Browse > Article
http://dx.doi.org/10.4490/algae.2022.37.9.2

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)
Publication Information
ALGAE / v.37, no.3, 2022 , pp. 185-204 More about this Journal
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
Bahia de La Paz; Coolia species; epiphytic dinoflagellates; Gulf of California; ITS1 / 5.8S / ITS2; LSU rDNA; morphology; taxonomy;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 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.
2 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).
3 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).
4 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.   DOI
5 Ronquist, F. & Huelsenbeck, J. P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.   DOI
6 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.   DOI
7 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.   DOI
8 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.   DOI
9 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.   DOI
10 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.   DOI
11 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.   DOI
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 Swofford, D. 2002. 2002PAUP*. Phylogenetic analysis using parsimony (* and other methods), version 4 b10. Sinauer Associates, Sunderland, MA.
14 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.   DOI
15 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.   DOI
16 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.
17 Bomber, J. W. & Aikman, K. E. 1989. The Ciguatera Dinoflagellates. Biol. Oceanogr. 6:291-311.
18 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.   DOI
19 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.
20 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.   DOI
21 Guillard, R. R. L. & Hargraves, P. E. 1993. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32:234-236.   DOI
22 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.   DOI
23 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.
24 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.   DOI
25 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.
26 Faust, M. A. 1995. Observation of sand-dwelling toxic dinoflagellates (Dinophyceae) from widely differing sites, including two new species. J. Phycol. 31:996-1003.   DOI
27 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.   DOI
28 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.   DOI
29 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.   DOI
30 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.   DOI
31 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.   DOI
32 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.
33 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.
34 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.   DOI
35 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.   DOI
36 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.   DOI
37 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.   DOI
38 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.   DOI
39 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.   DOI
40 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.
41 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.   DOI
42 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.   DOI
43 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.   DOI
44 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.
45 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.
46 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.   DOI
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.   DOI
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.   DOI
49 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.   DOI
50 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.
51 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.   DOI
52 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.   DOI
53 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.   DOI
54 Katoh, K. & Standley, D. M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30:772-780.   DOI
55 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.
56 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.   DOI
57 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.   DOI
58 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.   DOI
59 Hoppenrath, M. 2022. Prorocentrales. IOC-UNESCO taxonomic reference list of harmful micro algae. Available from: http://www.marinespecies.org/hab. Accessed Jun 17, 2022.
60 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.
61 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.   DOI
62 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.   DOI
63 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.   DOI
64 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.   DOI
65 Meunier, A. 1919. Microplancton de la mer Flamande. 3me partie. Les Peridiniens. Mem. Mus. R. Hist. Nat. Belg. 8:1-111.
66 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.   DOI
67 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.   DOI
68 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.   DOI
69 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.   DOI
70 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.
71 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.   DOI
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.   DOI
73 Okolodkov, Y. B. & Garate-Lizarraga, I. 2006. An annotated checklist of dinoflagellates (Dinophyceae) from the Mexican Pacific. Acta Bot. Mex. 74:1-154.   DOI
74 Posada, D. 2008. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25:1253-1256.   DOI
75 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.   DOI
76 Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihoodbased phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.   DOI
77 Tester, P. A., Litaker, R. W. & Berdalet, E. 2020. Climate change and harmful benthic microalgae. Harmful Algae 91:101655.   DOI
78 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.   DOI
79 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).
80 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.   DOI
81 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).
82 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.   DOI