Harmful algal blooms during 2008-2010 in the Gulf of Nicoya, Costa Rica

Authors

  • Emilia Calvo-Vargas Universidad Nacional, Costa Rica
  • Karen Berrocal-Artavia Universidad Nacional, Costa Rica
  • Jorge Boza-Abarca Universidad Nacional, Costa Rica

DOI:

https://doi.org/10.15359/revmar.8-1.9

Keywords:

Harmful algal blooms, dominant microalgae, environmental conditions, El Niño, La Niña, Gulf of Nicoya

Abstract

Harmful Algal Blooms (HABs) events were analyzed in this study at four monitoring stations in the Gulf of Nicoya between January 2008 and December 2010. Water samples were collected at 1 and 5 m deep during each HAB event. Furthermore, the following physicochemical parameters were measured in situ: Secchi disk depth, temperature, salinity, dissolved oxygen, and saturation percentage of oxygen in water. Radiation and precipitation data was provided by the National Meteorological Institute of Costa Rica. The concentration of dominant microalgae and associated species was determined. A total of 11 events were recorded, 72.7% during rainy season and 27.3% during dry season, most of them during the La Niña atmospheric phenomenon. Dominant species included the following dinoflagellates; Alexandrium monilatum, Levanderina fissa, Cochlodinium polykrikoides and Prorocentrum minimum, as well as diatom Skeletonema costatum and cyanobacterium Trichodesmium erythraeum. The most frequent associated species were dinoflagellates Dinophysis caudata, Prorocentrum micans, Tripos fusus, Tripos furca and Protoperidinium conicum. HABs in the Gulf of Nicoya were more frequent during the rainy season, probably due to the contributions of the Tempisque, Barranca and Grande de Tárcoles rivers to the estuarine system. This seasonality, together with the alterations caused by El Niño and La Niña atmospheric phenomena, determined the development of HABs in the Gulf of Nicoya during the study period.

Author Biographies

Emilia Calvo-Vargas, Universidad Nacional

Escuela de Ciencias BiológicasEstación de Biología Marina Juan Bertoglia Richards

Karen Berrocal-Artavia, Universidad Nacional

Escuela de Ciencias BiológicasEstación de Biología Marina Juan Bertoglia Richards

Jorge Boza-Abarca, Universidad Nacional

Escuela de Ciencias BiológicasEstación de Biología Marina Juan Bertoglia Richards

References

Alpermann, T. J., Tillman, U., Beszteri, B., Cembella, A. D. & Uwe, J. (2010). Phenotypic variation and genotypic diversity in a planktonic population of the toxigenic marine dinoflagellate Alexandrium tamarense (Dinophyceae). J. Phycol., 46, 18-32. doi: 10.1111/j.1529-8817.2009.00767.x.

Anderson, D. M., Kulis, D. M., Sullivan, J. J., Hall, S. & Lee, C. (1990). Dynamics and physiology of saxitoxin production by the dinoflagellates Alexandrium spp. Mar. Biol., 104, 511-524. doi: 10.1007/BF01314358.

Anderson, D. M., Cembella, A. D. & Hallegraeff, G. M. (2012). Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management. Annu. Rev. Mar. Sci., 4, 143-176. doi: 10.1146/annurev-marine-120308-081121.

Andresen, E., Lohscheider, J., Šetlikova, E., Adamska, I., Šimek, M. & Küpper, H. (2010). Acclimation of Trichodesmium erythraeum lSM101 to high and low irradiance analysed on the physiological, biophysical and biochemical level. New Phytologist, 185(1), 173-188. doi: 10.1111/j.1469-8137.2009.03068.x.

Basti, L., Nagai, S., Go, J., Okano, S., Nagai, K., Watanabe, R., … & Tanaka, Y. (2015). Differential inimical effects of Alexandrium spp. and Karenia spp. on cleavage, hatching, and two larval stages of Japanese pearl oyster Pinctada fucata martensii. Harmful Algae, 43, 1-12. doi: 10.1016/j.hal.2014.12.004.

Berden-Zrimec, M., Flander-Putrle, V., Drinovec, L., Zrimec, A. & Monti, M. (2008). Growth, delayed fluorescence and pigment composition of four Prorocentum minimum strains growing at two salinities. Biol. Res., 41, 11-23. doi: 10.4067/S0716-97602008000100003.

Calvo, E. (2002). Factores bióticos y abióticos relacionados con la distribución del dinoflagelado tóxico Pyrodinium bahamense var. compressum (Plate 1906) en el Golfo de Nicoya, Costa Rica. Tesis de Licenciatura no publicada, Universidad Nacional, Heredia, Costa Rica.

Calvo, E., Víquez, R. & García, A. (2005). Alexandrium monilatum (Howell) Balech Bloom in the Gulf of Nicoya, Puntarenas. In The Intergovernmental Oceanographic Commission of UNESCO (Eds.), Harmful Algae News, 29, 1-2.

Calvo, E. (2012). Comportamiento del microfitoplancton marino en el Golfo de Nicoya, Costa Rica: Variación estacional, floraciones nocivas y efectos de El Niño y La Niña durante 2008 a 2010. Tesis de Maestría no publicada, Universidad Nacional, Heredia, Costa Rica.

Calvo Vargas, E., Boza Abarca, J. & Berrocal Artavia, K. (2014). Efectos de El Niño y La Niña sobre el comportamiento del microfitoplancton marino y las variables fisicoquímicas durante el 2008 a 2010 en el Golfo de Nicoya, Costa Rica. Rev. Mar. Cost., 6, 115-133. doi: http://dx.doi.org/10.15359/revmar.6.8.

Carrillo, O. L., Cortés-Altamirano, R., Leiva-Cerezo, V. & Ramírez, V. (2007). Cochlodinium catenatum on Guatemala coast (2004 & 2007). In The Intergovernmental Oceanographic Commission of UNESCO (Eds.), Harmful Algae News, 33, 15-17.

Carvalho, M., Gianesella, S. M. F. & Saldanha-Corrêa, F. M. P. (2008). Trichodesmium erythraeum Bloom on the Continental Shelf off Santos, Southeast Brazil. Braz. J. Oceanogr., 56(4), 307-311. doi: 10.1590/S1679-87592008000400006.

Castellví, J. (1963). Pigmentos de la diatomea marina Skeletonema costatum (Grev.) en su dependencia de los factores ambientales y de la dinámica de las poblaciones. Inv. Pesq., 24, 129-137.

Castro, E. & León, S. (1998). El estado del arte de la investigación en valoración de aguas degradadas en regiones marino-costeras: El caso del Golfo de Nicoya. Informe Preliminar. Centro Internacional de Política Económica para el Desarrollo Sostenible-CINPE, Heredia, Costa Rica.

Chang, S. K., Lee, S. G., Lee, C. K., Kim, H. G. & Jung, J. (1999). Reactive oxygen species as causative agents in the icthyotoxicity of red tide dinoflagellate Cochlodinium polykrikoides. J. Plankton Res., 21(11), 2105-2115. doi: 10.1093/plankt/21.11.2105.

Choi, J. K., Min, J. E., Noh, J. H., Han, T. H., Yoon, S., Park, Y. J., … & Park, J. H. (2014). Harmful algal bloom (HAB) in the East Sea identified by the Geostationary Ocean Color Imager (GOCI). Harmful Algae, 39, 295-302. doi: 10.1016/j.hal.2014.08.010.

Cortés-Lara, M. C., Cortés-Altamirano, R. & Sierra-Beltrán, A. P. (2004). Presencia de Cochlodinium catenatum (Gymnodiniales: Gymnodiniaceae) en mareas rojas de Bahía Banderas, Pacífico mexicano. Rev. Biol. Trop., 52(Suppl. 1), 35-49.

Da-Zhi, W., Shu-Gang, Z., Hai-Feng, G., Leo, C. & Hua-Sheng, H. (2006). Paralytic shellfish toxin profiles and toxin variability of the genus Alexandrium (Dinophyceae) isolated from the southeast China Sea. Toxicon, 48(2), 138-151. doi: 10.1016/j.toxicon.2006.04.002.

Gallegos, C. L. & Bergstrom, P. W. (2005). Effect of a Prorocentrum minimum bloom on light availability for and potential impacts on submersed aquatic vegetation in upper Chesapeake Bay. Harmful Algae, 4, 553-574. doi: 10.1016/j.hal.2004.08.016 .

Gárate-Lizárraga, I., López-Cortés, D. J., Bustillos-Guzmán, J. J. & Fernández-Sandoval, F. (2004). Blooms of Cochlodinium polykrikoides (Gymnodiniaceae) in the Gulf of California, Mexico. Rev. Biol. Trop., 52(Suppl. 1), 51-58.

Gárate-Lizárraga, I., Muñetón-Gómez, M. & Maldonado-López, V. (2006). Florecimiento del dinoflagelado Gonyaulax polygramma frente a la Isla Espíritu Santo, Golfo de California, México. Rev. Invest. Mar., 27(1), 31-39.

Gárate-Lizárraga, I. & Muciño-Márquez, R. E. (2012). Blooms of Trichodesmium erythraeum and T. thiebautii (Cyanobacteria, Oscillatoriales) in the Bahía de La Paz, Gulf of California. Oceánides, 27(1), 61-64.

Gárate-Lizárraga, I., Sevilla-Torres, G., Álvarez-Añorve, M., Aguirre-Bahena, F., Violante-González, J. & Rojas-Herrera, A. (2013). First record of a red tide caused by Gyrodinium instriatum (Dynophyceae: Gymnodiniales) in Bahía de Acapulco, Guerrero. Oceánides, 28(1), 43-47.

Gárate-Lizárraga, I. (2013). Bloom of Cochlodinium polykrikoides (Dynophyceae: Gymnodiniales) in Bahía de La Paz, Gulf of California. Mar. Pollut. Bull., 67, 217-222. doi: 10.1016/j.marpolbul.2012.11.031.

Gárate-Lizárraga, I. (2014). Proliferation of

Levanderina fissa and Polykrikos hartmannii (Dinophyceae: Gymnodiniales) in Bahía de La Paz, Gulf of California, México. Oceánides, 29(2), 25-35.

Grzebyk, D. & Berland, B. (1996). Influences of temperature, salinity and irradiance on growth of Prorocentrum minimum (Dinophyceae) from Mediterranean Sea. J. Plankton Res., 18(10), 1837-1849. doi: 10.1093/plankt/18.10.1837.

Grzebyk, D., Denardou, A., Berland, B. & Pouchus, Y. F. (1997). Evidence of a new toxin in the red-tide dinoflagellate Prorocentrum minimum. J. Plankton Res., 19(8), 1111-1124. doi: 10.1093/plankt/19.8.1111.

Hansen, G. & Moestrup, Ø. (1998). Fine-structural Characterization of Alexandrium catenella (Dinophyceae) with special emphasis on the flagellar apparatus. Eur. J. Phycol., 33, 281-291.

Hargraves, P. & Víquez, R. (1981). The dinoflagellate red tide in Golfo of Nicoya, Costa Rica. Rev. Biol. Trop., 29(1), 31-38.

Hargraves, P. & Víquez, R. (1985). Spatial and temporal distribution of phytoplankton in the Gulf of Nicoya, Costa Rica. Bull. Mar. Sci., 37(2), 577-585.

Heil, C., Glibert, P. & Fan, C. (2004). Prorocentrum minimum (Pavillard) Schiller A review of a harmful algal bloom species of growing worldwide importance. Harmful Algae, 4(3), 449-470. doi: 10.1016/j.hal.2004.08.003.

Huo, W. Y. & Shu, J. J. (2005, noviembre). Outbreak of Skeletonema costatum bloom and its relations to environmental factors in Jiaozhou Bay, China. Ponencia presentada in el WSEAS International Conference on Environment, Ecosystems and Development, Venecia, Italia.

Ibelings, B. W., Backer, L. C., Kardinaal, W. E. A. & Chorus, I. (2014). Current approaches to cyanotoxin risk assessment and risk management around the globe. Harmful Algae, 40, 63-74. doi: 10.1016/j.hal.2014.10.002.

Juhl, A. R. (2005). Growth rates and elemental composition of Alexandrium monilatum, a red-tide dinoflagellate. Harmful Algae, 4, 287-295. doi: 10.1016/j.hal.2004.05.003.

Kranz, S. A., Levitan, O., Richter, K., Prášil, O., Berman, I. & Björn, R. (2010). Combined effects of CO2 and light on the N2-fixing cyanobacterium Trichodesmium IMS101: physiological responses. Plant Physiol., 154, 334-345. doi: 10.1104/pp.110.159145.

Kress, N., León, S., Brenes, C., Brenner, S. & Arroyo, G. (2001). Horizontal transport and seasonal distribution of nutrients, dissolved oxygen and chlorophyll-a in the Gulf of Nicoya, Costa Rica: a tropical estuary. Cont. Shelf Res., 763, 1-16.

Kudela, R. M., Ryan, J. P., Blakely, M. D., Lane, J. Q. & Peterson, T. D. (2008). Linking the physiology and ecology of Cochlodinium to better understand harmful algal bloom events: A comparative approach. Harmful Algae, 7, 278-292. doi: 10.1016/j.hal.2007.12.016.

León, S., Kress, N., Brenes, C. & Brenner, S. (1998-1999). Una contribución a la ecología del Golfo de Nicoya. Uniciencia, 15-16, 35-37.

Lim, P. T. & Ogata, T. (2005). Salinity effect on growth and toxin production of four tropical Alexandrium species (Dinophyceae). Toxicon, 45, 699-710. doi: 10.1016/j.toxicon.2005.01.007.

Matsuoka, K., Iwataki, M. & Kawami, K. (2008). Morphology and taxonomy of chain-forming species of the genus Cochlodinium (Dinophyceae). Harmful Algae, 7, 261-270. doi: 10.1016/j.hal.2007.12.002.

May, S. P., Burkholder, J. M., Shumway, S. E., Hégaret, H. & Wikfors, G. H. (2010). Effects of the toxic dinoflagellate Alexandrium monilatum on survival, grazing and behavioral response of three ecologically important bivalve molluscs. Harmful Algae, 9, 281-293. doi: 10.1016/j.hal.2009.11.005.

Nagasoe, S., Kim, D., Shimasaki, Y., Oshima, Y., Yamaguchi, M. & Honjo, T. (2006). Effects of temperature, salinity and irradiance on the growth of the red tide dinoflagellate Gyrodinium instriatum Freudenthal et Lee. Harmful Algae, 5, 20-25. doi: 10.1016/j.hal.2005.06.001.

Nagasoe, S., Shikata, T., Yamasaki, Y., Matsubara, T., Shimasaki, Y., Oshima, Y. & Honjo, T. (2010). Effects of nutrients on growth of the red-tide dinoflagellate Gyrodinium instriatum Freudenthal et Lee and a possible link to blooms of this species. Hidrobiologia, 651, 225-238. doi: 10.1007/s10750-010-0301-0.

Narayana, S., Chitra, J., Tapase, S. R., Thamke, V., Karthick, P., Ramesh, Ch., … Mohanraju, R. (2014). Toxicity studies of Trichodesmium erythraeum (Ehrenberg, 1830) bloom extracts, from Phoenix Bay, Port Blair, Andamans. Harmful Algae, 40, 34-39. doi: 10.1016/j.hal.2014.10.003.

Negri, A., Bunter, O., Jones, B. & Llewellyn, L. (2004). Effects of the bloom-forming alga Trichodesmium erythraeum on the pearl oyster Pinctada maxima. Aquaculture, 232, 91-102. doi: 10.1016/S0044-8486(03)00487-3.

Peña, V. & Pinilla, G. A. (2002). Composición, distribución y abundancia de la comunidad fitoplanctónica de la ensenada de Utría, Pacífico colombiano. Rev. Biol. Mar. Oceanogr., 37(1), 67-81.

Richlen, M. L., Morton, S. L., Jamali, E. A., Rajan, A. & Anderson, D. M. (2010). The catastrophic 2008-2009 red tide in the Arabian gulf region, with observations on the identification and phylogeny of the fish-killing dinoflagellate Cochlodinium polykrikoides. Harmful Algae, 9, 163-172. doi: 10.1016/j.hal.2009.08.013.

Sarno, D., Kooistra, W. H. C. F., Balzano, S., Hargraves, P. E. & Zingone, A. (2007). Diversity in the genus Skeletonema (Bacillariophyceae): III. Phylogenetic position and morphological variability of Skeletonema costatum and Skeletonema grevillei, with the description of Skeletonema ardens sp. nov. J. Phycol., 43, 156-170. doi: 10.1111/j.1529-8817.2006.00305.x.

Satpathy, K. K., Mohanty, A. K., Sahu, G., Prasad, M. V. R., Venkatesan, R., Natesan, U. & Rajan, M. (2007). On the occurrence of Trichodesmium erythraeum (Ehr) bloom in the coastal waters of Kalpakkam, east coast of India. Indian J. Sci. Technol., 1(2), 1-9.

Siqueira, A., Kolm, H. E. & Pereira, F. (2006). Offshore distribution patterns of the cyanobacterium Trichodesmium erythraeum ehrenberg and associated phyto- and bacterioplankton in the southern Atlantic coast (Paraná, Brazil). Braz. Arch. Biol. Technol., 49(2), 323-337. doi: 10.1590/S1516-89132006000300018.

SPSS. (2006). Statistical Package for the social science for Windows, version 17.0. Chicago, EE. UU.: SPSS Inc.

Taş, S. & Okuş, E. (2011). A review on the bloom dynamics of a harmful dinoflagellate Prorocentrum minimum in the Golden Horn Estuary. Turkish J. Fish. Aquat. Sci., 11, 673-681.

Taylor, J. D., Kegel, J. U., Lewis, J. M. & Medlin, L. K. (2014). Validation of the detection of Alexandrium species using specific RNA probes tested in a microarray format: Calibration of signal using variability of RNA content with environmental conditions. Harmful Algae, 37, 17-27. doi: 10.1016/j.hal.2014.05.001.

Thillairajasekar, K., Duraipandivan, V., Perumal, P. & Ignacimuthu, S. (2009). Antimicrobial activy of Trichodesmium erythraeum (Ehr) (microalga) from south east coast of Tamil Nadu, India. Int. J. Integr. Biol., 5(3), 167-170.

Uchida, T., Kamiyama, T. & Matsuyama, Y. (1997). Predation by a photosynthetic dinoflagellate Gyrodinium instriatum on loricated ciliates. J. Plankton Res., 19(5), 603-608. doi: 10.1093/plankt/19.5.603.

Vargas-Montero, M., Freer, E., Jiménez-Montealegre, R. & Guzmán, J. C. (2006). Occurrence and predominance of the fish killer Cochlodinium polykrikoides onthe Pacific coast of Costa Rica. S. Afr. J. Marine Sci., 28(2), 215-217. doi: 10.2989/18142320609504150.

Vargas-Montero, M., Freer, E., Guzmán, J. C. & Vargas, J. C. (2008). Florecimientos de dinoflagelados nocivos en la costa pacífica de Costa Rica. Hidrobiológica, 18(1 Supl.), 15-23.

Víquez, R. & Hargraves, P. E. (1995). Annual Cycle of Potentially Harmfull Dinoflagellates in the Golfo de Nicoya, Costa Rica. Bull. Mar. Sci., 57(2), 467-475.

Witek, B. & Plínski, M. (2000). The first recorded bloom of Prorocentrum minimum (Pavillard) Schiller in the coastal zone of the Gulf of Gdańsk. Oceanologia, 42(1), 29-36.

Yamaguchi, K., Oshima, Y., Oda, T. & Hongo, T. (2011). Cell contact-dependent lethal effect of the dinoflagellate Heterocapsa circularisquama on phytoplankton-phytoplankton interactions. J. Sea Res., 65, 76-83. doi: 10.1016/j.seares.2010.07.006.

Yamasaki, Y., Shikata, T., Nukata, A., Ichiki, S., Nagasoe, S., Matsubara, T., … & Honjo, T. (2009). Extracellular polysaccharide-protein complexes of a harm alga mediate the allelopathic control it exerts within the phytoplankton community. ISME Journal, 3, 808-817. doi: 10.1038/ismej.2009.24.

Yamasaki, Y., Ohmichi, Y., Shikata, T., Hirose, M., Shimasaki, Y., Oshima, Y. & Honjo, T. (2010). Species-specific allelopathic effects of the diatom Skeletonema costatum. Thalassas, 27(1), 21-32.

Zhuang, Y., Zhang, H., Hannick, L. & Lin, S. (2015). Metatranscriptome profiling reveals Versatile N-nutrient utilization, CO2 limitation, oxidative stress, and active Toxin production in an Alexandrium fundyense bloom. Harmful Algae, 42, 60-70. doi: 10.1016/j.hal.2014.12.006.

Published

2016-03-05

How to Cite

Calvo-Vargas, E., Berrocal-Artavia, K., & Boza-Abarca, J. (2016). Harmful algal blooms during 2008-2010 in the Gulf of Nicoya, Costa Rica. Journal of Marine and Coastal Sciences, 8(1), 129-149. https://doi.org/10.15359/revmar.8-1.9

Issue

Section

Scientific articles

How to Cite

Calvo-Vargas, E., Berrocal-Artavia, K., & Boza-Abarca, J. (2016). Harmful algal blooms during 2008-2010 in the Gulf of Nicoya, Costa Rica. Journal of Marine and Coastal Sciences, 8(1), 129-149. https://doi.org/10.15359/revmar.8-1.9

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