Epiphytic dinoflagellates of Thalassia testudinum in two coastal systems of the Colombian Caribbean

Authors

  • Natalia Arbelaez M. Universidad Nacional de Colombia sede Caribe - Cecimar e Instituto de Investigaciones Marinas y Costeras - Invemar
  • José Ernesto Mancera Pineda Universidad Nacional de Colombia sede Bogotá
  • Beatriz Reguera Instituto Español de Oceanografía (IEO) Centro Oceanográfico de Vigo

DOI:

https://doi.org/10.25268/bimc.invemar.2017.46.2.725

Keywords:

Toxic dinoflagelates, Colombian Caribbean, Benthic HABs, Seagrass.

Abstract

Studies on potentially toxic epibenthic dinoflagellates have been increased in the last years due to growing number of harmful events attributed to some of these microalgae. These events represent a risk to human health, as well as to diverse economic activities. With the aim of confirming the presence of these dinoflagellates in Tayrona National Natural Park, Colombian Caribbean, monthly samples of the seagrass Thalassia testudinum were collected between January 2014 and December 2015 in two coastal systems (Bay and Lagoon) located in Chengue Bay (11°20´ N y 74°07´W). Grass leaves were manually collected, placed in plastic bags with seawater and transferred to laboratory for detachment of epibenthic microalgae by vigorous shaking. To identify the species, three types of microscopy were used (optical, inverted with epifluorescence and scanning electron microscopy). Fourteen species of potentially toxic epiphytic dinoflagellates, distributed in four genera (Gambierdiscus, Coolia, Ostreopsis and Prorocentrum) were identified. Prorocentrum was the most representative genus. Ostreopsis cf. ovata, P. hoffmannianum and P. lima were the most frequent species in the Bay, whereas Prorocentrum sp. 1 and P. rhathymum were the most frequent in the Lagoon. This study depicts the main features of the observed species, considering that precise identification at species level is required for any ecological study that seeks to provide elements for risk management against the toxic or harmful effects caused by epibenthic dinoflagellates.

Dimensions

PlumX

Visitas

1469

Downloads

Download data is not yet available.

References

Almazán-Becerril. A., S. Escobar-Morales, G. Rosiles-González and F. Valadez. 2015. Benthic-epiphytic dinoflagellates from the northern portion of the

Mesoamerican Reef System. Bot. Mar., 58(2): 115–128.

Álvarez, R. 1997. Primer caso de ciguatera en el Caribe colombiano por Seriola zonata (Mitchill, 1815) (Pisces: Carangidae). Biomédica, 17: 67-68.

Álvarez, R. 1999. Tres brotes de ictiosarcotoxicosis por ingestión de Sphyraena barracuda (Walbaum) y Seriola zonata (Mitchill) en el Caribe de Colombia.

Biomédica, 9:35-38.

Álvarez-León, R., G. Ramírez-Triana y E. Wedler. 1995. Registro de las condiciones ambientales de la laguna sur (bahía de Chengue, Caribe colombiano)

entre 1981-1984. Rev. Acad. Colomb. Cienc., 19 (74): 509-525.

An, T., J. Winshell, G. Scorzetti, J.W. Fell and K.S. Rein. 2010. Identification of okadaic acid production in the marine dinoflagellate Prorocentrum

rhathymum from Florida Bay. Toxicon, 55(2-3): 653–657.

Arcila-Herrera, H., J. Mendoza-Ayora, F. González-Franco, L. Montero-Cervantes y A. Castelo-Navarrete. 2001. Revisión de una enfermedad poco

conocida: la ciguatera. Rev Biomed., 12:27-34.

Ashton, M., T. Tosteson and C. Tosteson. 2003. The effect of elevated temperature on the toxicity of the laboratory cultured dinoflagellate Ostreopsis

lenticularis (Dinophyceae). Rev. Biol. Trop., 4:1-6.

Besada, E.G., L.A. Loeblich and A.R. Loeblich. 1982. Observations on tropical, benthic dinoflagellates from ciguatera-endemic areas: Coolla, Gambierdiscus,

and Ostreopsis. Bull. Mar. Sci., 32(3): 723-735.

Bomber, J. W. and K. E. Aikman. 1989. The ciguatera dinoflagellates. Biol. Oceanogr., 6: 291–311.

Brissard, C., C. Herrenknecht, V. Séchet, F. Hervé, F. Pisapia, J. Harcouet, R. Lémée, N. Chomérat, P. Hess and Z. Amzil. 2014. Complex toxin profile of

French Mediterranean Ostreopsis cf. ovata strains, seafood accumulation and ovatoxins prepurification. Mar. Drugs, 12: 2851-2876.

Celis, J.S. y J.E. Mancera-Pineda. 2015. Análisis histórico de la incidencia de ciguatera en las islas del Caribe durante 31 años: 1980 – 2010. Bol. Invest.

Mar. Cost., 44: 7-32.

Chomérat, N., D.Y. Sellos, F. Zentz and E. Nézan. 2010. Morphology and molecular phylogeny of Prorocentrum consutum sp nov. (Dinophyceae), a new

benthic dinoflagellate from south Brittany (northwestern France). J. Phycol., 46(1): 183-194.

Ciminiello, P., C. Dell’Aversano, E. Fattorusso, M. Forino, L. Tartaglione, C. Grillo and N. Melchiorre. 2011. Putative palytoxin and its new analogue,

ovatoxin-a, in Ostreopsis ovata collected along the Ligurian coasts during the 2006 toxic outbreak. J. Am. Soc. Mass. Spect., 19: 111-120.

Ciminiello, P., C. Dell’Aversano, E. Dello Iacovo, E. Fattorusso, M. Forino, L. Tartaglione, G. Benedettini, M. Onorari, F. Serena, C. Battocchi, S. Casabianca

and A. Penna. 2014. First finding of Ostreopsis cf. ovata toxins in marine aerosols. Environ. Sci. Technol., 48(6): 3532-3540.

Cortés-Altamirano, R. and A.P. Sierra-Beltrán. 2003. Morphology and taxonomy of Prorocentrum mexicanum and reinstatement of Prorocentrum

rhathymum (Dinophyceae). J. Phycol., 39: 221-225.

Del Favero, G., S. Silva, M. Pelin, E. D’Orlando, C. Florio, P. Lorenzon, M. Poli and A. Tubaro. 2012. Sanitary problems related to the presence of

Ostreopsis spp. in the Mediterranean Sea: a multidisciplinary scientific approach. Ann. Ist. Super. Ann. Ist. Super. Sanità, 48(4): 407-414.

Delgado, G. 2005. Dinoflagelados bentónicos tóxicos asociados a la ciguatera: abundancia, toxicidad y relación con los factores ambientales en un área del

litoral noroccidental de Cuba. Tesis doctorado Ciencias del Mar, Centro Invest. Biol. Noroeste S.C. La Paz, México. 72 p.

Delgado, G., G. Popowski, C. García, N. Lagos and C.H. Lechuga-Devéz. 2005. Presence of DSP-toxins in Prorocentrum lima (Ehrenberg) Dodge in Cuba.

Rev. Invest. Mar., 26(3): 229-234.

Delgado, G., C.H. Lechuga-Devéze, G. Popowski, L. Troccoli and C.A. Salinas. 2006. Epiphytic dinoflagellates associated with ciguatera in the northwestern

coast of Cuba. Rev. Biol. Trop., 54(2): 299-310.

Dickey, R.W., S.C. Bobzin, D.J. Faulkner, F.A. Bencsath and D. Andrzejewski. 1990. Identification of okadaic acid from a Caribbean dinoflagellate,

Prorocentrum concavum. Toxicon, 28(4): 371-377.

Faust, M. A. 1990. Morphologic details of six benthic species of Prorocentrum (Pyrrhophyta) from a mangrove island, Twin Cays, Belize, including two

new species. J. Phycol., 26: 548–558.

Faust, M.A. 1992. Observations on the morphology and sexual reproduction of Coolia monotis (Dinophyceae). J. Phycol., 28: 94-104.

Faust, M.A. 1995. Observation of sand-dwelling toxic dinoflagellates (Dinophyceae) from widely differing sites, including two new species. J. Phycol., 31:

-1003.

Faust, M.A. 1999. Three new Ostreopsis species (Dinophyceae): O. marinus sp. nov., O. belizeanus sp. nov., and O. caribbeanus sp. nov. Phycologia, 38(2):

-99.

Faust, M.A. 2009. Ciguatera-causing dinoflagellates in a coral-reef-mangrove ecosystem, Belize. Atoll Res. Bull., 569: 1-32.

Faust, M.A. and R.A. Gulledge. 2002. Identifying harmful marine dinoflagellates. Smithson. Contr. U.S Nat. Herb., 42:1–144.

Faust, M.A., S.L. Morton and J.P. Quod. 1996. Further SEM study of marine dinoflagellates: The genus Ostreopsis (Dinophyceae). J. Phycol., 32: 1053-

Faust, M.A., J. Larsen and Ø. Moestrup. 1999. Potentially toxic phytoplankton. 3. Genus Prorocentrum (Dinophyceae). ICES Identification Leaflets for

Plankton. Ed. J.A. Lindley. Natural Environment Research Council. Copenhaguen. 24 p.

Fraga, S., A. Penna, I. Bianconi, B. Paz and M. Zapata. 2008. Coolia canariensis sp nov. (Dinophyceae), a new nontoxic epiphytic benthic dinoflagellate

from the Canary Islands. J. Phycol., 44: 1060–1070.

Fraga, S., F. Rodríguez, A. Caillaud, J. Diogène, N. Raho and M. Zapata. 2011. Gambierdiscus excentricus sp. nov. (Dinophyceae), a benthic toxic

dinoflagellate from the Canary Islands (NE Atlantic Ocean). Harmful Algae, 11: 10–22.

Fraga, S., F. Rodríguez, P. Riobó and I. Bravo. 2016. Gambierdiscus balechii sp. nov (Dinophyceae), a new benthic toxic dinoflagellate from the Celebes

Sea (SW Pacific Ocean). Harmful Algae, 58: 93-105.

Fritz L. and R.E. Trimer. 1985. A rapid and simple technique utilizing calcofluor white MR2 for visualization of dinoflagellate technology. J. Phycol., 21:

-64.

Fukuyo, Y. 1981. Taxonomical study on benthic dinoflagellates collected in coral reefs. Bull. Jpn. Soc. Sci. Fish., 47:967–78.

Gaitán, J.D. 2007. Ictiotoxismo por consumo de barracuda (Sphyraena barracuda) y morena manchada (Gymnothorax moringa) en la comunidad de

pescadores artesanales de Tasajera, Caribe colombiano. Duazary, 4(2): 160-167.

Gallitelli, M., N. Ungaro, L.M. Addante, V. Procacci, N.G. Silveri and C. Sabbá. 2005. Respiratory illness as a reaction to tropical algal blooms occurring in

a temperate climate. JAMA, 293(21): 2599-2600.

Gómez, F., D. Qiu, E. Otero-Morales, R.M. Lopes and S. Lin. 2016. Circumtropical distribution of the epiphytic dinoflagellate Coolia malayensis

(Dinophyceae): Morphology and molecular phylogeny from Puerto Rico and Brazil. Phycol. Res., 64: 194–199.

Gómez, F., D. Qiu and S. Lin. 2017. The synonymy of the toxic dinoflagellates Prorocentrum mexicanum and P. rhathymum and the description of P.

steidingerae sp. nov. (Prorocentrales, Dinophyceae). J. Eukaryot. Microbiol., 0: 1-10.

Gorbi, S., R. Bocchetti, A. Binelli, S. Bacchiocchi, R. Orletti, L. Nanetti, F. Raffaelli, A. Vignini,S. Accoroni, C. Totti and F. Regoli. 2012. Biological effects

of palytoxin-like compounds from Ostreopsis cf. ovata: A multibiomarkers approach with mussels Mytilus galloprovincialis. Chemosphere, 89:

-632.

Granéli, E., N.K. Vidyarathna, E. Funari, P.R.T. Cumaranatunga and R. Scenati. 2011. Can increases in temperature stimulate blooms of the toxic benthic

dinoflagellate Ostreopsis ovata?. Harmful Algae, 10: 165–172.

Guiry, M.D. and G.M 2016. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org; Consultado

/01/2016.

Hallegraeff, G.M., D.M. Anderson and A.D. Cembella. 2004. Manual on harmful marine microalgae. Monographs on Oceanographic Methodology,

UNESCO. París. 793 P.

Herrera-Sepúlveda, A., L. Medlin, G. Murugan, A.P. Sierra-Beltrán, A.A. Cruz-Villacorta and N.Y. Hernández-Saavedra. 2015. Are Prorocentrum

hoffmannianum and Prorocentrum belizeanum (Dinophyceae, Prorocentrales) the same species? An integration of morphological and molecular

data. J. Phycol., 51: 173-188.

Holland, W., W. Litaker, C.R. Tomas, S.R. Kibler, A.R. Place, E.D. Davenport and P.A. Tester. 2013. Differences in the toxicity of six Gambierdiscus

(Dinophyceae) species measured using an in vitro human erythrocyte lysis assay. Toxicon, 65: 15-33.

Holmes M., R.J. Lewis, M.A. Poli and N.C. Gillespie. 1991. Strain dependent production of ciguatoxin precursors (gambiertoxins) by Gambierdiscus toxicus

(Dinophyceae) in culture. Toxicon, 29(6): 761-75.

Holmes, M., R. Lewis, A. Jones and A. Wong. 1995. Cooliatoxin, the first toxin from Coolia monotis (Dinophyceae). Nat. Toxins, 3:355-362.

Hoppenrath, M., N. Chomérat, T. Horiguchi, M. Schweinkert, Y. Nagahama and S. Murray. 2013. Taxonomy and phylogeny of the benthic Prorocentrum

species (Dinophyceae) — A proposal and review. Harmful Algae, 27: 1-28.

Hoppenrath, M., S. A. Murray, N. Chomérat and T. Horiguchi. 2014. Marine benthic dinoflagellates – unveiling their worldwide biodiversity. Ed.

Senckenberg. Stuttgart. 276 p.

Jeong, H.J., A.S. Lim, S.H. Hang, W.O. Yih, N.S. Kang, S.Y Lee, Y.D. Yoo and H.S Kim. 2012. First report of the epiphytic dinoflagellate Gambierdiscus

caribaeus in the temperate waters off Jeju Island, Korea: morphology and molecular characterization. J. Eukaryot. Microbiol., 59(6): 637–650.

Karafas, S., R. York and C. Tomas. 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.

Leaw, C-P., P-T. Lim, K-W. Cheng, B-K. Ng and G. Usup. 2010. Morphology and molecular characterization of a new species of thecate benthic dinoflagellate,

Coolia malayensis sp. nov (Dinophyceae). J. Phycol., 46: 162-171.

Lee, J.S., T. Igarashi, S. Fraga, E. Dahl, P. Hovgaard and T. Yasumoto. 1989. Determination of diarrhetic shellfish toxins in various dinoflagellate species.

J. Appl. Phycol., 1: 147-152.

Lenoir, S., L. Ten-Hage, T. Turquet, J.P. Quod, C. Bernard and M.C. Hennion. 2004. First evidence of palytoxin analogues from an Ostreopsis mascarenensis

(Dinophyceae) benthic bloom in southwestern Indian Ocean. J. Phycol., 40: 1042–1051.

Levasseur, M., J. Couture, A.M. Weise, S. Michaud, M. Elbrächter, G. Sauvé and E. Bonneau. 2003. Pelagic and epiphytic summer distributions of

Prorocentrum lima and P. mexicanum at two mussel farms in the Gulf of St. Lawrence, Canada. Aquat. Microb. Ecol., 30: 283–293.

Lewis, R.J., M. Inserra, I. Vetter, W.C. Holland, D.R. Hardison, P.A. Tester and R.W. Litaker. 2016. Rapid extraction and identification of maitotoxin and

ciguatoxin-like toxins from Caribbean and Pacific Gambierdiscus using a new functional bioassay. PLoS One, 11(7): e0160006.

Litaker, R.W., M. Vandersea, M. Faust, S. Kibler, M. Chinain, M. Holmes, W. Holland and P. Tester. 2009. Taxonomy of Gambierdiscus including four

new species, Gambierdiscus caribaeus, Gambierdiscus carolinianus, Gambierdiscus carpenteri and Gambierdiscus ruetzleri (Gonyaulacales,

Dinophyceae). Phycologia, 48(5): 344–390.

Litaker, R.W., M. Vandersea, M. Faust, S. Kibler, A.W. Nau, W. Holland, M. Chinain, M. Holmes and P.A. Tester. 2010. Global distribution of ciguatera

causing dinoflagellates in the genus Gambierdiscus. Toxicon, 56: 711–730.

Mancera-Pineda, J.E., B. Gavio y G. Arencibia. 2009. Floraciones algales nocivas, intoxicación por microalgas e impactos en el desarrollo regional: el caso

de San Andrés isla, Caribe colombiano, 46-62. En: Mancera-Pineda, J.E., O. Sierra y S. Pérez. (Eds.) 2009. Cuadernos del Caribe, 13, 78 p.

Martínez-Cruz, M.E., Y. Okolodkov, A.C. Aguilar-Trujillo and J.A. Herrera-Silveira. 2015. Epiphytic dinoflagellates on the seagrass Thalassia testudinum

at Dzilam, southeastern Gulf of Mexico. Cymbella, 3: 2-9.

Mohammad-Noor, N., N. Daugbjerg, Ø. Moestrup and A. Anton. 2007. Marine epibenthic dinoflagellates from Malaysia - a study of live cultures and

preserved samples based on light and scanning electron microscopy. Nord. J. Bot., 24(6): 629-690.

Mohammad-Noor, N., Ø. Moestrup, N. Lundholm, S. Fraga, A. Adam, M.J. Holmes and E. Saleh. 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.

Morton, S.L. and J.W. Bomber. 1994. Maximizing okadaic acid content from Prorocentrum hoffmannianum Faust. J. Appl. Phycol., 6: 41-44.

Murakami, Y., Y. Oshima and T. Yasumoto. 1982. Identification of okadaic acid as a toxic component of a marine dinoflagellate Prorocentrum lima. Nippon

Suisan Gakk., 48: 69–72.

Nascimento, S., E.V. Corrêa, M. Menezes, D. Varela, J. Paredes and S. Morris. 2012. Growth and toxin profile of Ostreopsis cf. ovata (Dinophyta) from Río

de Janeiro, Brazil. Harmful Algae, 13: 1-9.

Okolodkov, Y., F. Merino-Virgilio, J. Aké- Castillo, A. Aguilar-Trujillo, S. Espinosa-Matías and J. Herrera-Silveira. 2014. Seasonal changes in epiphytic

dinoflagellate assemblages near the northern coast of the Yucatan Peninsula, Gulf of Mexico. Acta Bot. Mex., 107: 121-151.

Parsons, M.L., K. Aligizaki, M.-Y. Dechraoui Bottein, S. Fraga, S.L. Morton, A. Penna and L. Rhodes. 2012. Gambierdiscus and Ostreopsis: Reassessment

of the state of knowledge of their taxonomy, geography, ecophysiology, and toxicology. Harmful Algae, 14: 107–129.

Penna, A., M. Vila, S. Fraga, M.G. Giacobbe, F. Andreoni, P. Riobó and C. Vernesi. 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.

Peraza, R. y Á. Moreira. 2012. Composición y abundancia de dinoflagelados epibentónicos tecados potencialmente tóxicos de la Ensenada Guajimico,

región Centro-Sur de Cuba. Rev. Cub. Invest. Pesq., 29: 59-66.

Reguera, B., R. Alonso, A. Moreira y S. Méndez. 2011. Guía para el diseño y puesta en marcha de un plan de seguimiento de microalgas productoras de

toxinas. IOC Manuals and Guides 59, COI de UNESCO y OIEA, París y Viena, 46 p + Anexos.

Rhodes, L., J. Adams, T. Suzuki, L. Briggs and I. Garthwaite. 2000. Toxic marine epiphytic dinoflagellates, Ostreopsis siamensis and Coolia monotis

(Dinophyceae), in New Zealand. N. Z. J. Mar. Fresh., 34: 371-383.

Rodríguez, A., J.E. Mancera-Pineda and B. Gavio. 2010. Survey of benthic dinoflagellates associated to beds of Thalassia testudinum in San Andrés Island,

Seaflower Biosphere Reserve, Caribbean Colombian. Acta Biol. Col., 15(2): 231 – 248.

Rodríguez-Ramírez, A., J. Nivia-Ruíz y J. Garzón-Ferreira. 2004. Características estructurales y funcionales del manglar de Avicennia germinans en la Bahía

de Chengue (Caribe colombiano). Bol. Invest. Mar. Cost., 33: 223-244.

Steidinger, K. and K. Tangen. 1996. Dinoflagellates. 387-598. In: C.R. Tomas (Ed.). 1996. Identifying Marine Diatoms and Dinoflagellates. Academic Press,

New York.

Su-Myat and K. Koike. 2013. A red tide off the Myanmar coast: Morphological and genetic identification of the dinoflagellate composition. Harmful Algae,

(7):149–158.

Tester, P.A., S. Kibler, W. Holland, G. Usup, M. Vandersea, C.P. Leaw, L.P. Teen, J. Larsen, N. Mohammad-Noor, M.A. Faust and R.W. Litaker. 2014.

Sampling harmful benthic dinoflagellates: Comparison of artificial and natural substrate methods. Harmful Algae, 39: 8–25.

Tichadou, L., M. Glaizal, A. Armengaud, H. Grossel, R. Lemée, R. Kantin, J.L. Lasalle, G. Drouet, L. Rambaud , P. Malfait and L. De Haro. 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(8): 839-844.

Torigoe, K., M. Murata and T. Yasumoto. 1988. Prorocentrolide, a toxic nitrogenous macrocycle from a marine dinoflagellate, Prorocentrum lima. J. Am.

Chem. Soc., 110: 7876-7877.

Tosteson, T.R., D.L. Ballantine, C.G. Tosteson, V. Hensley and A.T. Bardales. 1989. Associated bacterial flora, growth, and toxicity of cultured benthic

dinoflagellates Ostreopsis lenticularis and Gambierdiscus toxicus. Appl. Environ. Microbiol., 55(1): 137-41.

Tubaro A., P. Durando, G. Del Favero, F. Ansaldi, G. Icardi, J.R. Deeds and S. Sosa. 2011. Case definitions for human poisonings postulated to palytoxins

exposure. Toxicon, 57(3): 478-495.

Valerio, L. y J. Díaz. 2007. Dinoflagelados epifitos potencialmente tóxicos presentes en praderas de Thalassia testudinum en las costas nororientales de

Venezuela. Rev. Fac. Agron., 24(1): 39-43.

Valerio, L. y J. Díaz. 2008. Distribución de dinoflagelados epifitos potencialmente tóxicos asociados a praderas de Thalassia testudinum en la isla la Tortuga,

la bahía de Mochima y golfo de Cariaco, Venezuela. Bol. Inst. Oceanogr., 47(1): 47-58.

Vila, M., E. Garcés and M. Masó. 2001. Potentially toxic epiphytic dinoflagellate assemblages on macroalgae in the NW Mediterranean. Aquat. Microb.

Ecol., 26: 51–60.

Yasumoto, T., N. Seino, Y. Murakami and M. Murata. 1987. Toxins produced by benthic dinoflagellates. Biol. Bull., 172: 128-131.

Published

2017-11-27

How to Cite

1.
Arbelaez M. N, Mancera Pineda JE, Reguera B. Epiphytic dinoflagellates of Thalassia testudinum in two coastal systems of the Colombian Caribbean. Bol. Investig. Mar. Costeras [Internet]. 2017 Nov. 27 [cited 2024 Nov. 22];46(2). Available from: http://boletin.invemar.org.co/ojs/index.php/boletin/article/view/758
سرور مجازی ایران Decentralized Exchange

Issue

Section

Research Articles

Most read articles by the same author(s)

فروشگاه اینترنتی