ALGAE

  • 제36권3호
  • /
  • Pages.175-193
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  • 2021
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  • 1226-2617(pISSN)
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  • 2093-0860(eISSN)
한국조류학회(藻類) (The Korean Society of Phycology)
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Characterization of Coolia spp. (Gonyaucales, Dinophyceae) from Southern Tunisia: first record of Coolia malayensis in the Mediterranean Sea

  • 투고 : 2020.11.21
  • 심사 : 2021.06.02
  • 발행 : 2021.09.15
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초록

This study provides the first report of the presence of Coolia malayensis in the Mediterranean Sea, co-occurring with C. monotis. Isolated strains from the Gulf of Gabès, Tunisia (South-eastern Mediterranean) were identified by morphological characterization and phylogenetic analysis. Examination by light and scanning electron microscopy revealed no significant morphological differences between the Tunisian isolates and other geographically distant strains of C. monotis and C. malayensis. Phylogenetic trees based on ITS1-5.8S-ITS2 and D1-D3/28S rDNA sequences showed that C. monotis strains clustered with others from the Mediterranean and Atlantic whereas the C. malayensis isolate branched with isolates from the Pacific and the Atlantic, therefore revealing no geographical trend among C. monotis and C. malayensis populations. Ultrastructural analyses by transmission electron microscopy revealed the presence of numerous vesicles containing spirally coiled fibers in both C. malayensis and C. monotis cells, which we speculate to be involved in mucus production.

키워드

과제정보

We are grateful to Dr. Isabella Percopo (Electron Microscopy Service, Stazione Zoologica Anton Dohrn) for their assistance in scanning electron microscopy analyses. This work is carried out under the MOBIDOC scheme, funded by the EU through the EMORI program and managed by the ANPR. This study was partially supported by the European funded project "Improving National Capacities in Observation and Management of Marine Environment in Tunisia" (INCOMMET, 295009).

참고문헌

  1. Abdennadher, M., Bellaaj Zouari, A., Feki Sahnoun, W., Alverca, E., Penna, A. & Hamza, A. 2017. Ostreopsis cf. ovata in the Gulf of Gabes (south-eastern Mediterranean Sea): morphological, molecular and ecological characterization. Harmful Algae 63:56-67. https://doi.org/10.1016/j.hal.2017.01.009
  2. Abdennadher, M., Bellaaj Zouari, A., Feki Sahnoun, W., Dammak Walha, L., Mahfoudi, M. & Hamza, A. 2020. A long-term study on Coolia monotis distribution from the South-east Mediterranean Sea. Cont. Shelf. Res. 211:104267. https://doi.org/10.1016/j.csr.2020.104267
  3. Adachi, M., Sako, Y. & Ishida, Y. 1994. Restriction fragment length polymorphism of ribosomal DNA internal transcribed spacer and 5.8S regions in Japanese Alexandrium species (Dinophyceae). J. Phycol. 30:857-865. https://doi.org/10.1111/j.0022-3646.1994.00857.x
  4. 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. Bull. Jpn. Soc. Sci. Fish. 45:67-71. https://doi.org/10.2331/suisan.45.67
  5. Aligizaki, K. & Nikolaidis, G. 2006. The presence of the potentially toxic genera Ostreopsis and Coolia (Dinophyceae) in the north Aegean Sea, Greece. Harmful Algae 5:717-730. https://doi.org/10.1016/j.hal.2006.02.005
  6. Al-Yamani, F. Y. & Saburova, M. A. 2010. Illustrated guide on the flagellates of Kuwait's intertidal soft sediments. Kuwait Institute for Scientific Research, Safat, 197 pp.
  7. Andersen, R. A. 2005. Algal culturing techniques. Elsevier Academic Press, Burlington, MA, 565 pp.
  8. Armi, Z., Turki, S., Trabelsi, E. & Maiz, N. B. 2010. First recorded proliferation of Coolia monotis (Meunier, 1919) in the North Lake of Tunis (Tunisia) correlation with environmental factors. Environ. Monit. Assess. 164:423-433. https://doi.org/10.1007/s10661-009-0903-z
  9. Balech, E. 1956. Etude des Dinoflagelles du sable de Roscoff. Rev. Algol. 2:29-52.
  10. Ben-Gharbia, H., Yahia, O. K. -D., Amzil, Z., Chomerat, N., Abadie, E., Masseret, E., Sibat, M., Triki, H. Z., Nouri, H. & Laabir, M. 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 8:297. https://doi.org/10.3390/toxins8100297
  11. Ben Ismail, S., Sammari, C., Gasparini, G. P., Beranger, K., Brahim, M. & Aleya, L. 2012. Water masses exchanged through the Channel of Sicily: evidence for the presence of new water masses on the Tunisian side of the channel. Deep Sea Res. I Oceanogr. Res. Pap. I 63:65-81. https://doi.org/10.1016/j.dsr.2011.12.009
  12. Ben Ismail, S., Schroeder, K., Sammari, C., Gasparini, G. P., Borghinic, M. & Aleya, L. 2014. Interannual variability of water mass properties in the Tunisia-Sicily Channel. J. Mar. Syst. 135:14-28. https://doi.org/10.1016/j.jmarsys.2013.06.010
  13. Besada, E. G., Loeblich, L. A. & Loeblich, A. R. 3rd. 1982. Observations on tropical, benthic dinoflagellates from ciguatera-endemic areas: Coolia, Gambierdiscus, and Ostreopsis. Bull. Mar. Sci. 32:723-735.
  14. Bianchi, C. N. & Morri, C. 2000. Marine biodiversity of the Mediterranean Sea: situation, problems and prospects for future research. Mar. Pollut. Bull. 40:367-376. https://doi.org/10.1016/S0025-326X(00)00027-8
  15. Calic, M., Ljubimir, S., Bosak, S. & Car, A. 2018. First records of two planktonic Indo-Pacific diatoms: Chaetoceros bacteriastroides and C. pseudosymmetricus in the Adriatic Sea. Oceanologia 60:101-105. https://doi.org/10.1016/j.oceano.2017.07.005
  16. Claparede, E. & Lachmann, J. 1859. Etudes sur les infusoires et les rhizopodes. Mem. l'Inst. Natl. Genev. 6:261-482.
  17. Dammak-Zouari, H., Hamza, A. & Bouain, A. 2009. Gymnodiniales in the Gulf of Gabes (Tunisia). Cah. Biol. Mar. 50:153-170.
  18. David, H., Laza-Martinez, A., Miguel, I. & Orive, E. 2014. Broad distribution of Coolia monotis and restricted distribution of Coolia cf. canariensis (Dinophyceae) in the Atlantic coast of the Iberian Peninsula. Phycologia 53:342-352. https://doi.org/10.2216/13-214.1
  19. David, H., Laza-Martinez, A., Rodriguez, F., Fraga, S. & Orive, E. 2019. Coolia guanchica sp. nov. (Dinophyceae) a new epibenthic dinoflagellate from the Canary Islands (NE Atlantic Ocean). Eur. J. Phycol. 55:76-88. https://doi.org/10.1080/09670262.2019.1651400
  20. Dolapsakis, N. P., Kilpatrick, M. W., Economou-Amilli, A. & Tafas, T. 2006. Morphology and rDNA phylogeny of a Mediterranean Coolia monotis (Dinophyceae) strain from Greece. Sci. Mar. 70:67-76.
  21. Faust, M. A. 1995. Observation of sand-dwelling toxic dinoflagellates (Dinophyceae) from widely differing sites, including two new species. J. Phycol. 31:996-1003. https://doi.org/10.1111/j.0022-3646.1995.00996.x
  22. Faust, M. A. 2009. Ciguatera-causing dinoflagellates in a coral-reef mangrove ecosystem, Belize. Atoll Res. Bull. 569:1-32. https://doi.org/10.5479/si.00775630.569.1
  23. Felsenstein, J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17:368-376. https://doi.org/10.1007/BF01734359
  24. Fraga, S., Penna, A., Bianconi, I., Paz, B. & Zapata, M. 2008. Coolia canariensis sp. nov. (Dinophyceae), a new nontoxic epiphytic benthic dinoflagellate from the Canary Islands. J. Phycol. 44:1060-1070. https://doi.org/10.1111/j.1529-8817.2008.00555.x
  25. Fredj, G., Bellan-Santin, D. & Meinardi, M. 1992. Etat des connaissances sur la faune marine mediterraneenne. Bull. l'Inst. Oceanogr. Monaco 9:133-145.
  26. Galil, B. S. 2009. Taking stock: inventory of alien species in the Mediterranean Sea. Biol. Invasions 11:359-372. https://doi.org/10.1007/s10530-008-9253-y
  27. Giussani, V., Sbrana, F., Asnaghi, V., Vassalli, M., Faimali, M., Casabianca, S., Penna, A., Ciminiello, P., Dell'Aversano, C., Tartaglione, L., Mazzeo, A. & Chiantore, M. 2015. Active role of the mucilage in the toxicity mechanism of the harmful benthic dinoflagellate Ostreopsis cf. ovata. Harmful Algae 44:46-53. https://doi.org/10.1016/j.hal.2015.02.006
  28. Gomez, F. 2003a. Checklist of Mediterranean free-living dinoflagellates. Bot. Mar. 46:215-242. https://doi.org/10.1515/BOT.2003.021
  29. Gomez, F. 2003b. The toxic dinoflagellate Gymnodinium catenatum: an invader in the Mediterranean Sea. Acta Bot. Croat. 62:65-72.
  30. Gomez, F. 2006. Endemic and Indo-Pacific plankton in the Mediterranean Sea: a study based on dinoflagellate records. J. Biogeogr. 33:261-270. https://doi.org/10.1111/j.1365-2699.2005.01373.x
  31. Gomez, F., Echevarria, F., Garcia, C. M., Prieto, L., Ruiz, J., Reul, A., Jimenez-Gomez, F. & Varela, M. 2000. Microplankton distribution in the Strait of Gibraltar: coupling between organisms and hydrodynamic structures. J. Plankton Res. 22:603-617. https://doi.org/10.1093/plankt/22.4.603
  32. Gomez, F., Qiu, D., Otero-Morales, E., Lopes, R. M. & Lin, S. 2016. Circumtropical distribution of the epiphytic dinoflagellate Coolia malayensis (Dinophyceae): morphology and molecular phylogeny from Puerto Rico and Brazil. Phycol. Res. 64:194-199. https://doi.org/10.1111/pre.12134
  33. Guillard, R. R. L. & Hargraves, P. E. 1993. Stichochrysis inmobilis is a diatom, not a chrysophyte. Phycologia 32:234-236. https://doi.org/10.2216/i0031-8884-32-3-234.1
  34. Halim, Y. 1960. Etude quantitative et qualitative du cycle ecologique des Dinoflagelles dans les eaux de Villefranche-sur-Mer. Ann. Inst. Oceanogr. 38:123-232.
  35. Hallegraeff, G. M. 1993. A review of harmful algal blooms and their apparent global increase. Phycologia 32:79-99. https://doi.org/10.2216/i0031-8884-32-2-79.1
  36. Hattour, A. & Ben Mustapha, K. 2013. Le couvert vegetal marin du golfe de Gabes: Cartographie et reseau de surveillance de l'herbier de Posidonie. Institut National des Sciences et Technologies de la Mer, Salammbo, 164 pp.
  37. Haywood, A. J., Steidinger, K. A., Truby, E. W., Bergquist, P. R., Bergquist, P. L., Adamson, J. & MacKenzie, L. 2004. Comparative morphology and molecular phylogenetic analysis of three new species of the genus Karenia (Dinophyceae) from New Zealand. J. Phycol. 40:165-179. https://doi.org/10.1111/j.0022-3646.2004.02-149.x
  38. 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 Sci. J. 49:211-221. https://doi.org/10.1007/s12601-014-0021-x
  39. Holmes, M. J., Lewis, R. J., Jones, A. & Hoy, A. W. 1995. Cooliatoxin, the first toxin from Coolia monotis (Dinophyceae). Nat. Toxins 3:355-362. https://doi.org/10.1002/nt.2620030506
  40. Honsell, G., Bonifacio, A., De Bortoli, M., Penna, A., Battocchi, C., Ciminiello, P., Dell'Aversano, C., Fattorusso, E., Sosa, S., Yasumoto, T. & Tubaro, A. 2013. New insights on cytological and metabolic features of Ostreopsis cf. ovata Fukuyo (Dinophyceae): a multidisciplinary approach. PLoS ONE 8:e57291. https://doi.org/10.1371/journal.pone.0057291
  41. Ismael, A. A. 2014. First record of Coolia monotis Meunier along Alexandria coast: Egypt. Egypt. J. Aquat. Res. 40: 19-25. https://doi.org/10.1016/j.ejar.2014.02.002
  42. 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. https://doi.org/10.1016/j.hal.2015.05.002
  43. Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35:1547-1549. https://doi.org/10.1093/molbev/msy096
  44. 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. J. Phycol. 55:565-577. https://doi.org/10.1111/jpy.12833
  45. Laza-Martinez, A., Orive, E. & Miguel, I. 2011. Morphological and genetic characterization of benthic dinoflagellates of the genera Coolia, Ostreopsis, and Prorocentrum from the south-eastern Bay of Biscay. Eur. J. Phycol. 46:45-65. https://doi.org/10.1080/09670262.2010.550387
  46. Leaw, C. P., Lim, P. T., Ahmad, A. & Usup, G. 2001. Genetic diversity of Ostreopsis ovata (Dinophyceae) from Malaysia. Mar. Biotechnol. 3:246-255. https://doi.org/10.1007/s101260000073
  47. Leaw, C. -P., Lim, P. -T., Chen, K. -W., Ng, B. -K. & Usup, G. 2010. Morphology and molecular characterization of a new species of thecate benthic dinoflagellate, Coolia malayensis sp. nov. (Dinophyceae). J. Phycol. 46:162-171. https://doi.org/10.1111/j.1529-8817.2009.00778.x
  48. Leaw, C. P., Tan, T. H., Lim, H. C., Teng, S. T., Yong, H. L., Smith, K. F., Rhodes, L., Wolf, M., Holland, W. C., Vandersea, M. W., Litaker, R. W., Tester, P. A., Gu, H., Usup, G. & Lim, P. T. 2016. New scenario for speciation in the benthic dinoflagellate genus Coolia (Dinophyceae). Harmful Algae 55:137-149. https://doi.org/10.1016/j.hal.2016.02.010
  49. Leung, P. T. Y., Yan, M., Yiu, S. K. F., Lam, V. T. T., Ip, J. C. H., Au, M. W. Y., Chen, C. -Y., Wai, T. -C. & Lam, P. K. S. 2017. Molecular phylogeny and toxicity of harmful benthic dinoflagellates Coolia (Ostreopsidaceae, Dinophyceae) in a sub-tropical marine ecosystem: the first record from Hong Kong. Mar. Pollut. Bull. 124:878-889. https://doi.org/10.1016/j.marpolbul.2017.01.017
  50. Lewis, N. I., Wolny, J. L., Achenbach, J. C., Ellis, L., Pitula, J. S., Rafuse, C., Rosales, D. S. & McCarron, P. 2018. Identification, growth and toxicity assessment of Coolia Meunier (Dinophyceae) from Nova Scotia, Canada. Harmful Algae 75:45-56. https://doi.org/10.1016/j.hal.2018.04.001
  51. Loukil-Baklouti, A., Feki-Sahnoun, W., Hamza, A., Abdennadher, M., Mahfoudhi, M., Bouain, A. & Jarboui, O. 2018. Controlling factors of harmful microalgae distribution in water column, biofilm and sediment in shellfish production area (South of Sfax, Gulf of Gabes) from southern Tunisia. Cont. Shelf Res. 152:61-70. https://doi.org/10.1016/j.csr.2017.11.003
  52. Madeira, F., Park, Y. M., Lee, J., Buso, N., Gur, T., Madhusoodanan, N., Basutkar, P., Tivey, A. R. N., Potter, S. C, Finn, R. D. & Lopez, R. 2019. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res. 47:W636-W641. https://doi.org/10.1093/nar/gkz268
  53. Mendes, M. C. Q., Nunes, J. M. C., Fraga, S., Rodriguez, F., Franco, J. M., Riobo, P., Branco, S. & Menezes, M. 2019. Morphology, molecular phylogeny and toxinology of Coolia and Prorocentrum strains isolated from the tropical South Western Atlantic Ocean. Bot. Mar. 62:125-140. https://doi.org/10.1515/bot-2018-0053
  54. Meunier, A. 1919. Microplankton de la Mer Flamande. III. Les Peridiniens. Mem. Mus. R. Hist. Nat. Belg. 8:116-144.
  55. Mikulski, C. M., Morton, S. L. & Doucette, G. J. 2005. Development and application of LSU rRNA probes for Karenia brevis in the Gulf of Mexico, USA. Harmful Algae 4:49-60. https://doi.org/10.1016/j.hal.2003.11.001
  56. Mohammad Noor, N., Adam, A., Saad, S., Khodzori, F. A. & Shaleh, S. R. M. 2019. Substrate preference and effects of medium with soil extract on growth of genus Coolia (Dinophyceae). J. Sustain. Sci. Manag. 14:71-81.
  57. Mohammad-Noor, N., Moestrup, O., Lundholm, N., Fraga, S., Adam, A., Holmes, M. J. & Saleh, E. 2013. Autecology and phylogeny of Coolia tropicalis and Coolia malayensis (Dinophyceae), with emphasis on taxonomy of C. tropicalis based on light microscopy, scanning electron microscopy and LSU rDNA. J. Phycol. 49:536-545. https://doi.org/10.1111/jpy.12062
  58. Momigliano, P., Sparrow, L., Blair, D. & Heimann, K. 2013. The diversity of Coolia spp. (Dinophyceae Ostreopsidaceae) in the Central Great Barrier Reef Region. PLoS ONE 8:e79278. https://doi.org/10.1371/journal.pone.0079278
  59. Moncer, M., Hamza, A., Feki-Sahnoun, W., Mabrouk, L. & Bel Hassen, M. 2017. Variability patterns of epibenthic microalgae in eastern Tunisian coasts. Sci. Mar. 81:487-498. https://doi.org/10.3989/scimar.04651.17A
  60. Nascimento, S. M., da Silva, R. A. F., Oliveira, F., Fraga, S. & Salgueiro, F. 2019. Morphology and molecular phylogeny of Coolia tropicalis, Coolia malayensis and a new lineage of the Coolia canariensis species complex (Dinophyceae) isolated from Brazil. Eur. J. Phycol. 54:484-496. https://doi.org/10.1080/09670262.2019.1599449
  61. Nguyen, N. L. & Larsen, J. 2004. Gonyaulacales. In Larsen, J. & Nguyen, N. L. (Eds.) Guide to the Identification of Potentially Toxic Microalgae in Vietnamese Waters. Opera Bot. 140, Copenhagen, pp. 73-116.
  62. Office de la Marine Marchande et des Ports. 2019. Rapport annuel. Office de la Marine Marchande et des Ports, La Goulette, 46 pp.
  63. 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 60:1203-1214. https://doi.org/10.1016/j.toxicon.2012.08.005
  64. Penna, A., Vila, M., Fraga, S., Giacobbe, M. G., Andreoni, F., Riobo, P. & Vernesi, C. 2005. Characterization of Ostreopsis and Coolia (Dinophyceae) isolates in the western Mediterranean Sea based on morphology, toxicity and internal transcribed spacer 5.8S rDNA sequences. J. Phycol. 41:212-225. https://doi.org/10.1111/j.1529-8817.2005.04011.x
  65. Reynolds, C. S. 2007. Variability in the provision and function of mucilage in phytoplankton: facultative responses to the environment. Hydrobiologia 578:37-45. https://doi.org/10.1007/s10750-006-0431-6
  66. Rhodes, L., Smith, K., Harwood, T. & Bedford, C. 2014a. Novel and toxin-producing epiphytic dinoflagellates isolated from sub-tropical Raoul Island, Kermadec Islands group. N. Z. J. Mar. Freshw. Res. 48:594-599. https://doi.org/10.1080/00288330.2014.963127
  67. Rhodes, L., Smith, K., Papiol, G. G., Adamson, J., Harwood, T. & Munday, R. 2014b. Epiphytic dinoflagellates in subtropical New Zealand, in particular the genus Coolia Meuneir. Harmful Algae 34:36-41. https://doi.org/10.1016/j.hal.2014.02.004
  68. Rhodes, L. L. & Thomas, A. E. 1997. Coolia monotis (Dinophyceae): a toxic epiphytic microalgal species found in New Zealand (note). N. Z. J. Mar. Freshw. Res. 31:139-141. https://doi.org/10.1080/00288330.1997.9516751
  69. Scholin, C. A., Herzog, M., Sogin, M. & Anderson, D. M. 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. J. Phycol. 30:999-1011. https://doi.org/10.1111/j.0022-3646.1994.00999.x
  70. Shah, M. M. R., Samarakoon, K. W., Ko, J. -Y., Chaminda Lakmal, H. H., Lee, J. -H., An, S. -J., Jeon, Y. -J. & Lee, J. -B. 2014. Potentiality of benthic dinoflagellate cultures and screening of their bioactivities in Jeju Island, Korea. Afr. J. Biotechnol. 13:792-805. https://doi.org/10.5897/AJB2013.13250
  71. Tamura, K. 1992. Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Mol. Biol. Evol. 9:678-687.
  72. Tamura, K. & Nei, M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10:512-526.
  73. Tawong, W., Nishimura, T., Sakanari, H., Sato, S., Yamaguchi, H. & Adachi, M. 2015. Characterization of Gambierdiscus and Coolia (Dinophyceae) isolates from Thailand based on morphology and phylogeny. Phycol. Res. 63:125-133. https://doi.org/10.1111/pre.12074
  74. Ten-Hage, L., Turquet, J., Quod, J. P. & Coute, A. 2000. Coolia areolata sp. nov. (Dinophyceae), a new sand-dwelling dinoflagellate from the southwestern Indian Ocean. Phycologia 39:377-383. https://doi.org/10.2216/i0031-8884-39-5-377.1
  75. Tibirica, C. E. J. A., Sibat, M., Fernandes, L. F., Bilien, G., Chomerat, N., Hess, P. & Mafra, L. L. Jr. 2020. Diversity and toxicity of the genus Coolia Meunier in Brazil, and detection of 44-methyl gambierone in Coolia tropicalis. Toxins 12:327. https://doi.org/10.3390/toxins12050327
  76. Vila, M., Garces, E. & Maso, M. 2001. Potentially epiphytic dinoflagellate assemblages on macroalgae in the NW Mediterranean. Aquat. Microbiol. Ecol. 26:51-60. https://doi.org/10.3354/ame026051
  77. Wakeman, K. C., Yamaguchi, A., Roy, M. C. & Jenke-Kodama, H. 2015. Morphology, phylogeny and novel chemical compounds from Coolia malayensis (Dinophyceae) from Okinawa, Japan. Harmful Algae 44:8-19. https://doi.org/10.1016/j.hal.2015.02.009
  78. Zhang, H., Lu, S., Cen, J., Li, Y., Li, Q. & Wu, Z. 2020. Morphology and molecular phylogeny of three species of Coolia (Dinophyceae) from Hainan Island, South China Sea. J. Oceanol. Limnol. Advanced publication. https://doi.org/10.1007/s00343-020-9326-z.