Ostreopsis cf. ovata and Ostreopsis lenticularis (Dinophyceae: Gonyaulacales) in the Galapagos Marine Reserve

Authors

DOI:

https://doi.org/10.3989/scimar.05035.08A

Keywords:

dinoflagellates, harmful algal blooms, molecular phylogeny, Ostreopsis cf. ovata, Ostreopsis lenticularis, SEM, taxonomy, toxicity

Abstract


The genus of benthic dinoflagellates Ostreopsis is of particular interest because some species negatively impact human health and coastal marine ecosystems. Ostreopsis populations from a remote area, such as the Galapagos Marine Reserve with its unique biodiversity, can provide significant data. Samples of epibionthic dinoflagellates were collected from two islands (Santa Cruz and Santa Fé) in 2017. Species of the genera Gambierdiscus, Amphidinium, Coolia and Ostreopsis were found. Ostreopsis strains were isolated to characterize their morphology, molecular biology and toxicity. Three dif­ferent morphotypes of Ostreopsis based on dorsoventral and width diameters (n=369) were distinguished. The small cell morphotype was dominant in ten samples, with abundances of up to 33405 cells g-1 fresh weight of macroalgae. A total of 16 strains were isolated from field samples with subsequent polymerase chain reaction amplifications of rDNA, 5.8S rDNA and internal transcribed space regions; 13 strains (small cell morphotype) clustered in the O. cf. ovata Atlantic/Indian/Pacific clade; and 3 strains (large cell morphotype) clustered in the Ostreopsis lenticularis genotype from the type locality. The strains proved to be non-toxic. The presence of these genera/species represents a potential threat to marine ecosystems, and it is thus important to consider benthic species in the surveillance of harmful algae blooms in the reserve.

Downloads

Download data is not yet available.

References

Accoroni S., Totti C. 2016. The toxic benthic dinoflagellates of the genus Ostreopsis in temperate areas: a review. Adv. Oceanogr. Limnol. 7: 1-15. https://doi.org/10.4081/aiol.2016.5591

Accoroni S., Romagnoli T., Penna A., et al. 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 PMid:27633521

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

Andree K.B., Fernandez-Tejedor M., Elandaloussi L.M., et al. 2011. Quantitative PCR coupled with melt curve analysis for detection of selected Pseudo-nitzschia spp. (Bacillariophyceae) from the northwestern Mediterranean Sea. Appl. Environ. Mi­crob. 77: 1651-1659. https://doi.org/10.1128/AEM.01978-10 PMid:21193668 PMCid:PMC3067299

Arbelaez N.M., Mancera Pineda J.E., Reguera B. 2017. Epiphytic dinoflagellates of Thalassia testudinum in two coastal systems of the Colombian Caribbean. Bol. Invest. Mar. Cost. - INVE­MAR 46: 9-40.

Ashton M., Tosteson T., Tosteson C. 2003. The effect of elevated temperature on the toxicity of the laboratory cultured dinoflag­ellate Ostreopsis lenticularis (Dinophyceae). Rev. Biol. Trop. 51: 1-6.

Banks S. 2002. Ambiente físico. In: Danulat E., Edgar G.J. (eds), Reserva Marina de Galápagos. Línea base de la biodiversidad. Fundación Charles Darwin/Servicio Parque Nacional Galápa­gos, Santa Cruz, Galápagos, Ecuador, pp. 29-42.

Berdalet E., Tester P.A., Chinain M., et al. 2017. Harmful algal blooms in benthic systems: Recent progress and future research. Oceanography 30: 36-45. https://doi.org/10.5670/oceanog.2017.108

Boisnoir A., Pascala P.Y., Cordonniera S., et al. 2019. Spatio-temporal dynamics and biotic substrate preferences of benthic dinoflagellates in the Lesser Antilles, Caribbean Sea. Harmful Algae 81: 18-29. https://doi.org/10.1016/j.hal.2018.11.012 PMid:30638495

Carnicer O., Tunin-Ley A., Andree K.B., et al. 2015. Contribu­tion to the genus Ostreopsis in Reunion Island (Indian Ocean): Molecular, morphologic and toxicity characterization. Cryptog­amie Algol. 36: 101-119. https://doi.org/10.7872/crya.v36.iss1.2015.101

Carnicer O., García-Altares M., Andree K.B., et al. 2016a. First evidence of Ostreopsis cf. ovata in the eastern tropical Pacific Ocean, Ecuadorian coast. Bot. Mar. 59: 267-274. https://doi.org/10.1515/bot-2016-0022

Carnicer O., García-Altares M., Andree K.B., et al. 2016b. Ostre­opsis cf. ovata from western Mediterranean Sea: Physiological responses under different temperature and salinity conditions. Harmful Algae 57: 98-108. https://doi.org/10.1016/j.hal.2016.06.002 PMid:30170726

Carnicer O., De La Fuente P., Canepa A., et al. 2019. Marine dino­flagellate assemblage in the Galápagos Marine Reserve. Front. Mar. Sci. 6: 235. https://doi.org/10.3389/fmars.2019.00235

Chang F.H., Shimizu Y., Hay B., et al. 2000. Three recently record­ed Ostreopsis spp. (Dinophyceae) in New Zealand: Temporal and regional distribution in the upper North Island from 1995 to 1997. New Zeal. J. Mar. Fresh. Res. 34: 29-39. https://doi.org/10.1080/00288330.2000.9516913

Chomérat N., Bilien G., Derrien A., et al. 2019. Ostreopsis lenticu­laris Y. Fukuyo (Dinophyceae, Gonyaulacales) from French Polynesia (South Pacific Ocean): A revisit of its morphology, molecular phylogeny and toxicity. Harmful Algae 84: 95-111. https://doi.org/10.1016/j.hal.2019.02.004 PMid:31128817

Chomérat N., Bilien G., Couté A., et al. 2020. Reinvestigation of Ostreopsis mascarenensis Quod (Dinophyceae, Gonyaulacales) from Reunion Island (SW Indian Ocean): molecular phylogeny and emended description. Phycologia 59: 140-153. https://doi.org/10.1080/00318884.2019.1710443

Ciminiello P., Dell'Aversano C., Dello Iacovo E., et al. 2011. LC-MS of palytoxin and its analogues: State of the art and future perspectives. Toxicon 57: 376-389. https://doi.org/10.1016/j.toxicon.2010.11.002 PMid:21070802

Ciminiello P., Dell'Aversano C., Dello Iacovo E., et al. 2013. Investigation of toxin profile of Mediterranean and Atlantic strains of Ostreopsis cf. siamensis (Dinophyceae) by liquid chromatography-high resolution mass spectrometry. Harmful Algae 23: 19-27. https://doi.org/10.1016/j.hal.2012.12.002

Ciminiello P., Dell'Aversano C., Dello Iacovo E., et al. 2015. Liq­uid chromatography-high-resolution mass spectrometry for palytoxins in mussels. Anal. Bioanal. Chem. 407: 1463-1473. https://doi.org/10.1007/s00216-014-8367-6 PMid:25486923

Cortés-Lara M.C., Cortés-Altamirano R., Sierra-Beltrán A., et al. 2005. Ostreopsis siamensis (Dinophyceae) a new tychoplank­tonic record from Isabel Island National Park, Pacific Mexico. Harmful Algae News (IOC Newsletter on toxic algae and algal blooms) 28: 4-5.

David H., Laza-Martínez A., Miguel I., et al. 2013. Ostreopsis cf. siamensis and Ostreopsis cf. ovata from the Atlantic Iberian Peninsula: Morphological and phylogenetic characterization. Harmful Algae 30: 44-55. https://doi.org/10.1016/j.hal.2013.08.006

Del Favero G., Sosa S., Pelin M., et al. 2012. Sanitary problems related to the presence of Ostreopsis spp. in the Mediterranean Sea: a multidisciplinary scientific approach. Annali dell'Istituto superiore di sanità48: 407-414. https://doi.org/10.4415/ANN_12_04_08 PMid:23247137

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. Front. Mar. Sci. 6: 148 https://doi.org/10.3389/fmars.2019.00148

Edgar G.J., Banks S.A., Brandt M., et al. 2010. El Niño, grazers and fisheries interact to greatly elevate extinction risk for Galapagos marine species. Global Change Biol. 16: 2876-2890. https://doi.org/10.1111/j.1365-2486.2009.02117.x

Faust M.A. 1999. Three new Ostreopsis species (Dinophyceae): O. marinus sp. nov., O. belizeanus sp. nov., and O. caribeanus sp. nov. Phycologia 38: 92-99. https://doi.org/10.2216/i0031-8884-38-2-92.1

Faust M.A., Morton S.L. 1995. Morphology and ecology of the ma­rine dinoflagellate Ostreopsis labens sp. nov. (Dinophyceae). J. Phycol. 31: 456-463. https://doi.org/10.1111/j.0022-3646.1995.00456.x

Faust M.A., Morton S.L., Quod J.P. 1996. Further SEM study of marine dinoflagellates: the genus Ostreopsis (Dinophyceae). J. Phycol. 32: 1053-1065. https://doi.org/10.1111/j.0022-3646.1996.01053.x

Fritz L., Triemer R.E. 1985. A rapid simple technique utilizing Cal­cofluor White M2R for the visualization of dinoflagellate thecal plates. J. Phycol. 21: 662-664. https://doi.org/10.1111/j.0022-3646.1985.00662.x

Fukuyo Y. 1981. Taxonomical study on benthic dinoflagellates col­lected in coral reefs. Bull. Japan. Soc. Sci. Fish 47: 967-978. https://doi.org/10.2331/suisan.47.967

Gárate-Lizárraga I., González-Armas R., Okolodkov Y.B. 2018. Occurrence of Ostreopsis lenticularis (Dinophyceae: Gon­yaulacales) from the Archipiélago de Revillagigedo, Mexican Pacific. Mar. Pollut. Bull. 128: 390-395. https://doi.org/10.1016/j.marpolbul.2018.01.020 PMid:29571387

García-Altares M., Tartaglione L., Dell'Aversano C., et al. 2014. The novel OVTX-g and isobaric PLTX (so far referred to as putative PLTX) from Ostreopsis cf. ovata (NW Mediterranean Sea): structural insights by LC-high resolution MSn. Anal. Bio­anal. Chem. 407: 1191-1204. https://doi.org/10.1007/s00216-014-8338-y PMid:25492088

Guillard R.R.L. 1975. Culture of phytoplankton for feeding marine invertebrates. In: Smith W.L., Chanley M.H. (eds), Culture of marine invertebrate animals. Plenum Press, New York, pp. 29-60. https://doi.org/10.1007/978-1-4615-8714-9_3

Hachani M.A., Dhib A., Fathallia A., et al. 2018. Harmful epiphytic dinoflagellate assemblages on macrophytes in the Gulf of Tu­nis. Harmful Algae 77: 29-42. https://doi.org/10.1016/j.hal.2018.06.006 PMid:30005800

Hickman C.P.Jr. 2009. Evolutionary responses of marine inverte­brates to insular isolation in Galapagos. Galapagos Res. 66: 32-42.

Holland W.C., Litaker R.W., Tomas C.R., et al. 2013. Differences in the toxicity of six Gambierdiscus (Dinophyceae) species measured using an in vitro human erythrocyte lysis assay. Toxi­con. 65: 15-33. https://doi.org/10.1016/j.toxicon.2012.12.016 PMid:23313447 PMCid:PMC6468995

Holmes M.K. 1998. Gambierdiscus yasumotoi sp. nov. (Dinophy­ceae), a toxic benthic dinoflagellate from southeastern Asia. J. Phycol. 34: 661-668. https://doi.org/10.1046/j.1529-8817.1998.340661.x

Hoppenrath M., Murray S.A., Chomérat N., et al. 2014. Marine benthic dinoflagellates - unveiling their worldwide biodiversity. Schweizerbart'sche Verlagsbuchhandlung, Stuttgart, Germany, 276 pp.

Hoshaw R.W., Rosowski, J.R. 1973. Methods for microscopic algae. In: Stein J.R. (ed), Handbook of phycological methods: culture methods and growth measurements. Cambridge Univer­sity Press, Cambridge, pp. 53-67.

Hwang B.S., Yoon E.Y., Kim H.S., et al. 2013. Ostreol A: a new cytotoxic compound isolated from the epiphytic dinoflagellate Ostreopsis cf. ovata from the coastal waters of Jeju Island, Ko­rea. Bioorg, Med. Chem. Lett. 23: 3023-3027. https://doi.org/10.1016/j.bmcl.2013.03.020 PMid:23562061

Irola-Sansores E.D., Delgado-Pech B., García-Mendoza E., et al. 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

John U., Litaker R.W., Montresor M., et al. 2014. Formal revision of the Alexandrium tamarense species complex (Dinophyceae) taxonomy: the introduction of five species with emphasis on molecular-based (rDNA) classification. Protist 165: 779-804. https://doi.org/10.1016/j.protis.2014.10.001 PMid:25460230 PMCid:PMC4457362

Keith I., Dawson T.P., Collins K.J., et al. 2016. Marine invasive species: establishing pathways, their presence and potential threats in the Galapagos Marine Reserve. Pac. Conserv. Biol. 22: 377-385. https://doi.org/10.1071/PC15020

Kislik E., Saltos G., Torres G., et al. 2017. Biological hotspots in the Galápagos Islands: Exploring seasonal trends of ocean climate drivers to monitor algal blooms. Int. J. Bioeng. Life Sci. 11: 824-834.

Kumar S., Stecher G., Li M., et al. 2018. MEGA X: Molecular evo­lutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35: 1547-1549. https://doi.org/10.1093/molbev/msy096 PMid:29722887 PMCid:PMC5967553

Larsson M.E., Laczka O.F., Harwood D.T., et al. 2018. Toxicology of Gambierdiscus spp. (Dinophyceae) from tropical and tem­perate Australian waters. Mar. Drugs 16: 7. https://doi.org/10.3390/md16010007 PMid:29301247 PMCid:PMC5793055

Laza-Martínez 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

Laza-Martínez A., David H., Riobó P., et al. 2016. Characterization of a strain of Fukuyoa paulensis (Dinophyceae) from the west­ern Mediterranean Sea. J. Eukaryot. Microbiol. 63: 481-497. https://doi.org/10.1111/jeu.12292 PMid:26686980

Leaw L.C., Teen L.P., Ahmad A., et al. 2001. Genetic diversity of Ostreopsis ovata (Dinophyceae) from Malaysia. Mar. Biotech­nol. 3: 246-255. https://doi.org/10.1007/s101260000073 PMid:14961362

Lenoir S., Ten-Hage L., Turquet J., et al. 2004. First evidence of palytoxin analogues from an Ostreopsis mascarenensis (Di­nophyceae) benthic bloom in southwestern Indian Ocean. J. Phycol. 40: 1042-1051. https://doi.org/10.1111/j.1529-8817.2004.04016.x

Litaker R.W., Vandersea M.W., Kibler S.R., et al. 2007. Recogniz­ing dinoflagellate species using ITS rDNA sequences. J. Phy­col. 43: 344-355. https://doi.org/10.1111/j.1529-8817.2007.00320.x

Litaker R.W., Vandersea M.W., Faust M.A., et al. 2010. Global distribution of ciguatera causing dinoflagellates in the genus Gambierdiscus. Toxicon 56: 711-730. https://doi.org/10.1016/j.toxicon.2010.05.017 PMid:20561539

Litaker R.W., Holland W.C., Hardison D.R., et al. 2017. Ciguatox­icity of Gambierdiscus and Fukuyoa species from the Carib­bean and Gulf of Mexico. PLoS ONE 12: e0185776. https://doi.org/10.1371/journal.pone.0185776 PMid:29045489 PMCid:PMC5646788

Liu Y., Xie L., Morrison J.M., et al. 2014. Ocean circulation and water mass characteristics around the Galápagos Archipelago simulated by a multiscale nested ocean circulation model. Int. J. Oceanogr. 2014: 198686. https://doi.org/10.1155/2014/198686

Maciel-Baltazar E. 2015. Dinoflagelados (Dinoflagellata) tóxicos de la costa de Chiapas, México, Pacífico centro oriental. Cuad. Invest. UNED 7: 39-48. https://doi.org/10.22458/urj.v7i1.860

Mendes M.C.Q., Nunes J.M.C., Menezes M., et al. 2017. Toxin production, growth kinetics and molecular characterization of Ostreopsis cf. ovata isolated from Todos os Santos Bay, tropi­cal southwestern Atlantic. Toxicon 138: 18-30. https://doi.org/10.1016/j.toxicon.2017.08.007 PMid:28801157

Menegotto A., Rangel T.F. 2018. Mapping knowledge gaps in ma­rine diversity reveals a latitudinal gradient of missing species richness. Nat. Commun. 9: 4713. https://doi.org/10.1038/s41467-018-07217-7 PMid:30413710 PMCid:PMC6226500

Moreira A., Rodríguez F., Riobó P., et al. 2012. Notes on Ostreopsis sp. from southern-central coast of Cuba. Cryptogamie Algol. 33: 217-224. https://doi.org/10.7872/crya.v33.iss2.2011.217

Munday R., Murray S., Rhodes L.L., et al. 2017. Ciguatoxins and maitotoxins in extracts of sixteen Gambierdiscus isolates and one Fukuyoa isolate from the South Pacific and their toxicity to mice by intraperitoneal and oral administration. Mar. Drugs 15: 208. https://doi.org/10.3390/md15070208 PMid:28665362 PMCid:PMC5532650

Muromtsev A.M. 1963. The principal hydrology features of the Pacific Ocean. Jerusalem Post Press, Jerusalem, Israel, 417 pp.

Nascimento S.M., Correa E.V., Menezes M., et al. 2012. Growth and toxin profile of Ostreopsis cf. ovata (Dinophyta) from Rio de Janeiro, Brazil. Harmful Algae 13: 1-9. https://doi.org/10.1016/j.hal.2011.09.008

Núñez-Vázquez E.J., Almazán-Becerril A., López-Cortés D.J., et al. 2019. Ciguatera in Mexico (1984-2013). Mar. Drugs 17: 13. https://doi.org/10.3390/md17010013 PMid:30597874 PMCid:PMC6356608

Penna A., Vila M., Fraga S., et al. 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

Penna A., Fraga S., Battocchi C., et al. 2010. A phylogeographi­cal study of the toxic benthic dinoflagellate genus Ostreopsis Schmidt. J. Biogeogr. 37: 830-841. https://doi.org/10.1111/j.1365-2699.2009.02265.x

Penna A., Battocchi C., Capellacci S., et al. 2014. Mitochondrial, but not rDNA, genes fail to discriminate dinoflagellate species in the genus Ostreopsis. Harmful Algae 40: 40-50. https://doi.org/10.1016/j.hal.2014.10.004

Quintana-Manotas H., Mercado-Gómez J. 2017. Composición de dinoflagelados epífitos y forófitos en la Costa norte del golfo de Morrosquillo, Sucre, Colombia. Rev. Colombiana Cienc. Anim. 9: 129-140. https://doi.org/10.24188/recia.v9.n2.2017.550

Randall J.E. 2005. Review of clupeotoxism, an often fatal illness from the consumption of clupeoid fishes. Pac. Sci. 59: 73-77. https://doi.org/10.1353/psc.2005.0013

Rhodes L.L., Smith K.F., Verma A., et al. 2017. The dinoflagellate genera Gambierdiscus and Ostreopsis from subtropical Raoul Island and North Meyer Island, Kermadec Islands. New Zeal. J. Mar. Fresh. Res. 51: 490-504. https://doi.org/10.1080/00288330.2016.1270337

Riobó P., Paz B., Franco J.M., et al. 2008. Proposal for a simple and sensitive haemolytic assay for palytoxin: toxicological dynam­ics, kinetics, ouabain inhibition and thermal stability. Harmful Algae 7: 415-429. https://doi.org/10.1016/j.hal.2007.09.001

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: e27983. https://doi.org/10.1371/journal.pone.0027983 PMid:22164222 PMCid:PMC3229513

Schaeffer B.A., Morrison J.M., Kamykowski D., et al. 2008. Phy­toplankton biomass distribution and identification of productive habitats within the Galápagos Marine Reserve by MODIS, a surface acquisition system, and in-situ measurements. Remote Sens. Environ. 112: 3044-3054. https://doi.org/10.1016/j.rse.2008.03.005

Suzuki T., Watanabe R., Uchida H., et al. 2012. LC-MS/MS analy­sis of novel ovatoxin isomers in several Ostreopsis strains col­lected in Japan. Harmful Algae 20: 81-91. https://doi.org/10.1016/j.hal.2012.08.002

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.

Tartaglione L., Mazzeo A., Dell'Aversano C., et al. 2016. Chemical, molecular, and eco-toxicological investigation of Ostreopsis sp. from Cyprus Island: structural insights into four new ovatoxins by LC-HRMS/MS. Anal. Bioanal. Chem. 408: 915-932. https://doi.org/10.1007/s00216-015-9183-3 PMid:26608282

Tartaglione L., Dello Iacovo E., Mazzeo A., et al. 2017. Variability in toxin profiles of the Mediterranean Ostreopsis cf. ovata and in structural features of the produced ovatoxins. Environ. Sci. Technol. 51: 13920-13928. https://doi.org/10.1021/acs.est.7b03827 PMid:29131595

Tawong W., Nishimura T., Sakanari H., et al. 2014. Distribution and molecular phylogeny of the dinoflagellate genus Ostreopsis in Thailand. Harmful Algae 37: 160-171. https://doi.org/10.1016/j.hal.2014.06.003

Terajima T., Uchida H., Abe N., et al. 2018. Simple structural elu­cidation of ostreocin-B, a new palytoxin congener isolated from the marine dinoflagellate Ostreopsis siamensis, using comple­mentary positive and negative ion liquid chromatography/quad­rupole time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. 32: 1001-1007. https://doi.org/10.1002/rcm.8130 PMid:29611245

Tibiriçá C.E.J.A., Leite I.P., Batista T.V.V., et al. 2019. Ostreopsis cf. ovata bloom in Currais, Brazil: Phylogeny, toxin profile and contamination of mussels and marine plastic litter. Toxins 11: 446. https://doi.org/10.3390/toxins11080446 PMid:31357621 PMCid:PMC6723160

Tichadou L., Glaizal M., Armengaud A., et al. 2010. Health im­pact of unicellular algae of the Ostreopsis genus blooms in the Mediterranean Sea: experience of the French Mediterranean coast surveillance network from 2006 to 2009. Clin. Toxicol. 48: 839-844. https://doi.org/10.3109/15563650.2010.513687 PMid:20923395

Torres G., Andrade C. 2014. Dinámica del plancton marino costero con relación al flujo de mareas en Bahía Aeolián en septiembre 2006 (Baltra-Galápagos-Ecuador). OceanDocs: Repository of Ocean Publications.

Uchida H., Taira Y., Yasumoto T. 2013. Structural elucidation of palytoxin analogs produced by the dinoflagellate Ostreopsis ovata IK2 strain by complementary use of positive and nega­tive ion liquid chromatography/quadrupole time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. 27: 1999-2008. https://doi.org/10.1002/rcm.6657 PMid:23939968

Vargas-Montero M., Morales A., Cortés J. 2012. Primer informe del género Gambierdiscus (Dinophyceae) y otros dinoflage­lados bentónicos en el Parque Nacional Isla del Coco, Costa Rica, Pacífico Tropical Oriental. Rev. Biol. Trop. 60 (Suppl. 3): 187-199.

Verma A., Hoppenrath M., Harwood T., et al. 2016. Molecular phy­logeny, morphology and toxigenicity of Ostreopsis cf. siamen­sis (Dinophyceae) from temperate south-east Australia. Phycol. Res. 64: 146-159. https://doi.org/10.1111/pre.12128

Vila M., Abós-Herràndiz R., Isern-Fontanet J., et al. 2016. Estab­lishing the link between Ostreopsis cf. ovata blooms and human health impacts using ecology and epidemiology. Sci. Mar. 80: 107-115. https://doi.org/10.3989/scimar.04395.08A

Yépez Rendón J.B., Keith I., Ramírez Sarmiento A.K., et al. 2018. Presencia de microalgas epibentónicas en el Pacífico Este Tropical. Hallazgos 21 (Supl. especial): 1-23.

Zhang H., Lu S., Li Y., et al. 2018. Morphology and molecular phylogeny of Ostreopsis cf. ovata and O. lenticularis (Dino­phyceae) from Hainan Island, South China Sea. Phycol. Res. 66: 3-14. https://doi.org/10.1111/pre.12192

Published

2020-09-15

How to Cite

1.
Carnicer O, Okolodkov YB, Garcia-Altares M, Keith I, Andree KB, Diogène J, Fernández-Tejedor M. Ostreopsis cf. ovata and Ostreopsis lenticularis (Dinophyceae: Gonyaulacales) in the Galapagos Marine Reserve. scimar [Internet]. 2020Sep.15 [cited 2021Sep.27];84(3):199-213. Available from: https://scientiamarina.revistas.csic.es/index.php/scientiamarina/article/view/1865

Issue

Section

Featured Article