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Marine macroalgal biodiversity of northern Madagascar: morpho-genetic systematics and implications of anthropic impacts for conservation

Biodiversity and Conservation volume 30, pages 1501–1546 (2021)Cite this article

Abstract

A floristic survey of the marine algal biodiversity of Antsiranana Bay, northern Madagascar, was conducted during November 2018. This represents the first inventory encompassing the three major macroalgal classes (Phaeophyceae, Florideophyceae and Ulvophyceae) for the little-known Malagasy marine flora. Combining morphological and DNA-based approaches, we report from our collection a total of 110 species from northern Madagascar, including 30 species of Phaeophyceae, 50 Florideophyceae and 30 Ulvophyceae. Barcoding of the chloroplast-encoded rbcL gene was used for the three algal classes, in addition to tufA for the Ulvophyceae. This study significantly increases our knowledge of the Malagasy marine biodiversity while augmenting the rbcL and tufA algal reference libraries for DNA barcoding. These efforts resulted in a total of 72 new species records for Madagascar. Combining our own data with the literature, we also provide an updated catalogue of 442 taxa of marine benthic macroalgae from Madagascar, comprising 85 Phaeophyceae, 1 Compsopogonophyceae, 240 Florideophyceae and 116 Ulvophyceae. This diversity holds 29 (ca. 6.5%) endemic species to Madagascar. Our results are discussed in the context of increasing threats to biodiversity on Madagascar’s coastal reefs from both anthropic and anthropogenic activities including sewage effluent runoffs and unsustainable agricultural practices such as massive deforestation, leading to ecosystem shifts to algal dominance on reefs, which are recommended to be addressed through integrated land-sea management in a Reef-to-Ridge conservation approach.

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References

  • Ahamada S et al (2004) Status of the coral reefs of the south west Indian Ocean island states. In: Wilkinson C (ed) Status of coral reefs of the world, vol 1. Australian Institute of Marine Science, Townsville, pp 189–212

    Google Scholar 

  • Andriamampandry A (1988) Beckerella pterocladioides sp. Nov. et Gelidium madagascariense sp. Nov. deux espèces de Gelidiales-rhodophytes de Fort-Dauphin (Madagascar). Cryptogamie Algol 9:243–259

    Google Scholar 

  • Arias-González JE, Fung T, Seymour RM, Garza-Pérez JR, Acosta-González G, Bozec Y-M, Johnson CR (2017) A coral-algal phase shift in Mesoamerica not driven by changes in herbivorous fish abundance. PLoS One 12:e0174855

    PubMed  PubMed Central  Google Scholar 

  • Babinot J-F, Colin J-P, Randrianasolo A (2009) Les ostracodes de l’Albien-Turonien moyen de la région d’Antsiranana (Nord Madagascar): systématique, paléoécologie et paléobiogéographie. Carnets de Geol 2009/01:1–25

    Google Scholar 

  • Belle EM, Stewart GW, De Ridder B, Komeno RJ, Ramahatratra F, Remy-Zephir B, Stein-Rostaing RD (2009) Establishment of a community managed marine reserve in the Bay of Ranobe, southwest Madagascar. Madag Conserv Dev 4:31–37

    Google Scholar 

  • Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2012) GenBank. Nucleic Acids Res 41:D36–D42

    PubMed  PubMed Central  Google Scholar 

  • Blomster J, Maggs CA, Stanhope MJ (1999) Extensive intraspecific morphological variation in Enteromorpha muscoides (Chlorophyta) revealed by molecular analysis. J Phycol 35:575–586

    Google Scholar 

  • Bolton J, Oyieke H, Gwada P (2007) The seaweeds of Kenya: checklist, history of seaweed study, coastal environment, and analysis of seaweed diversity and biogeography. S Afr J Bot 73:76–88

    Google Scholar 

  • Boo GH, Le Gall L, Rousseau F, de Reviers B, Coppejans E, Anderson R, Boo SM (2015) Phylogenetic relationships of Gelidiella (Gelidiales, Rhodophyta) from Madagascar with a description of Gelidiella incrassata sp. nov. Cryptogamie Algol 36:219–237

    Google Scholar 

  • Boo GH, Le Gall L, Hwang IK, Boo SM (2016) Pterocladiella feldmannii sp. Nov. and P. hamelii sp. Nov. (Gelidiales, Rhodophyta), two new species uncovered in Madagascar during the Atimo Vatae Expedition. Cryptogamie Algol 37:179–198

    Google Scholar 

  • Boo GH, Gall LL, Hwang IK, Miller KA, Boo SM (2018) Phylogenetic relationships and biogeography of Ptilophora (Gelidiales, Rhodophyta) with descriptions of P. aureolusa, P. malagasya, and P. spongiophila from Madagascar. J Phycol 54:249–263

    CAS  PubMed  Google Scholar 

  • Borgesen F (1940) Some marine algae from Mauritius. I Chlorophyceae Det Kongelige. Danske Videnskabernes Selskab Biologiske Meddelelser 14:1–81

    Google Scholar 

  • Borgesen F (1941) Some marine algae from Mauritius. II Phaeophyceae Det Kongelige. Danske Videnskabernes Selskab Biologiske Meddelelser 16:1–81

    Google Scholar 

  • Borgesen F (1942) Some marine algae from Mauritius. III. Rhodophyceae. Part 1 Porphyridiales, Bangiales, Nemalionales Det Kongelige. Danske Videnskabernes Selskab Biologiske Meddelelser 17:1–64

    Google Scholar 

  • Borgesen F (1943) Some marine algae from Mauritius. III. Rhodophyceae. Part 2 Gelidiales, Cryptonemiales, Gigartinales Det Kongelige. Danske Videnskabernes Selskab Biologiske Meddelelser 19:1–85

    Google Scholar 

  • Borgesen F (1944) Some marine algae from Mauritius. III. Rhodophyceae. Part 3 Rhodymeniales Det Kongelige. Danske Videnskabernes Selskab Biologiske Meddelelser 19:5–32

    Google Scholar 

  • Borgesen F (1945) Some marine algae from Mauritius. Part 4 Ceramiales Det Kongelige. Danske Videnskabernes Selskab Biologiske Meddelelser 19:1–68

    Google Scholar 

  • Borgesen F (1946) Some marine algae from Mauritius An additional list of species to Part I Chlorophyceae Det Kongelige. Danske Videnskabernes Selskab Biologiske Meddelelser 20:3–64

    Google Scholar 

  • Borgesen F (1948) Some marine algae from Mauritius Additional lists to the Chlorophyceae and Phaeophyceae Det Kongelige. Danske Videnskabernes Selskab Biologiske Meddelelser 20:3–55

    Google Scholar 

  • Borgesen F (1949) Some marine algae from Mauritius Additions to the parts previously published Det Kongelige. Danske Videnskabernes Selskab Biologiske Meddelelser 21:3–48

    Google Scholar 

  • Borgesen F (1950) Some marine algae from Mauritius. Additions to the parts previously published II Det Kongelige. Danske Videnskabernes Selskab Biologiske Meddelelser 18:3–46

    Google Scholar 

  • Borgesen F (1951) Some marine algae from Mauritius Additions to the parts previously published, III Det Kongelige. Danske Videnskabernes Selskab Biologiske Meddelelser 18:3–44

    Google Scholar 

  • Borgesen F (1952) Some marine algae from Mauritius Additions to the parts previously published, IV Det Kongelige. Danske Videnskabernes Selskab Biologiske Meddelelser 18:3–72

    Google Scholar 

  • Borgesen F (1953) Some marine algae from Mauritius Additions to the parts previously published, V Det Kongelige. Danske Videnskabernes Selskab Biologiske Meddelelser 21:3–62

    Google Scholar 

  • Borgesen F (1954a) Some marine algae from Mauritius Additions to the parts previously published, VI Det Kongelige. Danske Videnskabernes Selskab Biologiske Meddelelser 22:4–51

    Google Scholar 

  • Borgesen F (1954b) Two new species of Laurencia from Mauritius. Botanisk Tidsskrift 51:48–52

    Google Scholar 

  • Borgesen F (1957) Some marine algae from Mauritius Final part Det Kongelige. Danske Videnskabernes Selskab Biologiske Meddelelser 23:3–35

    Google Scholar 

  • Bringloe TT, Dunton KH, Saunders GW (2017) Updates to the marine algal flora of the Boulder Patch in the Beaufort Sea off Northern Alaska as revealed by DNA Barcoding. Arctic 70:343–348

    Google Scholar 

  • Bringloe TT, Sjøtun K, Saunders GW (2019) A DNA barcode survey of marine macroalgae from Bergen (Norway). Mar Biol Res 15:1–10

    Google Scholar 

  • Bringloe TT et al (2020) Phylogeny and evolution of the brown algae Crit Rev. Plant Sci 39:281–321. https://doi.org/10.1080/07352689.2020.1787679

    CAS  Article  Google Scholar 

  • Brooks TM et al (2006) Global biodiversity conservation priorities. Science 313:58–61

    CAS  PubMed  Google Scholar 

  • Brown KT, Bender-Champ D, Kubicek A, van der Zande R, Achlatis M, Hoegh-Guldberg O, Dove SG (2018) The dynamics of coral-algal interactions in space and time on the southern. Great Barrier Reef Front Mar Sci 5:181

    Google Scholar 

  • Brown CJ et al (2019) A guide to modelling priorities for managing land-based impacts on coastal ecosystems. J Appl Ecol 56:1106–1116

    Google Scholar 

  • Carlson RR, Foo SA, Asner GP (2019) Land use impacts on coral reef health: a ridge-to-reef perspective. Front Mar Sci 6:562

    Google Scholar 

  • CBD (2020) Convention on biological diversity. Country profile: Madagascar. https://www.cbd.int/countries/profile/?country=mg. Consulted 16 July 2020.

  • Chamberlain YM, Norris RE (1994) Pneophyllum amplexifrons (Harvey) comb. nov., a mastophoroid crustose coralline red algal epiphyte from Natal. South Africa Phycologia 33:8–18

    Google Scholar 

  • Coppejans E, Leliaert F, De Clerck O (2000) Annotated list of new records of marine macroalgae for Kenya and Tanzania, since Isaac’s and Jaasund’s publications. Biologisch Jaarboek Dodonaea 67:31–93

    Google Scholar 

  • Coppejans E, Leliaert F, Verbruggen H, De Clerck O, Schils T, De Vriese T, Marie D (2004) The marine green and brown algae of Rodrigues (Mauritius, Indian Ocean). J Nat Hist 38:2959–3020

    Google Scholar 

  • Costa FO et al (2012) A ranking system for reference libraries of DNA barcodes: application to marine fish species from Portugal. PLoS One 7:e35858

    CAS  PubMed  PubMed Central  Google Scholar 

  • De Clerck O, Coppejans E, Schils T, Verbruggen H, Leliaert F, De Vriese T, Marie D (2004) The marine red algae of Rodrigues (Mauritius, Indian Ocean). J Nat Hist 38:3021–3057

    Google Scholar 

  • De Clerck O, Bolton JJ, Anderson R, Coppejans E (2005a) Guide to the seaweeds of KwaZulu-Natal, vol 33. Scripta Botanica Belgica, National Botanic Garden of Belgium

    Google Scholar 

  • De Clerck O, Gavio B, Fredericq S, Cocquyt E, Coppejans E (2005b) Systematic reassessment of the red algal genus Phyllymenia (Halymeniaceae, Rhodophyta). Eur J Phycol 40:169–178

    Google Scholar 

  • De Clerck O, Verbruggen H, Huisman JM, Faye EJ, Leliaert F, Schils T, Coppejans E (2008) Systematics and biogeography of the genus Pseudocodium (Bryopsidales, Chlorophyta), including the description of P. natalense sp. nov. from South Africa. Phycologia 47:225–235

    Google Scholar 

  • De Jong YSDM, Hitipeuw C, Prud’homme van Reine WF (1999) A taxonomic, phylogenetic and biogeographic study of the genus Acantophora (Rhodomelaceae, Rhodophyta). Blumea 44:217–249

    Google Scholar 

  • Del Cortona A et al (2017) The plastid genome in cladophorales green algae is encoded by hairpin chromosomes. Curr Biol 27:3771.e3776-3782.e3776

    Google Scholar 

  • Di Carlo G, Tombolahy M (2011) Seagrasses and algae of North-Eastern Madagascar. In: Obura D, Di Carlo G, Rabearisoa A, Oliver T (eds) A rapid marine biodiversity assessment of the coral reefs of northeast Madagascar, vol 61. RAP Bull Biol Assessment Conservation International, Arlington, VA, pp 44–52

    Google Scholar 

  • Dixon RR, Mattio L, Huisman JM, Payri CE, Bolton JJ, Gurgel CFD (2014) North meets south–Taxonomic and biogeographic implications of a phylogenetic assessment of Sargassum subgenera Arthrophycus and Bactrophycus (Fucales, Phaeophyceae). Phycologia 53:15–22

    Google Scholar 

  • Donque G (1972) The climatology of Madagascar. In: Biogeography and ecology in Madagascar. Springer, pp 87–144

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    CAS  PubMed  PubMed Central  Google Scholar 

  • Farghaly MS (1980) Algues benthiques de la Mer Rouge et du bassin occidental de l’Océan Indien (étude taxonomique et essai de répartition, notamment des Udotéacées). Ph. D. thesis, Montpellier: Université des Sciences et Techniques du Langedoc, France

  • Feldmann G (1945) Révision du genre Botryocladia Kylin (Rhodophycées-Rhodyméniacées). Bull Soc Hist Afr Nord 35:49–61

    Google Scholar 

  • Fujita M, Suzuki J, Sato D, Kuwahara Y, Yokoki H, Kayanne H (2013) Anthropogenic impacts on water quality of the lagoonal coast of Fongafale Islet Funafuti Atoll, Tuvalu. Sustain Sci 8:381–390

    Google Scholar 

  • Gabriel D, Schils T, Neto AI, Paramio L, Fredericq S (2009) Predaea feldmannii subsp. azorica (Nemastomataceae, Nemastomatales), a new subspecies of red algae (Rhodophyta) from the Azores. Cryptogamie Algol 30:251–270

    Google Scholar 

  • Gabriel D, Parente MI, Neto AI, Raposo M, Schils T, Fredericq S (2010) Phylogenetic appraisal of the genus Platoma (Nemastomatales, Rhodophyta), including life history and morphological observations on P. cyclocolpum from the Azores. Phycologia 49:2–21

    Google Scholar 

  • Gade DW (1996) Deforestation and its effects in highland Madagascar. Mt Res Dev 16:101–116

    Google Scholar 

  • Goodman SM, Benstead JP (2003) Natural history of Madagascar. University of Chicago Press, Chicago and London

    Google Scholar 

  • Goodman SM, Benstead JP (2005) Updated estimates of biotic diversity and endemism for Madagascar. Oryx 39:73–77

    Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate Maximum-Likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    CAS  PubMed  Google Scholar 

  • Guiry MD, Guiry GM (2020) AlgaeBase. World-wide electronic publication. National University of Ireland, Galway. http://www.algaebase.org. Accessed 15 Aug 2020.

  • Hall DJ, Fučíková K, Lo C, Lewis LA, Karol KG (2010) An assessment of proposed DNA barcodes in freshwater green algae. Cryptogamie Algol 31:529–555

    Google Scholar 

  • Harper GJ, Steininger MK, Tucker CJ, Juhn D, Hawkins F (2007) Fifty years of deforestation and forest fragmentation in Madagascar. Environ Conserv 34:325–333

    Google Scholar 

  • Harris AR (2011) Out of sight but no longer out of mind: a climate of change for marine conservation in Madagascar. Madag Conserv Dev 6:7–14

    Google Scholar 

  • Harris A, Manahira G, Sheppard A, Gouch C, Sheppard C (2010) Demise of Madagascar’s once great barrier reef: changes in coral reef conditions over 40 years. Atoll Res Bull 574:1–18

    Google Scholar 

  • Hernandez-Kantun JJ et al (2016) Reassessment of branched Lithophyllum spp. (Corallinales, Rhodophyta) in the Caribbean Sea with global implications. Phycologia 55:619–639

    CAS  Google Scholar 

  • Hind KR, Starko S, Burt JM, Lemay MA, Salomon AK, Martone PT (2019) Trophic control of cryptic coralline algal diversity. Proc Natl Acad Sci USA 116:15080–15085

    CAS  PubMed  Google Scholar 

  • Hofmann LC, Nettleton JC, Neefus CD, Mathieson AC (2010) Cryptic diversity of Ulva (Ulvales, Chlorophyta) in the Great Bay Estuarine System (Atlantic USA): introduced and indigenous distromatic species. Eur J Phycol 45:230–239

    Google Scholar 

  • Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36:W5–W9

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kato A, Baba M (2019) Distribution of Lithophyllum kuroshioense sp. nov., Lithophyllum subtile and L. kaiseri (Corallinales, Rhodophyta), but not L. kotschyanum, in the northwestern. Pacific Ocean Phycologia 58:648–660

    CAS  Google Scholar 

  • Koh YH, Kim MS (2018) DNA barcoding reveals cryptic diversity of economic red algae, Pyropia (Bangiales, Rhodophyta): description of novel species from Korea. J Appl Phycol 30:3425–3434

    CAS  Google Scholar 

  • Kraft GT (1977) Studies of marine algae in the lesser-known families of the Gigartinales (Rhodophyta) I The Acrotylaceae. Aust J Bot 25:97–140

    Google Scholar 

  • Le Gall L, Peña V, Gey D, Manghisi A, Dennetiere B, de Reviers B, Rousseau F (2015) A new species of Stenogramma was uncovered Indian Ocean during the expedition Atimo Vatae: Stenogramma lamyi sp. Nov. Cryptogamie Algol 36:189–198

    Google Scholar 

  • Leliaert F, Coppejans E (2004) Crystalline cell inclusions: a new diagnostic character in the Cladophorophyceae (Chlorophyta). Phycologia 43:189–203

    Google Scholar 

  • Leliaert F, Smith DR, Moreau H, Herron MD, Verbruggen H, Delwiche CF, De Clerck O (2012) Phylogeny and molecular evolution of the green algae. Crit Rev Plant Sci 31:1–46

    Google Scholar 

  • Leliaert F et al (2018) Patterns and drivers of species diversity in the Indo-Pacific red seaweed. Portieria J Biogeogr 45:2299–2313

    Google Scholar 

  • Maina J et al (2012) Linking coral river runoff proxies with climate variability, hydrology and land-use in Madagascar catchments. Mar Pollut Bull 64:2047–2059

    CAS  PubMed  Google Scholar 

  • Maina J, De Moel H, Zinke J, Madin J, McClanahan T, Vermaat JE (2013) Human deforestation outweighs future climate change impacts of sedimentation on coral reefs. Nat Commun 4:1–7

    Google Scholar 

  • Manghisi A, Le Gall L, Ribera MA, Bonillo C, Gargiulo GM, Morabito M (2014) The Mediterranean endemic new genus Felicinia (Halymeniales, Rhodophyta) recognized by a morphological and phylogenetic integrative approach. Cryptogamie Algol 35:221–243

    Google Scholar 

  • Manghisi A, Morabito M, Boo GH, Boo SM, Bonillo C, De Clerck O, Le Gall L (2015) Two novel species of Yonagunia (Halymeniales, Rhodophyta) were uncovered in the South of Madagascar during the Atimo-Vatae Expedition. Cryptogamie Algol 36:199–217

    Google Scholar 

  • Marcot-Coqueugniot J, Boudouresque CF, Thomassin B (1988) Peyssonnelia (Rhodophyta: Peyssonneliaceae) des fonds sedimentaires des recifs coralliens de la region de Tulear (sud-ouest de Madagascar). Bot Mar 31:263–282

    Google Scholar 

  • Mattio L, Payri C (2010) Assessment of five markers as potential barcodes for identifying Sargassum subgenus Sargassum species (Phaeophyceae, Fucales). Cryptogamie Algol 31:467–485

    Google Scholar 

  • Mattio L, Bolton JJ, Anderson RJ (2015) Contribution to the revision of the genus Sargassum (Fucales, Phaeophyceae) in Madagascar using morphological and molecular data. Cryptogamie Algol 36:143–169

    Google Scholar 

  • Mollion J (1998) The seaweed resources of Madagascar and Reunion Islands. In: Critchley AT, Ohno M (eds) Seaweed Resources of the World. Japan International Cooperation Agency, Yokosuka, pp 398–402

    Google Scholar 

  • Mollion J (2017) Seaweeds of Madagascar: a field guide to the most common seaweeds of the Southern shores and their exploitation. 1 edn. CreateSpace Independent Publishing Platform,

  • Mollion J (2020) The seaweed resources of Madagascar. Bot Mar 63:97–104

    Google Scholar 

  • Morelli TL et al (2020) The fate of Madagascar’s rainforest habitat Nat. Clim Change 10:89–96

    Google Scholar 

  • Nakamura N, Kayanne H, Takahashi Y, Sunamura M, Hosoi G, Yamano H (2020) Anthropogenic anoxic history of the Tuvalu atoll recorded as annual black bands in coral. Sci Rep 10:1–9

    Google Scholar 

  • N’Yeurt ADR, Iese V (2015) The proliferating brown alga Sargassum polycystum in Tuvalu South Pacific: assessment of the bloom and applications to local agriculture and sustainable energy. J Appl Phycol 27:2037–2045

    Google Scholar 

  • Oliveira EC, Osterlund K, Mtolera M (2005) Marine plants of Tanzania: a field guide to the seaweeds and seagrasses. Botany Department, Stockholm University

  • Papini M, Benvenuti M (2008) The Toarcian-Bathonian succession of the Antsiranana Basin (NW Madagascar): facies analysis and tectono-sedimentary history in the development of the East Africa-Madagascar conjugate margins. J Afr Earth Sci 51:21–38

    Google Scholar 

  • Poong S-W, Lim P-E, Phang S-M, Sunarpi H, West JA, Kawai H (2014) A molecular-assisted floristic survey of crustose brown algae (Phaeophyceae) from Malaysia and Lombok Island, Indonesia based on rbcL and partial cox1 genes. J Appl Phycol 26:1231–1242

    CAS  Google Scholar 

  • Robba L, Russell SJ, Barker GL, Brodie J (2006) Assessing the use of the mitochondrial cox1 marker for use in DNA barcoding of red algae (Rhodophyta). Am J Bot 93:1101–1108

    CAS  PubMed  Google Scholar 

  • Rousseau F et al (2017) Molecular phylogenies support taxonomic revision of three species of Laurencia (Rhodomelaceae, Rhodophyta), with the description of a new genus. Eur J Taxon 2017:1–19

    Google Scholar 

  • Santelices B (1994) A reassessment of the taxonomic status of Gelidium amansii (Lamouroux) Lamouroux. In: Taxonomy of Economic Seaweeds, vol 4. Abbott, I. A., La Jolla: California Sea Grant College Program [Report T-CSGCP-031], pp 37–53

  • Saunders GW (2010) An evaluation of rbcL, tufA UPA, LSU and ITS as DNA barcode markers for the marine green macroalgae. Cryptogamie Algol 31:487–528

    Google Scholar 

  • Saunders GW, Kucera H (2010) An evaluation of rbcL, tufA UPA, LSU and ITS as DNA barcode markers for the marine green macroalgae. Cryptogamie Algol 31:487–528

    Google Scholar 

  • Saunders GW, McDevit DC (2013) DNA barcoding unmasks overlooked diversity improving knowledge on the composition and origins of the Churchill algal flora. BMC Ecol 13:9

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schils T, Coppejans E (2002) Gelatinous red algae of the Arabian Sea, including Platoma heteromorphum sp. nov. (Gigartinales, Rhodophyta). Phycologia 41:254–267

    Google Scholar 

  • Schils T, Coppejans E, Verbruggen H, De Clerck O, Leliaert F (2004) The marine flora of Rodrigues (Republic of Mauritius, Indian Ocean): an island with low habitat diversity or one in the process of colonization? J Nat Hist 38:3059–3076

    Google Scholar 

  • Sekimoto S, Klochkova TA, West JA, Beakes GW, Honda D (2009) Olpidiopsis bostrychiae sp. nov.: an endoparasitic oomycete that infects Bostrychia and other red algae (Rhodophyta). Phycologia 48:460–472

    Google Scholar 

  • Sherwood AR, Boedeker C, Havens AJ, Carlile AL, Wilcox MD, Leliaert F (2019) Newly discovered molecular and ecological diversity within the widely distributed green algal genus Pseudorhizoclonium (Cladophorales, Ulvophyceae). Phycologia 58:83–94

    CAS  Google Scholar 

  • Silva PC, Basson PW, Moe RL (1996) Catalogue of the benthic marine algae of the Indian Ocean. Univ Calif Publ Bot 79:1259

    Google Scholar 

  • Steen F, Vieira C, Leliaert F, Payri EC, De Clerck O (2015) Biogeographic affinities of Dictyotales from Madagascar: a phylogenetic approach. Cryptogamie Algol 36:129–141

    Google Scholar 

  • Tronchin E, Freshwater DW, Bolton J (2003) A re-evaluation of the genera Beckerella and Ptilophora (Gelidiales, Rhodophyta) based on molecular and morphological data. Phycologia 42:80–89

    Google Scholar 

  • Turland NJ et al (2018) International Code of Nomenclature for algae, fungi, and plants (Shenzhen Code) adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017. Koeltz Botanical Books

  • Verbruggen H, Costa JF (2015) Molecular survey of Codium species diversity in southern Madagascar. Cryptogamie Algol 36:171–187

    Google Scholar 

  • Vieira C, D’hondt S, De Clerck O, Payri CE (2014) Toward an inordinate fondness for stars, beetles and Lobophora? Species diversity of the genus Lobophora (Dictyotales, Phaeophyceae) in New Caledonia. J Phycol 50:1101–1119

    CAS  PubMed  Google Scholar 

  • Vieira C et al (2016) Shedding new light on old algae: matching names and sequences in the brown algal genus Lobophora (Dictyotales, Phaeophyceae). Taxon 65:689–707. https://doi.org/10.12705/654

    Article  Google Scholar 

  • Vieira C, Camacho O, Sun Z, Fredericq S, Leliaert F, Payri C, De Clerck O (2017) Historical biogeography of the highly diverse brown seaweed Lobophora (Dictyotales, Phaeophyceae). Mol Phylogen Evol 110:81–92. https://doi.org/10.1016/j.ympev.2017.03.007

    Article  Google Scholar 

  • Vieira C, Morrow KM, D’Hondt S, Camacho O, Engelen AH, Payri C, De Clerck O (2020) Diversity, ecology, biogeography and evolution of the prevalent brown algal genus Lobophora in the Greater Caribbean sea, including the description of five new species. J Phycol 56:592–607

    CAS  PubMed  Google Scholar 

  • Voarintsoa NRG, Raveloson A, Barimalala R, Razafindratsima OH (2019) ‘Malagasy’ or ‘Madagascan’? Which English term best reflects the people, the culture, and other things from Madagascar? Sci African 4:e00091

    Google Scholar 

  • West JA, Zuccarello GC, Hommersand M, Karsten U, Görs S (2006) Observations on Bostrychia radicosa comb. nov. (Rhodomelaceae, Rhodophyta). Phycol Res 54:1–14

    Google Scholar 

  • West JA, Scott JL, West KA, Karsten U, Clayden SL, Saunders GW (2008) Rhodachlya madagascarensis gen. et sp. nov.: a distinct acrochaetioid represents a new order and family (Rhodachlyales ord. nov., Rhodachlyaceae fam. nov.) of the Florideophyceae (Rhodophyta). Phycologia 47:203–212

    Google Scholar 

  • Won BY, Cho TO, Fredericq S (2009) Morphological and molecular characterization of species of the genus Centrocercas (Ceramiaceae, Ceramiales), including two new species. J Phycol 45:227–250

    PubMed  Google Scholar 

  • Wynne MJ (1982) Duckerella, a new genus of Delesseriaceae (Rhodophyta) from Madagascar. Phycologia 21:236–242

    Google Scholar 

  • Wynne MJ (2013) The red algal families Delesseriaceae and Sarcomeniaceae. Koeltz Scientific Books, Königstein

    Google Scholar 

  • Yang EC et al (2010) New taxa of the Porphyridiophyceae (Rhodophyta): Timspurckia oligopyrenoides gen. et sp. nov. and Erythrolobus madagascarensissp. nov. Phycologia 49:604–616

    CAS  Google Scholar 

  • Zuccarello GC, Kikuchi N, West JA (2010) Molecular phylogeny of the crustose Erythropeltidales (Compsogonophyceae, Rhodophyta): new genera Pseudoerythrocladia and Madagascaria and the evolution of the upright habit. J Phycol 46:363–373

    Google Scholar 

Download references

Acknowledgements

Sampling for this study took place within the framework of the capacity-building program “Gestion des collections et des données biologiques” organized by the Royal Museum for Central Africa, Belgium. We are grateful to Professor Abdoul, Dean of the Faculty of Science and Ms. Amélie Landy Soambola at the University of Antsiranana for providing logistical support for field collections. We thank Ms. Aurore Mathys for her assistance with photography and sampling. We thank Dr. Lydiane Mattio for her help in identifying Fucales species. We are indebted to Professor Michael Guiry of the National University of Ireland, Galway for his kind assistance in obtaining algal type and distributional records from AlgaeBase. CV is an International Research Fellow of the Japan Society for the Promotion of Science. The research leading to the results presented in this publication was carried out with infrastructure funded by EMBRC Belgium – FWO project GOH3817N.

Funding

This work was supported by the Belgian Development Cooperation through a framework agreement project (2013–2018) with the Royal Museum for Central Africa and Ghent University (Ghent, Belgium) with infrastructure funded by European Marine Biological Resource Centre Belgium/Research Foundation—Flanders Project GOH3817N. The authors thank the Japan Society for the Promotion of Science (JSPS) for additional financial support including a Grant-in-Aid for Science (grant number 19F19796).

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Authors and Affiliations

  1. Kobe University Research Center for Inland Seas, Rokkodai, Nadaku, Kobe, Japan

    Christophe Vieira & Hiroshi Kawai

  2. Phycology Research Group and Center for Molecular Phylogenetics and Evolution, Ghent University, Ghent, Belgium

    Christophe Vieira, Sofie D’Hondt, Lan-Anh Thi Tran & Olivier De Clerck

  3. Pacific Centre for Environment and Sustainable Development, the University of the South Pacific, Private Mail Bag, Suva, Fiji

    Antoine De Ramon N’Yeurt

  4. University of Antsiranana, Antsiranana, Madagascar

    Faravavy A. Rasoamanendrika

  5. Department of Ecology, Institute of Tropical Biology, Hochiminh city, Vietnam

    Lan-Anh Thi Tran

  6. Biological and Data Management Unit, Royal Museum for Central Africa, Tervuren, Belgium

    Didier Van den Spiegel

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  1. Christophe Vieira
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Correspondence to Christophe Vieira.

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Vieira, C., De Ramon N’Yeurt, A., Rasoamanendrika, F.A. et al. Marine macroalgal biodiversity of northern Madagascar: morpho-genetic systematics and implications of anthropic impacts for conservation. Biodivers Conserv 30, 1501–1546 (2021). https://doi.org/10.1007/s10531-021-02156-0

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Keywords

  • Seaweed
  • DNA-barcoding
  • Conservation
  • Florideophyceae
  • Phaeophyceae
  • Flora
  • Ulvophyceae