Egyptian J. of Phycol. Vol.22, 2021 A review on the distribution records of mangroveassociated heterocytous cyanobacteria: an update Arun T. Ram 1* and Tessy Paul P. 2 1. 2. Research & PG Department of Botany, M.E.S. Asmabi College, P.Vemballur, Kodungallur, Thrissur District, Kerala – 680 671 Department of Botany, Christ College (Autonomous), Irinjalakuda, Thrissur District, Kerala- 680 125 1&2 Affiliated to University of Calicut Abstract: Microorganisms associated with mangrove habitats have an important role in this ecosystem, contributing significantly to its productivity and ecosystem maintenance. Studies on the distribution of mangroves inhabiting cyanobacterial diversity are scarce and meagre. This study aims to record the occurrence and geographic distribution of the heterocytous cyanobacteria in mangrove environments during 43 years of research carried out by different countries in the world. We consulted 33 publications (national and international journals and books published from 1977 to 2020). There are a total of 70 heterocytous cyanobacterial species. The dominant family was Nostocaceae with 27 species, followed by Calotrichaceae with 12 species, Rivulariaceae and Scytonemataceae with 10 species each, Aphanizomenonaceae with 5 species, Hapalosiphonaceae with 2 species, Chlorogloeopsidaceae, Heteroscytonemataceae, Microchaetaceae and Tolypothrichaceae with one species each. This study will be a contribution to our knowledge of cyanobacterial biodiversity in mangrove ecosystems and generate data for future taxonomic, ecological and biogeographic studies. Keywords: Cyanobacteria, heterocytous, mangrove environment, biodiversity. Introduction Cyanobacteria are the most ancestral lineage responsible for the generation of an oxygen-rich atmosphere that originated before 3.0 Ga (Schirrmeister et al., 2015). Taxonomic classification of cyanobacteria is the only method for understanding their diversity and diversification processes (Komarek, 2013). The modern taxonomic classification of cyanobacteria must be continually revised to * Corresponding author email: aruntram@gmail.com (ISSN: 1110-8649) Arun T. Ram and Tessy Paul P. incorporate data resulting from the polyphasic evaluation of cyanobacterial diversity. Komarek and Anagnostidis (1998) classified cyanobacteria into 14 families based on the presence or absence of false branching, true branching and heterocytes, for discussion, they used the terms ‘heterocytes’ and ‘hormogonia’ rather than ‘heterocysts’ and ‘hormogones’, as recommended by the International Association for Cyanophyte Research (IAC) (Mollenhauer et al., 1994). Cyanobacteria play a pivotal role in mangrove ecosystems as they are the primary producers of organic carbon and nitrogen. Many cyanobacterial species provide nitrogen by biological nitrogen fixation and as a significant group within the diazotrophic guild, contribute to the availability of nitrogen in the system (Toledo et al., 1995). Studies on the nitrogen-fixing capability of cyanobacteria in mangroves have been carried out in a few regions of the world (Ramachandran and Venugopalan, 1987; Kyaruzi et al., 2003; Boopathi, 2011). Some studies focused on cyanobacteria that grow on the surface of mangrove tree trunks, aerial roots, pneumatophores and leaves and their contribution to biological nitrogenfixing capability has been assessed (Mann and Steinke, 2003; Lugomela and Bergman, 2002). Data on mangrove-associated cyanobacteria are scarce throughout the world. Research on this topic is particularly rare and is restricted to certain regions (Lambert et al., 1987). To the best of our knowledge, the first published literature appeared in 1977 (Potts and Whitton, 1977) who reported the occurrence of heterocytous mangrove-associated cyanobacteria Calothrix crustacea Thuret ex Bornet & Flahault 1886 (Current name: Scytonematopsis crustacea (Thuret ex Bornet & Flahault) Kovacik & Komarek 1988) from the intertidal zone of the lagoon shores of West Island, Aldabra. The general aim of this work is to provide an updated revision of the diversity and distribution of previously recorded cyanobacteria in mangrove ecosystems. The need for conducting surveys to fulfil research gaps in this field, including the global distribution pattern of mangroveassociated cyanobacteria, can be used as a reliable database for future major research studies in this field. Egyptian J. of Phycol. Vol. 22, 2021 - 120 - A review on the distribution records of mangrove- associated heterocytous cyanobacteria: an update Materials and Methods The data on heterocytous cyanobacteria associated with mangroves has been compiled solely from published works of literature from 1977-2020. We used 33 research papers and books published nationally and internationally to create a catalogue of cyanobacterial species and the articles in which they are cited. Cyanobacteria can be found in diverse habitats, including epipsammic/edaphic, epizoic, epiphytic, planktic, benthic, and epilithic forms, all of which are common in mangrove ecosystems. The occurrence of cyanobacterial species may not be explicitly indicated in some publications; instead, such species are included under the category ‘mangrove environment’. Different methods for collecting cyanobacteria were discussed in the original research literature, which is cited in this study. The list is exclusively based on published works of literature. We considered only published works that referenced cyanobacteria at the species level of identification. Names of taxa are given with the proper author citation. Species are classified according to their respective families. The species are classified based on the current classification system proposed by Komarek et al. (2014) and Hauer and Komarek (2021) and the entities of the taxonomically accepted species are verified by Guiry and Guiry (2021). When a specific or infraspecific taxon is recorded under a synonym if cited, it is represented under the currently accepted names. Results and Discussion This study aims to compile a catalogue of mangroves inhabiting cyanobacteria and to revise and update the nomenclature to reflect current taxonomically accepted names for the previously documented species. From the 33 research articles and books published nationally and internationally from 1977 to 2020, we considered cyanobacteria to have species-level identification. The results indicated 70 heterocytous cyanobacterial species in which 47 are from mangrove environments, 17 epiphytic, 11 planktic, 12 epilithic, 5 epipsammic/edaphic, 2 Egyptian J. of Phycol. Vol. 22, 2021 - 121 - Arun T. Ram and Tessy Paul P. benthic, 1 epiphyllic and 1 epizoic, while 4 species co-occur among mangrove environments, epipsammic and epiphytic, 2 species co-occur in mangrove environments, epilithic and epiphytic, 4 species co-occur in both epiphytic and mangrove environments, 4 species co-occur in both planktic and mangrove environments, 1 species co-occurs in both epilithic and epizoic, 1 species co-occurs in both epilithic and mangrove environments, 1 species co-occurs in both planktic and benthic environments (Table 1). From this documentation study, the family Nostocaceae was the dominant family with 27 taxa, followed by Calotrichaceae had 12 taxa, Rivulariaceae and Scytonemataceae had 10 taxa each, Aphanizomenonaceae had 5 taxa, Hapalosiphonaceae had 2 taxa and Chlorogleopsidaceae, Heteroscytonemataceae, Microchaetaceae and Tolypothrichaceae had one species each (Figure 1). Tolypothrichaceae 1 Microchaetaceae 1 Heteroscytonemataceae 1 Chlorogleopsidaceae 1 Hapalosiphonaceae 2 Aphanizomenonaceae 5 Scytonemataceae 10 Rivulariaceae 10 Calotrichaceae 12 Nostocaceae 27 0 5 10 15 20 25 30 Number of species Figure 1: Graphical position and number of species from the mangrove-associated cyanobacteria according to family. Egyptian J. of Phycol. Vol. 22, 2021 - 122 - A review on the distribution records of mangrove- associated heterocytous cyanobacteria: an update Table 1: Occurrence of cyanobacterial species from the mangrove environments, habitat, country/provinces and their respective citations are provided. The updated species name was based on Algaebase; (=) symbol indicates the species synonyms if cited in the referred work. List of cyanobacterial species Habitat Country/ Province References Planktic India Sen and Naskar, 2003 Dolichospermum flosaquae (Brebisson ex Bornet & Flahault) P.Wacklin, L.Hoffmann & J.Komarek 2009 (=) Anabaena flosaquae Brebisson ex Bornet & Flauhault 1886 Dolichospermum spiroides (Klebhan) Wacklin, L.Hoffmann & Komarek 2009 (=) Anabaena spiroides Klebahn 1895 Mangrove environment India Barman et al., 2015 Mangrove environment India Bhuvaneshwari and Muruganandam, 2016 Priya et al., 2019 Nodularia spumigena Mertens ex Bornet & Flahault 1888 Mangrove environment India Ramamurthy and Abhinand, 2016 Mangrove Swamps Mangrove environment Mangrove environment Epipsammic Saudi Arabia India Hussain and Khoja, 1993 Sudha, 2005 India Sudha et al., 2007 Nigeria Essien et al., 2008 Epiphytic India Mangrove Swamps Saudi Arabia Nedumaran et al., 2008 Hussain and Khoja, 1993 Epiphytic Australia Huisman et al., 2015 Epiphytic Egypt Potts, 1980 Mangrove environment India Silambarasan et al., 2012 Nostocales - Aphanizomenonaceae Anabaenopsis arnoldii Aptekar 1926 Nodularia spumigena var. major Bornet & Flahault 1886 Nostocales – Calotrichaceae Calothrix aeruginosa Woronichin 1923 Calothrix bharadwajae G.De Toni 1939 Egyptian J. of Phycol. Vol. 22, 2021 - 123 - Arun T. Ram and Tessy Paul P. Calothrix breviarticulata West & G.S.West 1897 Calothrix brevissima G.S.West 1907 Calothrix castellii Bornet & Flahault 1886 Calothrix clavata G.S.West 1914 Calothrix confervicola C.Agardh ex Bornet & Flahault 1886 Calothrix contarenii Bornet & Flahault 1886 Calothrix fusca Bornet & Flahault 1886 Calothrix ghosei Bharadwaja 1935 Calothrix pulvinata C.Agardh ex Bornet & Flahault 1886 Egyptian J. of Phycol. Vol. 22, 2021 Mangrove environment Epiphytic, Edaphic Mangrove environment Epiphytic Saudi Arabia Pakistan India Mohammed and AlShehri, 2015 Bano and Siddiqui, 2007 Silambarasan et al., 2012 Boopathi, 2011 Mangrove environment Micrbial mat, Mangrove Swamps Epipsammic India Barman et al., 2015 Saudi Arabia Hussain and Khoja,1993 Epiphytic Aldabra Islands Africa Potts and Whitton, 1980 Lambert et al., 1989 Epiphytic Africa Steinke et al., 2003 Mangrove environment Mangrove environment Mangrove environment Mangrove environment Mangrove environment Epilithic India Sudha, 2005 India Sudha et al., 2007 India Sakthivel and Kathiresan, 2013 Bhuvaneshwari and Muruganandam, 2016 Priya et al., 2019 India India India Pakistan Mangrove environment India Bano and Siddiqui, 2007 Bhuvaneshwari and Muruganandam, 2016 Priya et al., 2019 Mangrove Swamps, Epilithic Epiphytic Saudi Arabia Hussain and Khoja, 1993 India Nedumaran et al., 2008 - 124 - A review on the distribution records of mangrove- associated heterocytous cyanobacteria: an update Calothrix scopulorum C.Agardh ex Bornet & Flahault 1886 Epilithic Egypt Potts, 1980 Epiphytic Africa Lambert et al., 1989 Epiphytic Africa Silva, 1991 Microbial mat, Mangrove Swamps Epiphytic Saudi Arabia Hussain and Khoja, 1993 Africa Steinke et al., 2003 Mangrove environment Mangrove environment Mangrove environment Mangrove environment India Sudha, 2005 India Sudha et al., 2007 India Saudi Arabia Sakthivel and Kathiresan, 2013 Mohammed and AlShehri, 2015 Epiphytic Pakistan Mangrove environment India Mangrove environment India Joseph and Saramma, 2016 Mangrove environment Mangrove environment Mangrove environment India Sudha, 2005 India Sudha et al., 2007 India Ramamurthy and Abhinand, 2016 Epilithic Egypt Potts, 1980 Epizoic India Sen and Naskar, 2003 Nostocales – Chlorogloeopsidaceae Chlorogloea fritschii A.K.Mitra 1950; Nostoc fritschii (Mitra) Schwabe & El Ayouty 1966 Bano and Siddiqui, 2007 Sakthivel and Kathiresan, 2013 Nostocales – Hapalosiphonaceae Hapalosiphon welwitschii West & G.S.West 1897 Mastigocoleus testarum Lagerheim ex Bornet & Flahault 1886 Egyptian J. of Phycol. Vol. 22, 2021 - 125 - Arun T. Ram and Tessy Paul P. Nostocales – Heteroscytonemataceae Heteroscytonema crispum (Bornet ex De Toni) G.B.McGregor & Sendall 2018 (=) Scytonema crispum Bornet ex De Toni 1907 Epiphytic Australia Huisman et al., 2015 Mangrove environment India Sakthivel and Kathiresan, 2013 Epilithic Pakistan Mangrove environment India Bano and Siddiqui, 2007 Sakthivel and Kathiresan, 2013 Mangrove environment Mangrove environment Mangrove environment Mangrove environment Microbial mat India Nostocales – Microchaetaceae Microchaete grisea Thuret ex Bornet & Flahault 1886 Nostocales – Nostocaceae Anabaena iyengarii Bharadwaja 1935 Anabaena orientalis S.C.Dixit 1936 Anabaena oscillarioides Bory ex Bornet & Flahault 1886 Anabaena sphaerica Bornet & Flahault 1886 Anabaena torulosa Lagerheim ex Bornet & Flahault 1886 Cylindrospermum majus Kutzing ex Bornet & Flahault 1888 Egyptian J. of Phycol. Vol. 22, 2021 Mangrove environment Mangrove environment Mangrove environment Mangrove environment Mangrove environment India Silambarasan et al., 2012 Sakthivel and Kathiresan, 2013 Bhuvaneshwari and Muruganandam, 2016 Priya et al., 2019 Saudi Arabia Hussain and Khoja, 1993 India Silambarasan et al., 2012 Sakthivel and Kathiresan, 2013 Barman et al., 2015 India India India India Saudi Arabia India Mohammed and AlShehri, 2015 Ramamurthy and Abhinand, 2016 Mangrove environment India Silambarasan et al., 2012 Planktic India Nedumaran et al., 2008 - 126 - A review on the distribution records of mangrove- associated heterocytous cyanobacteria: an update Desmonostoc muscorum (C.Agardh ex Bornet & Flahault) Hrouzek & Ventura 2013 (=) Nostoc muscorum C.Agardh ex Bornet & Flahault 1888 Hydrocoryne enteromorphoides (Grunow ex Bo rnet & Flahault) Umezaki & M.Watanabe 1994 Nostoc carneum C.Agardh ex Bornet & Flahault 1886 Nostoc commune Vaucher ex Bornet & Flahault 1888 Nostoc ellipsosporum Rabenhorst ex Bornet & Flahault 1886 Nostoc linckia Bornet ex Bornet & Flahault 1886 (=) Nostoc piscinale Kutzing ex Bornet & Flahault 1886 Planktic, Benthic Mangrove environment Mangrove environment Mangrove Swamps, Pelagic Mangrove environment Mangrove environment Mangrove environment Mangrove environment Epiphytic India Saudi Arabia Ram and Shamina, 2015 Ramamurthy and Abhinand, 2016 Ram and Shamina, 2017 Hussain and Khoja, 1993 India Barman et al., 2015 India Barman et al., 2015 India Barman et al., 2015 India Ram and Shamina, 2017 Sen and Naskar, 2003 India India India Mangrove environment Mangrove environment Mangrove environment Mangrove environment India Nostoc oryzae (F.E.Fritsch) J.Komarek & K.Anagnostidis 1989 (=) Anabaena oryzae F.E.Fritsch 1949 Nostoc paludosum Kutzing ex Bornet & Flahault 1886 Nostoc microscopicum Carmichael ex Bornet & Flahault 1886 Nostoc passerinianum Bornet & Thuret ex Born et & Flahault 1886 Nostoc punctiforme Hariot 1891 Egyptian J. of Phycol. Vol. 22, 2021 India Bhuvaneshwari and Muruganandam, 2016 Priya et al., 2019 India Shamina et al., 2014 India Ram and Shamina, 2017 Epiphytic India Boopathi, 2011 Mangrove environment Mangrove environment India Nedumaran et al., 2008 Ram and Shamina, 2017 Benthic India Mangrove environment Planktic India - 127 - India India Ram and Shamina, 2015 Ram and Shamina, 2017 Sen and Naskar, 2003 Arun T. Ram and Tessy Paul P. Raphidiopsis curvata Fritsch & M.F.Rich 1930 Planktic India Sen and Naskar, 2003 Raphidiopsis indica R.N.Singh 1942 Planktic India Sen and Naskar, 2003 Mangrove environment India Sakthivel and Kathiresan, 2013 Mangrove environment India Ramamurthy and Abhinand, 2016 Planktic India Sen and Naskar, 2003 Mangrove environment India Joseph and Saramma, 2016 Planktic India Sen and Naskar, 2003 Rock pool water, Coastal waters of mangrove waters Mangrove environment Pakistan Bano and Siddiqui, 2007 India Silambarasan et al., 2012 Planktic India Sen and Naskar, 2003 Mangrove Swamps Planktic Saudi Arabia India Mangrove environment Planktic India Hussain and Khoja, 1993 Nedumaran et al., 2008 Barman et al., 2015 Planktic India Richelia intracellularis J.Schmidt 1901 Trichormus doliolum (Bharadwaja) Komarek & Anagnostidis 1989 (=) Anabaena doliolum Bharadwaja 1935 Trichormus khannae (Skuja) Komarek & Anagnostidis 1989 (=) Anabaena khannae Skuja 1949 Trichormus anomalus (F.E.Fritsch) Komarek & Anagnostidis 1989 (=) Anabaena anomala F.E.Fritsch 1949 Trichormus ellipsosporus (F.E.Fritsch) Komarek & Anagnostidis 1989 (=) Anabaena variabilis var. ellipsospora F.E. Fritsch 1949 Trichormus gelatinicola (Ghose) Komarek & Anagnostidis 1989 (=) Anabaena gelatinicola Ghose 1924 Trichormus variabilis (Kutzing ex Bornet & Flahault) Komarek & Anagnostidis 1989 (=) Anabaena variabilis Kutzing ex Bornet & Flahault 1886 Wollea ambigua (C.B.Rao) R.Y.Singh 1942 (=) Anabaena ambigua C.B.Rao 1937 Egyptian J. of Phycol. Vol. 22, 2021 - 128 - India Kannan and Vasantha, 1992 Nedumaran et al., 2008 A review on the distribution records of mangrove- associated heterocytous cyanobacteria: an update Nostocales – Rivulariaceae Dichothrix baueriana Bornet & Flahault 1886 Mangrove environment Mangrove environment Mangrove environment Mangrove Swamps, Epilithic Epiphytic Saudi Arabia Silambarasan et al., 2012 Sakthivel and Kathiresan, 2013 Ramamurthy and Abhinand, 2016 Hussain and Khoja, 1993 Australia Huisman et al., 2015 Phyllonema aviceniicola Alvarenga, Rigonato, Branco, Melo & M.F.Fiore 2016 Kyrtuthrix dalmatica Ercegovic 1929 Epiphyllic Brazil Alvarenga et al., 2016 Epilithic Egypt Potts, 1980 Kyrtuthrix maculans (Gomont) I.Umezaki 1958 Epilithic Egypt Potts, 1980 Epipsammic Egypt Potts, 1980 Epiphytic Australia Epiphytic Australia Beanland and Woelkerling, 1983 Huisman et al., 2015 Rivularia bullata Berkeley ex Bornet & Flahault 1886 Epiphytic Africa Lambert et al., 1989 Epiphytic Africa Steinke et al., 2003 Rivularia polyotis Roth ex Bornet & Flahault 1886 Epiphytic Australia Mangrove Swamps Epiphytic Saudi Arabia Egypt Beanland and Woelkerling, 1983 Hussain and Khoja, 1993 Gab-Alla, 2000 Epiphytic Africa Lambert et al., 1989 Epilithic Epilithic Saudi Arabia India Hussain and Khoja, 1993 Sen and Naskar, 2003 Epiphytic Africa Steinke et al., 2003 Mangrove environment Brazil Nogueira and Ferrieira-Correia, 2001 Dichothrix penicillata Zanardini ex Bornet & Flahault 1886 Dichothrix utahensis Tilden 1898 Gardnerula corymbosa De Toni 1936 Rivularia atra Roth ex Bornet & Flahault 1886 India India India Nostocales – Scytonemataceae Scytonema hofmanii C.Agardh ex Bornet & Flahault 1886 Scytonema arcangelii Bornet & Flahault 1886 Egyptian J. of Phycol. Vol. 22, 2021 - 129 - Arun T. Ram and Tessy Paul P. Scytonema bohneri Schmidle 1901 Scytonema chiastum Geitler 1925 Scytonema insulare C.L.Sant'Anna 1988 Scytonema leptobasis S.L.Ghose 1931 Scytonema saleyeriense Weber Bosse 1913 Scytonema varium Kutzing ex Bornet & Flahault 1886 Scytonematopsis crustacea (Thuret ex Bornet & Flahault) Kovacik & Komarek 1988 (=) Calothrix crustacea Thuret ex Bornet & Flahault 1886 mangrove environment Planktic India Barman et al., 2015 India Mangrove environment mangrove environment Mangrove environment India Planktic India Mangrove environment Mangrove Swamps Mangrove environment Mangrove environment Mangrove environment Epipsammic India Saudi Arabia Aldabra Epiphytic Egypt Ram and Shamina, 2015 Ram and Shamina, 2017 Silambarasan et al., 2012 Nogueira and Ferrieira-Correia, 2001 Ram and Shamina, 2015 Ram and Shamina, 2017 Hussain and Khoja, 1993 Silambarasan et al., 2012 Sakthivel and Kathiresan, 2013 Mohammed and AlShehri, 2015 Potts and Whitton, 1977 Potts, 1980 Epipsammic Aldabra Islands Epiphytic Potts and Whitton, 1980 Silva, 1991 Mangrove Swamps, Epilithic Saudi Arabia Hussain and Khoja,1993 Mangrove environment Epiphytic India Dhargalkar, 1994 Pakistan Saifullah et al., 1997 Epiphytic India Sen and Naskar, 2003 Mangrove environment Mangrove environment India Sudha, 2005 India Sudha et al., 2007 Epiphytic Egyptian J. of Phycol. Vol. 22, 2021 - 130 - India Brazil Saudi Arabia India India A review on the distribution records of mangrove- associated heterocytous cyanobacteria: an update Scytonematopsis pilosa (Harvey ex Bornet & Flahault) I.Umezaki & M.Watanabe 1994 (=) Calothrix pilosa Harvey ex Bornet & Flahault 1886 Epilithic Egypt Potts, 1980 Mangrove environment India Joseph and Saramma, 2016 Nostocales – Tolypothricaceae Tolypothrix tenuis Kutzing ex Bornet & Flahault 1886 While compiling the elaborate list of cyanobacterial diversity with a special focus on mangrove environments, we consider only the specimen taxonomically identified up to the species level. It is noticed that research on mangrove-associated cyanobacterial diversity has become more focused since 1990 and a significant rise in biodiversity research has been recorded over recent decades. However, no taxonomic studies have been published as of 2020. There is a total lack of knowledge on the taxonomy of mangrove-associated cyanobacteria and are very scarce and meagre. As a result, the diversity and ecological importance of these habitats are highly neglected. Based on existing data, it is clear that cyanobacterial floristic surveys should be carried out in diverse biotopes of tropical regions that are still to be explored as they can greatly contribute to our understanding of geographic distribution as well as relevant information for the taxonomy of these organisms. Recent developments in polyphasic approaches will help to explore a good percentage of the cyanobacterial community that can be exploited for the benefit of mankind. Acknowledgements The authors are thankful to the Management, Principal and Head, Research & PG Department of Botany, MES Asmabi College, Kodungallur, Thrissur, Kerala for providing the necessary facilities to carry out the work. Egyptian J. of Phycol. Vol. 22, 2021 - 131 - Arun T. Ram and Tessy Paul P. 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