Oceanography The Official Magazine of
The Oceanography Society
Volume 31 Issue 04

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Volume 31, No. 4
Pages 145 - 153

Toxigenic Dinoflagellates and Associated Toxins in San Jorge Gulf, Argentina

Elena Fabro Bernd KrockAmérico I. TorresFlavio E. PaparazzoIrene R. SchlossGustavo A. FerreyraGastón O. Almandoz
Article Abstract

The occurrence of harmful algal blooms (HABs) is a global problem, and particularly in San Jorge Gulf (SJG), Argentina, which supports important fisheries, HABs represent a risk to human health. We studied the diversity and distribution of toxigenic dinoflagellates in the SJG using toxin detection and quantification, and assessed the connections between cell densities, toxins, and oceanographic parameters. Phytoplankton net samples were taken for microscopic and liquid chromatography-​tandem mass spectrometry (LC-MSMS) analyses during an expedition aboard R/V Coriolis II in February 2014. Solid phase adsorption toxin tracking (SPATT) devices were also deployed to determine the presence of dissolved lipophilic toxins in sea­water. Toxigenic dinoflagellate species and associated toxins showed different distribution patterns in the north and the south SJG. Protoceratium reticulatum and Dinophysis acuminata, together with yessotoxin and pectenotoxins, were predominantly detected in the northern SJG, mainly associated with low-nutrient, warmer waters. By contrast, Alexandrium catenella and paralytic shellfish toxins showed the highest relative abundances in the southern SJG, associated with high-nutrient, low-temperature waters. Cellular toxin content was also differently affected by environmental parameters, highlighting the complexity of HABs in this area. Spirolides were detected by SPATT for the first time in the SJG, suggesting the occurrence of A. ostenfeldii.

Citation

Fabro, E., B. Krock, A.I. Torres, F.E. Paparazzo, I.R. Schloss, G.A. Ferreyra, and G.O. Almandoz. 2018. Toxigenic dinoflagellates and associated toxins in San Jorge Gulf, Argentina. Oceanography 31(4):145–153, https://doi.org/10.5670/oceanog.2018.417.

References

Akselman, R. 1996. Estudios ecológicos en el Golfo de San Jorge y adyacencias (Atlántico sudoccidental). Distribución, abundancia y variación estacional del fitoplancton en relación a factores fisico-químicos y la dinámica hidrográfica. PhD Dissertation, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, 234 pp.

Akselman, R., B. Krock, T.J. Alpermann, U. Tillmann, M. Borel, G.O. Almandoz, and M. E. Ferrario. 2015. Protoceratium reticulatum (Dinophyceae) in the austral southwestern Atlantic and the first report on YTX-production in shelf waters of Argentina. Harmful Algae 45:40–52, https://doi.org/10.1016/​j.hal.2015.03.001.

Almandoz, G.O., N.G. Montoya, M.P. Hernando, H.R. Benavides, M.O. Carignan, and M.E. Ferrario. 2014. Toxic strains of the Alexandrium ostenfeldii complex in southern South America (Beagle Channel, Argentina). Harmful Algae 37:100–109, https://doi.org/10.1016/j.hal.2014.05.011.

Álvarez, G., E. Uribe, R. Díaz, M. Braun, C. Marino, and J. Blanco. 2011. Bloom of the Yessotoxin producing dinoflagellate Protoceratium reticulatum (Dinophyceae) in Northern Chile. Journal of Sea Research 65(4):427–434, https://doi.org/10.1016/​j.seares.2011.03.008.

Aune, T., R. Sorby, T. Yasumoto, H. Ramstad, and T. Landsverk. 2002. Comparison of oral and intraperitoneal toxicity of yessotoxins towards mice. Toxicon 40:77–82, https://doi.org/10.1016/S0041-0101(01)00192-1.

Balech, E. 1988. Los dinoflagelados del Atlántico Sudoccidental. Instituto Español de Oceanografía, Madrid, 310 pp.

Blossom, H., N. Daugbjerg, and P.J. Hansen. 2012. Toxic mucus traps: A novel mechanism that mediates prey uptake in the mixotrophic dinoflagellate Alexandrium pseudogonyaulax. Harmful Algae 17:40–53, https://doi.org/10.1016/​j.hal.2012.02.010.

Bogazzi, E., A. Baldoni, A. Rivas, P. Martos, R. Reta, J.M. Orensanz, M. Lasta, and P. Dell´Arciprete. 2005. Spatial correspondence between areas of concentration of Patagonian scallop (Zygochlamys patagonica) and frontal systems in the Southwestern Atlantic. Fisheries Oceanography 14:359–376, https://doi.org/​10.1111/j.1365-2419.2005.00340.x.

Carreto, J.I., H.R. Benavides, R.M. Negri, and P.D. Glorioso. 1986. Toxic red-tide in the Argentine Sea. Phytoplankton distribution and survival of the toxic dinoflagellate Gonyaulax excavata in a frontal area. Journal of Plankton Research 8:15–28, https://doi.org/10.1093/plankt/8.1.15.

Carreto, J.I., M.O. Carignan, N.G. Montoya, and D.A. Cucchi Colleoni. 2007. Ecología del fitoplancton en los sistemas frontales del Mar Argentino. Pp. 11–31 in El Mar Argentino y sus recursos Pesqueros. J.I. Carreto and C. Bremec, eds, Instituto Nacional de Investigación y Desarrollo Pesquero, Mar del Plata, Argentina.

Cembella, A.D., A.G. Bauder, N.I. Lewis, and M.A. Quilliam. 2001. Association of the gonyaulacoid dinoflagellate Alexandrium ostenfeldii with spirolide toxins in size-fractionated plankton. Journal of Plankton Research 23(12):1,413–1,419, https://doi.org/10.1093/plankt/23.12.1413.

Ciocco, N.F., M. Lasta, M. Narvarte, C. Bremec, E. Bogazzi, J. Valero, and J.M. Orensanz. 2006. Scallops in Argentina. Pp. 1,251–1,292 in Scallops: Ecology and Aquaculture, 2nd ed. S. Shumway and G.J. Parsons, eds, Elsevier, Amsterdam.

Collos, Y., C. Gagne, M. Laabir, and A. Vaquer. 2004. Nitrogenous nutrition of Alexandrium catenella (Dinophyceae) in cultures and in Thau Lagoon, Southern France. Journal of Phycology 40:96–103, https://doi.org/10.1046/j.1529-8817.2004.03034.x.

Fabro, E. 2018. Dinoflagelados toxígenos en el Mar Argentino. Diversidad, abundancia y toxinas asociadas. PhD Dissertation, Facultad de Ciencias Naturales de la Universidad Nacional de La Plata, Buenos Aires, Argentina, 197 pp.

Fabro, E., G.O. Almandoz, M.E. Ferrario, M.S. Hoffmeyer, R.E. Pettigrosso, R. Uibrig, and B. Krock. 2015. Co-occurrence of Dinophysis tripos and pectenotoxins in Argentinean shelf waters. Harmful Algae 42:25–33, https://doi.org/10.1016/​j.hal.2014.12.005.

Fabro, E., G.O. Almandoz, M.E. Ferrario, U. John, U. Tillmann, K. Toebe, B. Krock, and A. Cembella. 2017. Morphological, molecular and toxin analysis of field populations of Alexandrium genus from the Argentina Sea. Journal of Phycology 53(6):1,206–1,222, https://doi.org/10.1111/jpy.12574.

Fabro, E., G.O. Almandoz, M.E. Ferrario, U. Tillmann, A. Cembella, and B. Krock. 2016. Distribution of Dinophysis species and their association with lipophilic phycotoxins in plankton from the Argentine Sea. Harmful Algae 59:31–41, https://doi.org/​10.1016/​j.hal.2016.09.001.

Fernández, M., J.I. Carreto, J. Mora, and A. Roux. 2005. Physico-chemical characterization of the benthic environment of the Golfo San Jorge, Argentina. Journal of the Marine Biological Association of the United Kingdom 6(85):1,317–1,328, https://doi.org/10.1017/S002531540501249X.

Franco, J.M., B. Paz, P. Riobó, G. Pizarro, R. Figueroa, S. Fraga, and I. Bravo. 2006. First report of the production of spirolides by Alexandrium peruvianum (Dinophyceae) from the Mediterranean Sea. Pp. 174–175 in 12th International Conference on Harmful Algae Programme and Abstracts, Copenhagen, Denmark.

Gerssen, A., I.E. Pol-Hofstad, M. Poelman, P.P. Mulder, H.J. Van den Top, and J. De Boer. 2010. Marine toxins: Chemistry, toxicity, occurrence and detection, with special reference to the Dutch situation. Toxins 2:878–904, https://doi.org/10.3390/toxins2040878.

Giménez, E.M., G. Winkler, M. Hoffmeyer, and G.A. Ferreyra. 2018. Composition, spatial distribution, and trophic structure of the zooplankton community in San Jorge Gulf, southwestern Atlantic Ocean. Oceanography 31(4):154–163, https://doi.org/​​10.5670/oceanog.2018.418.

Guerrini, F., P. Ciminiello, C. Dell’Aversano, L. Tartaglione, E. Fattorusso, L. Boni, and R. Pistocchi. 2007. Influence of temperature, salinity and nutrient limitation on yessotoxin production and release by the dinoflagellate Protoceratium reticulatum in batch-cultures. Harmful Algae 6:707−717, https://doi.org/10.1016/​j.hal.2007.02.006.

Gracia Villalobos, L., N. Santinelli, V. Sastre, B. Krock, and J.L. Esteves. 2015. Dinophysis species associated with diarrhetic shellfish poisoning (DSP) episodes in North Patagonian gulfs (Chubut, Argentina). Journal of Shellfish Research 34:1,141–1,149, https://doi.org/​10.2983/035.034.0339.

Hattenrath-Lehmann, T., and C.J. Gobler. 2015. The contribution of inorganic and organic nutrients to the growth of a North American isolate of the mixotrophic dinoflagellate Dinophysis acuminate. Limnology and Oceanography 60:1,588–1,603, https://doi.org/10.1002/lno.10119.

Hattenrath-Lehmann, T.K., M.A. Marcoval, D.L. Berry, S. Fire, Z. Wang, S.L. Morton, and C.J. Gobler. 2013. The emergence of Dinophysis acuminata blooms and DSP toxins in shellfish in New York waters. Harmful Algae 26: 33–44, https://doi.org/10.1016/​j.hal.2013.03.005.

Hallegraeff, G.M. 2004. Harmful algal blooms: A global overview. Pp. 25–49 in Manual of Harmful Marine Microalgae. G.M. Hallegraeff, D.M. Anderson, and A.D. Cembella, eds, Intergovernmental Oceanographic Commission of UNESCO, Paris.

Houghton, C., M.P. Hernando, G. Malanga, B. Krock, and U. Tillmann. 2016. Temperature effects on growth, yessotoxin content, and oxidative stress of Protoceratium reticulatum from Argentina (South Atlantic Ocean). P. 116 in ICHA, The 17th International Conference on Harmful Algae, Brazil 2016, Abstract Book. October 9–14, 2016, Florianópolis Santa Catarina, Brazil.

ICES (International Council for the Exploration of the Sea). 2006. Report of the ICES/IOC Workshop on New and Classic Techniques for the Determination of Numerical Abundance and Biovolume of HAB Species: Evaluation of the Cost, Time-Efficiency and Intercalibration Methods (WKNCT). August 22–27, 2005, Kristineberg, Sweden, ICES CM 2005/C:10, 30 pp.

Krock, B., C.M. Borel, F. Barrera, U. Tillmann, E. Fabro, G.O. Almandoz, M.E. Ferrario, J.E. Garzón Cardona, B.P. Koch, C. Alonso, and R. Lara. 2015. Analysis of the hydrographic conditions and cyst beds in the San Jorge Gulf, Argentina, that favor dinoflagellate population development including toxigenic species and their toxins. Journal of Marine Systems 148:86–100, https://doi.org/10.1016/​j.jmarsys.​2015.01.006.

Krock, B., U. Tillmann, U. John, and A.D. Cembella. 2008. LC-MS/MS on board ship: Tandem mass spectrometry in the search for phycotoxins and novel toxigenic plankton from the North Sea. Analytical and Bioanalytical Chemistry 392:797–803, https://doi.org/10.1007/s00216-008-2221-7.

Lassus, P., N. Chomérat, P. Hess, and E. Nézan. 2016. Toxic and harmful microalgae of the World Ocean. Micro-algues toxiques et nuisibles de l’océan mondial. Pp. 523 in IOC Manuals and Guides 68 (English/French), Intl. Society for the Study of Harmful Algae (ISSHA), Intergovernmental Oceanographic Commission of UNESCO (IOC), Copenhagen, Denmark.

Latorre, M.P., I.R. Schloss, G.O. Almandoz, K. Lemarchand, X. Flores-Melo, V. Massé-Beaulne, and G.A. Ferreyra. 2018. Mixing processes at the pycnocline and vertical nitrate supply: Consequences for the microbial food web in San Jorge Gulf, Argentina. Oceanography 31(4):50–59, https://doi.org/10.5670/oceanog.2018.410.

LeGresley, M., and G. McDermott. 2010. Counting chamber methods for quantitative phytoplankton analysis: Haemocytometer, Palmer-Maloney cell and Sedgewick-Rafter cell. Pp. 25–30 in Microscopic and Molecular Methods for Quantitative Phytoplankton Analysis. B. Karlson, C. Cusack and E. Bresnan, eds, UNESCO, Paris.

Matano, R.P., E.D. Palma, and A.R. Piola. 2010. The influence of the Brazil and Malvinas Currents on the Southwestern Atlantic Shelf circulation. Ocean Science 6(4):983–995, https://doi.org/10.5194/os-6-983-2010.

Montoya, N.G., V.K. Fulco, M.O. Carignan, and J.I. Carreto. 2010. Toxin variability in cultured and natural populations of Alexandrium tamarense from southern South America: Evidences of diversity and environmental regulation. Toxicon 56(8):1,408–1,418, https://doi.org/10.1016/​j.toxicon.2010.08.006.

Nielsen, L.T., and T. Kiørboe. 2015. Feeding currents facilitate a mixotrophic way of life. The ISME Journal 9:2,117–2,127, https://doi.org/10.1038/ismej.2015.27.

Palma, E.D., R.P. Matano, and A.R. Piola. 2008. A numerical study of the Southwestern Atlantic Shelf circulation: Stratified ocean response to local and offshore forcing. Journal of Geophysical Research 113(C11), https://doi.org/​10.1029/2007JC004720.

Pérez, L.B., N. Santinelli, V. Sastre, A.A. Pérez, R. Peralta, and M. Bergalio. 2013. Morfología y presencia estacional de Alexandrium tamarense (Lebour) Balech en estaciones costeras del golfo San Jorge (Patagonia, Argentina). Naturalia 50.

Reguera, B., L. Velo-Suárez, R. Raine, and M.G. Park. 2012. Harmful Dinophysis species: A review. Harmful Algae 14:87–106, https://doi.org/10.1016/​j.hal.2011.10.016.

Rivas, A.L., and Pisoni, J.P. 2010. Identification, characteristics and seasonal evolution of surface thermal fronts in the Argentinean continental shelf. Journal of Marine Systems 79:134–143, https://doi.org/​10.1016/​j.jmarsys.2009.07.008.

Röder, K., F.M. Hantzsche, C. Gebühr, C. Miene, T. Helbig, B. Krock, M. Hoppenrath, B. Luckas, and G. Gerdts. 2012. Effects of salinity, temperature and nutrients on growth, cellular characteristics and yessotoxin production of Protoceratium reticulatum. Harmful Algae 15:59–70, https://doi.org/​10.1016/j.hal.2011.11.006.

Sar, E.A., I. Sunesen, A.B. Goya, A.S Lavigne, E. Tapia, C. García, and N. Lagos. 2012. First report of diarrheic shellfish toxins in mollusks from Buenos Aires Province (Argentina) associated with Dinophysis spp.: Evidence of okadaic acid, dinophysistoxin-1 and their acyl derivatives. Boletín de la Sociedad Argentina de Botánica 47:5–14.

Sastre, A.V., N.H. Santinelli, V. Willers, M.E. Solís, S. Díaz Ovejero, L.B. Pérez., A.A. Pérez, M.A. Fajardo, L. Gracia Villalobos, and G.R. Marino. 2013. Floraciones de Alexandrium tamarense y TPM en el Golfo San Jorge in Proceeding of XXXIV Jornadas Argentinas de Botánica, La Plata, Buenos Aires, Argentina.

Seeyave, S., T.A. Probyn, G.C. Pitcher, M.I. Lucas and D.A. Purdie. 2009. Nitrogen nutrition in assemblages dominated by Pseudo-nitzschia spp. Alexandrium catenella and Dinophysis acuminata off the west coast of South Africa. Marine Ecology Progress Series 379:91−107, https://doi.org/10.3354/meps07898.

Sjöqvist, C.O., and T. Lindholm. 2011. Natural co-​occurrence of Dinophysis acuminata (Dinoflagellata) and Mesodinium rubrum (Ciliophora) in thin layers in a coastal inlet. Journal of Eukaryotic Microbiology 58:365−372, https://doi.org/​​10.1111/​​j.1550-​7408.​2011.00559.x.

Skalar Analytical® V.B, 2005a. Skalar Methods - Analysis: Nitrate + Nitrite - Catnr. 461-031 + DIAMOND Issue 081505/MH/99235956. Breda, The Netherlands.

Skalar Analytical® V.B, 2005b. Skalar Methods - Analysis: Phosphate - Catnr. 503-010w/r + DIAMOND Issue 081505/MH/99235956. Breda, The Netherlands.

Skalar Analytical® V.B, 2005c. Skalar Methods - Analysis: Silicate -Catnr. 563-051 + DIAMOND Issue 081505/MH/99235956. Breda, The Netherlands.

Smayda, T.J., and C.S. Reynolds. 2001. Community assembly in marine phytoplankton: Application of recent models to harmful dinoflagellate blooms. Journal of Plankton Research 23:447–461, https://doi.org/10.1093/plankt/23.5.447.

Swanson, K.M., L.J. Flewelling, M. Byrd, A. Nunez, and T.A. Villareal. 2010. The 2008 Texas Dinophysis ovum bloom: Distribution and toxicity. Harmful Algae 9:190−199, https://doi.org/10.1016/​j.hal.2009.10.001.

Torres, A.I., F.E. Paparazzo, G.N. Williams, A.L. Rivas, M.E. Solís, and J.L. Esteves. 2018. Dynamics of macronutrients in the San Jorge Gulf during spring and summer. Oceanography 31(4):25–32, https://doi.org/​10.5670/oceanog.2018.407.

Van Dolah, F.M. 2000. Marine algal toxins: Origins, health effects, and their increased occurrence. Environmental Health Perspectives 108:133–141.

Wiese, M., P.M. D’Agostino, T.K. Mihali, M.C Moffitt, and B.A. Neilan. 2010. Neurotoxic alkaloids: Saxitoxin and its analogs. Marine Drugs 8:2,185–2,211.