Advertisement

Environmental Monitoring and Assessment

, Volume 186, Issue 10, pp 6627–6644 | Cite as

Seasonality in the distribution of dinoflagellates with special reference to harmful algal species in tropical coastal environment, Bay of Bengal

  • Gouri Sahu
  • A. K. Mohanty
  • M. K. Samantara
  • K. K. Satpathy
Article

Abstract

A study was carried out in the coastal waters of Kalpakkam, southeast coast of India, to find out the seasonal variation in dinoflagellate community structure. Samples were collected for a period of 4 years during 2006–2010. During the study 69 species of dinoflagellates were encountered among which Ceratium furca and Prorocentrum micans were most common during all the seasons. Genus Ceratium was found to be the most diverse one with 23 species which was followed by genus Protoperidinium with 16 species. Of 69 species, 27 species were considered as dominant based on their abundance during pre-monsoon (PRM), monsoon (MON) and post-monsoon (POM) periods. Relatively high density and diversity of dinoflagellates were encountered during the PRM period as compared to the MON and POM periods. Abundance pattern of dinoflagellates for three seasons showed the following trend: PRM > POM > MON. Salinity showed a positive correlation with dinoflagellate community showing its importance in dinoflagellate growth and sustenance. Ammonia and phosphate developed negative correlation with dinoflagellate density indicating the utilization of these nutrients by the dinoflagellate community. The presence of three dinoflagellate associations, broadly representing the three seasons experienced at this location, was evident from the cluster analysis. The study revealed presence of 19 relatively abundant toxic/red tide forming dinoflagellate species in the coastal waters of Kalpakkam.

Keywords

Phytoplankton Dinoflagellates Species diversity Toxin Tropical environment Bay of Bengal 

References

  1. Akiba, T., & Hattori, Y. (1949). Food poisoning caused by eating asari and oyster-toxic substance, venerupin. Japanese Journal of Experimental Medicine, 20, 271–284.Google Scholar
  2. Alkawri, A. A. S., & Ramaiah, N. (2010). Spatio-temporal variability of dinoflagellate assemblages in different salinity regimes in the west coast of India. Harmful Algae, 9, 153–162.CrossRefGoogle Scholar
  3. Anderson, D. M. (1989). Toxic algal blooms and red tides: a global perspective. In T. Okaichi, D. M. Anderson, & T. Nomoto (Eds.), Red tides: biology, environmental science and toxicology (pp. 11–16). New York: Elsevier.Google Scholar
  4. Anderson, D. M., Glibert, P. M., & Burkholder, J. M. (2002). Harmful algal blooms and eutrophication: nutrient sources, composition and consequences. Estuaries, 25, 704–726.CrossRefGoogle Scholar
  5. Baek, S. H., Shimode, S., Han, M., & Kikuchi, T. (2008). Growth of dinoflagellates, Ceratium furca and Ceratium fusus in Sagami Bay, Japan: the role of nutrients. Harmful Algae, 7, 729–739.CrossRefGoogle Scholar
  6. Bhat, S. R., & Matondkar, S. G. P. (2004). Algal blooms in the seas around India — networking for research and outreach. Current Science, 87, 1079–1083.Google Scholar
  7. Bhat, S. R., De Souza, P., Devi, L., Verlecar, X. N., & Naik, C. G. (2006). Multiple dimensions of global environmental change (pp. 419–431). India: TERI Press.Google Scholar
  8. Burkholder, J. M., Glibert, P. M., & Skelton, H. M. (2008). Mixotrophy, a major mode of nutrition for harmful algal species in coastal waters. Harmful Algae, 8, 77–93.CrossRefGoogle Scholar
  9. Buskey, E. J. (1997). Behavioral components of feeding selectivity of the heterotrophic dinoflagellate Protoperidinium pellucidum. Marine Ecology Progress Series, 153, 77–89.CrossRefGoogle Scholar
  10. Cardwell, R. D., Lopez, S., Carr, M. I., & Sanborn, E. W. (1979). Causes of oyster larvae mortality in southern Puget Sound (p. 73). Seattle, WA: National Oceanic and Atmospheric Administration.Google Scholar
  11. Chandran, R., & Ramamoorthi, K. (1984). Hydrobiological studies in the gradient zone of the Vellar Estuary: II. Nutrients. Mahasagar Bulletin of the National Institute of Oceanography, 17, 133–140.Google Scholar
  12. Cloern, J. E., & Dufford, R. (2005). Phytoplankton community ecology: principles applied to San Francisco Bay. Marine Ecology Progress Series, 285, 11–28.CrossRefGoogle Scholar
  13. D’Costa, P. M. D., Anil, A. C., Patil, J. S., Hegde, S., D’Silva, M. S., & Chourasia, M. (2008). Dinoflagellates in a mesotrophic, tropical environment influenced by monsoon. Estuarine, Coastal and Shelf Science, 77, 77–90.CrossRefGoogle Scholar
  14. Devassy, V. P., & Bhat, S. R. (1991). The killer tides. Science Reporter, 28(5), 16–19.Google Scholar
  15. Devassy, V. P., & Bhattathiri, P. M. A. (1981). Distribution of phytoplankton and chlorophyll a around little Andaman Islands. Indian Journal of Marine Science, 10, 248–252.Google Scholar
  16. Dodge, J. D. (1975). The Prorocentrales (Dinophyceae). II. Revision of the taxonomy within the genus Prorocentrum. Botanical Journal of the Linnean Society, 71, 103–125.CrossRefGoogle Scholar
  17. Dodge, J. D. (1982). Marine Dinoflagellates of the British Isles (p. 303). London: Her Majesty's Stationery Office.Google Scholar
  18. Escalera, L., Pazos, Y., Morono, A., & Reguera, B. (2007). Noctiluca scintillans may act as a vector of toxigenic microalgae. Harmful Algae, 6(3), 317–320.CrossRefGoogle Scholar
  19. Fleming, L. E., Kirkpatrick, B., Backer, L. C., Walsh, C. J., et al. (2011). Review of Florida red tide and human health effects. Harmful Algae, 10(2), 224–233.CrossRefGoogle Scholar
  20. Gaines, G., Elbrächter, M. (1987). Heterotrophic nutrition. In: Taylor, F. J. R. (Ed.) The biology of dinoflagellates. Botanical Monograph, 21:224–268.Google Scholar
  21. Giannakourou, A., Orlova, T. Y., Assimakopoulou, G., & Pagou, K. (2005). Dinoflagellate cysts in recent marine sediments from Thermaikos Gulf, Greece: effects of resuspension events on vertical cyst distribution. Continental Shelf Research, 25, 2585–2596.CrossRefGoogle Scholar
  22. Glibert, P. M., & Legrand, C. (2006). The diverse nutrient strategies of harmful algae: focus on osmotrophy. In E. Granéli & J. Turner (Eds.), The ecology of harmful algae (pp. 163–176). New York: Springer-Verlag.CrossRefGoogle Scholar
  23. Glibert, P., and Pitcher, G. (2001). Global ecology and oceanography of harmful algal blooms. Science Plan. Baltimore, MD: SCOR and IOC, 86 pp.Google Scholar
  24. Glibert, P. M., Heil, C. A., Hollander, D., Revilla, M., Hoare, A., Alexander, J., et al. (2004). Evidence for dissolved organic nitrogen and phosphorous uptake during a Cyanobacterial bloom in Florida Bay. Marine Ecology Progress Series, 280, 73–83.CrossRefGoogle Scholar
  25. Glibert, P. M., Seitzinger, S., Heil, C. A., Burkholder, J. M., Parrow, M. W., Codispoti, L. A., et al. (2005). The role of eutrophication in the global proliferation of harmful algal blooms. New perspectives and new approaches. Oceanography, 18, 198–209.CrossRefGoogle Scholar
  26. Glibert, P. M., Harrison, J., Heil, C., & Seitzinger, S. (2006). Escalating worldwide use of urea—a global change contributing to coastal eutrophication. Biogeochemistry, 77, 441–463.CrossRefGoogle Scholar
  27. Godhe, A., & Karunasagar, I. (1996). Gymnodinium catenatum on west coast of India. Harmful Algae News, 15, 1.Google Scholar
  28. Gopalkumar, G., Sulochanan, B., & Venkatesan, V. (2009). Bloom of Noctiluca scintillans (Macartney) in Gulf of Mannar, southeast coast of India. Journal of Marine Biological Association of India, 51(1), 75–80.Google Scholar
  29. Gotsis-Skretas, O., & Frigilos, N. (1990). Contribution to eutrophication and phytoplankton ecology in the Thermaikos Gulf. Thalassographica, 13, 1–12.Google Scholar
  30. Gotsis-Skretas, O., & Ignatiades, L. (2005). Phytoplankton in pelagic and coastal waters. In E. Papathanassiou & A. Zenetos (Eds.), State of the Hellenic Marine Environment (pp. 187–193). Athens, Greece: HCMR.Google Scholar
  31. Gotsis-Skretas, O., Ignatiades, L., Pavlidou, A., Metaxatos, A., Papadopoulos, A., Pappas, G. (2003). Alexandrium spatio-temporal distribution in the strategy areas (WP1) March 2002–October 2002: Greek Area; In: Second Year Report of the EU Project “STRATEGY” New Strategy of Monitoring and Management of HABs in the Mediterranean Sea, Annex III, pp. 1–14.Google Scholar
  32. Granéli, E., Turner, J. T. (Eds.). (2006). Ecological Studies, In: Ecology of harmful algae, Springer-Verlag, Berlin, Heidelberg.Google Scholar
  33. Grasshoff, K., Ehrhardt, M., & Kremling, K. (1983). Methods of seawater analysis. New York: Wiley-VCH.Google Scholar
  34. Gribble, K. E., Nolan, G., & Anderson, D. M. (2007). Biodiversity, biogeography, and potential trophic impact of Protoperidinium spp. (Dinophyceae) off the southwestern coast of Ireland. Journal of Plankton Research, 29, 931–947.CrossRefGoogle Scholar
  35. Hallegraeff, G. M. (1991). Aquaculturists Guide to Harmful Australian Microalgae (p. 111). Hobart: Fishing Industry Training Board of Tasmania/CSIRO Division of Fisheries.Google Scholar
  36. Hallegraeff, G. M. (1993). A review of harmful algal blooms and their apparent global increase. Phycologia, 32, 79–99.CrossRefGoogle Scholar
  37. Halstead, B. W., & Schantz, E. J. (1984). Paralytic shellfish poisoning (Vol. 76, pp. 1–60). Geneva: WHO Offset Publ., World Health Organization.Google Scholar
  38. Harrison, W. G. (1976). Nitrate metabolism of the red tide dinoflagellate Gonyaulax polyedra Stein. Journal of Experimental Marine Biology and Ecology, 21, 199–209.CrossRefGoogle Scholar
  39. Heil, C. A., Glibert, P. M., & Fan, C. (2005). Prorocentrum minimum (Pavillard) Schiller — a review of a harmful algal bloom species of growing worldwide importance. Harmful Algae, 4, 449–470.CrossRefGoogle Scholar
  40. Heil, C. A., Revilla, M., Glibert, P. M., & Murasko, S. (2007). Nutrient quality drives phytoplankton community composition on the West Florida Shelf. Limnology and Oceanography, 52, 1067–1078.CrossRefGoogle Scholar
  41. Heisler, J., Glibert, P. M., Burkholder, J. M., Anderson, D. M., Cochlan, W., Dennison, W. C., et al. (2008). Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae, 8, 3–13.CrossRefGoogle Scholar
  42. Horstman, D. A. (1981). Reported red water outbreaks and their effects on fauna of the west and south coasts of South Africa 1959–1980. Fisheries Bulletin of South Africa, 15, 71–88.Google Scholar
  43. Ignatiades, L., & Gotsis-Skretas, O. (2010). A review on toxic and harmful algae in Greek coatal waters (E. Mediterranean Sea). Toxins, 2, 1019–1037.CrossRefGoogle Scholar
  44. Ignatiades, L., Georgopoulos, D., & Karydis, M. (1995). Description of phytoplanktonic community of the oligotrophic waters of S.E. Aegean Sea. Marine Ecology, 16, 13–26.CrossRefGoogle Scholar
  45. Ishimaru, T., Inoue, H., Fukuyo, Y., Ogata, T., Kodama, M. (1988). Culture of Dinophysis fortii and D. acuminata with the cryptomonad, Plagioselmis sp. In: Aibara, K., Kumagai, S., Ohtsubo, K., Yoshizawa, T. (Eds.), Mycotoxins and Phycotoxins. Jap. Ass. Mycotoxicol., Tokyo, Special issue No. 1, pp. 19–20.Google Scholar
  46. Jacobson, D. M., & Anderson, D. M. (1996). Widespread phagocytosis of ciliates and other protists by marine mixotrophic and heterotrophic thacate dinoflagellates. Journal of Phycology, 32, 279–285.CrossRefGoogle Scholar
  47. Jeong, H. J., Park, J. Y., Nho, J. H., Park, M. O., Ha, J. H., Seong, K. A., Jeng, C., Seong, C. N., Lee, K. Y., & Yih, W. H. (2005a). Feeding by red tide dinoflagellates on the cyanobacterium Synechococcus. Aquatic Microbial Ecology, 41, 1331–2143.Google Scholar
  48. Jeong, H. J., Yoo, D. Y., Park, J. Y., Song, J. Y., Kim, S. T., Lee, S. H., Kim, K. Y., & Yih, W. H. (2005b). Feeding by phototrophic red-tide dinoflagellates: five species newly revealed and six species previously known to be mixotrophic. Aquatic Microbial Ecology, 40, 133–150.CrossRefGoogle Scholar
  49. Jeong, H. J., Yoo, Y. D., Kim, J. S., Seong, K. A., Kang, N. S., & Kim, T. H. (2010). Growth, Feeding and Ecological Roles of the Mixotrophic and Heterotrophic Dinoflagellates in Marine Planktonic Food Webs. Ocean Science Journal, 45(2), 65–91.CrossRefGoogle Scholar
  50. Jocelyn, D.C., Penelope, A., Randall, L., and Suthers, I. (2000). Noctiluca scintillans – An indicator of coastal eutrophication. In: HAB ninth conference Tasmania, www.utas.edu.au/docs/plant-science/HAB2000/abstracts/docs.
  51. Joseph, K. J., & Pillai, V. K. (1975). Seasonal and spatial distribution of phytoplankton in Cochin backwaters. Bulletin of the Department of Marine Science University of Cochin, 7, 171–180.Google Scholar
  52. Karunasagar, I., Gowda, H. S. V., Subburaj, M., Venugopal, M. N., & Karunasagar, I. (1984). Outbreak of paralytic shellfish poisoning in Mangalore west coast of India. Current Science, 53, 247–249.Google Scholar
  53. Karunasagar, I., Joseph, B., Philipose, K. K., & Karunasagar, I. (1998). Another outbreak of PSP in India. Harmful Algae News, 17, 1.Google Scholar
  54. Kirkpatrick, B., Fleming, L., Squicciarini, E. D., Backer, L. C., Clark, R., Abrahamb, W., et al. (2004). Literature review of Florida red tide: implications for human health effects. Harmful Algae, 3, 99–115.CrossRefGoogle Scholar
  55. Koizumi, Y., Kohno, J., Matsuyama, N., Uchida, T., & Honjo, T. (1996). Environmental features and the mass mortality of fish and shellfish during the Gonyaulax polygramma red tide occurred in and round Uwajima Bay, Japan, in 1994. Nippon Suisan Gakkaishi, 62, 217–224.CrossRefGoogle Scholar
  56. Koukaras, K., & Nikolaidis, G. (2004). Dinophysis blooms in Greek coastal waters (Thermaikos Gulf, NW Aegean Sea). Journal of Plankton Research, 26, 445–457.CrossRefGoogle Scholar
  57. Kudela, R., Pitcher, G., Probyn, T., Figueiras, F., Moita, T., & Trainer, V. (2005). Harmful algal blooms in coastal upwelling systems. Oceanography, 18(2), 184–197.CrossRefGoogle Scholar
  58. Lagus, A., Suomela, J., Weithoff, G., Heikkilä, K., Helminen, H., & Sipura, J. (2004). Species-specific differences in phytoplankton responses to N and P enrichments and the N:P ratio in the Archipelago Sea, northern Baltic Sea. Journal of Plankton Research, 26(7), 779–798.CrossRefGoogle Scholar
  59. Landsberg, J. H. (2002). The effects of harmful algal blooms on aquatic organisms. Reviews of Fishery Science, 10, 113–390.CrossRefGoogle Scholar
  60. Lawrence, J. E., Grant, J., Quilliam, M. A., Bauder, A. G., & Cembella, A. D. (2000). Colonization and growth of the toxic dinoflagellate Prorocentrum lima and associated fouling macroalgae on mussels in suspended culture. Marine Ecology Progress Series, 201, 147–154.CrossRefGoogle Scholar
  61. Lee, J. S., lgarashi, T., Fraga, S., Dahl, E., Hovgaard, P., & Yasumoto, T. (1989). Determination of diarrhetic shellfish toxins in various dinoflagellate species. Journal of Applied Phycology, 1, 147–152.CrossRefGoogle Scholar
  62. Li, A., Stoecker, D. K., Coats, D. W., & Adam, E. J. (1996). Ingestion of fluorescently labeled and phycoerythrin-containing prey by mixotrophic dinoflagellates. Aquatic Microbial Ecology, 10, 139–147.CrossRefGoogle Scholar
  63. Li, J., Glibert, P. M., Zhou, M., LU, S., & Lu, D. (2009). Relationships between nitrogen and phosphorous forms and ratios and the development of dinoflagellate blooms in the East China Sea. Marine Ecology Progress Series, 383, 11–26.CrossRefGoogle Scholar
  64. Lok, A., Metin, G., Acarli, S., & Goulletquer, P. (2010). Harmful Algal Blooms (HABS) and Black Mussel Mytilus galloprovincialis (Linnaeus, 1758) Culture in Izmir Bay (Iskele-Urla) –Turkey: Preliminary Results on the Annual Feeding Cycle Using a Qualitative Approach. Turkish Journal of Fisheries and Aquatic Sciences, 10, 527–536.CrossRefGoogle Scholar
  65. Maclean, J. L., & White, A. W. (1985). Toxic dinoflagellate blooms in Asia: a growing concern. In D. M. Anderson, A. W. White, & D. G. Boden (Eds.), Toxic dinoflagellates (pp. 517–520). New York, USA: Elsevier.Google Scholar
  66. Mandelli, E. F., Burkholder, P. R., Doheny, T. E., & Brody, R. B. (1970). Studies of primary productivity in coastal waters of southern Long Island, New York. Marine Biology, 7, 153–160.CrossRefGoogle Scholar
  67. Marasigan, A. N., Sato, S., Fukuyo, Y., & Kodama, M. (2001). Accumulation of a high level of diarrhetic shellfish toxins in the green mussel Perna viridis during a bloom of Dinophysis caudata and Dinophysis miles in Saipan Bay, Panay Island, the Philippines. Fisheries Science, 67, 994–996.CrossRefGoogle Scholar
  68. Margalef, R. (1951). Diversidad de especies en las communidades naturals. Publicaciones Institute Biologia Aplicada, 9, 5–27.Google Scholar
  69. Mendon, M. R., Katti, R. J., Rajesh, K. M., & Gupta, T. R. C. (2002). Diversity of dinoflagellates in the sea off Manglore. Indian Journal of Fisheries, 49, 45–50.Google Scholar
  70. Minnhagen, S., Kim, M., Salomon, P. S., Yih, W., Granéli, E., & Park, M. G. (2011). Active uptake of kleptoplastids by Dinophysis caudata from its ciliate prey Myrionecta rubra. Aquatic Microbial Ecology, 62, 99–108.CrossRefGoogle Scholar
  71. Mortensen, A. M. (1985). Massive fish mortalities in the Faroe Islands caused by a Gonyaulax excavata red tide. In D. M. Anderson, A. W. White, & D. G. Baden (Eds.), Toxic dinoflagellates (pp. 165–170). New York: Elsevier.Google Scholar
  72. Mouritsen, N. T., & Richardson, K. (2003). Vertical microscale patchiness in nano- and microplankton distributions in a stratified estuary. Journal of Plankton Research, 25, 783–797.CrossRefGoogle Scholar
  73. Naqvi, S. W. A., George, M. D., Narvekar, P. V., Jayakumar, D. A., Shailaja, M. S., Sardessai, S., et al. (1998). Severe fish mortality associated with 'red tide' observed in the sea off Cochin. Current Science, 75, 543–544.Google Scholar
  74. Nikolaidis, G., Koukaras, K., Aligizaki, K., Heracleous, A., Kalopesa, E., Moschandreou, K., Tsolaki, E., & Mantoudis, A. (2005). Harmful microalgal episodes in Greek coastal waters. Journal of Biological Research (Thessaloniki), 3, 77–85.Google Scholar
  75. Nikolaidis, G., Koukaras, K., Aligizaki, K., Kalopesa, E., Moschandreou, K., Tsolaki, E. (2006). Phytoplankton. In: Monitoring of Water Quality in the Coastal Area of Kalamitsi—Preveza (2nd phase), Final Report, Aristotle University of Thessaloniki (A.U.Th.): Thessaloniki, Greece, pp. 90–106.Google Scholar
  76. Nygaard, K., & Tobiesen, A. (1993). Bacterivory in algae: a survival strategy during nutrient limitation. Limnology and Oceanography, 38, 273–279.CrossRefGoogle Scholar
  77. Oshima, Y., Buckley, L. J., Alam, M., & Shimizu, Y. (1977). Heterogeneity of paralytic shellfish poisons. Three new toxins from cultured Gonyaulax tamarensis cells, Mya arenaria and Saxidomus giganteus. Comparative Biochemistry and Physiology, 57C, 31–34.Google Scholar
  78. Padmakumar, K. B., Menon, N. R., Sanjeevan, V. N. (2012). Is occurrence of harmful algal blooms in the Exclusive Economic zone of India on the Rise? doi: 10.1155/2012/263946.
  79. Park, M. G., Kim, M., Kim, S., & Yih, W. (2010). Does Dinophysis caudate (Dinophyceae) have permanent plastids? Journal of Phycology, 46, 236–242.CrossRefGoogle Scholar
  80. Parsons, T. R., Matia, Y., & Lalli, C. M. (1984). A manual of chemical and biological methods for sea water analysis (pp. 14–17). Maxwell, New York: Pergamon.CrossRefGoogle Scholar
  81. Paul, J. T., Ramaiah, N., & Sardesai, S. (2008). Nutrient regimes and their effect on distribution of phytoplankton in the Bay of Bengal. Marine Environmental Research, 66, 337–344.CrossRefGoogle Scholar
  82. Peperzak, L. (2003). Climate change and harmful algal blooms in the North Sea. Acta Ecologica, 24, S139–S144.CrossRefGoogle Scholar
  83. Pielou, P. P. (1966). The measurement of diversity in different types of biological collections. Journal of Theoretical Biology, 13, 131–144.CrossRefGoogle Scholar
  84. Pinto, J.S., Silva, E.S. (1956). The toxicity of Cardium edule L. and its possible relation to the dinoflagellate Prorocentrum micans Ehr. Notas e Estudos de Instituto Biologica Marinha, 12, 1–20.Google Scholar
  85. Rao, S. D. V. (1969). Asterionella japonica bloom and discolouration off Waltair, Bay of Bengal. Limnology and Oceanography, 14, 632–634.CrossRefGoogle Scholar
  86. Rensel, J. E., & Prentice, E. F. (1980). Factor controlling growth and survival of cultured spot prawn, Pandalus platyceros, in Puget Sound, Washington. Fisheries Bulletin, 78, 781–788.Google Scholar
  87. Resende, P., Azeiteiro, U. M., Gonçalves, F., & Pereira, M. J. (2007). Distribution and ecological preferences of diatoms and dinoflagellates in the west Iberian Coastal zone (North Portugal). Acta Oecologica, 32, 224–235.CrossRefGoogle Scholar
  88. Sanders, R. W., Porter, K. G., & Caron, D. A. (1990). Relationship between phototrophy and phagotrophy in the mixotrophic chrysophyte Poterioochromonas malhamensis. Microbial Ecology, 19, 97–109.CrossRefGoogle Scholar
  89. Satapathy, K.K. 1996. Studies on the chemical features of cooling water systems in the context of scaling, biofouling and corrosion control. PhD thesis, Madras University, Chennai, India.Google Scholar
  90. Satpathy, K. K., & Nair, K. V. K. (1990). Impact of power plant discharge on the physico-chemical characteristics of Kalpakkam coastal waters. Mahasagar, 23, 117–125.Google Scholar
  91. Satpathy, K. K., Mohanty, A. K., Sahu, G., Sarkar, S. K., Natesan, U., Venkatesan, R., et al. (2010). Variations of physicochemical properties in Kalpakkam coastal waters, east coast of India, during southwest to northeast monsoon transition period. Environmental Monitoring and Assessment, 171, 411–424.CrossRefGoogle Scholar
  92. Shannon, C. E., & Weaver, W. (1963). The mathematical theory of communication. Urbana, IL: University of Illinois Press.Google Scholar
  93. Shimizu, Y. (1983). Unexpected developments in red tide research. Maritimes, 4, 62–71.Google Scholar
  94. Shimizu, Y., Alam, M., Oshima, Y., & Fallon, W. E. (1975). Presence of four toxins in red tide infested clams and cultured Gonyaulax tamarensis cells. Biochemical and Biophysical Research Communications, 66, 731–737.CrossRefGoogle Scholar
  95. Shumway, S. (1990). A review of the effects of algal blooms on shellfish and aquaculture. Journal of World Aquaculture Society, 21, 65–104.CrossRefGoogle Scholar
  96. Smalley, G. W., & Coats, D. W. (2002). Ecology of the red-tide Dinoflagellate Ceratium furca: distribution, mixotrophy and grazing impact on ciliate populations of Chesapeake Bay. Journal of Eukaryotic Microbiology, 49, 63–73.CrossRefGoogle Scholar
  97. Smalley, G. W., Coats, D. W., & Adam, E. J. (1999). A new method for using fluorescent microspheres to determine grazing rates on ciliates by the mixotrophic dinoflagellate Ceratium furca. Aquatic Microbial Ecology, 17, 167–179.CrossRefGoogle Scholar
  98. Smalley, G. W., Coats, D. W., & Stoecker, D. K. (2003). Feeding in the mixotrophic dinoflagellate Ceratiumfurca is influenced by intracellular nutrient concentrations. Marine Ecology Progress Series, 262, 137–151.CrossRefGoogle Scholar
  99. Smayda, T. J. (1989). Primary production and the global epidemic of phytoplankton blooms in the sea: a linkage? In E. M. Cosper, V. M. Bricelj, & E. J. Carpenter (Eds.), Novel phytoplankton blooms. Coastal and Estuarine Studies, No. 35 (pp. 449–484). New York: Springer-Verlag.CrossRefGoogle Scholar
  100. Smayda, T. J. (1990). Novel and nuisance phytoplankton bloom in the sea: evidence for a global epidemic. In E. Grane´li, B. Sundstrom, L. Edler, & D. M. Anderson (Eds.), Toxic marine phytoplankton (pp. 29–40). New York: Elsevier.Google Scholar
  101. Smayda, T. J. (1997). Harmful algal blooms: their ecotoxicology and general relevance to phytoplankton blooms in the sea. Limnology and Oceanography, 42, 1137–1153.CrossRefGoogle Scholar
  102. Smayda, T. J. (2002). Adaptive ecology, growth strategies and global bloom expansion of dinoflagellates. Journal of Oceanography, 58, 281–294.CrossRefGoogle Scholar
  103. Smayda, T. J., & Reynolds, C. S. (2003). Strategies of marine dinoflagellate survival and some rules of assembly. Journal of Sea Research, 49, 95–106.CrossRefGoogle Scholar
  104. Smayda, T. J., & White, A. W. (1990). Has there been a global expansion of algal blooms? If so is there a connection with human activities? In E. Granelli (Ed.), Toxic marine phytoplankton (pp. 516–557). New York, USA: Elsevier.Google Scholar
  105. Spatharis, S., Dolapsakis, N. P., Economou-Amilli, A., Tsirtsis, G., & Danielidis, D. B. (2009). Dynamics of potentially harmful microalgae in a confined Mediterranean Gulf—Assessing the risk of bloom formation. Harmful Algae, 8, 736–743.CrossRefGoogle Scholar
  106. Strom, S. L. (1991). Growth and grazing rates of the herbivorous dinoflagellate Gymnodinium sp. from the open subarctic Pacific Ocean. Marine Ecology Progress Series, 78, 103–113.CrossRefGoogle Scholar
  107. Subramanyan, R. (1968). The Dinophyceae of the Indian Sea. Marine Biological Association of India, 3, 118–133.Google Scholar
  108. Taylor, F. J. R. (1973). General features of dinoflagellate material collected by the Anton Bruun during IIOE. In B. Zeitzschel (Ed.), The biology of the Indian Ocean: biological studies (pp. 155–169). Berlin: Springer Verlag.CrossRefGoogle Scholar
  109. Taylor, F. J. R., Fukuyo, Y., Larsen, J., & Hallegraeff, G. M. (2003). Taxonomy of harmful dinoflagellates. In G. M. Hallegraeff et al. (Eds.), Manual on harmful marine microalgae (pp. 389–432). Paris: UNESCO-IOC.Google Scholar
  110. Taylor, F. J. R., Fukuyo, Y., & Larsen, J. (1995). Taxonomy of harmful dinoflagellates. In G. M. Hallegraeff, D. M. Anderson, & A. D. Cembella (Eds.), Manual on Harmful Marine Microalgae. IOC Manuals and Guides No. 33 (pp. 283–317). France: UNESCO.Google Scholar
  111. Taylor, F. J. R., Fukuyo, Y., & Larsen, J. (2004). Taxonomy of harmful dinoflagellates. In G. M. Hallegraeff, D. M. Anderson, & A. D. Cembella (Eds.), Manual on Harmful Marine Microalgae, IOC Manuals and Guides No. 33 (Vol. 33, pp. 383–432). France: UNESCO.Google Scholar
  112. Taylor, F. J. R., Hoppernath, M., & Saldarriaga, J. F. (2008). Dinoflagellate diversity and distribution. Biodiversity and Conservation, 17, 407–418.CrossRefGoogle Scholar
  113. Tomas, C. R. (1997). Identifying marine phytoplankton (p. 858). New York: Academic Press.Google Scholar
  114. Toriumi, S. (1980). Prorocentrum species (Dinophyceae) causing red tide in Japanese coastal waters. Bulletin of the Plankton Society of Japan, 27, 105–112.Google Scholar
  115. Vargas-Montero, M., & Freer, E. (2004). Presence of the dinoflagellates Ceratium dens, C. fusus and C. furca (Gonyaulacales: Ceratiaceae) in Golfo de Nicoya, Costa Rica. Revista de Biologia Tropical, 52(suppl 1), 115–120.Google Scholar
  116. Weiler, C. S. (1980). Population structure and in situ division rates of Ceratium in oligotrophic water of the North Pacific central gyre. Limnology and Oceanography, 25, 610–619.CrossRefGoogle Scholar
  117. White, A. W. (1976). Growth inhibition caused by turbulence on the marine dinoflagellate Gonyaulax excavata. Journal of the Fisheries Research Board of Canada, 33, 2598–2602.CrossRefGoogle Scholar
  118. White, A. W. (1980). Recurrence of kills of Atlantic herring (Clupea harengus harengus) caused by dinoflagellate toxins transferred through herbivorous zooplankton. Canadian Journal of Fisheries and Aquatic Sciences, 37, 2262–2265. doi: 10.1139/f80-083.CrossRefGoogle Scholar
  119. Yasumoto, T. (1990). Marine microorganisms toxins - an overview. In E. Graneli, B. Sundstrom, L. Edler, & D. M. Anderson (Eds.), Toxic Marine Phytoplankton (pp. 3–8). New York: Elsevier.Google Scholar
  120. Yasumoto, T., Oshima, Y., Sugawara, W., Fukuyo, Y., Oguri, H., Igarashi, T., & Fujita, H. (1980). Identification of Dinophysis fortii as the causative organism of diarrhetic shellfish poisoning. Bulletin of the Japanese Society of Scientific Fisheries, 46, 1405–1411.CrossRefGoogle Scholar
  121. Yoo, K. I. (1991). Population dynamics of dinoflagellate community in Masan bay with a note on the impact of environmental parameters. Marine Pollution Bulletin, 23, 185–188.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Gouri Sahu
    • 1
  • A. K. Mohanty
    • 1
  • M. K. Samantara
    • 1
  • K. K. Satpathy
    • 1
  1. 1.Environmental Safety DivisionIndira Gandhi Center for Atomic ResearchKalpakkamIndia

Personalised recommendations