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Morphological and molecular characterization of the genus Coolia (Dinophyceae) from Bahía de La Paz, southwest Gulf of California

  • Morquecho, Lourdes (Programa de Planeacion Ambiental y Conservacion, Centro de Investigaciones Biologicas del Noroeste (CIBNOR)) ;
  • Garate-Lizarraga, Ismael (Instituto Politecnico Nacional, Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN)) ;
  • Gu, Haifeng (Department of Marine Biodiversity, Third Institute of Oceanography, Ministry of Natural Resources)
  • Received : 2022.01.24
  • Accepted : 2022.09.02
  • Published : 2022.09.15
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Abstract

The genus Coolia A. Meunier 1919 has a global distribution and is a common member of epiphytic dinoflagellate assemblages in neritic ecosystems. Coolia monotis is the type species of the genus and was the only known species for 76 years. Over the past few decades, molecular characterization has unveiled two species complexes that group morphologically very similar species, so their limits are often unclear. To provide new knowledge on the biogeography and species composition of the genus Coolia, 16 strains were isolated from Bahía de La Paz, Gulf of California. The species were identified by applying morphological and molecular approaches. The morphometric characteristics of all isolated Coolia species were consistent with the original taxa descriptions. Phylogenetic analyses (large subunit [LSU] rDNA D1 / D2 and internal transcribed spacer [ITS] 1 / 5.8S / ITS2) revealed a species assemblage comprising Coolia malayensis, C. palmyrensis, C. tropicalis, and the C. cf. canariensis lineage. This is the first report of Coolia palmyrensis and C. cf. canariensis in Mexico and C. tropicalis in the Gulf of California. Our results strengthen the biogeographical understanding of these potentially harmful epiphytic dinoflagellate species.

Keywords

Acknowledgement

Jorge Angulo-Calvillo and Enrique Calvillo-Espinoza provided technical assistance in the field as divers and boat drivers. Amada Reyes-Salinas, Alejandra Mazariegos-Villarreal and Ariel Cruz-Villacorta provided technical assistance. Thelma Castellanos, Angel Carrillo and Goretty Caamal provided technical advice and infrastructure of the Molecular Microbial Ecology Laboratory. All are at CIBNOR. Yuri Okolodkov (Universidad Veracruzana) assisted during the 2016 macroalgae sampling. Laura E. Gomez-Lizarraga (SAMEB, ICMyL-UNAM) also provided technical assistance. This study was supported by the CIBNOR project 20014, and the CONACYT A1-S-37026 grant. IGL was supported by SIP-20190272 and COFAA. Taylor Morey provided English revision. Maria Elena Sanchez-Salazar edited the English manuscript.

References

  1. Abdennadher, M., Zouari, A. B., Medhioub, W., Penna, A. & Hamza, A. 2021. Characterization of Coolia spp. (Gonyaucales, Dinophyceae) from Southern Tunisia: first record of Coolia malayensis in the Mediterranean Sea. Algae 36:175-193. https://doi.org/10.4490/algae.2021.36.6.2
  2. Accoroni, S., Romagnoli, T., Penna, A., Capellacci, S., Ciminiello, P., Dell'Aversano, C., Tartaglione, L., Abboud-Abi Saab, M., Giussani, V., Asnaghi, V., Chiantore, M. & Totti, C. 2016. Ostreopsis fattorussoi sp. nov. (Dinophyceae), a new benthic toxic Ostreopsis species from the eastern Mediterranean Sea. J. Phycol. 52:1064-1084. https://doi.org/10.1111/jpy.12464
  3. Adachi, M., Sako, Y. & Ishida, Y. 1996. Analysis of Alexandrium (Dinophyceae) species using sequences of the 5.8S ribosomal DNA and internal transcribed spacer regions. J. Phycol. 32:424-432. https://doi.org/10.1111/j.0022-3646.1996.00424.x
  4. Akselman, R. & Fraga, S. 2022. Other Gonyaulacales, IOCUNESCO taxonomic reference list of harmful micro algae. Available from: https://www.marinespecies.org/hab. Accessed Jun 20, 2022.
  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. Almazan-Becerril, A., Escobar-Morales, S., Rosiles-Gonzalez, G. & Valadez, F. 2015. Benthic-epiphytic dinoflagellates from the northern portion of the Mesoamerican Reef System. Bot. Mar. 58:115-128. https://doi.org/10.1515/bot-2014-0093
  7. Almazan-Becerril, A., Rosiles-Gonzalez, G., Escobar-Morales, S., Rodriguez-Palacios, M. & Hernandez-Becerril, D. U. 2012. Dinoflagelados bentonicos del Arrecife Mesoamericano: Caribe Mexicano. Informe final SNIBCONABIO. Proyecto No. HJ033. Available from: https://www.gbif.org/es/dataset/ad9da392-a0ae-492f-ad51-24bf0fe1264c (in Spanish). Accessed Jun 20, 2022.
  8. Anderson, D. M., Kulis, D. M. & Binder, B. J. 1984. Sexuality and cyst formation in the dinoflagellate Gonyaulax tamarensis: cyst yield in batch cultures. J. Phycol. 20:418-425. https://doi.org/10.1111/j.0022-3646.1984.00418.x
  9. Benson, D. A., Cavanaugh, M., Clark, K., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J. & Sayers, E. W. 2013. GenBank. Nucleic Acids Res. 41:D36-D42.
  10. Boc, A., Diallo, A. B. & Makarenkov, V. 2012. T-REX: a web server for inferring, validating and visualizing phylogenetic trees and networks. Nucleic Acids Res. 40:W573-W579. https://doi.org/10.1093/nar/gks485
  11. Bomber, J. W. & Aikman, K. E. 1989. The Ciguatera Dinoflagellates. Biol. Oceanogr. 6:291-311.
  12. Caruana, A. M. N. & Amzil, Z. 2018. Microalgae and toxins. In Levine, I. A. & Fleurence, J. (Eds.) Microalgae in Health and Disease Prevention. Elsevier, Amsterdam, pp. 263-305.
  13. David, H., Laza-Martinez, A., Miguel, I. & Orive, E. 2014. Broad distribution of Coolia monotis and restricted distribution of Coolia cf. canariensis (Dinophyceae) on the Atlantic coast of the Iberian Peninsula. Phycologia 53:342-352. https://doi.org/10.2216/13-214.1
  14. David, H., Laza-Martinez, A., Rodriguez, F., Fraga, S. & Orive, E. 2020. 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
  15. de Queiroz-Mendes, M., de Castro-Nunes, J., 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
  16. Doblin, M. A., Blackburn, S. I. & Hallegraeff, G. M. 1999. Comparative study of selenium requirements of three phytoplankton species: Gymnodinium catenatum, Alexandrium minutum (Dinophyta) and Chaetoceros cf. tenuissimus (Bacillariophyta). J. Plankton Res. 21:1153-1169. https://doi.org/10.1093/plankt/21.6.1153
  17. 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.
  18. 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
  19. 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
  20. Fraga, S. & Rodriguez, F. 2014. Genus Gambierdiscus in the Canary Islands (NE Atlantic Ocean) with description of Gambierdiscus silvae sp. nov., a new potentially toxic epiphytic benthic dinoflagellate. Protist 165:839-853. https://doi.org/10.1016/j.protis.2014.09.003
  21. Fraga, S., Rodriguez, F., Bravo, I., Zapata, M. & Maranon, E. 2012. Review of the main ecological features affecting benthic dinoflagellate blooms. Cryptogam. Algol. 33:171-179. https://doi.org/10.7872/crya.v33.iss2.2011.171
  22. Fraga, S., Rodriguez, F., Caillaud, A., Diogene, J., Raho, N. & Zapata, M. 2011. Gambierdiscus excentricus sp. nov. (Dinophyceae), a benthic toxic dinoflagellate from the Canary Islands (NE Atlantic Ocean). Harmful Algae 11:10-22. https://doi.org/10.1016/j.hal.2011.06.013
  23. Fraga, S., Rodriguez, F., Riobo, P. & Bravo, I. 2016. Gambierdiscus balechii sp. nov. (Dinophyceae), a new benthic toxic dinoflagellate from the Celebes Sea (SW Pacific Ocean). Harmful Algae 58:93-105. https://doi.org/10.1016/j.hal.2016.06.004
  24. Garate-Lizarraga, I., Gonzalez-Armas, R., Verdugo-Diaz, G., Okolodkov, Y. B., Perez-Cruz, B. & Diaz-Ortiz, J. A. 2019. Seasonality of the dinoflagellate Amphidinium cf. carterae (Dinophyceae: Amphidiniales) in Bahia de La Paz, Gulf of California. Mar. Pollut. Bull. 146:532-541. https://doi.org/10.1016/j.marpolbul.2019.06.073
  25. GEOHAB. 2012. Global ecology and oceanography of harmful algal blooms. GEOHAB Core Research Project. In Berdalet, E., Tester, P. & Zingone, A. (Eds.) Harmful Algal Blooms in Benthic Systems. IOC of UNESCO and SCOR, Paris and Newark, pp. 1-64.
  26. 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
  27. Guillard, R. R. L. & Hargraves, P. E. 1993. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32:234-236. https://doi.org/10.2216/i0031-8884-32-3-234.1
  28. Guillard, R. R. L. & Ryther, J. H. 1962. Studies on marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervaceae (Cleve) Gran. Can. J. Microbiol. 8:229-239. https://doi.org/10.1139/m62-029
  29. Guiry, M. D. & Guiry, G. M. 2021. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available from: http://www.algaebase.org. Accessed Dec 10, 2021.
  30. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
  31. Herrera-Sepulveda, A., Hernandez-Saavedra, N. Y., Medlin, L. K. & West, N. 2013. Capillary electrophoresis finger print technique (CE-SSCP): an alternative tool for the monitoring activities of HAB species in Baja California Sur Costal. Environ. Sci. Pollut. Res. Int. 20:6863-6871. https://doi.org/10.1007/s11356-012-1033-7
  32. Herzi, F., Jean, N., Zhao, H., Mounier, S., Mabrouk, H. H. & Hlaili, A. S. 2013. Copper and cadmium effects on growth and extracellular exudation of the marine toxic dinoflagellate Alexandrium catenella: 3D-fluorescence spectroscopy approach. Chemosphere 93:1230-1239. https://doi.org/10.1016/j.chemosphere.2013.06.084
  33. 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
  34. Hoppenrath, M. 2022. Prorocentrales. IOC-UNESCO taxonomic reference list of harmful micro algae. Available from: http://www.marinespecies.org/hab. Accessed Jun 17, 2022.
  35. Hoppenrath, M., Murray, S. A., Chomerat, N. & Horiguchi, T. 2014. Marine benthic dinoflagellates: unveiling their worldwide biodiversity. Kleine Senckenberg-Reihe, Band 54. Schweizerbart Science Publishers, Stuttgart, 276 pp.
  36. Irola-Sansores, E. D., Delgado-Pech, B., Garcia-Mendoza, E., Nunez-Vazquez, E. J., Olivos-Ortiz, A. & AlmazanBecerril, A. 2018. Population dynamics of benthic-epiphytic dinoflagellates on two macroalgae from coral reef systems of the Northern Mexican Caribbean. Front. Mar. Sci. 5:487. https://doi.org/10.3389/fmars.2018.00487
  37. 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. https://doi.org/10.1016/j.hal.2018.11.007
  38. Jeong, H. J., Yih, W., Kang, N. S., Lee, S. Y., Yoon, E. Y., Yoo, Y. D., Kim, H. S. & Kim, J. H. 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. 59:114-133. https://doi.org/10.1111/j.1550-7408.2012.00610.x
  39. 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
  40. Katoh, K. & Standley, D. M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30:772-780. https://doi.org/10.1093/molbev/mst010
  41. Kofoid, C. A. 1909. On Peridinium steini Jorgensen, with a note on the nomenclature of the skeleton of the Peridinidae. Arch. Protistenk. 16:25-47.
  42. Kretzschmar, A. L., Verma, A., Harwood, T., Hoppenrath, M. & Murray, S. 2017. Characterization of Gambierdiscus lapillus sp. nov. (Gonyaulacales, Dinophyceae): a new toxic dinoflagellate from the Great Barrier Reef (Australia). J. Phycol. 53:283-297. https://doi.org/10.1111/jpy.12496
  43. 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
  44. 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
  45. Leaw, C. -P., Lim, P. -T., Cheng, 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
  46. 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
  47. 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
  48. 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
  49. Li, X., Yan, M., Gu, J., Lam, V. T. T., Wai, T. -C., Baker, D. M., Thompson, P. D., Yiu, S. K. F., Lam, P. K. S. & Leung, P. T. Y. 2020. The effect of temperature on physiology, toxicity and toxin content of the benthic dinoflagellate Coolia malayensis from a seasonal tropical region. Water Res. 185:116264. https://doi.org/10.1016/j.watres.2020.116264
  50. Litaker, R. W., Vandersea, M. W., Faust, M. A., Kibler, S. R., Chinain, M., Holmes, M. J., Holland, W. C. & Tester, P. A. 2009. Taxonomy of Gambierdiscus including four new species, Gambierdiscus caribaeus, Gambierdiscus carolinianus, Gambierdiscus carpenteri and Gambierdiscus ruetzleri (Gonyaulacales, Dinophyceae). Phycologia 48:344-390. https://doi.org/10.2216/07-15.1
  51. Lundholm, N., Churro, C., Fraga, S., Hoppenrath, M., Iwataki, M., Larsen, J., Mertens, K., Moestrup, O. & Zingone, A. 2009 onwards. IOC-UNESCO taxonomic reference list of harmful micro algae. Available from: https://www.marinespecies.org/hab. Accessed Jun 20, 2022.
  52. Meunier, A. 1919. Microplancton de la mer Flamande. 3me partie. Les Peridiniens. Mem. Mus. R. Hist. Nat. Belg. 8:1-111.
  53. Mitrovic, S. M., Fernandez-Amandi, M., McKenzie, L., Furey, A. & James, K. J. 2004. Effects of selenium, iron and cobalt addition to growth and yessotoxin production of the toxic marine dinoflagellate Protoceratium reticulatum in culture. J. Exp. Mar. Biol. Ecol. 313:337-351. https://doi.org/10.1016/j.jembe.2004.08.014
  54. 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
  55. 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
  56. Morquecho, L. & Reyes-Salinas, A. 2004. Coleccion de Dinoflagelados Marinos (CODIMAR). Centro de Investigaciones Biologicas del Noroeste, S.C. La Paz, Baja California Sur, Mexico. Available from: https://www.cibnor.gob.mx/investigacion/colecciones-biologicas/codimar. Accessed Jun 20, 2022.
  57. Murray, J. S., Nishimura, T., Finch, S. C., Rhodes, L. L., Puddick, J., Harwood, D. T., Larsson, M. E., Doblin, M. A., Leung, P., Yan, M., Rise, F., Wilkins, A. L. & Prinsep, M. R. 2020. The role of 44-methylgambierone in ciguatera fish poisoning: acute toxicity, production by marine microalgae and its potential as a biomarker for Gambierdiscus spp. Harmful Algae 97:101853. https://doi.org/10.1016/j.hal.2020.101853
  58. 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
  59. Nishimura, T., Sato, S., Tawong, W., Sakanari, H., Yamaguchi, H. & Adachi, M. 2014. Morphology of Gambierdiscus scabrosus sp. nov. (Gonyaulacales): a new epiphytic toxic dinoflagellate from coastal areas of Japan. J. Phycol. 50:506-514. https://doi.org/10.1111/jpy.12175
  60. Nunez-Vazquez, E. J., Almazan-Becerril, A., Lopez-Cortes, D. J., Heredia-Tapia, A., Hernandez-Sandoval, F. E., BandSchmidt, C. J., Bustillos-Guzman, J. J., Garate-Lizarraga, I., Garcia-Mendoza, E., Salinas-Zavala, C. A. & CorderoTapia, A. 2019. Ciguatera in Mexico (1984-2013). Mar. Drugs 17:13.
  61. Nunez-Vazquez, E. J., Heredia-Tapia, A., Perez-Urbiola, J. C., Alonso-Rodriguez, R., Arellano-Blanco, J., CorderoTapia, A., Perez-Linares, J. & Ochoa, J. L. 2013. Evaluation of dinoflagellate toxicity implicated in recent HAB events in the Gulf of California, Mexico. In Holland, P., Rhodes, L. & Brown, L. (Eds.) Proceedings from HABTech 2003, APEC. A workshop on technologies for monitoring of harmful algal blooms and marine biotoxins. Report No. 906. Cawthron Institute, Nelson, p. 94.
  62. Okolodkov, Y. B., Campos-Bautista, G., Garate-Lizarraga, I., Gonzalez-Gonzalez, J. A. G., Hoppenrath, M. & Arenas, V. 2007. Seasonal changes of benthic and epiphytic dinoflagellates in the Veracruz reef zone, Gulf of Mexico. Aquat. Microb. Ecol. 47:223-237. https://doi.org/10.3354/ame047223
  63. Okolodkov, Y. B. & Garate-Lizarraga, I. 2006. An annotated checklist of dinoflagellates (Dinophyceae) from the Mexican Pacific. Acta Bot. Mex. 74:1-154. https://doi.org/10.21829/abm74.2006.1008
  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. Pinon-Gimate, A., Chavez-Sanchez, T., Mazariegos-Villarreal, A., Balart, E. F. & Serviere-Zaragoza, E. 2020. Species richness and composition of macroalgal assemblages of a disturbed coral reef in the Gulf of California, Mexico. Acta Bot. Mex. 127:e1653.
  66. Posada, D. 2008. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25:1253-1256. https://doi.org/10.1093/molbev/msn083
  67. Ramos-Santiago, A. E. 2021. Taxonomia integrativa y crecimiento de Coolia Meunier (Dinophyceae) en extractos de Dictyota dichotoma (Hudson) J.V. Lamouroux (Phaeophyceae) de la Bahia de La Paz, B.C.S., Mexico. B.S. thesis, Universidad del Mar, Campus Puerto Angel, Oaxaca, Mexico, 91 pp. (in Spanish).
  68. Reguera, B., Alonso, R., Moreira, A. & Mendez, S. 2011. Guia para el diseno y puesta en marcha de un plan de seguimiento de microalgas productoras de toxinas. Manuales y Guias de la COI, 59. COI de UNESCO and OIEA, Paris and Viena, 46 pp. (in Spanish).
  69. Rhodes, L. & Smith, K. F. 2018. A checklist of the benthic and epiphytic marine dinoflagellates of New Zealand, including Rangitahua/Kermadec Islands. N. Z. J. Mar. Freshw. Res. 53:258-277. https://doi.org/10.1080/00288330.2018.1492425
  70. Rhodes, L., Smith, K. F., Verma, A., Curley, B. G., Harwood, D. T., Murray, S., Kohli, G. S., Solomona, D., Rongo, T., Munday, R. & Murray, S. A. 2017. A new species of Gambierdiscus (Dinophyceae) from the south-west Pacific: Gambierdiscus honu sp. nov. Harmful Algae 65:61-70. https://doi.org/10.1016/j.hal.2017.04.010
  71. Ronquist, F. & Huelsenbeck, J. P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574. https://doi.org/10.1093/bioinformatics/btg180
  72. 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
  73. Sepulveda-Villarraga, M. 2017. Dinoflagelados potencialmente toxicos asociados a macroalgas en la Bahia de La Paz, B.C.S. M.S. thesis, Instituto Politecnico Nacional, Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN), La Paz, Mexico, 69 pp. (in Spanish).
  74. Smith, K. F., Rhodes, L., Verma, A., Curley, B. G., Harwood, D. T., Kohli, G. S., Solomona, D., Rongo, T., Munday, R. & Murray, S. A. 2016. A new Gambierdiscus species (Dinophyceae) from Rarotonga, Cook Islands: Gambierdiscus cheloniae sp. nov. Harmful Algae 60:45-56. https://doi.org/10.1016/j.hal.2016.10.006
  75. Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihoodbased phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. https://doi.org/10.1093/bioinformatics/btl446
  76. Swofford, D. 2002. 2002PAUP*. Phylogenetic analysis using parsimony (* and other methods), version 4 b10. Sinauer Associates, Sunderland, MA.
  77. 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
  78. Tester, P. A., Litaker, R. W. & Berdalet, E. 2020. Climate change and harmful benthic microalgae. Harmful Algae 91:101655. https://doi.org/10.1016/j.hal.2019.101655
  79. 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
  80. Vargas-Montero, M., Morales, A. & Cortes, J. 2012. First report of the genus Gambierdiscus (Dinophyceae) and other benthic dinoflagellates from Isla del Coco National Park, Costa Rica, Eastern Tropical Pacific. Rev. Biol. Trop. 60:187-199 (in Spanish).
  81. Verma, A., Hoppenrath, M., Dorantes-Aranda, J. J., Harwood, D. T. & Murray, S. A. 2016. Molecular and phylogenetic characterization of Ostreopsis (Dinophyceae) and the description of a new species, Ostreopsis rhodesae sp. nov., from a subtropical Australian lagoon. Harmful Algae 60:116-130. https://doi.org/10.1016/j.hal.2016.11.004
  82. 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