
diversity of microorganisms that live and interact with the seaweed host is known to
play a fundamental role in its health and resilience, particularly when faced with
environmental stress (Friedrich 2012; Egan et al. 2013). Most studies exploring
seaweed microbiomes have determined the diversity (species and genes) of microbes
living in association with a seaweed host (mainly on surfaces = epiphytic communi-
ties) (Egan et al. 2001, 2013; Burke et al. 2011a, b; Friedrich 2012; Hollants et al.
2013; Rout 2014; Wichard 2015; Dittami et al. 2016; Morris et al. 2016; Saha et al.
2016; Arnaud-Haond et al. 2017). These studies reveal a seaweed microbiota that is
complex and very diverse and consists of a number of partners of different origins
and evolutionary trajectories (Friedrich 2012; Egan et al. 2013). However, diversity
without context provides limited insights into the mechanisms underpinning the
assembly of the microbiome, community patterns, and the benefits for the seaweed
host. High diversity is not necessarily “better” or “healthier,” whereas lower diver-
sity is not necessarily indicative of less stable or less “healthy” community (Shade
2016). In fact, microbial diversity can change across latitudinal–temporal scales
linked to biotic and abiotic factors rather than to the health or resilience of the host
(Gilbert et al. 2012; Koskella et al. 2017). Therefore, moving away from taxonomic
diversity toward functional diversity linked to the seaweed host phenotype and per-
formance under characterized environmental conditions could help us to understand
ecological drivers that shape the Antarctic seaweed microbiome and its functional
stability/plasticity in changing environments.
Acknowledgments The work outlined in this review was partially supported by the Chilean
Antarctic Institute (INACH), the Commonwealth Scientific and Industrial Research Organisation
(CSIRO), the University of Hong Kong, and the Institute for Marine and Antarctic Studies (IMAS)
from the University of Tasmania. JDGE was supported by the Research Grants Council of Hong
Kong via the Early Career Scheme (Project ECS-27124318). MS was funded through the Deutsche
Forschungsgemeinschaft (DFG, grant ID: SCHM 3335/1-1).
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Chapter 15
Seaweeds in the Antarctic Marine Coastal
Food Web
Fernando R. Momo, Georgina Cordone, Tomás I. Marina, Vanesa Salinas,

Gabriela L. Campana, Mariano A. Valli, Santiago R. Doyle,
and Leonardo A. Saravia
Abstract Antarctic macroalgae are the basis of marine food webs in most coastal
environments, especially the more confined ones such as bays and fjords. Whether
through direct consumption or via detritus, their role in maintaining biodiversity is
F. R. Momo (*)
Instituto de Ciencias, Universidad Nacional de General Sarmiento,
Departamento de Ciencias Básicas, Universidad Nacional de Luján (UNLu), Luján, Buenos
Aires, Argentina
G. Cordone
Centro Nacional Patagónico (CCT CONICET-CENPAT), Centro para el Estudio de Sistemas
Marinos (CESIMAR), Puerto Madryn, Chubut, Argentina
e-mail: gcordone@cenpat-conicet.gob.ar
T. I. Marina
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Centro Austral de
Investigaciones Científicas (CADIC), Ushuaia, Tierra del Fuego, Argentina
e-mail: tomasimarina@cadic-conicet.gob.ar
V. Salinas · L. A. Saravia
Instituto de Ciencias, Universidad Nacional de General Sarmiento,
e-mail: vsalinas@campus.ungs.edu.ar; lsaravia@campus.ungs.edu.ar
G. L. Campana
M. A. Valli
S. R. Doyle
Instituto de Ecología y Desarrollo Sustentable (INEDES), Universidad Nacional de Luján
(UNLu), Luján, Buenos Aires, Argentina
e-mail: sdoyle@campus.ungs.edu.ar

https://doi.org/10.1007/978-3-030-39448-6_15
294 F. R. Momo et al.
essential. However, their relevance is due not only by direct trophic interactions but
also by indirect feedbacks, since macroalgae act as a habitat and refuge for multiple
benthic organisms and as a substrate for epiphytic microalgae. Macroalgae also
establish relations of exploitative competition, apparent competition, and mutual-
ism. The control over the biomass and diversity of the macroalgae itself does not
seem to be due to trophic interactions (top-down control) but rather to competition
and diverse abiotic factors such as substrata and light availability or physical distur-
bances (ice scouring). The extreme connectivity of trophic networks linked to algae
and their detritus determines that food webs are robust to local extinctions; however,
non-trophic interactions indicate that changes that affect the growth, biomass, and
distribution of macroalgae can have dramatic effects on the diversity of their associ-
ated fauna and, indirectly, on the networks of consumers of that fauna. In this chap-
ter, we present a detailed description of macroalgae relationship networks and
analyze the stability of the Antarctic community using food web theory.
Keywords Biological interactions · Community structure · Ecological networks ·

Trophic level
15.1 Introduction
Macroalgae and their detritus or fragments are the basal energy source of Antarctic
coastal food webs. Approximately 150 species of macroalgae have been reported at
Antarctica (Wiencke et al. 2014; Pellizzari et al. 2017; see also Chap. 2 by Oliveira
et al.). Several local studies proved that macroalgae together with microphytoben-
thos constitute a direct pathway of energy and matter into organisms that feed on
them (Wiencke et al. 2014; Ahn et al. 2016) and indirectly through detritus pathway
(Iken et al. 1997; Tatián et al. 2004; Amsler et al. 2005, 2012; Quartino et al. 2008;
Campana et al. 2018). Besides this, benthic algae in some locations can have high
primary productivity similar to or higher than phytoplankton production (Fogg
1977). Furthermore, Antarctic macroalgae constitute structural and even chemical
refuges from predation (Amsler et al. 1999, 2009), habitat for a variety of associated
fauna (Huang et al. 2007) that provide a large fraction of the secondary production
to the benthos (Gómez et al. 2009), and substrate for epiphytic communities
(Majewska et al. 2016). Thus, macroalgae play a fundamental role in the food web
being able to influence ecosystem dynamics and stability through propagation of
direct and indirect effects.
The network of interspecific relationships involving seaweeds is very complex
and includes not only consumption of algae but also several types of relations.
Direct interactions are, for instance, competition among different macroalgae spe-
cies for space (Smale and Barnes 2008; Quartino et al. 2013; Campana et al. 2009,
15 Seaweeds in the Antarctic Marine Coastal Food Web 295
2018), when hard substrate is a limiting resource, or for light (Klöser et al. 1994,
1996; Deregibus et al. 2016). On the other hand, seaweeds can establish relation-
ships with potentially harmful light-blocking epiphytes, whereas macroalgae pro-
vide a substrate for these organisms; however, seaweeds are chemically defended
against mesograzers (and other herbivores; see Chap. 18 by Amsler et al.) that, in
turn, use them as a refuge from predation: the macroalgae benefit in return because
the mesograzers remove epiphytic algae (Amsler et al. 2014), and in this way, com-
mensalism can become mutualism.
However, not only direct effects play an important role: several seaweed species
share predators and establish a complex dynamics that may be observed as much as
apparent competition or “apparent” mutualism depending on the density of preda-
tors and the closeness of macroalgae species involved. When a group of species
establish different types of interactions (i.e., trophic, commensalism, mutualism) in
an intricate manner, it is challenging to decide if the regulation of numbers or bio-
mass is mainly controlled by top-down, bottom-up, or wasp-waist effects or by dif-
ferent and nontrivial combinations of them. In consequence, it is necessary to take
into account the complexity of the ecosystem and all its ecological interactions (tro-
phic and non-trophic) to understand its stability in response to environmental
changes. In particular, macroalgal species are exposed to different environmental
disturbances such as sediment input or ice scouring (Sahade et al. 2015; Quartino
et al. 2013; Deregibus et al. 2016), resulting in a complex mosaic of effects. In this
sense, the understanding of the effects of climate change in the western Antarctic
Peninsula and a possible losses and gains in biodiversity urgently needs a deep
knowledge of the relations between species’ functional roles and the ecosystem
structure (Woodward et al. 2010).
15.2 Food Webs and Seaweeds
The complex network of interactions varies in space and time, and not all interac-
tions take place simultaneously (Poisot et al. 2015), but the interactions should not
be studied separately but be understood as a whole. For this purpose, we have a
powerful tool: the food web theory (Delmas et al. 2018).
After comparing 19 food web properties, Dunne et al. (2004) concluded that the
excessively low percentage of basal taxa in marine food webs compared to other
systems is clearly an artifact due to the poor resolution of primary producers and
consumer links to them. One of the methodological strengths of the food web stud-
ied here is the high taxonomic resolution of basal nodes. A good taxonomic resolu-
tion of the lower trophic levels, such as the macroalgal community, is essential to
understand ecosystem functioning, since there seems to be a species-specific selec-
tive consumption (Iken et al. 1997). Implications for ecosystem functioning and
stability are only possible to elucidate in food webs where the species involved in
energy and matter transfer processes are well represented.
A first step to identify the seaweeds embedded in the functional context of their
community is to visualize the food web in which they are integrated. For example,
Fig. 15.1 shows the food web of the Potter Cove ecosystem (Marina et al. 2018). We
can see that the base of the pyramid is filled with several macroalgal species accom-
panied by fresh and old detritus and microalgae. Arrows indicate matter and energy
fluxes through predation; the node size is proportional to its number of connections;
the placement of the node on the vertical coordinate is related to its weighted tro-
phic level. Also, macroalgae contribute to the detritivore pathway by decomposition
and accumulation in the cove, generating a link between macroalgae species and
detritus that is not represented in Fig. 15.1. However, we consider it in our studies
and conclusions.
An understanding of the relations between species functional roles and ecosystem
structure is an indispensable step toward the comprehension of change in the western
Antarctic Peninsula and subsequent biodiversity loss and gain (Woodward et al.
2010). Several network properties are commonly used to describe food webs (Dunne
et al. 2002): (1) number of species, S; (2) total number of interactions or trophic
links, L; (3) number of interactions per species or linkage density, L/S; (4) con-
nectance or trophic links divided by total number of possible interactions, C = L/S2;
(5) percentage of top species (species with preys, but without predators); (6) interme-
diate species (species having preys and predators); (7) basal species (species with
predators/consumers, but without preys); and (8) percentage of omnivores (species
eating prey from more than one trophic level). Additionally, the topology of the food
web can be studied by measuring three more properties: (9) characteristic path length
(ChPath), which is the average shortest path length between all pairs of species; (10)
clustering coefficient (CC), which is the average fraction of pairs of species one link
away from a species that are also linked to each other; and (11) distribution degree,
which is the fraction of trophic species P(k) that have k or more trophic links (both
predator and prey links) (Albert and Barabási 2002). These last three metrics give us
information related to the degree of self-organization shown by the web.
The trophic levels (TL) of species were calculated using the short-weighted TL
(Williams and Martinez 2004). Short-weighted trophic level is defined as the aver-
age of the shortest TL and prey-averaged TL. Shortest TL of a consumer in a food
web is equal to 1+ the shortest chain length from this consumer to any basal species.
Prey-averaged TL is equal to 1+ the mean TL of all consumer’s trophic resources,
calculated as follows:
S
TLi
TLj = 1 + ∑lij
nj.
i =1

where TLj is the trophic level of species j; S is the total number of species in the food
web; lij are the elements of the connection matrix with S rows and S columns; for
column j and row i, lij is 1 if species j consumes species i and 0 if not; and nj is the
number of prey species in the diet of species j. Therefore, short-weighted TL yields
a minimum estimate of TL and assumes a value of 1.0 for basal species (Williams
and Martinez 2004). We considered the mean TL of the web as the average of all
species’ TL.
Fig. 15.1 Food web of Potter Cove. Vertical position is related to trophic level. Node size is pro-
portional to the total degree (in and out). Node colors are by functional group. Nodes inside the
boxes are the basal species. Network was plotted with Visone (version 2.9.2). 1Notothenia cori-
iceps, 2Notothenia rossii, 3Lepidonotothen nudifrons, 4Trematomus newnesi, 5Trematomus bernac-
chii, 6Harpagifer antarcticus, 7Parachaenichthys charcoti, 8Chaenocephalus aceratus,
9
Protomyctophum sp., 10Callophyllis atrosanguinea, 11Curdiea racovitzae, 12Georgiella confluens,
13
Gigartina skottsbergii, 14Iridaea cordata, 15Myriogramme manginii, 16Neuroglossum delesseriae,
17
Palmaria decipiens, 18Pantoneura plocamioides, 19Picconiella plumosa, 20Plocamium cartilag-
ineum, 21Porphyra plocamiestris, 22Trematocarpus antarcticus, 23Adenocystis utricularis,
24
Ascoseira mirabilis, 25Desmarestia anceps, 26Desmarestia antarctica, 27Desmarestia menziesii,
28
Geminocarpus geminatus, 29Phaeurus antarcticus, 30Lambia antarctica, 31Monostroma hariotii,
32
Urospora penicilliformis, 33Ulothrix sp., 34Epiphytic diatoms, 35Benthic diatoms, 36Phytoplankton,
37
Aged detritus, 38Nereidae, 39Margarella antarctica, 40Austrodoris kerguelensis, 41Eatoniella sp.,
42
Nacella concinna, 43Laevilacunaria antarctica, 44Dacrydyum sp., 45Laternula elliptica,
46
Neobuccinum eatoni, 47Euphausia superba, 48Paradexamine sp., 49Eurymera monticulosa,
50
Pontogeneiella sp., 51Gondogeneia antarctica, 52Hyperiids, 53Pariphimedia integricauda,
54
Bovallia gigantea, 55Cheirimedon femoratus, 56Gitanopsis antarctica, 57Prostebbingia gracilis,
58
Waldeckia obesa, 59Hippo-Orcho (Hippomedon kergueleni and Orchomene plebs collapsed),
60
Oradarea bidentata, 61Serolis sp., 62Glyptonotus antarcticus, 63Plakarthrium puncattissimum,
64
Hemiarthrum setulosum, 65Ophionotus victoriae, 66Odontaster validus, 67Diplasterias brucei,
68
Odontaster meridionalis, 69Perknaster fuscus antarticus, 70Perknaster aurorae, 71Sterechinus
neumayeri, 72squids, 73Copepods, 74Ascidians, 75Octopus sp., 76Oligochaetes, 77Hydrozoa,
78
Bryozoa, 79Priapulids, 80Parborlasia corrugatus, 81Salpidae, 82Mysida, 83fresh detritus, 84necro-
mass, 85zooplankton, 86Haliclonidae sp., 87Stylo-Myca (Stylocordila borealis and Mycale acerata
collapsed), 88Rosella sp., 89Dendrilla antarctica, 90Urticinopsis antarctica, 91Malacobelemnon day-
toni. (Modified from Marina et al. 2018)
Fig. 15.2 Common-enemy graph for basal species of Potter Cove food web. Nodes represent spe-
cies and link indirect interactions (presence of shared predators). Only prey species are shown.
Node colors identify different preys (type of algae, or detritus, or microalgae). Node and link width
are proportional to the number of shared predators. (Modified from Marina et al. (2018) and
Cordone et al. (2018))
The influence of the seaweed community in Potter Cove ecosystem is notorious

not only in the structure of the food web but also in the functioning. For instance,
the maximum trophic level for Potter Cove food web is 4.27 (Marina et al. 2018),
lower than most other food webs studied (Dunne et al. 2002, 2004). This implies
that top and basal species (dominated by macroalgae) are separated by few interme-
diate taxa. Therefore, the transfers of energy or nutrients from the base to the top of
Potter Cove food web is small, so that the number of times chemical energy is trans-
formed from a consumer’s diet into a consumer’s biomass along the food web is
also small. The mean trophic level for the mentioned food web is also low (2.10),
which is a consequence of the fact that most predators at intermediate levels (e.g.,
amphipods, isopods, bivalves, Notothenia coriiceps) feed predominantly on algae
species and/or detritus, being mainly the product of dead and decomposed macroal-
gae in Potter Cove (Iken et al. 1998; Quartino et al. 2008; see also Chap. 8 by
Quartino et al.). The macroalgal detritus decomposes and is eaten by detritivores
and suspensivores (e.g., sponges, ascidians, bryozoans, cnidarians), supporting an
important amount of the secondary production (Tatián et al. 2004). The obtained
low mean trophic level for Potter Cove food web clearly shows what species-specific
and/or community studies have suggested. These characteristics of ecological com-
munities have a high impact on ecosystem functioning, such as nutrient and carbon
cycling, and trophic cascades (Post 2002).
However, our interest here is focused on macroalgae. To explore mainly their
interactions, we can use another useful information due to the secondary graph of
common-enemy graph (Fig. 15.2). This graph represents prey species linked with
each other according the existence of shared predators. In the representation of
Fig. 15.2, the thickness of each link joining a couple of nodes is proportional to the
number of enemies shared by these nodes. The common-enemy graph is hypercon-
nected having a high-density value of interactions per node (Cordone et al. 2018);
this is an indicator of the existence of multiple alternative energy paths. This hyper-
connectivity makes the prediction of indirect relationships between species very
difficult, as each interaction involves positive and negative effects between species
abundances (Holt and Lawton 1994).
15.3 Network Dynamics and Robustness
An immediate question that we can try to answer is the following: can we predict
the behavior of the community against the (local) extinction of some algae? This
important question cannot be easily answered by field observations or experiments;
however, we can carry out in silico experiments using our food web (Cordone et al.
2018). We made a virtual experiment trying to determinate if successive extinctions
of base species in Potter Cove could produce phase transitions in the emergent prop-
erties of the food web. With this objective, we simulated extinctions by deleting
nodes (seaweeds, detritus, microalgae) according to different sequences established
by the degree of each macroalgae (total number of trophic interactions per node)
and their biomass in Potter Cove. Four sequences of extinctions were used: random
order, degree in ascending and descending order, and biomass in ascending order.
The method quantifies secondary extinctions taking into account the existence of
different extinction thresholds (Schleuning et al. 2016). That means that a species
suffers a secondary extinction when it loses a given percentage of its preys (Solé and
Montoya 2001). We define the threshold (v) as the minimum level of energy neces-
sary for species’ survival. After each node removal, the fraction of original incom-
ing energy e(i) is calculated for each species i, and when this fraction is equal or less
than the threshold, the species is secondarily lost. The classical topological approach
assumes that v is equal to 0, so only when the energy inflow is null a species goes
extinct (Bellingeri and Bodini 2013).
The results of the in silico experiment considering different thresholds for
extinction and the four sequences of primary elimination are indicated in Fig. 15.3.
We found that the Potter Cove food web is relatively stable to macroalgae loss, but
a significant number of secondary extinctions were obtained beyond a 50% thresh-
old (Cordone et al. 2018). The elimination of macroalgae species from the Potter
Cove food web does not seems to generate a catastrophic cascade of secondary
extinctions, suggesting that the Potter Cove food web could be more robust than
other similar networks (Allesina et al. 2006). Most connected macroalgae shared
more predators, which could indicates that these macroalgae species are function-
ally redundant (i.e., species with equivalent trophic interactions). Functional
redundancy has important consequences in potential cascade extinctions, since it
increases food web resistance by means of availability of alternative preys (Borrvall
et al. 2000; Petchey et al. 2008). However, these results are tied to the limitations
Fig. 15.3 Secondary extinctions vs extinctions (total, primary plus secondary) when macroalgae
species and detritus are removed. The secondary extinctions after primary extinctions take place or
not depending on the numbers of preys that the predator needs to survive. This number is deter-
mined by the threshold of extinctions as the number of original preys multiplied by threshold. Each
box corresponds to a simulation in which the threshold of extinctions was constant and different
(0%, 25%, 50%, and 75%). The macroalgae loss was made following the four different sequences:
red, ascending degree; blue, descending degree; violet, random degree – mean and interval confi-
dence; and green, biomass – in ascending order
of our method. Typically, the topological approach underestimates the actual num-
ber of secondary extinctions and in consequence overestimates food web robust-
ness. The introduction of the threshold effect gives us a more accurate prediction
(Fig. 15.4).
Despite this, the topological approach enables the analysis of complex food
webs, since it only requires knowledge of network structure and could be used as
a proxy of food web stability (Eklöf et al. 2013). Furthermore, we have to
Fig. 15.4 This figure summarizes the effect of varying thresholds in the number of secondary
extinctions recorded. We tested thresholds from 5% to 95% by 5% when macroalgae are primary
lost (blue, 3; brown, 5; green, 10; red, 15; pink, 20). Points are means of secondary extinctions
when x number of primary extinctions took place at a particular threshold (by random simula-
tions). Shaded area represents confidence interval of the series. Secondary extinctions recorded at
a fixed threshold (0.25, 0.50, 0.75) from Fig. 15.3. (Modified from Cordone et al. 2018)
consider that this food web includes all recorded trophic interactions, though
these interactions do not always occur simultaneously in time and space. We can-
not ignore the potentially confounding effects of seasonality and spatial sampling
(Ings et al. 2009). In fact, the network is an average representation across seasons
and different habitats, and dynamic stability depends more on how interactions
are materialized in time and space. Some nodes are pulsatile, such as the massive
influx of Krill (Fuentes et al. 2016), which is difficult to reflect in a static descrip-
tion of the network topology. The consideration of all these factors might change
our estimation of the fragility of Potter Cove food web. Our current efforts are
focused on incorporating spatial and temporal variability into the modeling of
Potter Cove food web to achieve a more realistic picture of this ecosystem and its
macroalgae species.
15.4 Non-Trophic Interactions
Ecological systems are complex and multifaceted in the nature of their interactions
and should be defined not only by lists of co-occurring species but also by the vari-
ety of interactions that take place between them. In order to satisfy different require-
ments, species interact in many ways with multiple partners and make associations
that imply more than a trophic relationship. Great advances and multiple practical
applications have been developed since the study of the structure, intensity, and
dynamics of trophic interactions. However, ecological interactions between co-
existing species involve much more than simply feeding (Bascompte et al. 2003;
Kéfi et al. 2012; Pocock et al. 2012; Kéfi et al. 2015, 2016a).
Decades of empirical and theoretical studies have shown that specific non-trophic
interactions, such as habitat modification, stress minimization, ecosystem engineer-
ing, and behavioral changes, can play important roles for community structure and
ecosystem functioning (Pocock et al. 2012; Kéfi et al. 2015, 2016a). Some works
have recognized this importance and have focused their study on isolated networks
of non-trophic interactions such as mutualistic networks (Jordano et al. 2009) and,
more recently, have incorporated different types of interaction (e.g., mutualistic,
competition, and trophic) in a single network usually named “multiplex” (Kéfi et al.
2012, 2015, 2016b; Pocock et al. 2012; García-Callejas et al. 2018).
To know how important non-trophic interactions are for the ecosystem, function-
ing triggers many interesting questions around these relationship types: How many
direct non-trophic interactions are there and how are they distributed among spe-
cies? Do the topological properties of trophic and non-trophic networks differ? Can
simple species attributes help predict the type of interaction between two species?
Can trophic characteristics help predict the non-trophic webs (Kéfi et al. 2015)?
Here, we have focused on the first question to describe non-trophic interactions that
involve macroalgae species from the Potter Cove food web.
The number of non-trophic interactions identified in Potter Cove marine ecosys-
tem duplicates the number of trophic relationships: 1091 versus 454, respectively.
Here, non-trophic interactions include competition or negative interactions (−/−)
considered when a pair of species share at least one prey and represent the 74% of
the total number of non-trophic interactions; mutualism or positive interactions that
involve a benefit of both interacting species (+/+) that represent the 13.6% of the
total number of non-trophic interactions; and commensalism (+/0) and amensalism
(−/0) or neutral interactions in which one species benefit or not-benefit, respec-
tively, and the other species is not affected by the link, and these interactions repre-
sent the 12.4% of the total number of non-trophic interactions. The distribution of
these interactions (Fig. 15.5) depends on the trophic classification of the species in
basal, intermediate, or top species, e.g., competition, as we defined here, occurs
between intermediate and/or top species, which means that most non-trophic inter-
actions in Potter Cove ecosystem occur between species of high trophic levels. So,
we should wonder what the role of macroalgae in the non-trophic relationships is.
Fig. 15.5 Number of non-trophic interactions for basal, intermediate, and top species. Each color
represents a type of interaction
Many works highlight the importance of studying the structure of non-trophic

networks versus the trophic network by suggesting that, in general, trophic net-
works tend to be compartmentalized, while positive non-trophic networks are more
nested (Bascompte et al. 2003; Thébault and Fontaine 2010), which minimizes
competition, increases the number of co-existing species, and makes the community
more robust against random extinctions and diversity loss (Memmott et al. 2004;
Fortuna and Bascompte 2006).
In food webs, it is argued that modular patterns tend to increase the stability of
the network by retaining the impacts of disturbances within each module and mini-
mizing that impact on other modules in the network. In the particular case of Potter
Cove, it was observed that the food web has not modular characteristics, reason to
suppose that the network should be not very robust against random disturbances.
However, it has been shown that the trophic network is highly robust against differ-
ent types of disturbances, which makes it possible to assume that positive non-
trophic interactions could have a stabilizing role in the Potter Cove ecosystem.
Then, we should not fail to recognize that macroalgae are a key component of the
system because they represent, directly or indirectly, a stabilizing species.
15.5 Final Remarks
Network science offers a great opportunity to understand species in their context

and their relation to the community and the ecosystem. In our studies, the incorpora-
tion of a network perspective shows the relevance of macroalgae species to the
entire ecosystem of Potter Cove. We observed that Potter Cove food web is rela-
tively robust to local extinctions of macroalgal species under a topological approach
(considering extinction thresholds), but we also observed that a network collapse
could be reached by increasing the extinction threshold. This result demonstrates
that effects on single species could propagate to the entire network. Potter Cove
ecosystem is experiencing rapid climate-related changes in environmental factors
that have affected the benthic system, including the macroalgal community (Schloss
et al. 2012; Quartino et al. 2013; Sahade et al. 2015; Deregibus et al. 2016; Campana
et al. 2018). In this sense, species-specific responses of macroalgae to changing
environmental factors should be explored as negative effects at the species level
could propagate through the food web, leading to changes in the structure and func-
tion of this system.
Acknowledgments We wish to thanks the scientific and logistic assistance of Instituto Antártico
Argentino (IAA)/Dirección Nacional del Antártico (DNA). The academic interaction with the
Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research (AWI) was essential for
this work. We acknowledge the financial support by grants from CONICET-UNGS (PIO
14420140100035CO). This chapter also presents an outcome of the international Research
Network IMCONet funded by the Marie Curie Action IRSES IMCONet (FP7 IRSES, Action No.
318718). Many thanks to C. Gardel and I. Corsini for their assistance.
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Chapter 16
Trophic Networks and Ecosystem
Functioning
Marco Ortiz, Brenda B. Hermosillo-Núñez, and Ferenc Jordán
Abstract The geographic isolation of the Antarctic continent offers an interesting

opportunity to quantify and qualify the actual ecological conditions and the most
sensitive components from an ecosystem perspective. Antarctic coastal ecosystems
are under severe stress as a consequence of climate change, which could facilitate
biological invasions, reduced growth of macroalgal species, and local extinctions.
The application of network analysis, representing the interactions among multiple
species, allows us to quantify macroscopic (emergent) system properties, to assess
overall health, to predict the propagation of direct and indirect effects, and to iden-
tify keystone species complexes within these complex ecological systems. Three
theoretical frameworks are used here for this analysis: (1) ecological network analy-
sis (ENA) considering thermodynamics and information theory (providing mea-
sures such as Ascendency), (2) semiquantitative (qualitative) mathematics based on
the structure and local stability of community matrices (Loop Analysis), and (3)
topological studies on interaction networks considering central node sets and defin-
ing keystone species complexes (KSCs).
Therefore, the integration of ecosystemic properties and keystone species com-
plexes could help us to facilitate the design and assessment of conservation and
monitoring measures, especially when the Antarctic coastal marine ecosystems are
being severely stressed. The protection of the Antarctic environment – as a whole –
not only should be focused on biological populations and communities but also
M. Ortiz (*)
Instituto de Ciencias Naturales Alexander von Humboldt, Facultad de Ciencias del Mar y
Recursos Biológicos, Universidad de Antofagasta, Antofagasta, Chile
Instituto Antofagasta, Universidad de Antofagasta, Antofagasta, Chile
e-mail: marco.ortiz@uantof.cl
B. B. Hermosillo-Núñez
Instituto Antofagasta, Universidad de Antofagasta, Antofagasta, Chile
e-mail: brenda.hermosillo@uantof.cl
F. Jordán
Balaton Limnological Institute, MTA Centre for Ecological Research, Tihany, Hungary
Stazione Zoologica, Napoli, Italy
e-mail: jordan.ferenc@okologia.mta.hu

https://doi.org/10.1007/978-3-030-39448-6_16
310 M. Ortiz et al.
should consider changes in macroscopic properties, the propagation of direct and

indirect influences in the networks, and keystone species complexes, which emerge
using networks of interacting and coexisting species (or functional groups as system
components).
Keywords Ascendency framework · Coastal benthic-pelagic ecosystem ·

Keystone species · Macroscopic network properties · Multispecies modelling
16.1 Introduction
Different scientific strategies – not necessarily mutually exclusive- can be used to

study, assess, and attempt to predict the transformations in natural systems caused
by direct and indirect human activities. Within of these strategies, we choose the
quantitative and semiquantitative (qualitative) simulations permitting us to deter-
mine whole-system properties (of structure and dynamics) of Antarctic coastal
benthic-pelagic ecosystems (Pikitch et al. 2004). Antarctic coastal ecosystems face
several stressors as the increase in UV radiation, which reduces the growth of mac-
roalgae species (Richter et al. 2008), and the rise in temperature, which could mod-
ify the amount of the direct light to macroalgae and other organisms (King 1994;
Stark 1994). The impact of these stressors on the species and functional groups
could affect the structure of their trophic networks and their functioning of diverse
Antarctic ecosystems. Network analyses permit us to evaluate the macroscopic
properties at ecosystem scale, describing aspects related with growth, development,
complexity, and health (Odum 1969; Ulanowicz 1986; Levins 1998a, b; Costanza
and Mageau 1999). Likewise, another related analysis can be performed as the
propagation of direct and indirect effects (Hawkins 2004; Levins 1998a) and the
determination of species or functional groups that play key roles in these complex
ecological systems (Ortiz et al. 2013a).
The ecological concept of keystone species, introduced by Paine (1969) and
broadened by Power et al. (1996), has become a key issue in numerous research
programs in different communities and ecosystems around the planet (Mills et al.
1993; Power et al. 1996), especially given its use in the design and application of
conservation management and monitoring measures (Payton et al. 2002; Barua
2011; Ortiz et al. 2013a, b). Power et al. (1996) named a key species as a species
whose effect is large, and disproportionately large relative to its abundance.
Although the concept seems to be sufficiently clear, its determination in communi-
ties and ecosystems is complex, requiring observations and experiments that include
different spatiotemporal scales, levels of organization, and taxonomic groups
(Power et al. 1996; Libralato et al. 2006). Similarly, some purely experimental stud-
ies (Pace et al. 1999) have omitted the propagation of direct and indirect effects,
16 Trophic Networks and Ecosystem Functioning 311
despite the ecological importance of these processes it has been recognized (Wootton
1994; Patten 1997; Yodzis 2001).
Various studies have determined the role that different species play in their eco-
logical systems by using different network indices (Jordán et al. 2007; Luczkovich
et al. 2003; Jordán and Scheuring 2004; Allesina and Bodini 2004; Libralato et al.
2006; Benedek et al. 2007; Ortiz et al. 2013a, 2017; Valls et al. 2015; Giacaman-
Smith et al. 2016). Such analyses offer a complementary way to address some of the
limitations in the experimental identification of key groups. Quantitative trophic
analysis permits estimations of the strength of interactions between species or func-
tional groups by identifying the presence of keystone species, which occupy key
positions in the networks (Jordán and Scheuring 2004). At the same time, keystone-
ness can also be determined using semiquantitative or qualitative loop network
analysis. In this case, the key role of a species is defined as a dynamical conse-
quence of its changes, modifying the balance (prevalence) of positive and negative
feedbacks and, in turn, the local stability of the network (Ortiz et al. 2013a).
Likewise, following field observations (Daily et al. 1993), two independent contri-
butions have proposed methodological extensions toward multispecies approaches
to keystones. One was given by Benedek et al. (2007), which is based on the central-
ity of node sets, and the other proposed by Ortiz et al. (2013a) based on quantitative
and semiquantitative multispecies trophic models. In both cases, the keystone spe-
cies complexes (KSCs) consist of a core of species and/or functional groups linked
by strong interspecific interactions. These more holistic concepts could facilitate the
design of conservation and monitoring programs in ecosystems since it is not guar-
anteed that always a single species plays the key role.
The aim of this chapter was to determine the macroscopic system properties
(e.g., level of development, organization, maturity, and health) derived from
Ascendency theoretical framework (sensu Ulanowicz 1986, 1997) of a model
benthic-pelagic ecosystem at Fildes Bay, King George Island Peninsula (Fig. 16.1a).
The subtidal communities are dominated by the brown macroalgae species
Himmantothallus grandifolius and Desmarestia anceps; the red algae species
Gigartina skottsbergii, Trematocarpus antarcticus, and Plocamium cartilagineum;
the grazer species (gastropod) Nacella concinna; the asteroid predator species
Diplasterias brucei; and a variety of fish, sponge, bryozoan, and ascidian species
(Targett 1981; Huovinen and Gómez 2013; Valdivia et al. 2014, 2015). Considering
this network, dynamical simulations, local stability, and centrality of node sets
(KeyPlayer set) were performed to determine the keystone species complexes
(KSCs). Finally, the contribution of the components of KSCs on macroscopic sys-
tem properties will be also evaluated. For this purpose, quantitative and semiquan-
titative (qualitative) multispecies trophic network models will be used and analyzed.
The network model constructed represents exclusively transient states under short-
term dynamics.
312 M. Ortiz et al.
Fig. 16.1 Study area and sampling sites at Fildes Bay (King Georg Island, Antarctica) (GC
Glacier Collins, IA Island Artigas, IS Island Shoa, HT Half Three, EN Estrecho Nelson, GN Glacier
Nelson) (a) and the trophic model for the coastal ecosystem of Fildes Bay (Note: vertical position
approximates trophic level, and the circle is proportional to the compartment biomass) (b). For
details, see Appendix 16.A. (Adapted from Fig. 2 in Ortiz et al. 2017)
16.1.1 Q
uantitative and Semiquantitative Multispecies Trophic
Modelling
Trophic mass balance models were constructed using the Ecopath with Ecosim
(v.5.0) (EwE) software, which was first developed by Polovina (1984) and subse-
quently extended by Christensen and Pauly (1992) and Walters et al. (1997).
Ecopath allows the depiction of the flows of matter and/or energy in a stationary
state of an ecosystem within a given time, whereas Ecosim performs dynamic simu-
lations of the initial conditions (established with Ecopath) as a response to perturba-
tions (Christensen and Pauly 1992). The energy mass balance of a species or
functional group within a network is represented by linear differential equations for
each component in the model (Box 16.1). To employ Ecosim (see Walters and
Christensen 2007), an extension routine of Ecopath is included to define the con-
sumption by compartment which is represented by the control flow equation, allow-
ing to set if the flow control mechanism is top-down, bottom-up, or mixed (Box
16.1). We set the mixed control mechanism following the criteria of Ortiz (2008a,
b) and Ortiz et al. (2009, 2010, 2013a, b). We used Ecopath with Ecosim version
6.4, and details concerning this software package are given in Pauly et al. (2000).
The semiquantitative or qualitative trophic models were built using Loop
Analysis, which allows for the estimation of the local stability (as a measure of sus-
tainability) of an ecological system and the assessment of the propagation of both
direct and indirect effects as a response to external perturbations (Levins 1974,
1998a). This approach has been widely applied in different natural science fields
(Puccia and Levins 1991; Levins 1998b; Darmbacher et al. 2009; Ortiz and Levins
2011, 2017). The interactions are shown as signs that indicate the type of influence
each variable has upon another (positive, negative, or null). In ecological relation-
ships, the +1/−1 signs denote predator/prey or parasite/host interactions, +1/+1
signs express mutualism, +1/0 signs represent commensalism, and −1/0 signs show
amensalism. Loop Analysis is based on the relationships of differential equations
near equilibrium, Jacob-Levins’ community matrices, and their loop diagrams (Box
16.2). Local stability of the system is quantified using the Routh-Hurwitz criteria,
which require the following: (1) all feedbacks (on every level of complexity) must
be negative and (2) negative feedbacks on higher levels cannot be too great for com-
parison with the negative feedbacks on lower levels. Levins (1998a) proposes that
the system is more resistant (locally stable), whereas Fn (feedback corresponding to
higher level of complexity) is more negative (Box 16.2). The semiquantitative or
qualitative Jacob-Levins’ community matrices are based on the diet matrices used
for quantitative models (Ecopath with Ecosim). The polynomial equation required
for each community matrix was determined using the software LoopStability (Diaz-
Ávalos and Ortiz, laboratory uses).
314 M. Ortiz et al.
Box 16.1 The Ecopath with Ecosim (EwE) Theoretical Framework
The mass balance of a species or functional group within a trophic network is

represented by the following mathematical expression:
P n
Q
Bi EE i B j DC ji Yi BA i Ei 0 (16.1)
B j 1 B j
i

where Bi and Bj are the biomass value of prey i and predator j; P/Bi is the pro-
ductivity of prey i, which is equivalent to total mortality (Allen 1971); EEi is
the ecotrophic efficiency or the fraction of the total production of a group or
species used in the system; Yi is the fishing production per unit of area and
time (Y = fishing mortality × biomass); Q/Bi is the food consumption per bio-
mass unit j; DCji is the fraction of prey i in the average diet of predator j; BAi
is the biomass accumulation rate for i; and Ei is the net migration of i (emigra-
tion minus immigration) (Christensen and Walters 2004).
Based on this equation, the input and output of matter (energy) in each
compartment of the system can be balanced. This energy balance is assured
for each group with this equation:
Q P R UAF (16.2)
where Q is consumption, P is production, R is respiration, and UAF is unas-
similated food for each group or species of the system. Given the inclusion of
the factors BAi and Ei in Eq. (16.1), the focus of Ecopath is based on a steady
state. This situation allows changes in the network compartments when the
mathematical expression is expressed in a dynamic form.
To employ Ecosim (see Walters and Christensen 2007), an extension rou-
tine of Ecopath is included to define the consumption by compartment (Qij),
where Qij is represented by the following equation:
aij vij Bi B j
Qij (16.3)
2 vij aij B j

where aij represents the instantaneous mortality rate on prey i caused by a
single unit of predator j biomass. Similarly, aij can be understood as the rate of
effective search by predator j for prey i. Each aij is estimated directly from the
corresponding Ecopath models by aij = Qi/(BiBj), where Qi is the total con-
sumption of i. The vij represents the transfer rate between compartments i and
j. This parameter determines if the flow control mechanism is top-down, bot-
tom-up, or mixed.
Box 16.2 Loop Analysis Theoretical Framework
Loop Analysis estimates the local stability (as a component of sustainability)

of an ecological system and the assessment of the propagation of both direct
and indirect effects as a response to external perturbations (Levins 1974,
1998a). The effects are shown as signs that indicate the type of influence each
variable has upon another (positive, negative, or null). Interactions are
described according to pairwise sign combinations: +/− signs denote preda-
tor/prey or parasite/host interactions, +/+ signs express mutualism, +/0 signs
represent commensalism, and −/0 signs show amensalism or allelopathy.
Loop Analysis is based on the relationships of differential equations near equi-
librium, community matrices, and their loop diagrams. In a benthic system,
the element αij of the matrix and loop diagrams performs the effect of the
variable j in the growing of variable i, and this dynamic performs in the fol-
lowing way:
dXi
fi X1 , X 2 ,, X n ; C1 ,C2 ,,Cn (16.4)
dt
where the change on the time of variable Xi is a function fi of the other vari-
ables – Xn and parameters Cn – which are interconnected. The link of Xj to Xi
is similarly to αij in Levins (1968):
fi X X
ij (16.5)
X j

where x∗ indicates that it has been evaluated in equilibrium. The sign αij rep-
resents the link of j to i where the function of sign X is 1 when X > 0, 0 when
X = 0, and −1 when X < 0. Local stability of the system is quantified using the
Routh-Hurwitz criteria, which require the following: (1) all feedbacks (on
every level of complexity) must be negative and (2) negative feedbacks on
higher levels cannot be too great for comparison with the negative feedbacks
on lower levels. Levins (1998a) proposes that the system is more resistant
(locally stable), whereas Fn (feedback corresponding to higher level of com-
plexity) is more negative:
F0 n F1 n 1 F2 n 2  Fn 1 Fn 0 (16.6)

16.1.2 S
election of Model Components, Sampling Programs,
and Data Sources
Three intensive field studies were conducted during the austral summers of 2013,
2014, and 2015 to identify the biological components (species or functional groups)
of the system model and to estimate the average biomass (B), average density, and
316 M. Ortiz et al.
food sources of the selected components (Valdivia et al. 2014). Sampling was per-
formed to directly estimate the average biomass and density of the macrobenthic
species (between 5 and 30 m depth) at six stations within Fildes Bay (Fig. 16.1a).
The production (P) and turnover rates (productivity) (P/B) were estimated using the
following allometric Eq. 16.1:
Biomass 0.73
Production Density
Density

where 0.73 is the average exponent regression of annual production on body size for
macrobenthic invertebrates (for more details, see Warwick and Clarke 1993).
Food consumption rates were obtained from the literature (Cornejo-Donoso and
Antezana 2008; Ortiz 2008a; Ortiz et al. 2015; Pinkerton et al. 2010). To determine
the diets of N. concinna, Harpagifer antarcticus, Notothenia coriiceps, N. rossii,
and the asteroid species, the stomach and guts were revised, and the gut contents
were classified to the lowest possible taxonomic level; the frequency of occurrence
of each food item was then calculated. Several studies examining the trophic ecol-
ogy of several benthic and pelagic species were also used to determine the range of
food consumed (Cornejo-Donoso and Antezana 2008; Pinkerton et al. 2010; Kaehler
et al. 2000; Gili et al. 2001; Corbisier et al. 2004; Jacob et al. 2005; Norkko et al.
2007; Mincks et al. 2008).
A trophic model with 17 components was constructed for Fildes Bay. The com-
ponents represent the most abundant species or functional groups composed of mul-
tiple species. Seven components represented the following individual species: the
brown macroalgae H. grandifolius and D. anceps, the red algae G. skottsbergii, the
herbivores N. concinna and Margarella sp., the echinoid Sterechinus neumayeri,
and the asteroid D. brucei. The other components were functional groups that
included several species. These groups included multiple species of green (e.g.,
Monostroma hariotii), red (e.g., T. antarcticus and P. cartilagineum), and brown
(e.g., Ascoseira mirabilis and Halopteris obata) algae, respectively. The filter feeder
(FF) group was composed primarily of clams, hydrozoan, bryozoan, and sponge
species. The small epifauna (SE) component included gastropod, nematode, and
nemertean species. The group of other sea star species (SS) included principally
O. validus and Odontaster sp. The benthic fishes (BF) group was composed primar-
ily of H. antarcticus, N. coriiceps, and N. rossii. The three final groups were the
phytoplankton (Phy), zooplankton (Zoo), and detritus (Det) groups (Fig. 16.1b).
All the compartments are trophically linked by detritus – primarily as microbial
film and organic matter – because several studies have emphasized the importance
of bacteria as food for various species of molluscs (e.g., Epstein 1997; Grossmann
and Reichardt 1991; Plante and Mayer 1994; Plante and Shriver 1998), zooplankton
(Epstein 1997), and Echinodermata (Findlay and White 1983). The models were
constructed to depict the trophic relationships between the most important species
or functional groups in the benthic communities of Fildes Bay. Notably, the models
excluded the energy flows from epiphytes and the microphytobenthos, in addition to
those leading to seals and birds, because insufficient scientific information was
available for these groups. Although these exclusions reduced the realism of the
model’s configuration, the most dominant interdependencies and energy flows are
reflected. Moreover, such a system-level error, if consistent, should not impede a
comparative analysis of ecological systems placed under similar limitations (e.g.,
kelp forest of SE pacific coast).
Box 16.3 Macroscopic Network Properties

The macroscopic descriptors are based on Ulanowicz’s Ascendency analysis
that enables quantification of the level of development and organization of
ecosystems (Ulanowicz 1986, 1997). This approach stems from informa-
tion theory:
• Total System Throughput (TST). Indicates the size of the system, that is, the
total number of flows in the system:
n 1 n 2
TST Tij (16.7)
i j

where TST is the summation of all flows among compartments; i and j can
represent either an arbitrary system component or the environment.
• Average Mutual Information (AMI). Quantifies the organization of the sys-
tem in relation to the number and diversity of interactions between compo-
nents (complexity):
n2 n2 fij
AMI fij Qi log 2 (16.8)
Q

i j j
where fij is the fraction of flow in element ji in comparison to the TST; Qj
is the probability that species j is the host, calculated as the sum of flows in
the jth row divided by TST; Qi is the probability that i is the predator, cal-
culated as the sum of flows in the ith column divided by TST.
• Ascendency (A). Measures the growth and development of a system and
integrates TST and AMI of flows:
Tij T0,0
A Tij log (16.9)
T T

ij i ,0 0, j
where T is the summation of all flows among compartments (TST); i and j
are the prey and predator, respectively; 0 is the sum of flows of prey or
predators; with Ti,0 the flows from one prey to all their predators, T0,j is the
consumption of a predator over all its prey, and T0,0 is the total sum of flows
over prey and predators.
(continued)
318 M. Ortiz et al.
Box 16.3 (continued)
• Overhead (Ov). Quantifies the degrees of freedom preserved by the net-
work, can be used to estimate the ability of a network to withstand pertur-
bations, and can be estimated from the difference between the Development
Capacity and the Ascendency:
O C A (16.10)
• Development Capacity (C). Quantifies the upper limit of Ascendency:
C A O (16.11)
• Total Biomass/Total Throughput (TB/TST) ratio. Suggests different states
of system maturity (Christensen 1995).
• A/C and Ov/C ratios. Are used as indicators of ecosystem development and
the ability of the system to resist disturbances (Baird and Ulanowicz 1993;
Costanza and Mageau 1999; Kaufman and Borrett 2010).
• Relative Internal Ascendency (Ai/Ci ratio). Represent well-organized,
mature, and efficient systems that are therefore resistant against perturba-
tions (Baird et al. 1991; Baird and Ulanowicz 1993).
The balancing of models was performed on the basis of the following six criteria
proposed by Heymans et al. (2016): checking that (1) the ecotrophic efficiency (EE)
(for quantifying the proportion of production utilized by the next trophic level
through direct predation or fishing) of all compartments was <1.0 (Ricker 1968); (2)
the gross efficiency (GE) (gross food conversion efficiency) of all compartments
was <0.3 (Christensen and Pauly 1993); and when any inconsistency was detected,
the average biomass was modified within the confidence limits (± 1 standard devia-
tion); (3) the net efficiency (value for food conversion after accounting for unas-
similated food) of all compartments was >GE; (4) the respiration/assimilation
biomass (RA/AS) was <1.0; (5) respiration/biomass (RA/B) values for fish between
1 and 10 years−1 and for groups with higher turnover between 50 and 100 years−1;
and (6) the production/respiration (P/RA) was <1.0.
16.2 Macroscopic Ecosystem-Network Properties
The macrodescriptors based on Ulanowicz’s Ascendency (Ulanowicz 1986, 1997)

include the Total Biomass/Total Throughput (TB/TST) ratio, which suggests differ-
ent states of system maturity (Christensen 1995); Total System Throughput (TST),
which indicates the size of the system, that is, the total number of flows in the sys-
tem; Average Mutual Information (AMI), which quantifies the organization of the
system in relation to the number and diversity of interactions between components
(complexity) (Ulanowicz 1986, 1997); Ascendency (A), which measures the growth
and development of a system and integrates TST and AMI of flows; and Overhead
(Ov), which quantifies the degrees of freedom preserved by the network, can be
used to estimate the ability of a network to withstand perturbations and can be esti-
mated from the difference between the Development Capacity (C) and the
Ascendency (A) (Ulanowicz 1986): Development Capacity (C), which quantifies
the upper limit of Ascendency, and A/C and Ov/C ratios, which are used as indica-
tors of ecosystem development and the ability of the system to resist disturbances
(Ulanowicz 1986, 1997; Baird and Ulanowicz 1993; Costanza and Mageau 1999;
Kaufman and Borrett 2010). High values of the Relative Internal Ascendency (Ai/Ci
ratio) represent efficient systems that are therefore resistant against perturbations
(Baird et al. 1991; Baird and Ulanowicz 1993). For more details about macrode-
scriptors, see Box 16.3.
16.2.1 M
acroscopic Properties of Coastal Benthic-Pelagic
Ecosystem at Fildes Bay
The coastal benthic/pelagic ecological system of Fildes Bay dominated by brown

large macroalgae reached a Total System Throughput (TST) equals to 24,234.0 g
ww m−2 year−1; this magnitude was lower than that calculated for a kelp forest off
the Antofagasta Peninsula (Ortiz 2008a, 2010). However, compared to the benthic
communities of Tongoy Bay (Ortiz and Wolff 2002; Wolff 1994) and different estu-
aries around the world (Baird and Ulanowicz 1993; Patrício and Marques 2006;
Wolff et al. 2000), TST was higher in the Fildes Bay system. The Development
Capacity (C) accounted for 110,354.4 flow bits, Ascendency (A) accounted for
32,953.9 flow bits, and the A/C and Ov/C ratios were 29.8% and 70.1%, respec-
tively (Table 16.1). Notably, the A/C value calculated for the Fildes Bay ecological
system was one of the lowest compared to those obtained for other coastal areas
along the Chilean coast and around the globe (Table 16.2). The difference between
the A/C and the Ai/Ci ratios for the Fildes Bay model may indicate a dependency of
this system on external connections (sensu Baird et al. 1991).
Ulanowicz (1997) proposed estimating Relative Ascendency by model compo-
nent to evaluate the contribution of each group to the overall structure and function
of the system. In this case, detritus accounted for ~33%, followed by phyto-
zooplankton at ~26%, macroalgae at ~19%, filter feeders at ~7%, small epifauna at
~5%, and top predators at ~2%. Moreover, the sea star species groups, Chlorophyta,
and the red algae G. skottsbergii accounted for the complexity in the system; that is,
they exhibited the lowest percentage of Average Mutual Information (AMI) within
the Fildes model system (Table 16.2).
Macroscopic properties, such as the A/C ratio, Ov/C ratio, and Redundancy
values, indicate that Fildes Bay would be a less developed system but is more
resistant to disturbances than a kelp forest off the Mejillones Peninsula or the
320 M. Ortiz et al.
Table 16.1 Macroscopic Property Fildes Bay

properties of the trophic
Total System Throughput (TST) (g ww 21,432.00
network for the coastal
m−2 year−1)
benthic-pelagic ecosystem of
Fildes Bay (Antarctica) Total Biomass/Total System Throughput 0.1312
(TB/TST)
Ascendency (A) (g ww m−2 year−1 ∗ 29,758.60
bits)
Overhead (Ov) (g ww m−2 year−1 ∗ bits) 69,355.02
Development Capacity (C) (g ww m−2 99,114.87
year−1 ∗ bits)
Average Mutual Information (AMI) 1.39
A/C (%) 30.02
Ai/Ci (%) 14.00
Ov/C (%) 69.97
seagrass meadows of Tongoy Bay (Ortiz and Wolff 2002; Ortiz 2008a, 2010)
(Tables 16.1 and 16.2). This may be explained by the fact that Fildes Bay is nega-
tively affected by the Antarctic’s austral winters, which are characterized by lower
temperatures and freezing, leading to a reduction in the herbivore biomass and
thereby constraining the flow of energy/matter toward the upper trophic levels.
Additionally, as shown in Tables 16.1 and 16.2, the different estuaries and coral
reef systems appeared to be more developed (A/C and Ov/C) but less resistant to
perturbations compared to Fildes Bay and the benthic ecosystems studied along
the Chilean coast. This latter comparison should be taken with a degree of caution
because the trophic model constructed for Fildes Bay represents only a narrow
temporal window, and unknown system characteristics may emerge during the
rest of the year. The difference between the A/C and Ai/Ci ratios in the Fildes Bay
model system may primarily be a consequence of the omission of the flows to
birds and marine mammals from our analysis. The analysis of relative Ascendency
by component revealed that those groups that principally contributed to the over-
all structure and function of the Fildes Bay system (i.e., detritus, the phyto-zoo-
plankton complex, and macroalgae) differed from those that contributed to the
kelp forest (Mejillones Peninsula) (Ortiz 2008a, 2010) but were similar to those
within the benthic systems of Tongoy Bay and the La Rinconada Marine Reserve
(Antofagasta Bay) (Ortiz and Wolff 2002; Ortiz et al. 2010). This outcome indi-
cates that although a significant amount of the Antarctic system’s biomass is con-
centrated in macroalgae, these macroalgae would contribute fewer nutrients to the
coastal marine ecosystem than those within kelp forests (Duggins et al. 1989;
Ortiz 2008a, 2010).
Table 16.2 Macroscopic properties for system’s development and organization derived from
Ascendency network analysis for Fildes Bay (Antarctic) and other coastal ecosystems
Macroscopic properties of trophic networks
Ascendency theoretical framework (Ulanowicz 1986, 1997)
TST C A A/C Ov Ov/C
(g ww m−2 (flow (flow (flow
Coastal marine ecosystems year−1) bits) bits) % bits) %
Along the Chilean coast (SE Pacific)
Benthic/pelagic ecological 21,432.00 99,114.87 29,758.60 30.02 69,355.02 69.97
system of Fildes Bay1
Kelp ecological system 72,512.0 207,777.4 93,462.6 45.0 112,548.0 55.0
dominated by M. pyrifera,
Antofagasta Peninsula2
Kelp forest ecological system 50,105.0 200,609.4 77,613.5 38.7 117,678.9 61.3
dominated by L. trabeculata,
Kelp forest ecological system, 85,217.0 332,041.6 117,939.7 35.5 211,848.3 64.5
Seagrass habitat ecological 18,746.6 69,270.4 21,557.8 31.1 46,991.0 68.9
system of Tongoy Bay4
Mud habitat ecological system 17,451.3 59,139.0 19,354.8 32.7 39,433.4 67.3
of Tongoy Bay4
Benthic/pelagic ecological 20,834.9 80,689.8 26,312.6 32.6 54,377.2 67.4
system of Tongoy Bay5
La Rinconada Marine Reserve 20,124.0 80,321.0 24,375.1 30.3 55,945.9 69.7
coastal ecological system,
Antofagasta Bay6
Mejillones benthic/pelagic 29,429.8 142,897.9 34,395.1 24.1 108,353.1 75.9
ecological system of Mejillones
Bay7
Antofagasta benthic/pelagic 37,539.8 170,237.0 48,574.3 28.5 121,434.8 71.5
ecological system of
Antofagasta Bay7
Around the world
Coral reef ecosystem, 148,094.1 318,400.0 178,200.0 56.3 139,800.0 43.7
Chinchorro Bank, México8
Coral reef ecosystem, Mexican 194,758.4 890,301.6 308,428.7 34.64 581,872.9 65.35
Pacific Coast9
Mangrove estuary of Caeté, 10,558.6 44,741.4 12,261.6 27.0 31,129.8 63.0
Brazil10
Zostera meadows of Mondego 10,852.0 39,126.0 16,550.3 42.3 22,575.7 57.7
Estuary, Portugal11
Ems estuary in the 12,980.0 6085.0 2327.0 38.3 3758.0 61.7
Netherlands12
Benguela upwelling ecosystem, 8897.0 36,041.0 17,313.0 48.1 18,728.0 51.9
Namibia13
TST Total System Throughput, C System Capacity, A Ascendency
1
Current study, 2Ortiz (2008a), 3Ortiz (2010), 4Ortiz and Wolff (2002), 5Wolff (1994), 6Ortiz et al.
(2010), 7Ortiz et al. (2015), 8Rodriguez-Zaragoza et al. (pers. comm.), 9Hermosillo-Núñez et al.
(2018), 10Wolff et al. (2000), 11Patrício and Marques (2006), 12Baird and Ulanowicz (1993), and
13
Heymans and Baird (2000)
322 M. Ortiz et al.
16.3 Keystone Species Complex (KSC)
16.3.1 Functional Keystoneness Indices
Once the trophic model was balanced following the rules given by Heymans et al.
(2016), the functional keystone index (KSi) developed by Libralato et al. (2006) was
used. This index is an extension of the mixed trophic impacts (MTI, Ulanowicz and
Puccia 1990). Because every impact can be quantitatively positive or negative, a
new measure of the overall effect must be determined for each species or functional
group (εi) using the following mathematical Eq. 16.2:
n
i m
j i
2
ij

where mij corresponds to the elements of the MTI matrix and quantifies the direct
and indirect effects that each (affecting) species or group i has on any (affected)
group j of the food web. However, the effect of the change in a group’s biomass on
the group itself (i.e., mii) is not included. The contribution of biomass from every
species or functional group with respect to the total biomass of the network was
estimated using the following Eq. 16.3:
Bi
pi n
B k
i
where pi is the proportion of biomass of each species Bi with respect to the sum of
the total biomass Bk. Therefore, to balance the overall effect and the biomass, the
keystone index (KSi) for each species or functional group was established using the
Eq. 16.4, which integrates the Eqs. 16.2 and 16.3 as follows:
KSi log i 1 pi

This index assigns high values of functional keystoneness to those variables (spe-
cies) or functional groups that have low biomass and a high overall effect.
The propagation of direct and indirect effects and system recovery time (SRT)
magnitudes estimated by Ecosim were treated in the same way as those obtained
with MTI in order to obtain two additional functional keystone indices. The Ecosim
simulations were used to evaluate the propagation of instantaneous direct and indi-
rect effects and the system recovery time (SRT) (as a system resilience measure) in
response to a steady increase in the total mortality (Z) of all compartments (see
Eqs. 16.5 and 16.6) which was set equivalent to 10%, 30%, and 50%. This proce-
dure was done between the first and second year of simulation for all components
considered in the model. These three magnitudes (scenarios) were set for prediction
purposes as a measure of confidence. As the models studied represent only short-

term (transient) dynamics, the propagation of instantaneous effects was determined
by evaluating the changes of biomass in the remainder variables in the third year of
simulation. All dynamic simulations by Ecosim were carried out using the following
vulnerabilities (flow control): (1) bottom-up (prey controls the flow), (2) top-down
(predator controls the flow), and (3) mixed (both prey and predator control the flow)
(Boxes 16.1 and 16.3):
Z M natural mortality F fishing mortality

Production P Biomass B Z

After that, Eqs. 16.2, 16.3, and 16.4 were used to obtain one keystone species index
related to the propagation of direct and indirect effects (KSiEcosim1), and Eqs. 16.3
and 16.4 were used to obtain another functional keystone species index related to
SRT magnitudes (KSiEcosim2). These indices show, similar as the KSi index (Libralato
et al. 2006), high values of keystoneness associated to compartments with low bio-
mass and a high overall effect.
16.3.2 Topological Keystone Index
The structural keystone index (Ki) developed by Jordán et al. (1999) and Jordán
(2001), following Harary (1961), was also used in this work. This index is applica-
ble for trophic hierarchies (directed acyclic trophic networks) and considers direct
and indirect interactions in vertical directions (i.e., bottom-up and top-down). The
structural keystone index of the ith species or functional group (Ki) is calculated
using the following Eq. 16.7:
n n
1 1
Ki 1 K bc 1 K te
c 1 dc e 1 fe

where n is the number of predator species eating species i, dc is the number of prey
of the cth predator, Kbc is the bottom-up keystone index of the cth predator, and sym-
metrically we have m as the number of prey species eaten by species i, fe as the
number of predators of its eth prey, and Kte as the top-down keystone index of the
eth prey. Within this index, the first and second components represent the bottom-up
(Kbc) and top-down (Kte) effects, respectively. Finally, the keystone index (Ki) cor-
responds to the highest value as a product of the addition of bottom-up (Kbc) and
top-down (Kte) components. For more details on this method, see Jordán (2001) and
Vasas et al. (2007). The Ki index has been shown to be one of the most robust cen-
trality indices (Fedor and Vasas 2009). It is important to indicate that only bottom-
up and top-down components of Ki were used in the current work as a way to
324 M. Ortiz et al.
compare functional indices obtained using Ecosim simulations under comparable

flow control mechanisms.
16.3.3 Semiquantitative or Qualitative Keystone Index
A keystoneness index based on qualitative or semiquantitative loop models was also

calculated. Once the stabilized trophic matrix with Fn < 0 was obtained, the self-
dynamics of each variable corresponding to the principal diagonal were modified to
estimate two new perturbed magnitudes of local stability Fp. Based on the distance
(△) between Fn and Fp as shown in Eq. 16.8
 Fn Fp

it was possible to determine the change provoked by each variable on initial stability
(Fn), thereby obtaining a first qualitative keystone species index (KQiLA1) (selecting
only the largest change by variable). Because Loop Analysis does not consider the
abundance of the components, the difference (Δ) was treated in similar way to
Eq. 16.4 to obtain an additional keystone index (KQiLA2) in which high values of
keystoneness corresponded to variables with low biomass and a high overall effect.
Due to the qualitative-dialectic character of Loop Analysis, the prey-predator inter-
action is captured as a mixed control mechanism.
16.3.4 Centrality of Node Sets
Field studies suggest that in some situations, a small group of species behave as
keystones and they form a keystone species complex (Daily et al. 1993). The impor-
tance of this group is typically realized through their interspecific interaction net-
work, so a network approach to better understand multispecies keystone complexes
is reasonable. A particular approach was suggested by Borgatti (2003a) in order to
find the most central set of k nodes in a network. According to this, a topological
keystone species complex is defined as a solution of the KeyPlayer Problem (KPP)
(sensu Borgatti 2003a). The software KeyPlayer 1.44 (Borgatti 2003b) was used to
compute the importance of species combinations in maintaining the integrity of a
network. The importance of a set of nodes can be calculated by considering either
their fragmentation effect (KPP1) or their reachability effect (KPP2). In the first
case, we identify which k nodes should be deleted from the network of n nodes in
order to maximally increase its fragmentation. In the second case, we identify from
which k nodes the largest proportion of the other n–k nodes are reachable within a
certain distance. Based on fragmentation (F of KPP1), the best set of the deleted k
nodes can maximally increase the fragmentation of the network. This means an
increase of the number of components and a larger average distance generated

within individual components. We used k = 1, 2, and 3 with 10,000 simulations for
each. We also consider the distance-based reachability approach (Rd of KPP2). We
simply count the number of nodes that are reachable within a given distance of m = l
step from a given set of k nodes. We have chosen m = 2 steps and increased the size
of the KP set from k = 1 to k = 3. We applied 10,000 runs for each simulation. The
outcome was three sets of nodes (for k = 1, 2, 3) for each network, containing spe-
cies codes. For each k, the software presents the percentage of nodes outside the KP
set but reachable from it in one step. If this percentage reaches 100%, then the
whole network is reachable from the KP set and we cannot create larger KP sets.
16.3.5 K
eystone Species Complex in Benthic-Pelagic
Ecosystem at Fildes Bay
All individual indices integrated in the holistic keystone species complex (KSCi)
detected keystoneness for a variety of different species and functional groups, with
some agreement. In general terms, keystoneness properties were detected for spe-
cies of all different trophic levels, including primary producers, herbivores, and top
predators. Notably, the topological-structural (Ki) and the functional (KSi) indices
both identified sea stars (SS) as keystone species even though they are based on dif-
ferent algorithms. This outcome agrees partially with the field observations of
Gaymer and Himmelman (2008), who studied dominant sea star species in benthic
communities of northern Chile, establishing Meyenaster gelatinosus as a keystone
species in subtidal systems. Likewise, Ortiz et al. (2013a) determined that most of
the keystone species complexes identified by KSC indices in different ecological
systems along the Chilean coast include one asteroid species as the top predator.
The relevance of the sea star species determined in the present work also coincides
with the results described by Ortiz et al. (2009) regarding the longest system recov-
ery times (as a measure of “resilience”) being obtained in response to perturbations
on these species.
Similarly, both the qualitative and semiquantitative keystone indices (KQiLA1 and
KQiLA2) identified small epifauna (SE) to have keystoneness properties. This result
is very interesting because loop model predictions respond with a high degree of
certainty to external perturbations (Briand and McCauley 1978; Lane and Blouin
1985; Lane 1986; Hulot et al. 2000; Ortiz 2008b). Regarding the functional indices
based on Ecosim dynamical simulations (under three mortality levels and three
types of flow control mechanisms), KSiECOSIM1 and KSiECOSIM2 both identified the
group of Chlorophyta (Chloro), phytoplankton (Phyto), zooplankton (Zoo), the
small epifauna (SE), and the species S. neumayeri (Sn) (grazers) as having key-
stoneness. It is important to mention that it was not possible to determine species or
functional groups with keystoneness properties based on the functional KSiECOSIM2
index under a 30% increased mortality and using a top-down flow control mecha-
326 M. Ortiz et al.
Fig. 16.2 Keystone species complexes (KSC) determined for coastal benthic-pelagic ecosystem at
Fildes Bay (Antarctica) based on quantitative and semiquantitative networks (a) and centrality of
node sets (b). The share components are highlighted (Note: the circle and arrow mean negative and
positive effect, respectively). (Adapted from Fig. 3 in Ortiz et al. 2017)
nism because the model system does not return to initial steady-state conditions,
instead oscillating persistently. The core species as indicated by the keystone species
complex index (KSCi) for the coastal ecological system of Fildes Bay account by
24.2% of the total system biomass (Fig. 16.2a). Importantly, the KSC includes spe-
cies and functional groups that make up an ecological path clearly representing
three trophic levels.
The composition of the KeyPlayer sets is nested: For Fk = 1, the key group is phy-
toplankton (Phyto); for Fk = 2, the key groups are Phyto and benthic fishes (BF); and
for Fk = 3, the key groups are Phyto, BF, and the sea stars (SS). For Rkd=1 , the key
group is Phyto; for Rkd=2 , the key groups are Phyto and BF; and for Rkd=3 , the key
groups are Phyto, BF, and S. neumayeri (Sn). This means that the Phyto-Sn-SS
chain as well as BF together composes a core of species in this community
(Fig. 16.2b). The keystone species complex obtained by multinode centrality
represents 24.4% of the total system biomass, a value quite similar to the previous
approach. The multinode approach based on the KP indices thus not only partly
reinforces the identity of some key players (e.g., S. neumayeri) but also suggests
new key organisms (e.g., zooplankton). This latter result is well supported by the
literature (e.g., Stibor et al. 2004; Murphy et al. 2007). That phytoplankton that was
identified as a component of the KSC could be a consequence of the higher level of
primary productivity in Antarctic waters (Smith et al. 2007; Cornejo-Donoso and
Antezana 2008).
The keystone species complex indices (KSCi) determined for Fildes Bay inte-
grate fewer components than the one determined for the kelp forest of northern
Chile. However, both ecological systems share a sea urchin species (herbivore posi-
tioned at intermediate trophic level), a sea star species (top predator), and the
Chlorophyta (Chloro) (primary producers). After all, the outcomes obtained show
that the components with keystoneness properties in the benthic-pelagic system of
Fildes Bay are widely heterogeneous, coinciding with results reported for other
ecosystems (Power et al. 1996; Piraino et al. 2002; Libralato et al. 2006).
Furthermore, Jordán et al. (2007, 2008) reported similar findings after comparing
several structural and functional keystone species indices. Hermosillo-Núñez et al.
(2018) showed that in spite the wide trophic heterogeneity of components with key-
stoneness properties, it is possible to observe that the core set of species and func-
tional groups are trophically linked. Okey (2004) arrived at similar results by
defining keystone guilds or clusters of species with keystoneness properties based
on a trophic model in Alaska. Thus, we believe that the keystone species complex
index (KSC) for coastal benthic/pelagic ecological systems of Fildes Bay would
facilitate the design and assessment of conservation and monitoring measures, espe-
cially when the Antarctic coastal marine ecosystems are being severely stressed by
the direct effects of the global warming and UV radiation (Richter et al. 2008;
Pessoa 2012). The above notwithstanding, it is necessary also to recognize that the
use of the keystone species complex indices is still quite difficult because the tradi-
tional view of conservation and monitoring efforts is based principally on single
species such as keystone and/or niche-builder or bioengineer species. This mindset
undoubtedly imposes even greater challenges to understand how global changes,
covarying with variability of the natural system, act on networks of interacting
species.
16.4 C
ontribution of Keystone Species Complex
to Macroscopic Network Properties
In global terms, the species and functional group belonging to KSCs showed differ-
ent degrees of contribution to the ecosystem’s emergent properties (i.e., growth,
organization, development, maturity, and health) (Table 16.3). KSC index and cen-
trality of node sets account to lower magnitudes for all macroscopic properties
(Table 16.3). The total biomass of KSCs accounted <25% of the total system bio-
mass, coinciding with the classical keystone concept (sensu Power et al. 1996). A
particular case is the functional group of phytoplankton, which concentrated a little
more biomass, contributing to higher values of TST, AMI, and Ascendency.
Likewise, the functional groups of Chlorophyta (Chloro) and sea stars (SS) pre-
sented the higher percentage magnitudes of Ov/C and TB/TST ratios, mainly con-
tributing – in term of flow – to the system’s resistance against perturbations and to
the whole system’s cycling (promoting efficiency). Different indices for the deter-
328 M. Ortiz et al.
Table 16.3 Contribution of species and functional groups of KSCs on macroscopic network
properties derived from Ascendency (Ulanowicz 1986, 1997) of the coastal benthic-pelagic
ecosystem of Fildes Bay (Antarctica)
TB % TST % AMI % A% Ov/C (%) A/C (%) TB/TST (%)
(a) KSC index
SS 0.658 0.382 0.357 0.357 6.551 3.614 5.953
SE 2.364 4.254 4.743 4.740 5.866 5.943 1.920
Sn 1.226 1.922 2.103 2.104 6.082 5.206 2.204
Chloro 1.369 0.381 0.340 0.340 6.675 3.184 12.402
Phy 10.665 22.283 18.897 18.872 5.398 7.526 1.654
Contribution KSC 16.283 29.223 26.440 26.413 30.572 25.473 24.132
(b) K node sets
BF 1.161 1.146 1.074 1.077 6.308 4.435 3.502
SS 0.658 0.382 0.357 0.357 6.551 3.614 5.953
Sn 1.226 1.922 2.103 2.104 6.082 5.206 2.204
FF 6.309 6.223 6.904 6.910 5.490 7.217 3.503
Zoo 4.355 7.836 7.154 7.155 5.868 5.931 1.920
Phy 10.665 22.283 18.897 18.872 5.398 7.526 1.654
(c) KSC integrated
SS 0.658 0.382 0.357 0.357 6.551 3.614 5.953
Sn 1.226 1.922 2.103 2.104 6.082 5.206 2.204
Phy 10.665 22.283 18.897 18.872 5.398 7.526 1.654
SS sea stars, SE small epifauna, Sn S. neumayeri, Chloro Chlorophyta, Phy phytoplankton, BF
benthic fishes, FF filter feeders, Zoo zooplankton
mination of keystone species complexes (KSCs) are suitable when biomass content
is considered, and it is consistent when using the total flows of matter and/or energy
(TST), the contribution to complexity (AMI), and system development and heath
(Ascendency).
16.5 Constrains and Perspectives
Although we were well aware that the quantitative trophic model built and analyzed
in this study is a partial representation of the overall trophic seascape and interac-
tions underlying the dynamics within Fildes Bay’s coastal benthic/pelagic ecologi-
cal system, such limitations, however, occur in any type of model and are independent
of the model’s degree of complexity (Levins 1966; Ortiz and Levins 2011). In the
present study, the following limitations were identified: (1) The model only repre-
sented the austral summer condition, while the annual benthic/pelagic dynamics are
unknown; (2) system complexity was reduced in relation to the composition of sev-
eral functional groups, although the most abundant macroalgae, herbivore, and car-
nivore species were represented; and (3) regardless of the inherent, well-known
limitations and shortcomings of the Ecopath, Ecosim, Loop Analysis, and KeyPlayer
node sets theoretical frameworks, the constructed model and its dynamic simula-
tions represented underlying system processes based exclusively on short-term or
transient dynamics. In spite of these concerns, we claim that the most relevant tro-
phic relationships and energy/matter flows were well reflected in our model. Here,
the macroscopic properties and sensitive model compartments of the system were
quantified and compared adequately.
Likewise, the core species and functional groups that constituted the keystone
species complexes (KSCs) in the coastal ecological systems at Fildes Bay accounted
to lower magnitudes of total system biomass and macroscopic properties, coincid-
ing with those groups and species identified as keystones in experimental studies
using variations of the original keystone species concept (Menge et al. 1994; Estes
et al. 1998; Bond 2001). Several species or functional groups from different trophic
levels could have keystone properties. This result should not be considered as
ambiguous because populations inhabit heterogeneous and changing environments
(Levins 1968). This insight would support the design of putative conservation and
monitoring strategies in the Antarctic Peninsula, including a core of species or func-
tional groups linked trophically (Jordán et al. 2019), which could supplement the
unique species with keystone properties or those species considered as niche con-
structers (sensu Lewontin and Levins 2007) or bioengineers (sensu Jones et al.
1994). We claim that the adequacy of the description of ecosystem properties based
on only one species or functional group is limited, especially when the task is to
conserve and monitor complex ecosystems (Jordán et al. 2019). In this sense, the
determination of the keystone species complexes (KSCs) could assist within an
ecosystem-based conservation view under an ecological network context (sensu
Pikitch et al. 2004). Finally, it is relevant to assess the trajectory of the target spe-
cies, as they constitute compartments with a relevant role in the structure and tro-
phic functioning of the benthic-pelagic coastal ecosystem at Fildes Bay, Antarctica.
Acknowledgments This research was financed by the grant Proyecto Anillo ART1101

(CONICYT-PIA). We also thank the Instituto Antártico Chileno (INACH) for logistic support. The
work of Ferenc Jordán was supported by National Research, Development and Innovation Office –
NKFIH, grant OTKA K 116071.
330 M. Ortiz et al.
Appendix 16.A
Table 16.4 Parameter values entered (in bold), estimated (standard), and calculated (in italics) by
the Ecopath with Ecosim (EwE) software for the species and functional groups in the coastal
benthic-pelagic ecosystem of Fildes Bay (Antarctica)
Model compartments
Species/functional groups TL B P/B Q/B EE GE
(1) Benthic fishes (BF) 3.03 32.67 2.40 8.50 0.05 0.28
(2) Diplasterias brucei (Db) 2.98 37.83 1.40 5.00 0.18 0.28
(3) Sea stars (SS) 3.29 18.52 1.40 5.00 0.04 0.28
(4) Small epifauna (SE) 2.76 66.50 4.60 15.50 0.95 0.30
(5) Sterechinus neumayeri (Sn) 2.35 34.50 3.70 13.50 0.99 0.27
(6) Margarella sp. (Msp) 2.10 59.50 3.40 11.50 0.99 0.30
(7) Nacella concinna (Nc) 2.05 56.50 3.60 12.50 0.99 0.29
(8) Filter feeders (FF) 2.30 177.46 1.87 8.50 0.93 0.22
(9) Himmantothallus grandifolius (Hg) 1.00 597.67 2.10 – 0.35 –
(10) Desmarestia anceps (Da) 1.00 310.50 2.30 – 0.38 –
(11) Gigartina skottsbergii (Gs) 1.00 35.17 2.50 – 0.42 –
(12) Phaeophyceae (Phaeo) 1.00 650.50 2.80 – 0.39 –
(13) Chlorophyta (Chloro) 1.00 38.50 2.40 – 0.36 –
(14) Rhodophyta (Rhodo) 1.00 174.57 5.00 – 0.32 –
(15) Zooplankton (Zoo) 2.00 122.50 4.60 15.50 0.99 0.30
(16) Phytoplankton (Phy) 1.00 300.00 18.00 – 0.54 –
(17) Detritus (Det) 1.00 100.00 – – 0.07 –
TL trophic level, B biomass (g wet weight m−2), P/B productivity (year−1), Q/B consumption rate
(year−1), EE ecotrophic efficiency (dimensionless), GE gross efficiency (dimensionless)
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Part V
Chemical Ecology
Chapter 17
Chemical Mediation of Antarctic
Macroalga-Grazer Interactions
Charles D. Amsler, James B. McClintock, and Bill J. Baker
Abstract Macroalgal forests along the western Antarctic Peninsula (WAP) support
dense assemblages of small macroalgal-associated invertebrates, particularly
amphipods but also others including gastropods. Most of the macroalgal species,
including all the larger, ecologically dominant brown macroalgae, elaborate chemi-
cal defenses against herbivory to amphipods as well as fish and sea stars.
Consequently, the vast majority of the macroalgal biomass in these forests is unpal-
atable to potential consumers. A great deal of progress has been made on under-
standing these relationships during the past decade. Although the macroalgae are
seldom consumed by the associated invertebrates and fish, many of the inverte-
brates, particularly the amphipods, benefit from associating with the chemically
defended macroalgae because omnivorous fish avoid feeding on them. The amphi-
pods benefit their macroalgal hosts by greatly reducing biofouling by diatoms and
other epiphytic algae. This chapter reviews progress in understanding the chemical
defenses of Antarctic macroalgae. It also reviews the community-wide mutualistic
interaction between macroalgae and its associated amphipods as well as recent stud-
ies examining the extent to which this mutualistic interaction also occurs with
macroalgal-associated gastropods.
Keywords Amphipods · Biofouling · Chemical ecology · Herbivory · Mutualism ·

Trophic dynamics
C. D. Amsler (*) · J. B. McClintock

University of Alabama at Birmingham, Birmingham, AL, USA
e-mail: amsler@uab.edu; mcclinto@uab.edu
B. J. Baker
University of South Florida, Tampa, FL, USA
e-mail: bjbaker@usf.edu

https://doi.org/10.1007/978-3-030-39448-6_17
340 C. D. Amsler et al.
17.1 Introduction
Chemistry has many, often central, roles in important biotic interactions of organ-
isms ranging from bacteria to most if not all groups of eukaryotes (e.g., Eisner and
Meinwald 1995; Waters and Bassler 2005; Dicke and Takken 2006; Wyatt 2014).
Chemical signals mediate a wide variety of forms of communication both within
and between species (e.g., Waters and Bassler 2005; Baldwin et al. 2006; Müller-
Schwarze 2006; Wyatt 2014), and chemical compounds serve as defenses that help
organisms resist predation by herbivores or carnivores (e.g., Müller-Schwarze 2006;
Rosenthal and Berenbaum 2012), defenses against competitors (e.g., Inderjit and
Mallik 2002), and defenses against pathogens or biofoulers (e.g., Lane and Kubanek
2008). Such relationships are widespread in the marine environment (McClintock
and Baker 2001; Breithaupt and Thiel 2011; Brönmark and Hansson 2012; Puglisi
and Becerro 2019).
In marine macroalgae, some studies have examined chemical mediation of inter-
and intraspecific sensory ecology, but much more attention has been focused on
chemical mediation of defensive interactions, particularly defenses against herbiv-
ory (Amsler and Fairhead 2006; Amsler 2008, 2012). In the case of Antarctic mac-
roalgae, while chemical roles in sensory ecology have not been ignored (Zamzow
et al. 2010; Bucolo et al. 2012), the vast majority of studies to date have focused on
the chemical mediation of macroalga-herbivore interactions (Amsler et al. 2008,
2009a, 2014; Avila et al. 2008; Núñez-Pons and Avila 2014; von Salm et al. 2019).
Macroalgae are especially important in shallow water, hard bottom communities
along the northern and north-central regions of the western Antarctic Peninsula
(WAP) where they form undersea forests covering much of the benthos, often with
very high standing biomass (Wiencke and Amsler 2012; Wiencke et al. 2014).
However, their dominance decreases markedly toward the southern half of the WAP
(DeLaca and Lipps 1976; C.D. Amsler, personal observations), and while they are
present at many sites throughout the rest of coastal Antarctica, in these other areas
they are typically not present at the high levels of biomass or percent cover observed
in the northern WAP (Wiencke and Amsler 2012; Wiencke et al. 2014; Clark et al.
2017). To date, almost all studies of the chemical mediation of macroalga-
invertebrate interactions have been performed in macroalgal-dominated communi-
ties along the northern portion of the WAP. Consequently, this chapter focuses on
the northern WAP but includes what is known from other parts of coastal Antarctica.
17.2 Feeding Bioassay Methodology
One of the most basic questions concerning macroalgal interactions with sympatric
invertebrate or vertebrate animals is “do the animals consume the algae?” The stan-
dard methodology to determine if a macroalga or any other potential food item is
palatable to a potential consumer is, conceptually, quite simple and straightforward.
17 Chemical Mediation of Antarctic Macroalga-Grazer Interactions 341
One offers the potential food to a sympatric and otherwise ecologically relevant
potential consumer and asks if it is consumed (Hay et al. 1998). Depending on the
size of the consumer relative to the food item, the feeding bioassay can simply
determine if food item is eaten vs. not eaten or can measure how much is consumed
per unit time, in either case comparing the result to a control food item that is known
to be palatable to the animal.
If a macroalga or other food item is consumed by an animal, depending on the
overall questions being posed, one might ask a variety of specific questions about it
including its nutrient content or digestibility or its relative palatability or nutritive
value relative to other potential foods. If the macroalga is not palatable to the ani-
mal, a relevant question becomes “why not?” There are at least three reasons a
potential food could be unpalatable to a consumer. It might be physically defended
against consumption by being mechanically too tough to eat or by possessing spines
or other physical impediments to consumption (Littler and Littler 1980; Hay 1997).
Although not as common, it is also possible for a potential food item to be of such
low nutritive value that it is not energetically worthwhile for many animals to con-
sume (Bullard and Hay 2002). As further discussed throughout this chapter, a very
common reason that Antarctic macroalgae are unpalatable to sympatric potential
consumers is because of the production of chemical defenses that make them
unpalatable.
To establish a chemical role in feeding deterrence of a macroalga (or any other
possible food), the potential defensive chemicals, which typically are secondary
metabolites (Maschek and Baker 2008), need to be extracted from the macroalga
and used in further feeding bioassays (Hay et al. 1998). The first steps involve sol-
vents likely to extract a wide range of compounds, and the resulting mixtures are
referred to as crude extracts. There are many assumptions underlying extract bioas-
say methods as well as many variations on the extraction and bioassay protocols,
and it is likely that none are “perfect” at reproducing what occurs in nature. Bringing
attention to the various bioassay methods and organisms that have been used in
examining macroalga-consumer interactions in Antarctica and the inherent strengths
and limitations of each is a sub-goal of this chapter. Ideally, the protocol would
produce two or more crude extracts likely to capture all possible lipophilic and
hydrophilic secondary metabolites or other compounds that have a potential to be
responsible for feeding deterrence in intact macroalgal thalli. The assay procedure
would then present them to an ecologically relevant potential consumer in an artifi-
cial food that is as similar as possible to the chemical and nutritive composition of
the original, intact macroalgal thallus.
17.3 Antarctic Macroalgal Resistance to Herbivory
Faced with predation, a macroalga may continue to invest resources in growth and
reproduction at similar levels to those without predation, which is often referred to
as tolerating herbivory (Núñez-Farfán et al. 2007). Alternately they may invest
resources that would otherwise have been used for growth and/or reproduction into
resisting herbivores through the production of physical and/or chemical defenses
(Herms and Mattson 1992). These strategies are not always mutually exclusive
(Arnold and Targett 2003; Núñez-Farfán et al. 2007).
Studies of the palatability of fresh thallus material and/or crude chemical extracts
of WAP macroalgae have utilized amphipods, sea stars, and fish as “taste tester”
animals (Table 17.1). Of these, the amphipods and fish are probably the most eco-
logically relevant potential consumers. The rationale for utilizing sea stars in feed-
ing bioassays is discussed further below (Sect. 17.3.3). Overall, almost all of the
macroalgae that have been used in fresh thallus bioassays with amphipods and/or
fish have been unpalatable to at least one of the animal species (Table 17.1). The
exceptions to this are the small, filamentous brown algae Geminocarpus geminatus
and Elachista antarctica and the red algae Palmaria decipiens and Porphyra ploca-
miestris (Table 17.1). Clearly the vast majority of the enormous live macroalgal
standing biomass on the WAP is unpalatable to these potential and numerous
consumers.
17.3.1 Macroalgal Palatability and Resistance to Amphipods
Amphipods are by far the most numerous and the most speciose group of animals
that associate with macroalgae on the WAP (Richardson 1971, 1977; Huang et al.
2007; Aumack et al. 2011a) although smaller numbers of gastropods, isopods, cope-
pods, and ostracods are also found in association with WAP macroalgae (e.g.,
Amsler et al. 2015; Schram et al. 2016). Currently there are at least 564 known
Antarctic amphipod species (De Broyer and Jażdżewska 2014), and amphipod
abundances are particularly high on finely branched species. Estimated amphipod
densities range up to 308,000 and 32,000 individuals m−2 benthos in stands of the
ecologically dominant, overstory brown macroalgae Desmarestia menziesii and
Desmarestia anceps, respectively (Amsler et al. 2008).
Gondogeneia antarctica (Fig. 17.1a) is a member of family Pontogeneiidae and
one of the best-studied shallow water Antarctic amphipods overall (e.g., Obermüller
et al. 2007; Doyle et al. 2012; Kang et al. 2015). As one of the most common amphi-
pods which associate with macroalgae (Richardson 1971, 1977; Huang et al. 2007;
Aumack et al. 2011a; Barrera-Oro et al. 2019), it has been used extensively in feed-
ing bioassays with WAP macroalgae (Table 17.1) and also with some benthic mac-
roinvertebrates (Ma et al. 2009; Amsler et al. 2009c; authors’ unpublished data). In
nature, the diet of G. antarctica consists largely of diatoms, but it also includes
macroalgae, particularly filamentous algae and Palmaria decipiens, as an important
diet component (Aumack et al. 2017; Zenteno et al. 2019). In feeding bioassays,
G. antarctica readily consumes filamentous macroalgae; artificial foods using
freeze-dried, ground, filamentous macroalgae as a feeding stimulant; and P. decipi-
ens (Table 17.1). One disadvantage of the use of this amphipod in feeding bioassays
with macroalgal extracts in artificial foods is that in some instances, it is probably
Table 17.1 Summary of fresh WAP macroalgal thalli and crude extract bioassays with amphipods, sea stars, and fish
Amphipods Sea star Fish
Gondogeneia antarctica Cheirimedon femoratus Other species Odontaster validus Notothenia coriiceps
Macroalgal species Thal LpEx HpEx LpEx Thal LpEx HpEx Thal LpEx HpEx Thal LpEx HpEx
Class Phaeophyceae
Adenocystis utricularis a3 r3 a5 r3 r3 a8 a3 r3 a3 a3
1
Ascoseira mirabilis r a3 a3a r5 a3 a3 r8 a3 r3 a3 r6
Chordaria linearis r3
Cystosphaera jacquinotii a3 r3 r3 r3 r3 r3 r6
1 5 7 3
Desmarestia anceps r a3 r3 r r r3 a3,8 r3 r3 a r3,6
Desmarestia antarctica r1 a3 r3 r3 r3 r3 r3 a3
Desmarestia menziesii r3 a3 r5 r7 r3 r3 a8 a3 r3 r3 a3 r6
4
Elachista antarctica a a4
Geminocarpus geminatus a1 a3
Halopteris obovata r2 a2,3 a2,3 r2 a2 a2 a3 r3
Himantothallus grandifolius r1 r3 r3 r3 r3 r3 r3 a3 r3,6
Phaeurus antarcticus r3 r3 a3 r3
Class Rhodophyceae
Austropugetia crassab a3 r3 r3 a3 a3 r3 r3
Callophyllis atrosanguinea a3 a3 r3 a3 r3 r3 a3
17 Chemical Mediation of Antarctic Macroalga-Grazer Interactions
Curdiaea racovitzae r1 a3 a3 r3 r3 r3 r3
Cystoclonium obtusangulum r2 r2 r2 r2,7 r2 r2
Delisea pulchra r3 a3 r7 r3 r3 a3 r3
5
Georgiella confluens r a3 r8
Gigartina skottsbergii r1 r5 a3 a8 a3
3 3
Gymnogongrus antarcticus a a a3 r3
Gymnogongrus turquetii r1 r3 r3 r3 a3 r3 r3 r3 a3
Iridaea cordata r1 a3 r3 r3 a3 r3
343
(continued)
344
Amphipods Sea star Fish

Gondogeneia antarctica Cheirimedon femoratus Other species Odontaster validus Notothenia coriiceps
Macroalgal species Thal LpEx HpEx LpEx Thal LpEx HpEx Thal LpEx HpEx Thal LpEx HpEx
Myriogramme mangini r1 a3 a3 r3 r3 a3 r3
1 3 3 3
Myriogramme smithii r r a3 r r r3 r3 r3 a3
3
Nereoginkgo adiantifolia a
Palmaria decipiens a1,2,3 a2 a2 r5 r2,4 a4 a2 a2 a3 a3
Pantoneura plocamioides r2 r2 r2 r2,7 r2 a2 a3 r3 a3 a3
Paraglossum amsleri b a3 r3 r3 a3 a3
3 3
Paraglossum salicifolium b r3 r3 r a r3 r3 r3 a3
3
Phycodrys austrogeorgica a
Picconiella plumosa r2 r2 r2 r2 a7 r2 r2 a3 r2 a3
Plocamium cartilagineum r2,7 r2,3 r2,3 r2,7 a7 r2 a2 r3 r3 r3 r3 r3 a3
3 3
Plumariopsis peninsularis a3 r3 r r a3 r3 a3
3
Porphyra plocamiestris a a3
Trematocarpus antarcticus r1 a3 a3 r3 a3 a3 r3 a3 a3
Varimenia macropustulosa b r1 a3 a3 r3 a3 a3 r3
Class Ulvophyceae
Lambia antarctica a3 a3 r3 a3 a3 a3
Thal fresh thallus bioassays, LpEx lipophilic extract bioassays, HpEx hydrophilic extract bioassays, a thallus or extract in artificial food accepted in bioassay,
r thallus or extract in artificial food rejected in bioassay. Superscript numbers = references (see table endnote).
1
Amsler et al. (2009b), 2Aumack et al. (2010), 3Amsler et al. (2005), 4Bucolo et al. (2011), 5Núñez-Pons et al. (2012), 6Iken et al. (2009), 7Amsler et al. (2013),
8
Núñez-Pons and Avila (2014)
Prior names in Amsler et al. (2005): Austropugetia crassa as undescribed sp. 1, Paraglossum amsleri as Delesseria lancifolia, Paraglossum salicifolium as
Delesseria salicifolia, Varimenia macropustulosa as Pachymenia orbicularis in Amsler et al. (2005) and undescribed species A in Amsler et al. (2009b).
Pachymenia orbicularis was a misidentification in Amsler et al. (2005). The other changes resulted from taxonomic revisions.
a
Water-soluble, apparently activated defense inhibits feeding (McDowell et al. 2014b).
b
All or some bioassay data published under other species name (see table endnote).
C. D. Amsler et al.
Fig. 17.1 Common potential consumers of macroalgae on the western Antarctic Peninsula: (a)
Gondogeneia antarctica; (b) Paradexamine fissicauda; (c) Odontaster validus; (d) Notothenia
coriiceps. (Photos (a) and (b) by M.O. Amsler, (c) and (d) by B.J. Baker)
conservative in identifying crude extracts with feeding deterrence. In these feeding

bioassays, the extracts by themselves – presumably because of primary metabolites
therein – are commonly preferred over control foods at statistically significant lev-
els (Amsler et al. 2005; Schram et al. 2015). Indeed, when either lipophilic or
hydrophilic crude extracts of the filamentous green alga Cladophora repens, which
is the feeding stimulant usually used in the artificial foods, are added to the artificial
foods, they are significantly preferred to the C. repens-based artificial foods without
extracts (Amsler et al. 2005). Consequently, if there is no significant difference
between feeding rates on control and extract-containing artificial foods in a bioas-
say, could the extracts actually have been deterrent, but not enough to overcome the
inherent extra palatability of the extracts in general? Halopteris obovata and
Varimenia macropustulosa are species that were unpalatable to G. antarctica as
fresh thallus but in which feeding on one or both crude extracts was not significantly
different from the control food (Amsler et al. 2005; Aumack et al. 2010). This was
also true of Ascoseira mirabilis (Amsler et al. 2005), but there is an additional pos-
sible explanation for this as discussed below. Fresh thallus feeding bioassays using
G. antarctica have not been done with Callophyllis atrosanguinea, but it is unpalat-
able as fresh thallus to sea stars and fish (Table 17.1). There was no significant
preference of G. antarctica for either of its crude extracts (Amsler et al. 2005) sug-
gesting that there might be chemically based deterrence to amphipod herbivory.
There is a similar situation with Lambia antarctica although it is only unpalatable
as fresh thallus to sea stars (not to fish; Table 17.1) and only its hydrophilic crude
extract was not significantly different from the control food in feeding bioassay with
G. antarctica (Amsler et al. 2005).
Cheirimedon femoratus is the second most common amphipod that has been
used in feeding bioassays of Antarctic macroalgal extracts (Table 17.1). It is a mem-
ber of family Lysianassidae, which primarily consists of detritivores and necrovores
(Bousfield 1973). Consistent with that, it is commonly found in baited fish traps and
probably prefers carrion as a food when available (Bregazzi 1972). However, it also
feeds on detrital algal material, particularly as juveniles and ovigerous females
(Bregazzi 1972). Based on stable isotope analysis, Zenteno et al. (2019) classified
this species as a scavenger and reported a particularly high isotope signature appar-
ently originating from intertidal macroalgal sources. Cheirimedon femoratus has
been reported to be most common on sandy bottoms but also associated with rocky
substrata (Bregazzi 1972). Núñez-Pons et al. (2012) report that it associates with
live macroalgae at Deception Island (63°S latitude). Our group has examined liter-
ally hundreds of thousands if not more macroalgal-associated amphipods from
Anvers Island (64°S latitude) as well as smaller numbers from as far south as 68°S
and never found C. femoratus – indeed only very few members of its family (Huang
et al. 2007) – associated with macroalgae. However, we have sometimes found it
from Anvers Is. (but not further south) in airlift samples that included substratum
material from macroalgal communities as well as occasionally in baited fish traps
(authors, unpublished) suggesting that it is present in the macroalgal communities,
probably associated with the substratum, but not on the upright portions of the mac-
roalgae. Richardson (1977) reported very small numbers of C. femoratus relative to
other species associated with the overstory brown alga D. anceps at Signy Island
(60°S latitude), but his samples included holdfasts which ours usually did not. At
King George Island (62°S latitude), C. femoratus has been reported in low numbers
from samples including both macroalgae and surrounding substratum but com-
monly in the guts of fish from these communities (Barrera-Oro et al. 2019).
Even though Cheirimedon femoratus does not associate with intact macroalgae
in many locations along the WAP and as such may not be a primary factor in select-
ing for chemical defenses in the algae, the palatability of detached and degrading
macroalgal material to this amphipod is likely to be relevant to the flow of carbon
into the surrounding communities. Macroalgae, probably as detritus, are an impor-
tant carbon source to a wide variety of animals in these communities (Dunton 2001;
Corbisier et al. 2004; Aumack et al. 2017; Braeckman et al. 2019; Zenteno et al.
2019). Once dead, chemically defended brown macroalgae can begin to become
palatable to G. antarctica and probably other amphipods after a period of weeks
(Reichardt and Dieckmann 1985; Amsler et al. 2012a). However, they can survive a
very long time after being detached (Brouwer 1996; Amsler et al. 2012a), and drift
thalli probably need to be buried in sediments and begin microbial decomposition
to become palatable to many animals (Braeckman et al. 2019).
Cheirimedon femoratus has only been used in feeding bioassays with lipophilic
macroalgal extracts, but the results of those bioassays are generally comparable to
lipophilic extract feeding bioassays using Gondogeneia antarctica (Table 17.1).
One difference is that feeding deterrence of Desmarestia anceps to G. antarctica
was only in the hydrophilic extract while a lipophilic extract was unpalatable to
C. femoratus. It is possible that this is attributable to different extraction procedures
in the two studies (Amsler et al. 2005; Núñez-Pons et al. 2012) which could have
resulted in the compounds responsible for the response partitioning differently. A
second difference is that extracts of A. mirabilis were unpalatable to C. femoratus
but not to G. antarctica (Table 17.1), but as noted above, the conservative nature of
the G. antarctica extract bioassay could have resulted in a false negative. A more
perplexing difference is that the extract of P. decipiens was unpalatable to C. femo-
ratus (Núñez-Pons et al. 2012) since in our experience it is one of the few generally
palatable macroalgae in the community. It is readily consumed as fresh thallus by
G. antarctica (Amsler et al. 2009b, 2013; Aumack et al. 2010; Bucolo et al. 2011),
by the amphipod Oradarea bidentata (Bucolo et al. 2011), and by sea stars and fish
(Table 17.1). It is not palatable as fresh thallus to the amphipods Prostebbingia
gracilis and Paraphimedia integricauda (Aumack et al. 2010; Bucolo et al. 2011),
but this is almost certainly because of biophysical limitations since P. gracilis pref-
erentially consumes extracts of P. decipiens (Aumack et al. 2010) and P. integri-
cauda, which consumes primarily diatoms, has a mandible morphology unsuited for
grinding macroalgal thalli (Aumack et al. 2017).
Although the vast majority of WAP macroalgae are unpalatable to amphipods,
usually because of chemical defenses (Table 17.1), there is one amphipod species
known to consume otherwise chemically defended macroalgae. Plocamium
“cartilagineum”1 is unpalatable as thallus to the amphipods Gondogeneia antarc-
tica, Prostebbingia gracilis, Paraphimedia integricauda, Oradarea bidentata, and
Schraderia gracilis but readily consumed by Paradexamine fissicauda (Fig. 17.1b)
(Amsler et al. 2013). The unpalatability to most species is clearly due to defensive
chemistry as its extracts are highly deterrent in feeding bioassays with G. antarctica
and P. gracilis (Amsler et al. 2005; Aumack et al. 2010) as well as with sea stars and
fish (Table 17.1). Paradexamine fissicauda is also able to consume Picconiella plu-
mosa (Amsler et al. 2013) which is unpalatable both as fresh thallus and as crude
extracts to G. antarctica and P. gracilis (Aumack et al. 2010). However, P. fissi-
cauda does not consume the chemically defended red algae Pantoneura plocamioi-
des, Cystoclonium obtusangulum, or Delisea pulchra or the chemically defended
brown algae Desmarestia menziesii or Desmarestia anceps (Amsler et al. 2013).
Predators that are able to consume chemically defended organisms including mac-
roalgae are generally only able to do so in single species or in closely related taxa
with similar or identical defensive metabolites because the biochemical pathways
they use to detoxify and/or excrete the defensive metabolites are relatively com-
pound specific (Sotka and Whalen 2008; Sotka et al. 2009). Plocamium “cartilag-
ineum” and P. plumosa are in separate taxonomic orders (Plocamiales and
Ceramiales, respectively; Hommersand et al. 2009) which are not closely related
and which were recently estimated to have been divergent for close to 400 million
years (Yang et al. 2016). Although separate or convergent evolution of secondary
metabolites is not common, it does occur (e.g., Daly 2004; Cutignano et al. 2012),
1
This entity is genetically distinct from P. cartilagineum found elsewhere and certainly represents
a separate species, but to date, no formal alternative name has been proposed (Hommersand
et al. 2009).
and it is possible that defensive metabolites of P. “cartilagineum” and P. plumosa

are similar enough to allow both to be eaten by P. fissicauda. Paradexamine fissi-
cauda does not simply detoxify the halogenated secondary metabolite defenses of
P. “cartilagineum” but also incorporates at least some of them into its tissues where
they appear to deter predation on the amphipods by fish (Amsler et al. 2013).
Although such sequestration of chemical defenses from the diet for use by the con-
sumer as a defense against its own predators is known in terrestrial arthropods
(Eisner and Meinwald 1995) and in marine systems from some opisthobranch mol-
luscs (reviewed by Jormalainen and Honkanen 2008; Cimino and Ghiselin 2009;
Hay 2009), we are not aware of other examples of this phenomenon in marine
organisms.
While chemical defenses against amphipod herbivory are clearly very common
in WAP macroalgae, we know specific compounds involved in that unpalatability in
only a few cases. Purified phlorotannins from both Desmarestia anceps and
Cystosphaera jacquinotii (but not several other brown algae) are deterrent in feed-
ing bioassays with Gondogeneia antarctica (Iken et al. 2009) which is consistent
with the deterrence observed in the hydrophilic crude extracts of these species
(Table 17.1). Two halogenated monoterpenes, anverene and epi-plocamene D, from
Plocamium “cartilagineum” have been shown to deter feeding by G. antarctica
(Ankisetty et al. 2004). Antarctic P. “cartilagineum” produces a large number of
halogenated secondary metabolites (Young et al. 2013), and it is likely that addi-
tional compounds contribute to the strong unpalatability of this species in most
feeding bioassays. Similarly, it is possible that more than phlorotannins are respon-
sible for feeding deterrence in D. anceps or C. jacquinotii, particularly if differential
extraction is responsible for the differences discussed above between responses of
Cheirimedon femoratus and G. antarctica to crude extracts of D. anceps.
Secondary metabolites are not the only molecules that can be involved in chemi-
cal defense. For example, reactive oxygen species (ROS) are known to be involved
in defense against pathogens in a variety of macroalgae (Potin 2008; Thomas et al.
2014). Recent evidence suggests that this is probably true in Antarctic macroalgae
and also that ROS has the potential to be involved in deterring predation by small
grazers such as amphipods. Nine of 13 WAP macroalgae accumulated ROS within
their tissues within 70 min of wounding, and four of five species tested released
strong oxidants into the surrounding seawater within 1 min of wounding (McDowell
et al. 2014a). Palmaria decipiens, the only macroalgal species tested that is eaten by
Gondogeneia antarctica, increased ROS production at the site of grazing by G. ant-
arctica (McDowell et al. 2014a). Although P. decipiens is consumed as fresh thallus
by G. antarctica, as already noted, Ascoseira mirabilis is not (Table 17.1). Ascoseira
mirabilis produces ROS upon wounding in the light but not in the dark (McDowell
et al. 2016), and wounded A. mirabilis inhibits feeding of G. antarctica on P. decipi-
ens disks within the same experimental container (McDowell et al. 2014b). Although
hydrogen peroxide does not appear to be part of the ROS response in A. mirabilis,
it is in other Antarctic macroalgae (McDowell et al. 2014a), and addition of hydro-
gen peroxide at concentrations comparable to those released by macroalgae also
inhibits feeding by G. antarctica (McDowell et al. 2014b). ROS production in the
light has been shown to be dependent on photosynthetic electron transfer in a tem-

perate kelp species, and this is probably true in P. decipiens and A. mirabilis as well
(McDowell et al. 2015). The light dependence of this potential defense against her-
bivores likely has ecological consequences as amphipods are active and probably
feeding at night (authors’ personal observations). This includes species such as
G. antarctica moving off of chemically defended hosts to the palatable species
P. decipiens at night, presumably to feed (Aumack et al. 2011a).
17.3.2 Macroalgal Palatability and Resistance to Fish
The species of fish most commonly observed in WAP macroalgal forests, Notothenia
coriiceps (Fig. 17.1d), commonly has macroalgae in its guts when collected from
macroalgal communities (e.g., Iken et al. 1997; Zamzow et al. 2011) and apparently
selectively feeds on some macroalgal species including Palmaria decipiens (Iken
et al. 1997). In feeding bioassays with fresh thallus material, P. decipiens is one of
only four of 28 species tested that was consumed by N. coriiceps (Table 17.1). We
have observed N. coriiceps taking bites out of P. decipiens in laboratory aquaria and
observed P. decipiens individuals in nature with similar, apparent bites missing from
the thallus (authors, unpublished). Of the other three subtidal WAP macroalgal con-
sumed by the fish as fresh thallus, Porphyra plocamiestris is in a genus that is com-
monly palatable to animals, including humans, and is very thin and easily torn. It is
not surprising that it is palatable to the fish. Lambia antarctica is palatable as extract
to both amphipods and sea stars (Table 17.1) indicating no apparent chemical
defenses although it was rejected as thallus by sea stars (Table 17.1). Lambia ant-
arctica is not as physically tough as P. decipiens (Amsler et al. 2005) suggesting
that N. coriiceps should be able to bite off pieces of its thallus as it does with
P. decipiens. The fourth species the fish consumed as thallus, Gigartina skottsbergii
(Table 17.1), is different. It was the physically toughest of 30 species tested for
puncture resistance by Amsler et al. (2005). Although the fish swallowed the small
pieces used in the feeding bioassays, we believe that it is very unlikely that they
could remove pieces of thallus from an intact G. skottsbergii blade in nature.
Fewer extract feeding bioassays have been performed with Notothenia coriiceps
than with the amphipod Gondogeneia antarctica or sea star Odontaster validus
(Table 17.1). Of the 24 macroalgal species known to be unpalatable to N. coriiceps,
extract bioassays have not been performed with seven. Of the other 17 species,
extract bioassays indicate that chemical defenses can explain the unpalatability in
10. In four others, only one crude extract type has been bioassayed (Table 17.1), so
it is possible that defensive compounds could have been present in the other extract.
Only three species that were rejected as thallus have had both crude extract types
tested and shown to be palatable to the fish including Trematocarpus antarcticus
which similarly is unpalatable as thallus but not as either crude extract to amphipods
and sea stars (Table 17.1).
The only purified compounds that have been shown to deter feeding of Notothenia
coriiceps to date are phlorotannins. The strongest deterrent response was seen with
phlorotannins from Desmarestia menziesii, but pure phlorotannins from
Cystosphaera jacquinotii were also significantly rejected by the fish (Iken et al.
2009). It is important to note that these assays were done with isolated phlorotan-
nins, not simply methanolic extracts that would be enriched in phlorotannins and
are commonly what is used in “phlorotannin” feeding bioassays even though they
also contain other compounds (Amsler and Fairhead 2006). Such methanolic
extracts of Desmarestia anceps and Ascoseira mirabilis deterred N. coriiceps, but
the deterrence was lost when the extracts were purified further with other solvents
and a microcellulose column (Iken et al. 2009).
17.3.3 Macroalgal Palatability and Resistance to Sea Stars
The sea star Odontaster validus (Fig. 17.1c) is one of the most common benthic
invertebrates throughout much of coastal Antarctica (Janosik and Halanych 2010)
and is typically present in WAP macroalgal communities (Dearborn and Fell 1974).
Although sea stars are usually not considered as macroalgal predators, O. validus
was one of two species out of 20 WAP sea stars surveyed that had macroalgae in its
guts (McClintock 1994). Although rare, we have personally observed O. validus
individuals with their cardiac stomachs extended over macroalgal thalli with epi-
phytes, but it seems most probable that macroalgae reported within their guts came
from detrital fragments. So although it appears unlikely that sea star predation
would have been important in selecting for the production of chemical defenses, the
fact that they do not bite into their prey as amphipods and fish do could mean that
thallus toughness is not as important a factor in their food choices. Fresh thallus
bioassays with them, therefore, could provide useful biophysical information rela-
tive to feeding deterrence observed in other predators. The feeding bioassay system
our group uses with O. validus (Amsler et al. 2005) is relatively quick and, for crude
extract bioassays, can use artificial foods leftover from preparation of foods for
amphipod or fish bioassays, providing comparative information on chemical deter-
rence in a separate predator.
To date, more fresh thallus bioassays with different macroalgal species (35) have
been done with Odontaster validus than with either amphipods or fish (Table 17.1).
Of those 35 species, fresh thallus was consumed by O. validus in 13 of the species,
a much higher acceptance rate than in fresh thallus assays with amphipods or fish
(Table 17.1). Five of the 13 species accepted by the sea star were rejected as thallus
by one or more of the amphipod species or fish and in several of these instances,
crude extract bioassays with one or more of the other species did not explain the
unpalatability (Table 17.1). The O. validus assay results in these instances would be
consistent with the thallus unpalatability to amphipods or fish being biophysi-
cally based.
The two studies that have examined the palatability of lipophilic macroalgal
extracts with Odontaster validus (Amsler et al. 2005; Núñez-Pons and Avila 2014)
used not only different extraction solvent systems, as discussed previously (Sect.
17.3.1) for studies on amphipods by the two different research groups, but also
markedly different bioassay procedures. It is probably not surprising that results
differed in three of the four macroalgal species assayed in both studies (Table 17.1).
One other difference between the two studies was in the composition and extract
loading of the artificial foods. Amsler et al. (2005) coated extracts onto freeze-dried
powder of a palatable, intertidal, filamentous Antarctic green alga (Cladophora
repens) that was then incorporated into alginate-based foods. The “natural concen-
tration” of the extract was calculated on a volumetric basis relative to the volume of
the final artificial food pellet. The pellets were 5% dry C. repens powder in 2%
alginate which based on Peters et al. (2005) should have contained approximately
2% protein. That protein content is within but at the lower end of the range observed
for 36 species of WAP macroalgae (Peters et al. 2005). Núñez-Pons and Avila
(2014) used artificial foods composed of cubes of non-Antarctic shrimp which were
12.4% protein, a level at the very top of the range of protein contents in WAP mac-
roalgae (Peters et al. 2005). The lipophilic extracts were added on a dry weight basis
to the outside of the shrimp cubes, and while some would have soaked in, most
would have been retained near the surface which is the only place “tasted” by a
nonbiting sea star predator. So while the foods themselves were higher in nutritional
value – and, therefore, potentially more attractive foods – compared to those used
by Amsler et al. (2005), the potentially unpalatable extracts added to them were
probably presented to the sea stars at higher concentrations. Another difference
between the studies is that the Amsler et al. (2005) assay placed food items onto the
sea stars’ chemosensory tube feet and recorded whether or not the food that had
been “tasted” was moved to and retained at the mouth. Núñez-Pons and Avila (2014)
placed the sea stars on top of the food cubes and recorded whether they were con-
sumed in 24 hours, which captures the full complement of feeding behaviors (“tast-
ing” followed by consumption) and is probably a more ecologically robust bioassay
approach.
Purified phlorotannins from Desmarestia menziesii and Himantothallus grandi-
folius but not from five other brown macroalgal species significantly deter feeding
by Odontaster validus (Iken et al. 2009). Desmarestia menziesii also produces a
quinone derivative, menzoquinone, which deters O. validus feeding in bioassays
(Ankisetty et al. 2004).
17.3.4 M
acroalgal Palatability and Resistance to Sea Urchins
in McMurdo Sound
As discussed in Sect. 17.1, macroalgae occur throughout coastal Antarctica although

their biomass, percent cover of the bottom, and species richness all become lower
south of the northern WAP (Wiencke and Amsler 2012; Wiencke et al. 2014). Only
two species of fleshy macroalgae, Phyllophora antarctica and Iridaea cordata,

occur throughout most of the year at the southernmost extent of macroalgal distribu-
tion (and seasonally open water) in McMurdo Sound (Ross Sea; Miller and Pearse
1991). The sea urchin Sterechinus neumayeri is a very common and important con-
sumer in McMurdo Sound as well as throughout much of the rest of Antarctica
(Pearse and Giese 1966; Pawson 1969; Saucède et al. 2014) and an obvious poten-
tial predator on P. antarctica and I. cordata in McMurdo Sound. Unfortunately,
S. neumayeri does not reliably or reproducibly consume anything we have tested it
with in laboratory aquaria, and so typical feeding bioassays are not practical with it
because of the high variability caused by many animals not eating at all. To get
around this limitation, Amsler et al. (1998) developed a “phagostimulation” bioas-
say which measured how long a small disk of algal thallus or crude extracts on
feeding-stimulant-containing filter paper disks were retained at the urchins’ mouths
when forcibly placed there. While far from an ideal assay, the responses were quite
strong which allowed for statistically robust outcomes. Thallus disks from both spe-
cies were retained at the mouth less than half as long as a paper disk without feeding
stimulants. Both lipophilic and hydrophilic extracts added to filter paper disks with
a feeding stimulant were rapidly rejected, while solvent controls were retained at
the mouth for several-fold longer times, indicating that the unpalatability of fresh
thalli is chemically based (Amsler et al. 1998).
Even though Sterechinus neumayeri does not consume Phyllophora antarctica
or Iridaea cordata, it prefers to cover itself with them over other potential cover
objects if the algae are present (Amsler et al. 1999). Either the macroalgae or other
objects used as cover help protect S. neumayeri from predatory sea anemones by
acting as a detachable “shield” that the anemones’ tentacles stick to, allowing the
urchins to release the cover material and escape (Dayton et al. 1970; Amsler et al.
1999). The algae also benefit from this relationship because they are the preferred
cover items for the urchins. Anchor ice tears macroalgal thalli from the rock substra-
tum, and most of the algal biomass in the communities are held by urchins rather
than being attached to the rock substratum (Dayton et al. 1969; Miller and Pearse
1991; Amsler et al. 1999). The algae so retained within the photic zone remain
physiologically active (Schwarz et al. 2003) as well as reproductive (Amsler et al.
1999) and probably are responsible for most of the spore and gamete production
which maintains the populations.
17.4 M
acroalga-Invertebrate Interactions on the Western
Antarctic Peninsula
As discussed in Sect 17.3.1, amphipods are the most abundant invertebrates associ-
ated with WAP macroalgae. As also discussed in Sect. 17.3.1, the vast majority of
macroalgal species deter predation by amphipods using chemical defenses. This
includes all of the large, ecologically dominant brown macroalgae as well as most
of the common red macroalgae. Consequently, the vast majority of the WAP mac-
roalgal biomass is not available or, at least, not at all preferable, as food to the dense
amphipod assemblage. Although the amphipods are not consuming most of the
large macroalgae, they do consume epiphytic microalgae, filamentous algal epi-
phytes, and emergent filaments from endophytic algae (Amsler et al. 2009b, 2012b;
Aumack et al. 2011b, 2017) and thereby clearly benefit their macroalgal hosts by
sustaining photosynthesis, gas exchange, and nutrient uptake capacities. In addition
to consuming the smaller algae, the amphipods also benefit from associating with
the chemically defended macroalgae by gaining a refuge from an important preda-
tor, the common benthic fish Notothenia coriiceps (Zamzow et al. 2010, 2011).
Because macroalgae are the major structural component and primary producers in
these communities and because amphipods are the most abundant invertebrates, we
have previously described this association as a community-wide mutualism (Amsler
et al. 2014). This relationship is presented diagrammatically in the upper half of
Fig. 17.2. None of the individual components of this mutualism are unique to the
WAP, and comparisons and contrasts of the WAP communities to specific lower-
latitude communities are discussed at length by Amsler et al. (2014). However, the
overall importance of these two groups of organisms – the macroalgae which domi-
nate in terms of structure and primary productivity and the amphipods which are by
far the most abundant animals – to these nearshore communities makes the interac-
tion uniquely important compared to such interactions in lower-latitude communi-
ties (Amsler et al. 2014).
In addition to the “bottom-up” benefits to amphipods from gaining an associa-
tional refuge from fish predation, it is possible that the very high densities of amphi-
pods associated with macroalgae result in part from “top-down” influences of
predators on fish that prey on amphipods. Notothenia coriiceps is a benthic ambush
predator with relatively small home ranges (e.g., Daniels 1982; North 1996;
Campbell et al. 2008). Although it is common along the bottom beneath the mac-
roalgal canopy, it is rarely observed by divers up off the bottom within the canopy
(Casaux et al. 1990; authors’ personal observations). The smaller Harpagifer ant-
arcticus is found associated with small rocks in Antarctic macroalgal forests and is
also an amphipod predator with a cryptic lifestyle (Daniels 1983; Casaux 1998).
Several seal species including leopard seals have been observed with fish in their
gut contents or scat (Hall-Aspland and Rogers 2004; Casaux et al. 2009), and mem-
bers of our research group have observed and photographed leopard seals eating
N. coriiceps in shallow water (A. Shilling, personal communication). It is reason-
able to hypothesize that the cryptic behavior of the fish represents a nonconsumptive
effect of seal predators and thereby reduces predation on amphipods and other
macroalgal-associated invertebrates.
Another feature of these communities that is at least somewhat unique is that
free-living filamentous algae are very uncommon throughout most of the year in the
subtidal zone but filamentous algae are very common growing as endophytes within
subtidal macroalgae (Peters 2003; Amsler et al. 2009b). Filamentous macroalgae
are frequently observed in the WAP intertidal (e.g., Lamb and Zimmerman 1977;
Marcías et al. 2017; Valdivia et al. 2019), indicating that there is nothing about
Fig. 17.2 Schematic
representation of species
interactions between algae
and amphipods on the
western Antarctic
Peninsula. See text for
details. + indicates a
positive effect, 0 indicates
no effect, and − indicates a
negative effect. (From
Amsler et al. (2014). Used
with permission)
Antarctica that excludes free-living filamentous algae. Peters (2003) noted that
escape from herbivory has long been hypothesized as a selective factor favoring
endophytism (e.g., Kylin 1937) and postulated that the dense assemblages of amphi-
pods on subtidal WAP macroalgae probably selected for this pattern of filamentous
algae rarely being free-living but commonly being endophytic in the WAP subtidal.
This is potentially problematic with respect to the idea of WAP macroalgae and
amphipods being mutualists. While not always true (e.g., Gauna et al. 2009), fila-
mentous algal endophytes are commonly pathogenic to their macroalgal hosts (e.g.,
Apt 1988; Correa and Sánchez 1996; Faugeron et al. 2000). If such pathogenicity is
common in WAP endophytes and endophytism is driven by amphipod herbivory,
could amphipods truly be viewed as beneficial to the larger macroalgae? Schoenrock
et al. (2013) performed field experiments which showed that while endophytes
could reduce growth and/or survival of some species of macrophytes when present
in very high densities within the macroalgal thalli, this was not always true. In the
most heavily impacted species in terms of growth, Iridaea cordata, there was no
corresponding correlation between endophyte load and the density of either carpo-
sporangia or tetrasporangia, indicating no pathogenic impact on fecundity
(Schoenrock et al. 2015b). In laboratory experiments on nine macroalgal species,
almost no pathogenic impacts were seen on photosynthetic physiology, thallus
toughness, or susceptibility to grazers, and the few significant effects observed were
very mild (Schoenrock et al. 2015a). Consequently, although endophytes can some-
times be detrimental to their larger macroalgal hosts, overall, this almost certainly
does not negate the benefit macroalgae gain from having the dense assemblage of
associated amphipods (Fig. 17.2).
Although often not as abundant as amphipods, small gastropods are also com-
monly observed associated with WAP macroalgae (Richardson 1977; Picken 1979,
1980; Iken 1999; Amsler et al. 2015). Gastropods commonly consume microalgae
and filamentous macroalgae (Purchon 1977; Santhanam 2018) and consequently
could be analogous to amphipods in providing benefits to their macroalgal hosts by
controlling epiphytic algae (see also Chaps. 12 and 13). They may be particularly
important on the upper surfaces of large, blade-forming macroalgae such as

Himantothallus grandifolius and Gigartina skottsbergii where amphipods are not as
common as gastropods, at least during daylight hours (authors’ personal observa-
tions). Amsler et al. (2019) performed a mesocosm experiment which maintained
H. grandifolius blade sections either with no gastropods or with densities of gastro-
pods corresponding to natural gastropod densities on H. grandifolius. A very similar
mesocosm experiment had previously been done with or without natural densities of
amphipods by Aumack et al. (2011b). The gastropods controlled epiphytic diatom
densities on H. grandifolius blades (Amsler et al. 2019) but not to the extent that
amphipods were observed to do so for H. grandifolius (Aumack et al. 2011b). No
grazing marks from the gastropods were ever observed on the H. grandifolius thalli
either in the mesocosms or in an accompanying laboratory experiment, but almost
all of the gastropod species have radulae that are probably not able to rasp the tough
thalli of H. grandifolius (Amsler et al. 2019). That is unlikely to be the case for the
limpet Nacella concinna which was present in the experiment and has a very tough,
minerally hardened, chitinized radula. This limpet is presumably deterred from con-
suming its H. grandifolius hosts by the same chemical defenses observed to deter
feeding in other sympatric predators (Table 17.1).
The fish Notothenia coriiceps often consumes gastropods in addition to amphi-
pods in macroalgal communities (Zamzow et al. 2011). Although small gastropods
on chemically defended, branched macroalgae probably gain refuge from fish pred-
ators just as amphipods do, subjectively it is likely that a gastropod on a large bladed
macroalga such as Himantothallus grandifolius is just as available to a predatory
fish as it would be on bare rock. However, sea stars are also important predators of
Antarctic gastropods (McClintock 1994), and Odontaster validus is chemically
deterred from consuming H. grandifolius (Table 17.1). Because sea stars use their
tube feet both for locomotion and for chemically sensing their prey (Hennebert et al.
2013), Amsler et al. (2019) hypothesized that O. validus might be less likely to be
on H. grandifolius blades than on other possible substrata, giving gastropods on the
macroalga somewhat of an associational refuge from predation. This hypothesis
might be true, but was not supported in the one simple experiment performed
(Amsler et al. 2019). Overall, compared to the macroalga-amphipod mutualism
illustrated in Fig. 17.2, there are similarities in macroalga-gastropod interactions but
they are not identical.
17.5 Overview
A very high percentage of Antarctic macroalgal species deter potential herbivores

by elaborating chemical defenses. We are not aware of examples elsewhere in the
world where such a high percentage of the macroalgal flora is chemically defended.
In North Carolina (USA), few palatable macroalgal species are apparent in the sum-
mer, but this is because grazing fish remove palatable species that are apparent in
the winter and spring (Hay 1986; Hay and Sutherland 1988; Duffy and Hay 1994).
Most of the Antarctic macroalgal flora are composed of perennial species that are
present throughout all seasons (Wiencke and Clayton 2002; Wiencke et al. 2014)
(see Chaps. 1, 11, 12). This high prevalence of chemical defenses against herbivory
appears to be a fairly unique feature of Antarctic macroalgal forests. Chemical
defenses against carnivory are also very common in Antarctic invertebrates (e.g.,
Amsler et al. 2001; Avila et al. 2008; McClintock et al. 2010; Moles et al. 2015),
making Antarctica a powerful natural laboratory for the study of chemically medi-
ated predator-prey relationships.
Macroalgal forests along the WAP are similar to temperate kelp forests in being
dominated by large, perennial brown macroalgae (Wiencke and Amsler 2012). All
of the overstory brown algal species that dominate these WAP forests are chemi-
cally defended from herbivory. Consequently, while being similar to kelp forests in
some ways, their trophic dynamics differ greatly. Temperate kelps are usually palat-
able to abundant kelp forest consumers such as sea urchins, and the macroalgal
biomass and numerical dominance are usually maintained by “top-down” factors
controlling the herbivore populations (Steneck et al. 2002). Although top-down fac-
tors may have a role in allowing amphipods to be so abundant in WAP forests, as
discussed above in the Sect. 17.4, the general unpalatability to herbivores of the
Antarctic macroalgae suggests that their persistence and community dominance
would exist even if only through this “bottom-up” factor.
As also discussed in Sect. 17.5, while the hypothesis of a community-wide mutu-
alism between amphipods and macroalgae is well supported, there are similarities
but also important differences in the interactions of macroalgal-associated gastro-
pods and their hosts compared to the macroalga-amphipod relationship. While per-
haps not as abundant, at least in terms of biomass, other crustaceans such as
copepods, isopods, and ostracods also associate with canopy-forming macroalgae
(Schram et al. 2016), and polychaetes commonly associate with holdfasts of the
large macroalgae (Pabis and Sicinski 2010). The extent to which the relationships of
these other macroalgal-associated invertebrates and their hosts are similar to or dif-
ferent from the macroalga-amphipod mutualism illustrated in Fig. 17.2 has yet to be
examined.
Acknowledgments We are grateful to all our Antarctic field team members over the years, in
particular to M. Amsler who also provided constructive comments on an earlier version of this
chapter. The original version of this chapter also benefited from the constructive comments of
Martin Thiel and an anonymous reviewer. Our Antarctic chemical ecology research has been
generously supported by numerous awards from the NSF Antarctic Organisms and Ecosystem
program, most recently by PLR-1341333 (CDA, JBM) and PLR-1341339 (BJB).
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Chapter 18
Brown Algal Phlorotannins: An Overview
of Their Functional Roles
Abstract Phlorotannins are polyphenolic compounds, relatively hydrophilic,

formed by polymers of phloroglucinol and found exclusively in brown algae. These
molecules are located in vesicles denominated physodes (the soluble fraction) and
also complexed to polysaccharides in the cell wall (the insoluble fraction). Well
known as potential grazer deterrents, one of the most striking characteristics of
these compounds, due to a number of hydroxyl groups, is their antioxidant poten-
tial, which opens promising perspectives for pharmaceutical and biotechnological
uses. In Antarctic brown algae, especially endemic species of Desmarestiales, con-
stitutively high levels of phlorotannins (up to 12% of dry weight) have been mea-
sured. Although translocation has not been conclusively confirmed, the differential
allocation of phlorotannins in meristematic and reproductive tissues in some species
suggests their involvement in chemical defenses protecting essential metabolic
functions. Due to their UV-absorbing properties and peripheral localization in cells
and tissues, phlorotannins have been related with the increased tolerance to UV
radiation in various Antarctic brown algae. However, no induction of phlorotannins
by UV has been demonstrated, which strongly supports the idea that these mole-
cules are constitutive biochemical components of a suite of mechanisms against
multiple stressors. Due to their structural role as primary compounds, phlorotannins
are essential for various morpho-functional processes that in the case of Antarctic
algae allow them to thrive under extreme conditions. Overall, the significance of
phlorotannins in this group of algae has largely been recognized; however, funda-
mental aspects of their molecular expression, synthesis, and regulation still need to
be addressed, especially considering the climate change-driven environmental
scenarios.
Keywords Antioxidant activity · Brown algae · Phenolic compounds · Physodes ·

Secondary metabolites · UV-absorbing compounds


https://doi.org/10.1007/978-3-030-39448-6_18
Fig. 18.1 Chemical structure of some common phlorotannins extracted from brown algae
18.1 Introduction
Brown algal phenolics belong to a single structural class, the phlorotannins, which
are dehydropolymers of phloroglucinol (1,3,5-trihydroxybenzen). Depending on
the degree of polymerization, phlorotannins present a wide range of molecular
weights (between 140 and 40.000 Da; Ragan and Glombitza 1986). Thus, based
on the number of phloroglucinol units, the profiling of phlorotannins can vary
considerably among species (Steevensz et al. 2012). Within the phlorotannins
found in brown algae, the most common are fucols, phlorethols, fucophlorethols,
and eckols (Fig. 18.1), which vary depending on the type of chemical linkage,
e.g., ether Aryl-O-Aryl linkages in phlorethols or dibenzodioxin linkages in eck-
ols (Ragan and Glombitza 1986; La Barre et al. 2010). As secondary metabolites,
these substances play a series of putative roles in the cell, mainly as anti-herbivory
defense, antifouling activity, UV protectants, and antioxidants. Phlorotannins can
be present as soluble substances sequestered in vesicle-denominated physodes
and as insoluble fraction bound to polysaccharides in the cell wall (denominated
the insoluble fraction) (Fig. 18.2). Due to this, these compounds are regarded also
as primary compounds, essential during cell formation (Schoenwaelder 2002).
This has been corroborated by histological studies indicating that phlorotannins
18 Brown Algal Phlorotannins: An Overview of Their Functional Roles 367
Fig. 18.2 Localization of physodes and the different functional forms of phlorotannins in brown
algal cells. The relationship between exuded phlorotannins and extracellular phenolic bodies has
not been conclusively established
participate actively in wall configuration of zygotes (Kevekordes and Clayton

1999), are concentrated at the periphery of multicellular embryos of Fucus
(Schoenwaelder and Clayton 1998), and are actively synthesized during wound
healing and sealing after amputation of thallus regions simulating herbivory
(Lüder and Clayton 2004).
Because of their ubiquity, phlorotannins can be present in high concentrations in
some species. For example, in Antarctic brown algae, particularly endemic species
of Desmarestiales, constitutively high levels of phlorotannins have been measured,
forming up to 12% of dry weight (Table 18.1). However, it has been well demon-
strated that total phlorotannin content can vary significantly depending on a number
of biotic and abiotic factors (Van Alstyne and Pelletreau 2000; Pavia and Toth 2000;
Jormalainen et al. 2003; Gómez and Huovinen 2010).
Apart from their well-known role as herbivore deterrents (reviewed in Chap. 17
in this volume and by Iken et al. 2009), phlorotannins and various of their chemical
derivatives apparently have other important functions, especially in oxidative
metabolism and metal chelation (Stauber and Florence 1987), with far-reaching
implications for ecophysiology of brown algae (La Barre et al. 2010).
Table 18.1 Concentration of total phlorotannins (soluble and insoluble) in different Antarctic
brown algae
Phlorotannin
contents
Species Soluble Insoluble Remarks Reference
Percentage (mg g−1 DW)
Desmarestia anceps 117 ± 3 Average of different thallus Fairhead et al.
parts (Anvers Island) (2005a)
60 ± 19 1 and 37 m (Anvers Island) Iken et al. (2007)
60 ± 5.5 28 m (King George Island) Huovinen and
Gómez (2013)
30 10–15 m (Anvers Island) Schoenrock et al.
(2015)
80 ± 18 28 ± 4.9 20 m (King George Island) Gómez and
Huovinen (2015)
52 ± 15 15 m (King George Island) Flores-Molina et al.
(2016)
43–48 33 7–10 m depth (King George Rautenberger et al.
Island) (2015)
Desmarestia 52 ± 2 Average of different thallus Fairhead et al.
menziesii parts (Anvers Island) (2005a)
30 ± 12 1 and 37 m (Anvers Island) Iken et al. (2007)
85 ± 5.6 Apical parts; 17 m (King Huovinen and
George Island) Gómez (2013)
10 10–15 m (Anvers Island) Schoenrock et al.
(2015)
55 ± 15 20 m (King George Island) Gómez and
Huovinen (2015)
Island) (2015)
Ascoseira mirabilis 35 ± 25 1 and 37 m (Anvers Island) Iken et al. (2007)
15 ± 12 8 m (King George Island) Huovinen and
Gómez (2013)
12 ± 3 50 ± 10 1 m (King George Island) Huovinen and
Gómez (2015)
13 ± 3 15 ± 2.4 20 m (King George Island) Gómez and
Huovinen (2015)
10–12 20–23 7–10 m depth (King George Rautenberger et al.
Island) (2015)
Himantothallus 63 ± 8 1 and 37 m (Anvers Island) Iken et al. (2007)
grandifolius
Gómez (2013)
97 ± 20 49 ± 11 20 m (King George Island) Gómez and
Huovinen (2015)
Island) (2015)
(continued)
Phlorotannin
contents
Species Soluble Insoluble Remarks Reference
Cystosphaera 26 ± 16 1 and 37 m (Anvers Island) Iken et al. (2007)
jacquinotii
Gómez (2013)
75 ± 19 10 ± 3 15–20 m (King George Huovinen and
Island) Gómez (2015)
Desmarestia 42 ± 5.7 20 m (King George Island) Huovinen and
antarctica Gómez (2013)
Adenocystis 52 ± 4.4 Intertidal zone (King George Huovinen and
utricularis Island) Gómez (2013)
18.2 S
ynthesis and Cellular Localization of Phlorotannins:
Dual Functions as Secondary Metabolites
and Structural Compounds
Phlorotannins are synthesized via the acetate-malonate pathway through a type III
polyketide synthase (Herbert 1989; Meslet-Cladiere et al. 2013), and in terms of
their chemical properties, they differ from the condensed tannins of vascular plants
(Arnold and Targett 2002). It has been suggested that some fatty acids associated
with the Acetyl-CoA, a key intermediate in the polyketide pathway, could be
regarded as precursors of phlorotannins (Steinhoff et al. 2011). However, metabo-
lism of phenolics in algae has been much less studied, and key aspects of biosynthe-
sis and regulation are unknown.
Due to their reactivity, phlorotannins may easily form complexes with macro-
molecules, and they are sequestered in physodes through the formation of covalent,
hydrogen, or ionic bonds (the soluble fraction) (Fig. 18.2). Traditionally physodes
or phenolic precursors are thought to be synthesized in the chloroplast or at the
chloroplast membrane, and various authors have described an osmiophilic material
being released from chloroplasts (Evans and Holligan 1972; Feldmann and
Guglielmi 1972; Pellegrini 1980). An alternative explanation suggests that phenolic
material is produced in the chloroplast endoplasmic reticulum (CER), which may
play a role in the transport of phenolic precursors to cell vacuoles and physodes
(Pellegrini 1980; Clayton and Beakes 1983; Kaur and Vijayaraghavan 1992) or may
directly give rise to physodes (Feldmann and Guglielmi 1972; Oliveira and
Bisalputra 1973). When the physodes make contact with the plasmalemma, phloro-
tannins are released and polymerized in the apoplast (cell wall) forming complexes
with polysaccharides, e.g., alginic-acid-bound phlorotannins (Schoenwaelder and
Clayton 1999) (Fig. 18.2). Some studies have identified peroxidases in the cell wall
of Ascophyllum nodosum suggesting that phlorotannins excreted from the cells may
be modified through the activity of these enzymes (Vilter 1995). In fact, the process
of oxidative condensation and the linkage to alginic acids in the apoplast is appar-
ently driven by vanadium-dependent haloperoxidases (Potin and Leblanc 2006;
Salgado et al. 2009). Vreeland and Laetsch (1988) proposed that phenolic cross-
linking of alginate may occur in early wall formation in Fucus and that peroxidases
may be involved in the catalysis of phenolic condensation into alginate. During
early phases of growth, physode movements to regions of active wall formation
from the cell periphery to the rhizoid tip and to the impending plane of cytokinesis
are dependent on interactions with the cytoskeleton (Schoenwaelder and Clayton
1999). Hence, actin microfilaments may be acting as a general circulatory system
moving physodes around the cell, with microtubules directing physodes (and prob-
ably other wall components) to cell-wall deposition sites, both in the primary wall
and at cross-walls (Kevekordes and Clayton 1999; Schoenwaelder and Clayton
1999). Although the exudation of phlorotannins has been reported (Ragan and
Glombitza 1986; Toth and Pavia 2002; Koivikko et al. 2005), no clear evidence
exists that they are related with phenolic bodies described in embryos of Durvillaea
antarctica (Kevekordes and Clayton 1999). For example, it was demonstrated that
extracellular excretion of phenolic compounds in Eisenia bicyclis and Ecklonia
kurome corresponded to monomeric bromophenols, while phloroglucinol or poly-
meric phlorotannins were not detected (Shibata et al. 2006). On the other hand,
phlorotannins are strong chelators of metals, and thus, they are thought to partici-
pate in exudation-based detoxification mechanisms: they may sequester metal ions
in physodes (Smith and Harwood 1986), and through exudation processes, these
metal-complexing compounds may decrease the metal concentration or alter its spe-
ciation in the surrounding water (Gledhill et al. 1999). As physodes are more abun-
dant in peripheral cell layers, their role as a filter stopping metals from entering the
inner cells has been proposed (reviewed by Schoenwaelder 2002).
18.3 Phlorotannins as UV-Screening Substances
In contrast to terrestrial plants, where natural levels of UV radiation do not neces-

sarily result in damage (Paul and Gwynn-Jones 2003; Hideg et al. 2013), aquatic
organisms, especially subtidal seaweeds, can be impaired when they are exposed to
high solar radiation (Bischof et al. 2006a). Thus, synthesis and accumulation of
UV-screening substances is a common photoprotective strategy observed in several
groups of living organisms (Karentz et al. 1991; García-Pichel and Castenholz
1993; Cockell and Knowland 1999). In fact, various of these compounds have been
isolated and tested as bioactive substances for use in skin care, cosmetics, and phar-
maceutical products (reviewed in Pangestuti et al. 2018). Due to their chemical
properties, diverse phenolics are regarded as general anti-stress agents, including
UV protection and antioxidant activity, and apart from brown algae, they have been
reported in green (Menzel et al. 1983; Pérez-Rodriguez et al. 1998, 2001; Gómez
et al. 1998; Ross et al. 2005) and red algae (Athukorala et al. 2003; Yildiz et al.
2011; Heffernan et al. 2014; Cruces et al. 2018).
Fig. 18.3 Absorption of ethanol-water extract of apical fronds of Lessonia spicata exposed to UV
radiation for 24 h
Phlorotannins have been correlated with an increased tolerance to UV radiation

(Pavia et al. 1997; Swanson and Fox 2007; Gómez and Huovinen 2010; Steinhoff
2010). In general, phlorotannins absorb at wavelengths between 200 and 300 nm,
i.e., well in the UV-C range and at shorter UV-B wavelengths. When phlorotannins
are removed using polyvinylpolypyrrolidone (PVPP), absorption of algal extract
decreases by 70% in the range between 280 and 300 nm (Pavia et al. 1997). Although
the effectiveness of phlorotannins as UV-screening compounds is higher at the
UV-C range, absorption spectra of the different fractions of phlorotannins (phy-
sodes, cell-wall-bound and excreted phlorotannins) may be different. In fact, the
absorption peak of the trihydroxy-coumarin from Dasycladus vermicularis suffers
a shift when excreted to the seawater (Pérez-Rodriguez et al. 2001). Protection
against UV radiation by phlorotannins in early developmental phases has been dem-
onstrated in Fucus embryos and spores of Laminaria (Schoenwaelder et al. 2003;
Henry and Van Alstyne 2004; Roleda et al. 2010). In the kelp Lessonia spicata, 24-h
exposure to UV radiation increases the synthesis of phlorotannins, compared to
control without UV (Fig. 18.3). In this species, the UV-mediated increase in phloro-
tannins can minimize photodamage of key physiological processes and cellular
components, such as photosynthesis and DNA (Gómez and Huovinen 2010).
Interestingly, differences between species, season, and morpho-functional processes
have raised the question whether the photoprotective role of phlorotannins in brown
algae can be regarded as a constitutive or inducible mechanism. For example, in
Lessonia, the induction of phlorotannins by UV radiation has been shown to occur
only during the period when sporophytes actively grow (Gómez and Huovinen
2010). However, in Fucus vesiculosus, no UV induction of soluble phlorotannins
was found, which was related with a lack of upregulation of pksIII genes (Creis
et al. 2015). Overall, the few available studies point to a complex interplay between
the induction of soluble phlorotannins enclosed in physodes and their subsequent
deposition in the cell-wall matrix. Insoluble phlorotannins polymerized in the cell
wall are regarded as primary UV-shielding substances (Gómez and Huovinen 2010),
similar to cell-wall-bound phenolics reported in plants (Clarke and Robinson 2008).
Moreover, photoprotection is conferred not only via intracellular accumulation of
phlorotannins but also as a result of exudation to the surrounding water as has been
suggested for adult thalli and propagules of the giant kelp Macrocystis pyrifera
(Swanson and Druehl 2002).
18.4 Phlorotannins as Active Antioxidant Compounds
The formation of reactive oxygen species (ROS) is one of the primary expressions
of stress in marine algae, but they can also act as signaling molecules in several cel-
lular reactions (revised in Bischof and Rautenberger 2012). Phlorotannins are
known to act, not only as photoprotective substances but also as highly efficient
ROS scavengers (Nakai et al. 2006; Wang et al. 2009; Heffernan et al. 2014). Due
to the presence of various interconnected rings (up to eight) in their chemical struc-
ture, phlorotannins are regarded as potent antioxidants scavenging different types of
ROS, e.g., superoxide anions (O2−), peroxides, singlet oxygen (1O2), and hydroxyl
radicals (•OH) (Ahn et al. 2007; Koivikko et al. 2007). Thus, the hydroxyl groups
present in phlorotannins act as reducing agents, hydrogen donors, and singlet oxy-
gen (reviewed in Michalak 2006). It has been postulated that the relationship
between increased levels of ROS and phlorotannin induction in brown algae can
follow the methyl jasmonate signal transduction pathway, a plant defense-related
pathway reported commonly in plants during high ROS production (Arnold et al.
2001; Küpper et al. 2009). The evidence gained during the last decades appears to
indicate that operation of efficient and rapid ROS scavenging mechanisms based on
phenols can be regarded as an important physiological adaptation in seaweeds when
they are exposed to different environmental stressors, e.g., high solar irradiation,
metal pollution, or high temperature (Aguilera et al. 2002; Contreras et al. 2009;
Cruces et al. 2017).
18.4.1 Phlorotannins and UV-Induced Oxidative Stress
UV radiation is a primary factor inducing ROS in seaweeds, mostly by increasing

the activity of peroxidases and NADPH oxidase (Mackerness et al. 2001). During
exposure to high levels of UV radiation, the xanthophyll cycle is inhibited, which
increases ROS production and impedes an effective dissipation of excess absorbed
excitation energy of photosynthetically active radiation (PAR) (Dring 2005; Bischof
et al. 2006b; Lesser 2012). Thus, the increased electron fluxes result in a direct
photoreduction of oxygen in the Mehler reaction in PSI and lower activity of

Rubisco oxygenase, which exacerbate formation of ROS (e.g., superoxides) (Badger
et al. 2000). In cold temperate/Arctic kelp gametophytes, formation of ROS could
be demonstrated to occur predominantly in the peripheral cytoplasm or in plasmatic
vesicles (Müller et al. 2012). Under UV stress, a relationship between the content of
phlorotannins and antioxidant activity in various species of brown algae has been
reported.
Temperature can modify the phlorotannin response to UV radiation. In the sub-
Antarctic Lessonia spicata, Durvillaea antarctica, and Macrocystis pyrifera from
the coast of Chile, a rapid induction of soluble phlorotannins triggered by UV radia-
tion ameliorated the effects of oxidative stress on photochemical processes after
short-term thermal stress (Cruces et al. 2012). Interestingly, under elevated tem-
peratures >20 °C, the UV induction of phlorotannins ceases, and lipid peroxidation
increases in D. antarctica and L. spicata, suggesting that the ROS scavenging
potential of these sub-Antarctic species has a geographic component associated
with prevalent UV levels and temperature (Cruces et al. 2013). This can have impor-
tant consequences for stress tolerance in species living at the limits of their geo-
graphic distribution or those exposed to changing conditions of temperature and
solar radiation (e.g., polar, intertidal species). In fact, at a molecular level, oxidative
stress caused by UV radiation in the Arctic kelp Saccharina latissima is higher at
2 °C, which is reflected in upregulation of genes encoding for different ROS defense
mechanisms, especially antioxidant enzymes, but not phlorotannins (Heinrich et al.
2015). On the other hand, UV radiation does not directly regulate the expression of
genes involved in phlorotannin metabolism in the intertidal Fucus vesiculosus, sug-
gesting that UV induction of these substances relies on other processes or their
accumulation represents a constitutive metabolic strategy (Creis et al. 2015).
Because phlorotannins act also as primary, structural cell components, their accu-
mulation depends on cellular cycles and biomass formation. Hence, the constitutive
nature of phlorotannins confers side-by-side advantages to brown algae under mul-
tiples stress factors, including UV radiation (Arnold and Targett 2003; Gómez and
Huovinen 2010).
18.4.2 Phlorotannins and Their Interaction with Metals
Although the relationship between phlorotannins of brown algae and metals is not
fully understood, increasing evidence indicates that metal tolerance of seaweeds can
be associated with both internal and external metal-complexing ligands (Andrade
et al. 2010; Connan and Stengel 2011). Decreased levels of soluble phenolic com-
pounds in seaweeds (e.g., Scytosiphon lomentaria and Ulva compressa) have been
reported in copper-impacted sites (Ratkevicius et al. 2003; Contreras et al. 2005).
Metals are redox active and also participate in many reactions generating ROS. The
importance of phenolic compounds as key antioxidant agents during metal exposure
has been recognized in plants (reviewed by Sakihama et al. 2002). UV radiation is
known to induce or enhance the toxicity of certain organic contaminants (phototox-

icity) (Huovinen et al. 2001), and the presence of various metals has been reported
to have antagonistic effects on seaweeds (Andrade et al. 2006). In copper-impacted
areas, seaweeds (e.g. Ulva compressa) have been shown to develop oxidative stress,
and decreased levels of soluble phenolic compounds have been reported (Ratkevicius
et al. 2003; Contreras et al. 2005). Adverse effects of copper in the brown alga
Laminaria digitata were buffered by protective mechanisms regulated by lipid per-
oxide derivatives (Ritter et al. 2008). Proteins potentially involved in the control of
copper-mediated oxidative stress in the brown alga Scytosiphon gracilis were iden-
tified recently (Contreras et al. 2010). Species-specific antioxidant activity of the
soluble phlorotannins and its response to environmental stress (UV radiation, met-
als) has been shown in three Pacific kelps (Huovinen et al. 2010). Here, inorganic
nitrogen was shown to mitigate the adverse effects of copper: the impact of the
interaction of copper, nitrate, and UV radiation was species-specific, Lessonia spi-
cata showing the strongest responses in photosynthetic activity and Durvillaea ant-
arctica the strongest response in phlorotannins and their antioxidant activity.
Macrocystis pyrifera accumulated threefold more copper in its tissues than the other
kelps, but its photosynthetic activity was twofold less inhibited by copper than in
D. antarctica, suggesting higher metal tolerance of M. pyrifera, which was partly
explained by the decreased accumulation of copper in the algal tissues in the pres-
ence of nitrate (Huovinen et al. 2010).
Whether phlorotannins react increasing their ROS scavenging activity after
exposure to metals is not well known. When algae are exposed to metal stress,
increased exudation of organic compounds, including probably phlorotannins, may
retain free metals in form of extracellular complexing ligands. On the other hand,
detoxification of intracellular metals via algal exudates may also increase (Andrade
et al. 2010). Lessonia spicata from uncontaminated sites has been shown to have
capacity to rapidly respond to copper exposure by producing organic ligands that,
due to their complexing capacity in the water, can rapidly attenuate the level of
labile copper (Andrade et al. 2010), thus affecting its bioavailability.
18.5 Phlorotannins in Antarctic Seaweeds
An important feature of various endemic Antarctic brown algae is their high content
of phlorotannins. Different studies have reported total phlorotannin contents in
Antarctic brown algae ranging between 1% and 12% DW. In the case of insoluble
phlorotannins, values are between 1% and 5% DW (Table 18.1). Although some
cold-temperate genera (e.g., Fucus, Ascophyllum) can contain high concentrations
of phlorotannins (>10% DW), normally the maximal values detected in Antarctic
brown algae are higher than most of reported values from temperate, cold-temperate,
and Arctic species (Connan et al. 2004; Dubois and Iken 2012; Cruces et al. 2013;
Generalíc-Mekiníc et al. 2019). The high concentrations of phlorotannins in some
endemic Antarctic brown algae can be also evidenced by the abundance of physodes
Fig. 18.4 Ultrastructure and localization of phlorotannin-containing physodes in Antarctic brown

algae. (a) Desmarestia anceps; (b) Phaeurus antarcticus; (c) Halopteris obovata. Left: cross sec-
tions stained with toluidine blue; right: transmission electron microscopy of cortical cells indicat-
ing the presence of physodes (phy). Cell wall (cw) and chloroplasts (chl) are indicated
in the outer cell layers (Fig. 18.4). Herbivory is among the factors that may contrib-
ute to these high levels of phlorotannins (see Chap. 17 in this volume); however,
other intrinsic factors related to biomass formation can also play an important role.
Whether these high phlorotannin levels found in endemic brown algae living
between 5 and 30 m depth can also be associated with photoprotection against high
solar radiation has also been evaluated (Gómez and Huovinen 2015). In the follow-
ing sections of the present chapter, the variability in the contents of phlorotannins is
revised in the context of abiotic stress.
18.5.1 Depth Patterns in Phlorotannin Contents
The vertical distribution of endemic Antarctic brown algae can range from 1 to 2 m
down to 40 m or greater depths. This broad distribution is related with a suite of
photobiological adaptations operating in a range of different light fields (see Chap.
11 in this volume). Although Antarctic seaweeds are normally not exposed to high
UV levels, seasonal and oceanographic conditions can increase the eventual inci-
dence of harmful irradiances (the biological impact of this factor on different pro-
cesses related with algal distribution is revised in Chap. 11 by Gómez and Huovinen).
The hypothesis that phlorotannins of Antarctic seaweeds can also be related with the
light acclimation strategies has been tested in algae collected at different depths
(Fairhead et al. 2005a; Huovinen and Gómez 2013; Gómez and Huovinen 2015). In
eight brown algae collected along a depth gradient in King George Island, species
such as Desmarestia anceps, Cystosphaera jacquinotii, and Himantothallus grandi-
folius collected at depths >20 m showed the highest phlorotannin concentrations, in
contrast to shallow water or intertidal species such as Adenocystis utricularis or
Ascoseira mirabilis, which in general had the lowest values (Huovinen and Gómez
2013). However, when intraspecific variability of phlorotannins is examined, this
pattern can be different. In fact, Gómez and Huovinen (2015) analyzed the contents
of phlorotannins in conspecifics of Ascoseira mirabilis, Desmarestia anceps,
D. menziesii and Himantothallus grandifolius collected from 5/10, 20 to 30 m at
King George Island, and found that variation with depth was species-specific. For
example, in A. mirabilis, no changes with depth were detected, while in D. anceps
and D. menziesii, values increased in algae collected at 10 m depth compared to 20
or 30 m. Similar results have been reported in D. anceps from Anvers Island, West
Antarctic Peninsula, where higher phlorotannin contents were measured in shal-
lower locations (3–12 m) compared to samples collected between 18 and 30 m
depth (Fairhead et al. 2005a). Although many factors can preclude a conclusive
comparison between different studies (e.g., time of collection, study site, and the
characteristics of the depth gradient or differences in depths between samples), the
results appear to indicate that (a) endemic Antarctic brown algae from depth >20 m
in general show constitutively high levels of phlorotannins, (b) phlorotannin con-
tents and their vertical variability mirror differences in life adaptations developed to
cope with multiple abiotic or biotic variables, and (c) phlorotannins form part of a
trade-off between shade adaptation marked by high photosynthetic efficiencies at
low light and tolerance to high solar stress. Thus, phlorotannins act as multifunc-
tional substances that can be “mobilized” in any situation that poses a threat to the
algae (Gómez and Huovinen 2015) (see Sect. 18.5.3).
18.5.2 Phlorotannin Allocation in Antarctic Seaweeds
Although the Antarctic is devoid of kelps, which resemble plants in being structur-
ally complex, many Antarctic Desmarestiales and Ascoseira and Cystosphaera
show a complex thallus anatomy with morpho-functional processes analogous to
those described in Laminariales and Fucales (see Chap. 11 in this volume). In this
context, it has been commonly observed that concentrations of phlorotannins vary
strongly among different thallus parts (Van Alstyne et al. 1999; Connan et al. 2004;
Iken et al. 2007), stimulating researchers to propose diverse hypothesis explaining
whether this observed variability is related with functional processes at an organis-
mal level. Whether the unequal allocation of phlorotannins to different thallus
regions is related with putative benefits for the alga, e.g., protection of metabolic
performance, reproductive output, or, in general, to guarantee the algal fitness dur-
ing environmental stress, is a relevant question. The optimal defense theory (ODM;
Rhoades 1979) is one of the ecological models used to explain the differential dis-
tribution of phlorotannins in the brown algal thalli, suggesting that chemical
defenses are produced in direct proportion to the risk, i.e., the phenolic compounds
would be produced at a direct expense of other functions (Pavia et al. 2002). High
concentrations of phlorotannins may be expected when an environmental pressure,
e.g., grazing, is high (inducible response) on thallus parts that make an important
contribution to the whole fitness (e.g., meristematic or reproductive regions) or dur-
ing seasonal periods when algae are especially vulnerable. Results in Fucus and
Ecklonia (Steinberg 1985; Yates and Peckol 1993) and the sub-Antarctic kelps
Lessonia spicata and Macrocystis pyrifera (Pansch et al. 2008) indicate that phloro-
tannins could vary as predicted by the ODT. As has been reported for Ascophyllum
nodosum, production of phlorotannins can be highly costly at the expense of growth
(Pavia et al. 1999). Thereby, it has been proposed that due to these costs, synthesis
and accumulation of phenolics could indicate inducible rather than constitutive
defenses (Rhoades 1979), which has been confirmed in some studies of simulated
herbivory (Lüder and Clayton 2004). However, studies carried out in some Antarctic
species indicate that phlorotannin allocation not necessarily confers chemical
defense consistent with the ODM assumptions. For example, regarding the “value”
of different thallus parts in relation with perennial and annual growth strategies,
D. anceps did not show differences in phlorotannin contents between thallus parts
(Fairhead et al. 2005a; Iken et al. 2007); however, there were marked differences in
the toughness, and the chemical defenses in primary stems/stipes were much higher
than the laterals supporting the ODT model (Fairhead et al. 2005b). In contrast,
D. menziesii and Ascoseira mirabilis had higher phlorotannin concentrations in the
holdfasts compared to the branch or lamina regions. Due to that holdfasts were
regarded here as the most valuable thallus part conferring attachment, the patterns
in these species appear to meet well the ODT (Iken et al. 2007). It must be empha-
sized that the deterrent role of Antarctic phlorotannins against grazers and microbia
or as antifouling agents is species specific and probably depends on the type of
predominant phlorotannins and other not well-known qualitative properties of this
compounds (reviewed in Iken et al. 2009). The results agree with longitudinal pro-
files determined in the cold-temperate kelps Laminaria hyperborea and Laminaria
digitata (Connan et al. 2006) and Lessonia spicata (Gómez et al. 2016), where valu-
able regions and basal parts such as haptera or holdfasts and meristematic tissues
allocated the highest phlorotannins compared to the fronds, which can be regarded
as transient structures. These patterns can be associated with various longitudinal
profiles of physiological performance normally described for various kelps (Van
Alstyne et al. 1999; Gómez et al. 2005; Gruber et al. 2011).
In the case of photoprotective responses, it could be reasonable to argue that
valuable thallus regions, e.g., reproductive tissues, should be protected when they
are exposed to UV radiation (Holzinger et al. 2011). This hypothesis has also been
tested in two Antarctic brown algae by exposing reproductive and vegetative thallus
pieces to UV radiation during a short-term period (Huovinen and Gómez 2015). In
the brown alga Cystosphaera jacquinotii, the reproductive structures (receptacles
containing conceptacles) showed higher UV tolerance than its vegetative blades,
whereas in Ascoseira mirabilis, high UV tolerance was demonstrated in both vege-
tative and reproductive tissues. Interestingly, the reproductive structures of both
species of brown algae had higher levels of soluble phlorotannins than the vegeta-
tive tissues, and thus, allocation and proportions of soluble and insoluble, cell-wall-
bound phlorotannins could be related with the observed patterns of UV tolerance of
the different tissues. Observations of tissue cross sections under violet-blue light
excitation using epifluorescence microscopy confirmed a high allocation of pheno-
lic compounds (as blue autofluorescence) in C. jacquinotii, especially in its repro-
ductive structures (Fig. 18.5a). The study is among the first approaches to address
the defense strategies that Antarctic macroalgae exploit to protect their reproductive
structures. It is likely that the allocation of chemical defenses and UV-absorbing
compounds in reproductive tissues is a widespread strategy to ensure the viability of
spores and gametes during their maturation. For example, blue autofluorescence,
indicating the presence of phenolics compounds in reproductive tissues (carporan-
gia) of the Antarctic red algae Trematocarpus antarcticus (Fig. 18.5b), suggests that
not only phlorotannins but also other phenolics can be allocated providing protec-
tion to reproductive tissues.
It has been suggested that phlorotannins can be remobilized between tissues with
different metabolic demand and age (Arnold and Targett 2000). In Laminariales,
compounds as mannitol, amino acids, and other low-molecular-weight compounds
are transported through specialized cells to power meristematic growth through
translocation processes (Küppers and Kremer 1978; Gómez and Huovinen 2012).
Since phlorotannins are structural components in cells, it may be intuitively sug-
gested that these compounds or some key precursors may be mobilized along the
thallus. The abundance of low-molecular-weight phlorotannins (<1200 Da) in vari-
ous species of brown algae (Steevensz et al. 2012) supports also the idea that these
compounds might be rapidly remobilized. For example, accumulation of phlorotan-
nins in response to artificial wounding in the kelp Ecklonia radiata, including the
presence of physodes in medullary sieve elements (Lüder and Clayton 2004), sug-
gests that these compounds can be “transported” along the thallus. In fact, some
Fig. 18.5 Blue autofluorescence of phenolic compounds under violet-blue light excitation in (a)
reproductive receptacles of the brown alga Cystosphaera jacquinotii and (b) carposporangium in
the Antarctic red alga Trematocarpus antarcticus; (c) cross section of non-reproductive lamina of
brown alga Ascoseira mirabilis indicating presence of phenolic compounds in medullar “conduct-
ing channels”
Antarctic species such as Ascoseira mirabilis appear to have the anatomical prereq-
uisites as this alga shows “conducting channels” in its medulla (Fig. 18.5c), which
are suggested to have putative functions in remobilization of substances (Clayton
and Ashburner 1990). Overall, phlorotannins are important structural elements in
the algal thallus, and since growth is localized in specific regions, a trade-off
between phlorotannin synthesis, mobilization, and growth might be defined in these
species in a similar way as in terrestrial vascular plants.
18.5.3 Phlorotannins in Response to UV Radiation
Experimental evidence has pointed to a relatively high tolerance of Antarctic sea-

weeds to UV radiation in the short-term, which at least partly can be related to their
chemical defense mechanism based on phenolic substances. Indeed, Antarctic algae
exposed for 2 h to UV radiation at 2 °C showed very low inhibition of photosynthe-
sis measured as maximal quantum yield of fluorescence (Fv/Fm), which can reach up
to 35% in algae collected from depth >20 m. Even in algae growing at 30 m, inhibi-
tion of chlorophyll fluorescence did not exceed 10–15% (Huovinen and Gómez
2013). In the case of the brown algae, almost all have high levels of phlorotannins,
which due to their UV-absorbing characteristics are the main candidates conferring
photoprotection in these species (Huovinen and Gómez 2013; Gómez and Huovinen
2015; Núñez-Pons et al. 2018). However, testing these properties experimentally is
not an easy task. In fact, manipulative studies conducted in algae attaining high
concentrations of phenols, e.g., Desmarestia anceps, have not demonstrated induc-
tion in phlorotannins in response to UV (Fairhead et al. 2006; Gómez and Huovinen
2015; Flores-Molina et al. 2016). In contrast, some species with relatively low con-
centrations, such as Ascoseira mirabilis, show a slightly UV-mediated induction of
soluble phlorotannins (Rautenberger et al. 2015). As this species is normally found
at shallower depths (1–10 m), the results suggest that it can become exposed to
harmful solar radiation in summer, thus activating the synthesis of phlorotannins. In
all, photoprotection against excess solar radiation, e.g., via UV shielding, is a col-
lateral function in Antarctic seaweeds as these molecules form part of an integral
defense machinery operating in response to multiple stressors in the polar environ-
ment such as herbivores, antifouling, and changes in temperature or simply they are
synthesized to supply of structural elements during cell growth (as insoluble phlo-
rotannins). These multiple functional roles are explained by their high antioxidant
capacity, the most important chemical property of phlorotannins. In fact, soluble
phlorotannins have been positively correlated with the high antioxidant potential
determined in extracts of various species of Antarctic brown algae. This positive
correlation is observed in algae exposed to different conditions of UV radiation and
temperatures (Gómez and Huovinen 2015; Flores-Molina et al. 2016). Interestingly,
it has been demonstrated that UV effects on photosynthesis in Antarctic macroalgae
are modified by temperature: when algae are incubated at 7 °C, i.e., 5 °C above the
field temperature, inhibition of photosynthesis decreases, and recovery increases,
suggesting that, e.g., the PSII repair cycle is more effective at elevated temperature
resulting in a higher UV tolerance, at least in the short-term (Rautenberger et al.
2015). However, the relationship between the phlorotannin contents and the antioxi-
dant potential of extracts does not change with temperature (Fig. 18.6), reinforcing
the idea that in these species, phlorotannins are not UV-inducible compounds. This
raises questions related to the role of these compounds and their physiological con-
sequences under changing environmental conditions. For example, it is known that
during oxidative stress, Antarctic brown algae can active their enzymatic machinery
(e.g., superoxide dismutase, SOD), whose efficiency varies in response to environ-
mental gradients (Bischof and Rautenberger 2012). Thus, the operation of comple-
mentary mechanisms of ROS detoxifying less affected by, e.g., temperature or UV
radiation could be favored. In this context, it has been reported recently that under
high solar stress conditions, algae display a suite of complementary and consecutive
protective mechanisms based on energy dissipative downregulation of photosynthe-
sis, rapid pigment acclimation and PSII repair mechanisms, synthesis of phenolics
with specific UV absorption characteristics, and complementary ROS scavenging
mediated by antioxidant enzymes and phenols (Cruces et al. 2017).
Fig. 18.6 Relationship between phlorotannin content and antioxidant activity of extracts from
four Antarctic brown algae after exposure to UV radiation under different temperatures (Adapted
from Rautenberger et al. 2015)
Antarctic macroalgae are equipped with a suite of anti-stress mechanisms to cope

with the harsh polar environment, probably much more sophisticated and efficient
than previously thought. However, in the case of the putative roles of phlorotannins
in stress tolerance, many gaps still persist, especially those related with their synthe-
sis, the action of different forms of phlorotannins, and their turnover and regulation.
In the case of Antarctic algae, no data on gene expression exist, which precludes an
understanding of crucial aspects related with their multifunctional roles.
In Antarctic brown algae, processes related with synthesis and functional dynam-
ics of phlorotannins take place under constantly low temperatures of 0–2 °C, and
phlorotannin induction can be sensitive to changes in temperate and cold-temperate
species. This raises questions related with the effects of shifts in temperature on the
anti-stress properties of these substances in endemic Antarctic algae, where induc-
tion has not been reported.
Finally, the role of phlorotannins in response to new and emergent stressors, e.g.,
pollutants and acidification (OA), has been very little studied in Antarctic algae.
Although recent experimental essays carried out in Desmarestia anceps and D.
menziesii indicated that a combination of low pH and elevated temperature does not
result in marked effects in phlorotannin content, the shifts can have important and
not well-understood ecophysiological consequences (Schoenrock et al. 2015).
Acknowledgments The authors acknowledge the financial support from Conicyt Chile (FONDAP
15150003, Anillo-PIA ART1101, Fondecyt 1161129) and INACH T-20-09 from the Instituto
Antártico Chileno. The helpful assistance and collaboration of the members of our laboratories at
Universidad Austral de Chile as well as the staff of the Instituto Antártico Chileno during various
Antarctic expeditions are acknowledged.
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Index
A successional patterns, 243, 244

Abiotic factors, 175 successional processes, 242
Accelerated regional warming, 7 temporal and spatial reduction, 255
Actinobacteria, 286 UV radiation, 255
Adenocystis utricularis, 199 Antarctic benthic system, 14
Algal assemblages, 88 Antarctic biodiversity, 10
Alien competitors, 267, 269 Antarctic biota, 10
Alien macroalgae, 267, 268 Antarctic brown algae, 5
Alien species, 96 Antarctic Circumpolar Current (AAC),
Amphipods 4, 8, 267
assemblages, 269 circumpolar path, 49
chemical defenses, 347, 348 description, 44
description, 342 eddies, 47
feeding bioassays, 342 eastward movement, 84
Lambia antarctica, 349 Gigartina skottsbergii, 95
mortality rates, 270 high-level endemism, 44
populations, 271 mesoscale variability, 47
WAP ocean circulation in SO, 84
coastal food webs, 269 oceanic features, 44
macroalgae, 347 as oceanographic barriers, 46
macroalga-invertebrate primary fronts, 46
interactions, 352–355 Antarctic coastal areas
Antarctic algal succession carbon fluxes, 157, 158
glacier retreat, 252–253 macroalgae, 157, 158
grazing, 249–252 Antarctic coastal ecosystems, 15
UV-B, 248–249 Antarctic coastal systems, 8
Antarctic benthic algae Antarctic coastal zone, 174, 175
biological drivers, 255 Antarctic Convergence, 84
colonization processes, 255 Antarctic costal systems, 6
constraints and difficulties, 254 Antarctic cyanobacteria, 88
in situ succession, 253, 254 Antarctic Desmarestiales, 196
interannual changes, 243 Antarctic environment, 256
macroalgae, 243 algae, 25
sessile faunal assemblages, 242 benthic organisms, 25
structural patterns and changes, 244–248 diversity, 27
subtidal communities, 253 macroalgae, 27

https://doi.org/10.1007/978-3-030-39448-6
390 Index
Antarctic environment (cont.) B

physical and chemical, 25 Bacterial community diversity
temperature and salinity, 24 Actinobacteria, 286
Antarctic flora, 10 differences, 285
Antarctic high-intertidal tidepools, 272 epiphytic and endophytic bacterial, 286
Antarctic intertidal ecosystems, 52 marine prokaryotic, 284
Antarctic light regime, 4 PacBio SMRT sequencing, 285
Antarctic macroalgae, 89, 158, 252, 267 phylum Ochrophyta, 285
chemical roles, in sensory ecology, 340 predominant bacteria, 285
Antarctic marine ecosystems, 157 proteobacteria and Firmicutes, 286
Antarctic marine flora, 4, 7, 28 Benthic algae, 294
Antarctic marine macroalgae Benthic algal community, 160
ACC, 104 Benthic Antarctic grazers, 274
diversity, 104 Benthic communities
genetic diversity, 109–111 canopy-forming algae physiology, 230
population fragmentation, 109 structure and maintenance, 230
Quaternary glacial events, 106–108 Benthic primary producer communities, 243,
reconstruction, 105 245, 248
Antarctic maritime islands, 37 Biofouling, 340
Antarctic organisms, 16 Biogeographic barriers, 38
Antarctic ozone depletion, 6 Biogeographic processes
Antarctic Polar Front (APF), 9, 62–67, 69, 70, Antarctic Convergence, 84
74, 104–107, 116, 117 barriers and ecological corridors, 84
Antarctic Program, 88 clusters, 87
Antarctic rocky shores, 50, 52 cryptic species, 87
Antarctic seaweeds, 12 diversity and endemism, 86
ACC, 8, 9 eco-regions, isolation and
biogeographical regions, 8 endemism, 93–96
biomass values, 11 faunal provinces, 86
chlorophyceans, 10 GWR model, 86
climate change, 8, 16 meteorological and oceanographic
ecological succession, 12 patterns, 98
ecosystem level, 6 temperature, 86
environmental features, 10 Biological invasions
global climate changes, 7 anthropogenic threats, 266
inorganic and organic pollutants, 16 biological isolation, 266
logistical constraints, 15 isolated ecosystems, 266
long-term assessment, 15 macroalgae, 267
macromorphology, 26 Biomass reduction, 251
molecular ecology, 15 Blue autofluorescence, phenolic compounds, 379
photobiological adaptations, 132 Brown algae
photosynthetic shade adaptation, adverse effects, copper, 374
137, 138 dry weight, 367
phylogenetic relationships, 285 enzymatic machinery, 380
solar radiation, 11 old-temperate genera, 374
Antarctic terrestrial fauna, 45 phlorotannins
Anti-herbivory defences, 269 Cystosphaera jacquinotii, 378
Antioxidant activity, 370, 373, 374 depths, 376 (see also Phlorotannins)
Antioxidant capacity, 14 and metals, 373
Apparent optical properties (AOPs), 133 photoprotective role, 371
Aquatic organisms, 131 UV-absorbing characteristics, 380
Ascendency framework, 311, 317–319 UV protection and antioxidant activity, 370
Ascoseira mirabilis, 196 Brown species, 60, 62
Index 391
C D
Canopy-forming algae Dark respiration, 181
Desmarestiales, 232 Deception Island
functional groups, 231 aerial view, 91
physical disturbance, 230 anthropic activity, 92
taxonomic richness, 230 Chlorophyta, 92
Carbon balance (CB) circular-shaped volcano, 91
daily net CB, 182, 183 Crustose calcareous algae, 92
estimations, 11 definition, 90
glacier influence, 178 diversity, macroalgae, 92
glacier melting, 178 environmental changes, 91
irradiance vs. photosynthesis, 177 filamentous Cyanobacteria, 89
light availability, 179, 180 fumarolic emissions and thermal
mathematical models, 177 springs, 91
newly ice-free areas, 178 fungal species, 93
photosynthesis, 183, 184 geographical position, 85, 90
photosynthetic acclimation, human activity, 91
181, 182 microclimates, 91
positive CB, 177 tourism, 92
Potter Cove, 178 Denaturing-gradient gel electrophoresis
primary production, 176, 177 (DGGE), 283
turbidity, 177 Desmarestia anceps, 196
WAP, 178 Desmarestiales, 245, 247
Carbon flux, 157, 158, 163 Detached seaweeds
Changing light environment, 175 connectivity, 61
Cheirimedon femoratus, 346, 347 D. anceps and D. menziesii, 62
Chemical ecology drift brown algae, 67
defenses, 348, 349 drift D. anceps, 67
in feeding deterrence, macroalga, 341 green algae, 67
mediation, defensive interactions, 340 macroalgae, 62–67
Plocamium cartilagineum, 347 red algae, 62
signals, 340 decomposition rates, 68
Chemical signals, 340 stranded seaweeds, 62, 68, 69
Chilean South Patagonia (CSP), 268 Dispersal of organisms, 46
Chlorophyll fluorescence, 182 DNA damage, 135, 139, 206
Climate changes, 4, 87, 89, 174, 175, 211 Drifting seaweeds
Coastal benthic-pelagic ecosystems, 310, detached macroalgae, 62
319–321, 327, 328, 330 in hollows, 62
Coastal ecosystems, 310 Durvillaea antarctica, 46, 51–52
Coastal marine ecosystems, 156, 157 Dynamic growth models, 162–165
Coastal waters, 50 Dynamic photoinhibition, 138, 139
Colored dissolved organic matter (CDOM),
132, 141, 144
Community structure, 302 E
Constitutive anti-stress mechanisms, 14 Early colonizers, 244
Crude extracts, 341, 343–345, 347, 348, East Antarctic Peninsula (EAP), 37
350, 352 Ecological functions, 12
Cultivation-based methods, 282 Ecological systems, 302
Cyanobacteria, 88, 91, 92 Ecosystem engineering functions, 6
Cyclobutane pyrimidine dimers Ecosystem functioning, 295, 298, 302
(CPDs), 205 Ecosystem functions, 12
Cystosphaera jacquinotii, 64, 74, 75 Eddies, 47, 49
Cystosphaera jacquinotti, 60–62, 72, 74, 75 Ekman transport, 47
392 Index
Electron transport rates (ETR), 204, 205 life strategies and stress tolerance, 227–229
Endemic species, 28, 30, 31, 35 light use characteristics, 225–227
Endemism, 85, 86, 88, 96 morpho-genetic-based program, 218
Energy mass balance, 313 morphological plasticity, 218
Environmental factors phenotypic plasticity, 218
copper, 210 photochemical adjustments, 219
high solar radiation, 205–208 vertical zonation, 222–224
human activities, 210 Functional form groups, 219, 221
ocean acidification, 210 Functional groups, 219
reproduction, 210 Antarctic green algae, 222
salinity, 210 gross morphology, 220
temperature, 208, 209 L. antarctica and M. hariotii, 219
Environmental filtering, 266 Functional traits
Expansion-contraction model, 108 benthic communities, 230
biological interactions, 230
crustose species, 230
F form models, 230
Feeding bioassay, 340–341 low light conditions, 231
Filamentous fungi and yeasts, 282 polar coastal ecosystems, 229
Floating alga temperate ecosystems, 231
abiotic factors, 69–71
biotic factors, 71–72
C. jacquinotti, 60, 61 G
dispersal mechanism, 73 Gametogenesis, 196
kelps, 61 Gastropods, 354–356
M. pyrifera and D. antarctica, 70 Antarctic grazing, 270
physiological responses, 73–75 mesocosm experiments, 269
species, described, 60 GenBank data, 36
See also Detached seaweeds Generalized additive model (GAM), 157
Floating seaweeds, 9 Genetic diversity
biotic factors, 69–71 COI and TufA sequences data sets, 109, 110
cold-temperate, 70 genetic drift, 108
description, 62 Geographically weighted regression (GWR)
drift and stranded seaweeds, 61 model, 86
environmental change, 73 Gigartina skottsbergii, 198
flora and fauna, 61 Glacial refugia
in temperate latitudes, 72 Antarctic macroalgae, 115
nutrient abundance, 70 genetic diversity, 116, 117
Fluorescence in situ hybridization (FISH), 283 geothermal, 107
Fluorescence method, 204 ice coverage, 116
Food webs in situ marine refugia, 107
macroalgae, 294 LGM, 113
macroalgal community, 295 peri-Antarctic islands, 107
modular patterns, 303 population effective size, 116
network, 296, 301 population fragmentation, 108
Potter Cove ecosystem, 296–298 vs. single Antarctic refugium, 108–109
properties, 295, 296 “Glacier influence”, 178
robustness, 300 Glacier melting, 178
trophic levels (TL) of species, 296 Glacier retreat, 162, 164
Food web theory, 295 Global change phenomena, 256
Form and functions Global warming, 46, 166
functional groups, 219–222 Grazing, 13
heteromorphic phase expression, 218 algal communities development, 251
“the holy grail framework”, 219 amphipod, 252
Index 393
Antarctic benthos, 249 K

biotic filtering, 270 “Kelps”, 156
differential susceptibility, 251 Key species, 310
limpet, 252 KeyPlayer Problem (KPP), 324
Greenhouse gases (GHG), 96 Keystoneness, 311
Gross morphology, 219, 220, 223, 232 Keystone species, 310, 311
Gymnogongrus antarcticus, 197 Keystone species complexes (KSCs)
benthic-pelagic ecosystem, 325–327
central set of k nodes, 324
H functional keystone index (KSi), 322, 323
Heavy metals, 143 macroscopic network properties, 327
Herbivory qualitative/semiquantitative loop
macroalga-herbivore interactions, 340 models, 324
macroalgal palatability and resistance structural keystone index (Ki), 323, 324
to amphipods, 342–348
to fish, 349, 350
to sea stars, 350, 351 L
to sea urchins, 351–352 Laboratory culture techniques, 39
tolerating herbivory, 341 Last Glacial Maximum (LGM)
High solar radiation deglaciation, 106
CPDs, 206 genetic diversity, 113, 120
DNA damage, 206 glacial reconstructions, 107
MAA, 207 glacial refugia, 116
propagule physiology, 205 grounded ice, 116
propagules, 205 ice coverage, 116
stress factors, 205 ice sheet expansions, 107
UV-absorbing substances, 207 local refugium, 116
UV radiation, 206 photosynthetic macroalgae, ice impact, 115
UV-stress tolerance, 206 population contraction, macroalgae, 113
UV susceptibility, 207 Latitudinal–temporal scales, 287
UV tolerance, 207 Life history stages
UV wavelengths, 205 Antarctic seaweeds, 194, 195
High-throughput sequencing photosynthetic light requirements, 199–202
(HTS), 282 photosynthetic parameters, 204, 205
Himantothallus grandifolius, 181 season anticipators, 194–198
Hitch-hiking, 46, 50–52, 71, 72 season responders, 198, 199
“The holy grail framework”, 219 Life strategies and stress tolerance
Hymenocladiopsis prolifera, 197, 198 anatomical traits, 228
Hyperbolic tangent function, 181 assemblages, 229
biological indicator, 227
environmental stressors, 229
I intercalary meristem, 228
Ice melting, 162 morpho-functional implications, 228
Ice sheets and icebergs, 7 photoprotection, 228
Inherent optical properties (IOPs), 133 photosynthetic functionality, 228
Internal transcribed spacer region r and k strategies, 227
(ITS), 282 season anticipators, 227
Intertidal filamentous algae, 269 season responders, 227
Invasive and naturally dispersing non-native Light-absorbing impurities (LAIs), 143
species, 46, 48 Light absorption, 132, 133, 225
Invasive macroalgae, 266 Light availability, 179, 180
In vivo absorptance, 225, 226 Light climate, 133–137
Iridaea cordata, 198 See also Underwater light climate
394 Index
Light-independent carbon fixation (LICF), 5 complex, 280

Light penetration, 134, 136, 142, 144 environmental and biological systems, 284
Long-range atmospheric transport eukaryotes, 280
(LRAT), 143 implications, 281
Long-term successional patterns, 253 PCR, 282
Loop Analysis, 313, 315, 324, 329 profiling, 282, 283
Low water transparency, 11 seawater and sediments, 284
16S rRNA, 283
structure and diversity, 282
M Microphytobenthos, 249
Macroalgae, 156, 243 Microplastics, 143
Antarctic coastal food webs, 294 Molecular taxonomy
assemblages, 253 DNA barcodes, 36
common potential consumers, 342, 345 phenotypic plasticity, 35
detritivore pathway, 296 species, 36
direct interactions, 294 UPA, 36
food web, 294 Monostroma hariotii, 110, 111, 114, 117, 246
in Potter Cove, 298 Morpho-functional adaptations, 12, 232
in shallow water, 340 Morpho-functional traits, 222, 223
Macroalga-invertebrate interactions, WAP Multicellular algae, 218
common red macroalgae, 353 Multispecies modelling, 313
community-wide mutualism, 353 Mutualism, 353, 355, 356
endophytism, 354 Mutualistic networks, 302
free-living filamentous algae, 353 Mycosporine-like amino acids (MAAs), 139
gastropods, 354
Notothenia coriiceps, 353
pathogenicity, 354 N
Macroalgal biomass, 156, 159, 160 Nacella concinna, 268
Macroalgal colonization, 162 Net primary production (NPP), 157
Macroalgal community, 295, 304 Newly ice-free areas
Macroalgal rafts, 50–52 algae growth, 176
Macroalgal species, 295 costal shallow areas, 178
Macrocystis pyrifera, 61, 62, 65, 69–73, 75 glacial influence, 185
Macroscopic network properties glacier retreat, 162
A/C ratio, 319 macroalgal community, 162
coastal benthic/pelagic ecological in Potter Cove, 163, 166, 180, 181, 185
system, 319–321 seaweeds, Potter Cove, 185
ecosystem development, 319 WAP, 175, 184
Fildes Bay, 320 water column, 161
KSCs (see Keystone species Non-trophic interactions, 302, 303
complexes (KSCs))
macroscopic descriptors, 317
network analyses, 310 O
Ov/C ratio, 319 Ocean acidification, 210
redundancy values, 319 Ocean circulation, 48
Marine macroalgae, 266, 340 Oceanographic processes
Marine organisms, 45 ACC, 46, 49
Mass balance, 314 eddies, 47
Mesograzers, 268, 269 Ekman transport, 47
Metabolic carbon balance, see Carbon mesoscale variability, 47
balance (CB) ocean circulation, 48
Microbial communities primary fronts, 46
amplicon sequencing, 282 Stokes drift, 47, 48
Antarctic marine environments, 282 Oceanography, 84, 98
Index 395
Ochrophyta, 30–31 Physiognomy, 251

Ozone depletion, 140, 141, 143 Physiological thallus anatomy, 225, 227
Physodes, 366, 367, 369, 370, 372, 374, 378
Phytoplankton, 132, 134, 142
P Pollution, 143
PacBio SMRT sequencing, 285 Polycyclic aromatic hydrocarbons
Palmaria decipiens, 197 (PAHs), 143
Peracarid crustaceans, 50, 51 Polymerase chain reaction (PCR), 282, 284
Persistent organic pollutants (POPs), 143 Population bottleneck, 108, 109, 113, 120
Phaeurus antarcticus, 196 Potter Cove, 160, 162, 166, 296, 298, 299, 301
Phenolic compounds, 370, 373, 374, 377, 378 Primary production, 176
Phlorotannins, 73, 74 Pseudoperennial macroalgae, 244, 245
acetate-malonate pathway, 369
alginic-acid-bound, 369
allocation in Antarctic seaweeds, 377–379 Q
and antioxidant activity of extracts, 381 Quaternary climatic oscillations
in brown algae, 366 (QCO), 10
chemical structure, 366 Quaternary glacial cycles, 106, 107
-containing physodes, 375
in depth patterns, 368–369, 376
exudation, 370 R
herbivory, 375 Rafting, 46, 50
insoluble, 374 and long-distance dispersal, 61
interaction with metals, 373–374 floating seaweeds, 73
physodes, 366, 369 Rafts, 62, 70–73
polymerization, 366 Reactive oxygen species (ROS), 14, 372
response to UV radiation, 379–381 Regional warming, 142
ROS, 372 Rhodophyta, 32–35
scavenging, 372 Roaring Forties, 47
and UV-induced oxidative stress, 372–373 Rocky shores, 158
as UV-screening substances, 370–372 Rocky substrate, 243, 253, 254
Photosynthesis, 177, 183, 184, 208
CDOM, 132
endemic brown seaweeds, 137 S
high photosynthetic tolerance, 139 Salinity, 210
PAR (see Photosynthetically active Sea ice, 96, 97
radiation (PAR)) Seasonal ice cover, 136
shade adaptation, 137 Seasonality, 175
thinner ice cover, 136 Season anticipators
Photosynthesis-irradiance (P-E), 181 A. mirabilis, 196
Photosynthetic acclimation, 181, 182 Antarctic seaweeds, 194, 196
Photosynthetic activity, 209 D. anceps, 196
Photosynthetically active radiation (PAR), fertilization, 196, 197
132–134, 137–139, 176, 177, 179, gametogenesis, 196
180, 183–185 in late winter/spring, 176
Photosynthetic light requirements, 199–203 physiological process, 194
Photosynthetic organisms, 13 reproduction, 194, 197
Photosynthetic oxygen evolution, 181 seasonal growth, 197
Photosynthetic parameters, 204, 205 species, 197
Photosynthetic shade adaptation Season responders, 176, 198, 199
Antarctic seaweeds, 137, 138 Seaweed biomass, 157
Pneumatocysts, 60, 61 Seaweed distribution
Phylum Ochrophyta, 285 benthic communities, 37
Physicochemical changes, 87 macroalgae, 37
396 Index
Seaweed diversity structurally complex habitats, 248

assemblages, 98 subtidal assemblages, 245
biogeographical clusters, 87 succession stages, 246
Deception Island, 92 three-dimensional structure, 247
and endemism, 86 Subtidal macroalgae, 269
macroalgae, 92 Sunlight, 132
macroalgal assemblages, 87
red algae, 87
South Georgia, 94 T
Seaweed microbiomes Temperature, 86, 208, 209
evolutionary trajectories, 287 Terminal restriction fragment length
functional interactions, 281, 282 polymorphism (T-RFLP), 283
holobiont, 280, 287 Terrestrial biodiversity, 44
host-specific microbial taxa, 280 Terrestrial organisms, 44, 45
microbes, 280 Tolerance, 139, 142
structure and diversity, 282–284 Transoceanic dispersal, 46
Seaweed populations, 11 Trematocarpus antarcticus, 197
Seaweed processes, 84 Trophic dynamic, 356
Seaweed production, 166 Trophic levels, 295, 296
Seaweed propagules, 199, 207, 208, 210 Trophic mass balance models, 313
Seaweeds Tropospheric ultraviolet and visible (TUV)
food webs, 295–299 model, 134, 136
interactions, 295 Turbidity, 175, 177, 179, 183, 184, 211
Secondary metabolites, 366, 369–370 Two-species communities, 272, 273
Sedimentation, 270
Short-weighted trophic level, 296
Shotgun metagenomic sequencing, 282 U
Skottsberg, 246 Ultraviolet-B (UV-B)
Solar radiation, 69, 70, 131, 136, 138–140 benthic primary producer community, 248
Southern Ocean (SO) colonization/establishment, 248
ACC, 119 definition, 248
Antarctic Convergence, 84 DNA damage, 249
biogeographic patterns, 85–86 macroalgae, 249
biota distribution, 84 soft-bottom habitats, 248
climate changes, 120 Ultraviolet radiation (UVR), 268
endemism, 104 Ulva intestinalis
macroalgal anatomy, 105 average fitness ratios, 272
non-endemic Antarctic seaweeds, 105 competitive advantages, 270
physical fragmentation, 106 competitive exclusion, 273
waters, cooling and freezing, 120 frequency-dependent consumption, 274
16S ribosomal RNA gene (16S rRNA), gutweed, 270
283, 284 high-intertidal tidepools, 271, 272
Stranded seaweeds, 61–62, 68 invasion process, 272
Stokes drift, 47–49, 54 negative density, 272
Structural patterns and changes negative frequency dependence, 272
Antarctic subtidal sites, 247 two-species communities, 271
benthic diatoms, 245 Underwater light climate
characteristic trait, 247 AOPs, 133
communities, 247 IOPs, 133
diatom assemblages, 244 light attenuation and potential impact, 132
early colonizers, 244 optical properties, 132
filamentous chlorophytes, 246 penetration, UV wavelengths, 133
salinity and light availability, 246 Underwater optics, 132, 141
Skottsberg, 246 UV-absorbing compounds, 380
Index 397
UV radiation, 206, 209 UV tolerance, 72

on aquatic organisms, 135 UV transparency, 134
and CDOM, 141
deleterious effects, 138
harmful levels, 138 W
MAAs, 139 Warming and ozone depletion, 16
ozone hole, 135 Water column optics, 132, 133, 138
TUV model, 134 Western Antarctic Peninsula (WAP),
UV wavebands, 140 174, 175
UV susceptibility, 207 “Wrack”, 158

Antarctic Seaweeds Diversity, Adaptation and Ecosystem Services

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Iván

ISBN 978-3-030-39447-9 ISBN 978-3-030-39448-6 (eBook)

© Springer Nature Switzerland AG 2020

Valdivia, Chile Iván Gómez

Seaweeds represent a group of photoautotrophic organisms of vital importance for

Bremerhaven, Germany Christian Wiencke

Part II Diversity and Biogeography

3.3 Hitch-Hiking to the Antarctic: Passengers on Seaweed Rafts���������� 50

Part III Physiology, Productivity and Environmental Reponses

10.4 Concluding Remarks: Biology of Propagules under Climate

Part IV Biological Interactions and Ecosystem Processes

13.5 Concluding Remarks���������������������������������������������������������������������� 274

Part V Chemical Ecology

17.4 Macroalga-Invertebrate Interactions on the Western Antarctic

Abstract Seaweeds (macroalgae) represent the most striking benthic organisms in

Keywords Antarctic · Climate change · Antarctic marine flora · Ecosystem

I. Gómez (*) · P. Huovinen

© Springer Nature Switzerland AG 2020 3

1.1 Introduction: The Historical Context

In recent decades, important advances have been demonstrated in different areas of

p­ hotosynthetic responses had important implications for understanding the biologi-

1.2 Antarctic Seaweeds in the Wake of Climate Change

1.3 The Book

Based on recent quantitative, observational, and experimental evidences, this book

1.3.1 Diversity and Biogeography

Compared to other biogeographical regions in the Southern Hemisphere, e.g.,

1.3.2 Environment and Ecophysiology

be highly sensitive to environmental stressors. In Chap. 10, Navarro et al. make a

1.3.3 Ecological Functions

The ecological succession in Antarctic benthos determines the structure of the

community is dominated by microorganisms and benthic diatoms, which apparently

importantly to the emergent network properties, such as growth, organization,

1.3.4 Chemical Ecology

The high prevalence of chemical defenses observed in Antarctic seaweeds is

1.4 Gaps, Emerging Challenges, and Future Directions

Mariana C. Oliveira, Franciane Pellizzari, Amanda S. Medeiros,

Abstract Antarctica is characterized by extremes of climate and biogeographic iso-

M. C. Oliveira (*) · A. S. Medeiros

© Springer Nature Switzerland AG 2020 23

Keywords Benthic algae · Diversity · Endemic species · Maritime Antarctica ·

2.1 The Antarctic Environment

Antarctica is characterized by extremes of climate, which makes its habitats and

2.2 Seaweeds in Antarctica: Definition and Importance

Similar to the terrestrial plants, seaweeds – or marine macroalgae – are photosyn-

Fig. 2.2 Macromorphology of Antarctic seaweeds. (a) Crustose calcareous red alga

environmental conditions marked by low temperature and limited solar radiation.

Table 2.1 Compiled taxa list of Chlorophyta

Table 2.2 Compiled species list of Ochrophyta (Phaeophyceae and Chrysophyceae)

Table 2.3 Compiled taxa list of Rhodophyta

Some Antarctic macroalgae exhibit phenotypic plasticity, which leads to identifica-

global database that would combine molecular, morphological, and distributional

2.5 Seaweed Distribution in Antarctica

Seaweeds are conspicuous components of subtidal benthic communities; however,

2.6 Concluding Remarks: Gaps and Prospects for the Future

The knowledge on the seaweed diversity throughout Antarctica is essential, as they

Acknowledgments We thank PROANTAR (Brazilian Antarctic Program 557030/2009-9,

Clayton MN (1994) Evolution of Antarctic benthic algal flora. J Phycol 30:897–904

Nedzarek A, Rakusa-Suszcewski S (2004) Decomposition of macroalgae and the release of nutri-

Ceridwen I. Fraser, Adele Morrison, and Pamela Olmedo Rojas

Keywords Antarctic circumpolar current · Connectivity · Dispersal · Polar front ·

C. I. Fraser (*) · P. Olmedo Rojas

© Springer Nature Switzerland AG 2020 43

3.1 Antarctica’s Place in the World: An Isolated Continent?

3.1.3 Evidence for Dispersal of Organisms into the Antarctic

Valdivia, Chile Iván Gómez

Bremerhaven, Germany Christian Wiencke

Part II Diversity and Biogeography

3.3 Hitch-Hiking to the Antarctic: Passengers on Seaweed Rafts�� 50

Part III Physiology, Productivity and Environmental Reponses

10.4 Concluding Remarks: Biology of Propagules under Climate

Part IV Biological Interactions and Ecosystem Processes

13.5 Concluding Remarks�� 274

Part V Chemical Ecology

17.4 Macroalga-Invertebrate Interactions on the Western Antarctic

1.1 Introduction: The Historical Context

p hotosynthetic responses had important implications for understanding the biologi-

1.2 Antarctic Seaweeds in the Wake of Climate Change

1.3 The Book

1.3.1 Diversity and Biogeography

1.3.2 Environment and Ecophysiology

1.3.3 Ecological Functions

1.3.4 Chemical Ecology

1.4 Gaps, Emerging Challenges, and Future Directions

2.1 The Antarctic Environment

2.2 Seaweeds in Antarctica: Definition and Importance

2.5 Seaweed Distribution in Antarctica

2.6 Concluding Remarks: Gaps and Prospects for the Future

3.1 Antarctica’s Place in the World: An Isolated Continent?

3.1.3 Evidence for Dispersal of Organisms into the Antarctic

3.2.1 Ekman Transport

3.2.3 Wave-Driven Stokes Drift

3.2.4 Surface Currents

3.3.1 Characteristics of Rafting Species

3.4 Concluding Remarks

4.2 Detached Seaweeds in Antarctica

4.3 Abiotic Factors Influencing Floating Seaweeds

4.4 Biotic Factors Affecting Floating Seaweeds

4.5.1 Out of Antarctic: Is it Physiologically Feasible?

5.1 The Abiotic Setting of the Southern Ocean

5.2 Biogeographic Patterns

5.4 The Physiological Bases of Macroalgal Shifts

6.1 Historical Isolation of Antarctic Marine Macroalgae

6.5.2 One Refugium to Rule Them all

long-distance dispersal, a mechanism most probably facilitated by the strong oce-

6.6 Concluding Remarks

7.2 Optics of Antarctic Coastal Waters