Cite this paper:
Hang XIE, Jian ZOU, Chengzhi ZHENG, Yuchen QU, Kaixuan HUANG, Songhui LÜ. Biodiversity and distribution of benthic dinoflagellates in tropical Zhongsha Islands, South China Sea[J]. Journal of Oceanology and Limnology, 2022, 40(6): 2120-2145

Biodiversity and distribution of benthic dinoflagellates in tropical Zhongsha Islands, South China Sea

Hang XIE1,3, Jian ZOU1,3, Chengzhi ZHENG1,3, Yuchen QU1,3, Kaixuan HUANG1,3, Songhui LÜ1,2,3
1 Research Center of Harmful Algae and Marine Biology, College of Life Science and Technology, Jinan University, Guangzhou 510362, China;
2 Southern Marine Science and Engineering Guangdong Laboratory, Zhuhai 519000, China;
3 Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Jinan University, Guangzhou 510632, China
Benthic dinoflagellates have attracted increasing attention in recent years because of their toxicity and ability to form extensive harmful algal blooms. Ostreopsis producing palytoxin and its analogs, Gambierdiscus producing ciguatera toxins, and Prorocentrum producing okadaic acid and dinophysis toxins, have been concerned as serious human poisonings. We explored the benthic dinoflagellate biodiversity and distribution characteristics of a series of tropical reefs in 20–40-m water depth in wet season in the Zhongsha Islands in South China Sea using morphological, phylogenetic, and cell counting methods. Results show that benthic dinoflagellates in the islands are rich in biodiversity and 15 species from genera Amphidinium, Coolia, Ostreopsis, and Prorocentrum were identified: Amphidinium carterae, A. magnum, A. massartii, A. operculatum, Coolia canariensis, C. malayensis, C. palmyrensis, C. tropicalis, Ostreopsis cf. ovata, Prorocentrum concavum, P. cf. sculptile, P. emarginatum, P. hoffmannianum, P. lima, and P. rhathymum. Among them, A. magnum is reported for the first time in Chinese waters. The abundance of benthic dinoflagellates was relatively low at 88–4 345 cells/100 cm2 on sediment and 10–91 cells/g on macroalgae. Prorocentrum and Amphidinium were the dominant and subdominant genera, respectively. It is speculated that the low abundance of benthic dinoflagellates is closely related to the scarcity of macroalgae and stronger water motion at the depth >15 m in Zhongsha Islands. This study expanded the study in biodiversity of benthic dinoflagellates in Chinese waters, and revealed the distribution characteristics of harmful benthic microalgae in reef habitats.
Key words:    benthic dinoflagellates|Zhongsha Islands|South China Sea|biodiversity|distribution   
Received: 2021-10-01   Revised:
PDF (5108 KB) Free
Print this page
Add to favorites
Email this article to others
Articles by Hang XIE
Articles by Jian ZOU
Articles by Chengzhi ZHENG
Articles by Yuchen QU
Articles by Kaixuan HUANG
Articles by Songhui LÜ
Acaf L, Saab M A A, Khoury-Hanna M et al. 2020. Bloom dynamics of the newly described toxic benthic dinoflagellate Ostreopsis fattorussoi along the Lebanese coast (Eastern Mediterranean). Regional Studies in Marine Science, 38: 101338,
Accoroni S, Totti C, Romagnoli T et al. 2020. Distribution and potential toxicity of benthic harmful dinoflagellates in waters of Florida Bay and the Florida Keys. Marine Environmental Research, 155: 104891,
Adachi R, Fukuyo Y. 1979. The thecal structure of a marine toxic dinoflagellate Gambierdiscus toxicus gen. et sp.nov. collected in a ciguatera-endemic area. Nippon Suisan Gakkaishi, 45(1): 67-71,
Aligizaki K, Nikolaidis G F. 2008. Morphological identification of two tropical dinoflagellates of the genera Gambierdiscus and Sinophysis in the Mediterranean Sea.Journal of Biological Research-Thessaloniki, 9: 75-82.
Amzil Z, Sibat M, Chomerat N et al. 2012. Ovatoxin-a and palytoxin accumulation in seafood in relation to Ostreopsis cf. ovata blooms on the French Mediterranean coast.Marine Drugs, 10(2): 477-496,
Ben Gharbia H, Laabir M, Ben Mhamed A et al. 2019.Occurrence of epibenthic dinoflagellates in relation to biotic substrates and to environmental factors in Southern Mediterranean (Bizerte Bay and Lagoon, Tunisia): an emphasis on the harmful Ostreopsis spp., Prorocentrum lima and Coolia monotis. Harmful Algae, 90: 101704,
Ben-Gharbia H, Yahia O K, Amzil Z et al. 2016. Toxicity and growth assessments of three thermophilic benthic dinoflagellates (Ostreopsis cf. ovata, Prorocentrum lima and Coolia monotis) developing in the southern Mediterranean basin. Toxins, 8(10): 297,
Bienfang P, Oben B, DeFelice S et al. 2008. Ciguatera: the detection of neurotoxins in carnivorous reef fish from the coast of Cameroon, West Africa. African Journal of Marine Science, 30(3): 533-540,
Boisnoir A, Pascal P Y, Cordonnier S et al. 2018. Depth distribution of benthic dinoflagellates in the Caribbean Sea. Journal of Sea Research, 135: 74-83,
Boisnoir A, Pascal P Y, Cordonnier S et al. 2019a. Spatiotemporal dynamics and biotic substrate preferences of benthic dinoflagellates in the Lesser Antilles, Caribbean sea. Harmful Algae, 81: 18-29,
Boisnoir A, Pascal P Y, Marro S et al. 2019b. First spatial distribution of potentially toxic benthic dinoflagellates in the Lesser Antilles (Guadeloupe and Martinique), Caribbean Sea. Botanica Marina, 62(4): 309-322,
Calado A J, Craveiro S C, Moestrup Ø. 1998. Taxonomy and ultrastructure of a freshwater, heterotrophic Amphidinium(Dinophyceae) that feeds on unicellular protists. Journal of Phycology, 34(3): 536-554, Chinain M, Darius H T, Gatti C M et al. 2016. Update on ciguatera research in French Polynesia. SPC Fisheries Newsletter, 150: 42-51.
Chinain M, Gatti C M I, Darius H T et al. 2021. Ciguatera poisonings: a global review of occurrences and trends.Harmful Algae, 102: 101873,
Chinain M, Gatti C M, Roué M et al. 2020. Ciguatera-causing dinoflagellates in the genera Gambierdiscus and Fukuyoa:distribution, ecophysiology and toxicology. In: Rao D V S ed. Dinoflagellates. Nova Science Publishers, Inc., p.405-457.
Chomérat N, Bilien G, Viallon J et al. 2020. Taxonomy and toxicity of a bloom-forming Ostreopsis species(Dinophyceae, Gonyaulacales) in Tahiti island (South Pacific Ocean): one step further towards resolving the identity of O. siamensis. Harmful Algae, 98: 101888,
Chomérat N, Bilien G, Zentz F. 2019. A taxonomical study of benthic Prorocentrum species (Prorocentrales, Dinophyceae) from Anse Dufour (Martinique Island, eastern Caribbean Sea). Marine Biodiversity, 49(3): 1299-1319,
De Azevedo Tibiriçá C E J, Sibat M, Fernandes L F et al. 2020.Diversity and toxicity of the genus Coolia Meunier in Brazil, and detection of 44-methyl gambierone in Coolia tropicalis. Toxins, 12(5): 327,
Durán-Riveroll L M, Cembella A D, Okolodkov Y B. 2019. A Review on the biodiversity and biogeography of toxigenic benthic marine dinoflagellates of the coasts of Latin America. Frontiers in Marine Science, 6: 148,
Faust M A. 1990. Morphologic details of six benthic species of Prorocentrum (Pyrrophyta) from a Mangrove Island, Twin Cays, Belize, including two new species. Journal of Phycology, 26(3): 548-558,
Faust M A. 1994. Three new benthic species of Prorocentrum(Dinophyceae) from carrie bow Cay, Belize: P. sabulosum sp. nov., P. sculptile sp. nov., and P. arenarium sp.nov. Journal of Phycology, 30(4): 755-763,
Faust M A. 1995. Observation of sand-dwelling toxic dinoflagellates (Dinophyceae) from widely differing sites, including two new species. Journal of Phycology, 31(6): 996-1003,
Foden J, Purdie D A, Morris S et al. 2005. Epiphytic abundance and toxicity of Prorocentrum lima populations in the Fleet Lagoon, UK. Harmful Algae, 4(6): 1063-1074,
Fukuyo Y. 1981. Taxonomical study on benthic dinoflagellates collected in coral reefs. Nippon Suisan Gakkaishi, 47(8):967-978,
Gómez F. 2003. Checklist of mediterranean free-living dinoflagellates. Botanica Marina, 46(3): 215-242,
Guillard R R L, Hargraves P E. 1993. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia, 32(3): 234-236,
Guiry M D, Guiry G M. 2022. AlgaeBase. World-Wide Electronic Publication, National University of Ireland, Galway.
Hachani M A, Dhib A, Fathalli A et al. 2018. Harmful epiphytic dinoflagellate assemblages on macrophytes in the Gulf of Tunis. Harmful Algae, 77: 29-42,
Herrera-Sepúlveda A, Medlin L K, Murugan G et al. 2015.Are Prorocentrum hoffmannianum and Prorocentrum belizeanum (Dinophyceae, Prorocentrales), the same species? An integration of morphological and molecular data. Journal of Phycology, 51(1): 173-188,
Ho T V, Nguyen L N. 2014. Morphology and distribution of the three epiphytic dinoflagellate species Coolia monotis, C. tropicalis, and C. canariensis (Ostreopsidaceae, Gonyaulacales, Dinophyceae) from Vietnamese coastal waters. Ocean Science Journal, 49(3): 211-221,
Hoppenrath M, Chomérat N, Horiguchi T et al. 2013. Taxonomy and phylogeny of the benthic Prorocentrum species(Dinophyceae)—a proposal and review. Harmful Algae, 27: 1-28,
Jang S H, Jeong H J, Yoo Y D. 2018. Gambierdiscus jejuensis sp. nov., an epiphytic dinoflagellate from the waters of Jeju Island, Korea, effect of temperature on the growth, and its global distribution. Harmful Algae, 80: 149-157,
Jeong H J, Yih W, Kang N S et al. 2012. First report of the epiphytic benthic dinoflagellates Coolia canariensis and Coolia malayensis in the waters off Jeju Island, Korea: morphology and rDNA sequences. J. Eukaryot.Microbiol.,59(2): 114-133,
Jiang L C. 2019. Taxonomic Research of the Benthic Dinoflagellate Gambierdiscus and Amphidinum from the South China Sea and Studies on the Toxin Constituents of Gambierdiscus. Jinan University. p.1-88. (in Chinese)
Kang N S, Jeong H J, Lee S Y et al. 2013. Morphology and molecular characterization of the epiphytic benthic dinoflagellate Ostreopsis cf. ovata in the temperate waters off Jeju Island, Korea. Harmful Algae, 27: 98-112,
Karafas S, Teng S T, Leaw C P et al. 2017. An evaluation of the genus Amphidinium (Dinophyceae) combining evidence from morphology, phylogenetics, and toxin production, with the introduction of six novel species. Harmful Algae, 68: 128-151,
Karafas S, York R, Tomas C. 2015. Morphological and genetic analysis of the Coolia monotis species complex with the introduction of two new species, Coolia santacroce sp.nov. and Coolia palmyrensis sp. nov. (Dinophyceae).Harmful Algae, 46: 18-33,
Kudela R M, Berdalet E, Enevoldsen H et al. 2017. GEOHABthe global ecology and oceanography of harmful algal blooms program: motivation, goals, and legacy.Oceanography, 30(1): 12-21.
Larsson M E, Smith K F, Doblin M A. 2019. First description of the environmental niche of the epibenthic dinoflagellate species Coolia palmyrensis, C. malayensis, and C.tropicalis (Dinophyceae) from Eastern Australia. Journal of Phycology, 55(3): 565-577,
Leaw C P, Tan T H, Lim H C et al. 2016. New scenario for speciation in the benthic dinoflagellate genus Coolia(Dinophyceae). Harmful Algae, 55: 137-149,
Lee K H, Jeong H J, Park K et al. 2013. Morphology and molecular characterization of the epiphytic dinoflagellate Amphidinium massartii, isolated from the temperate waters off Jeju Island, Korea. Algae, 28(3): 213-231,
Lee L K, Lim Z F, Gu H et al. 2020. Effects of substratum and depth on benthic harmful dinoflagellate assemblages.Science Reports, 10(1): 11251,
Leung P T Y, Yan M, Lam V T T et al. 2018. Phylogeny, morphology and toxicity of benthic dinoflagellates of the genus Fukuyoa (Goniodomataceae, Dinophyceae)from a subtropical reef ecosystem in the South China Sea. Harmful Algae, 74: 78-97,
Leung P T Y, Yan M, Yiu S K F et al. 2017. Molecular phylogeny and toxicity of harmful benthic dinoflagellates Coolia (Ostreopsidaceae, Dinophyceae) in a sub-tropical marine ecosystem: the first record from Hong Kong.Marine Pollution Bulletin, 124(2): 878-889,
Lim A S, Jeong H J. 2021. Benthic dinoflagellates in Korean waters. Algae, 36(2): 91-109,
Lim Z F, Luo Z H, Lee L K et al. 2019. Taxonomy and toxicity of Prorocentrum from Perhentian Islands (Malaysia), with a description of a non-toxigenic species Prorocentrum malayense sp. nov. (Dinophyceae). Harmful Algae, 83:95-108,
Litaker R W, Vandersea M W, Faust M A et al. 2010. Global distribution of ciguatera causing dinoflagellates in the genus Gambierdiscus. Toxicon, 56(5): 711-730,
Luo Z H, Zhang H, Krock B et al. 2017. Morphology, molecular phylogeny and okadaic acid production of epibenthic Prorocentrum (Dinophyceae) species from the northern South China Sea. Algal Research, 22: 14-30,
Luo Z H, Zhang H, Li Q et al. 2022. Characterization of Amphidinium (Amphidiniales, Dinophyceae) species from the China Sea based on morphological, molecular, and pigment data. Journal of Oceanology and Limnology,
Mangialajo L, Ganzin N, Accoroni S et al. 2011. Trends in Ostreopsis proliferation along the Northern Mediterranean coasts. Toxicon, 57(3): 408-420,
Mangialajo L, Bertolotto R, Cattaneo-Vietti R et al. 2008.The toxic benthic dinoflagellate Ostreopsis ovata:quantification of proliferation along the coastline of Genoa, Italy. Marine Pollution Bullton, 56(6): 1209-1214,
Mohammad-Noor N, Daugbjerg N, Moestrup Ø et al. 2005.Marine epibenthic dinoflagellates from Malaysia-a study of live cultures and preserved samples based on light and scanning electron microscopy. Nordic Journal of Botany, 24(6): 629-690,
Monti M, Minocci M, Beran A et al. 2007. First record of Ostreopsis cfr. ovata on macroalgae in the Northern Adriatic Sea. Marine Pollution Bulletin, 54(5): 598-601,
Murray S, Patterson D J. 2002. The benthic dinoflagellate genus Amphidinium in south-eastern Australian waters, including three new species. European Journal of Phycology, 37(2): 279-298,
Mustapa N I, Yong H L, Lee L K et al. 2019. Growth and epiphytic behavior of three Gambierdiscus species(Dinophyceae) associated with various macroalgal substrates. Harmful Algae, 89: 101671,
Nascimento S M, Da Silva R A F, Oliveira F et al. 2019.Morphology and molecular phylogeny of Coolia tropicalis, Coolia malayensis and a new lineage of the Coolia canariensis species complex (Dinophyceae)isolated from Brazil. European Journal of Phycology, 54(3): 484-496, 1599449.
Nascimento S M, Mendes M C Q, Menezes M et al. 2017.Morphology and phylogeny of Prorocentrum caipirignum sp. nov. (Dinophyceae), a new tropical toxic benthic dinoflagellate. Harmful Algae, 70: 73-89,
Nascimento S M, Neves R A F, De’Carli G A L et al. 2020.Ostreopsis cf. ovata (Dinophyceae) molecular phylogeny, morphology, and detection of ovatoxins in strains and field samples from Brazil. Toxins, 12(2): 70,
Nishimura T, Sato S, Tawong W et al. 2013. Genetic diversity and distribution of the ciguatera-causing dinoflagellate Gambierdiscus spp. (Dinophyceae) in coastal areas of Japan. PLoS One, 8(4): ee60882,
Okolodkov Y B, Campos-Bautista G, Gárate-Lizárraga I et al. 2007. Seasonal changes of benthic and epiphytic dinoflagellates in the Veracruz reef zone, Gulf of Mexico.Aquatic Microbial Ecology, 47: 223-237,
Pagliara P, Caroppo C. 2012. Toxicity assessment of Amphidinium carterae, Coolia cfr. monotis and Ostreopsis cfr. ovata (Dinophyta) isolated from the northern Ionian Sea (Mediterranean Sea). Toxicon, 60(6): 1203-1214,
Parsons M L, Aligizaki K, Bottein M-Y D et al. 2012.Gambierdiscus and Ostreopsis: reassessment of the state of knowledge of their taxonomy, geography, ecophysiology, and toxicology. Harmful Algae, 14: 107-129, /10.1016/j.hal.2011.10.017.
Parsons M L, Preskitt L B J H. 2007. A survey of epiphytic dinoflagellates from the coastal waters of the island of Hawai‘i. Harmful Algae, 6(5): 658-669,
Penna A, Fraga S, Battocchi C et al. 2010. A phylogeographical study of the toxic benthic dinoflagellate genus Ostreopsis Schmidt. Journal of Biogeography, 37(5): 830-841,
Reñé A, Satta C T, López-García P et al. 2020. Re-evaluation of Amphidiniopsis (Dinophyceae) morphogroups based on phylogenetic relationships, and description of three new sand-dwelling species from the NW Mediterranean.Journal of Phycology, 56(1): 68-84,
Rhodes L, Smith K F. 2019. A checklist of the benthic and epiphytic marine dinoflagellates of New Zealand,including Rangitāhua/Kermadec Islands. New Zealand Journal of Marine and Freshwater Research, 53(2): 258-277,
Rhodes L. 2011. World-wide occurrence of the toxic dinoflagellate genus Ostreopsis Schmidt. Toxicon, 57(3):400-407,
Richlen M L, Lobel P S. 2011. Effects of depth, habitat, and water motion on the abundance and distribution of ciguatera dinoflagellates at Johnston Atoll, Pacific Ocean.Marine Ecology Progress Series, 421: 51-66,
Rodríguez F, Riobó P, Crespín G D et al. 2018. The toxic benthic dinoflagellate Prorocentrum maculosum Faust is a synonym of Prorocentrum hoffmannianum Faust.Harmful Algae, 78: 1-8,
Sato S, Nishimura T, Uehara K et al. 2011. Phylogeography of Ostreopsis along west Pacific coast, with special reference to a novel clade from Japan. PLoS One, 6(12): e27983,
Scholin C A, Herzog M, Sogin M et al. 1994. Identification of group-and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae). Ⅱ. Sequence analysis of a fragment of the LSU rRNA gene. Journal of Phycology, 30(6): 999-1011,
Shears N T, Ross P M. 2009. Blooms of benthic dinoflagellates of the genus Ostreopsis; an increasing and ecologically important phenomenon on temperate reefs in New Zealand and worldwide. Harmful Algae, 8(6): 916-925,
Taylor D L. 1971. On the symbiosis between Amphidinium klebsii [Dinophyceae] and Amphiscolops langerhansi[Turbellaria: Acoela]. Journal of the Marine Biological Association of the United Kingdom, 51(2): 301-313,
Torres-Ariño A, Okolodkov Y B, Herrera-Herrera N V. 2019.A checklist of phytoplankton and microphytobenthos of the southeastern Mexican Pacific. Cymbella, 5(1): 1-97.
Tripuraneni J, Koutsouris A, Pestic L et al. 1997. The toxin of diarrheic shellfish poisoning, okadaic acid, increases intestinal epithelial paracellular permeability.Gastroenterology, 112(1): 100-108,
Widiarti R, Anggrain F. 2012. The distribution of toxic dinoflagellates on sea grass Enhalus acoroides at Pari Island, Seribu Islands. Jurnal Ilmu dan Teknologi Kelautan Tropis, 4(2): 259-266,
Yasumoto T, Nakajima I, Bagnis R et al. 1977. Finding of a dinoflagellate as a likely culprit of ciguatera. Nippon Suisan Gakkaishi, 43(8): 1021-1026,
Yasumoto T, Seino N, Murakami Y et al. 1987. Toxins produced by benthic dinoflagellates. Biological Bulletin, 172(1): 128-131,
Yong H L, Mustapa N I, Lee L K et al. 2018. Habitat complexity affects benthic harmful dinoflagellate assemblages in the fringing reef of Rawa Island, Malaysia. Harmful Algae, 78: 56-68,
Zhang H, Li Y, Cen J Y et al. 2015. Morphotypes of Prorocentrum lima (Dinophyceae) from Hainan Island, South China Sea: morphological and molecular characterization. Phycologia, 54(5): 503-516,
Zhang H, Lü S H, Cen J Y et al. 2021. Morphology and molecular phylogeny of three species of Coolia(Dinophyceae) from Hainan Island, South China Sea.Journal of Oceanology and Limnology, 39(3): 1020-1032,
Zhang H, Lu S H, Li Y et al. 2018. Morphology and molecular phylogeny of Ostreopsis cf. ovata and O. lenticularis(Dinophyceae) from Hainan Island, South China Sea. Phycological Research, 66(1): 3-14,
Zhang H, Wu Z, Cen J Y et al. 2016. First report of three benthic dinoflagellates, Gambierdiscus pacificus, G.australes and G. Caribaeus (Dinophyceae), from Hainan Island, South China Sea. Phycological Research, 64(4):259-273,
Zheng J P, Li Q, Lv S H et al. 2017. Production of Palytoxins by two strains of Ostreopsis sp. (Dinophyceae) from Weizhou Island, Guangxi, China. Ecology and Environment Sciences, 26(4): 663-670, (in Chinese with English abstract)
Zou J, Li Q, Liu H et al. 2021. Taxonomy and toxin profile of harmful benthic Prorocentrum (Dinophyceae) species from the Xisha Islands, South China Sea. Journal of Oceanology and Limnology,
Zou J, Li Q, Lu S H et al. 2020. The first benthic harmful dinoflagellate bloom in China: morphology and toxicology of Prorocentrum concavum. Marine Pollution Bulletin, 158: 111313,
Copyright © Haiyang Xuebao