Abstract
During August and September 2007, the lower Chesapeake Bay and its tributaries experienced a massive bloom of Cochlodinium polykrikoides Margalef (>104 cells per milliliter) that persisted for over a month, was extremely patchy, and at times penetrated into the Atlantic Ocean. The onset of the bloom coincided with a period of intense rainfall and stormwater runoff after a protracted summer drought period. Genetic evidence showed this species to be distinct from many Asian strains but similar to other North American strains. Populations dominated by C. polykrikoides took up a variety of nitrogenous compounds to support their growth and were able to mobilize additional sources of organic nutrients through peptide hydrolysis. Bioassays determined that C. polykrikoides exerted a lethal affect on juvenile fish and shellfish, causing 100% mortality of juvenile fish (Cyprinodon variegates) in less than 24 h and 20% mortality in juvenile American oysters (~21 mm; Crassostrea virginica) within 72 h.
Similar content being viewed by others
References
Anderson, D.M., Y. Fukuyo, and K. Matsuoka. 2003. Cyst methodologies. In Manual on harmful marine microalgae, ed. G.M. Hallegraeff, D.M. Anderson, and A.D. Cembella, 165–189. France: UNESCO Publishing.
Azanza, R.V., L.T. David, R.T. Borja, I.U. Baula, and Y. Fukuyo. 2008. An extensive Cochlodinium bloom along the western coast of Palawan, Philippines. Harmful Algae 7: 324–330. doi:10.1016/j.hal.2007.12.011.
Coyne, K.J., D.A. Hutchins, C.E. Hare, and S.C. Cary. 2001. Assessing temporal and spatial variability in Pfiesteria piscicida distributions using molecular probing techniques. Aquatic Microbial Ecology 24: 275–285. doi:10.3354/ame024275.
Dempster, E.L., K.V. Pryor, D. Francis, J.E. Young, and H.J. Rogers. 1999. Rapid DNA extraction from ferns for PCR-based analyses. Biotechniques 27: 66–68.
Filippino, K.C., P.W. Bernhardt, and M.R. Mulholland. 2009. Nutrient dynamics and primary productivity in the Chesapeake Bay outflow plume during 2005 and 2006. Estuaries and Coasts 32: 410–424.
Gárrate-Lizárraga, I., D.J. Lopez-Cortes, J.J. Bustillis-Guzrnan, and R. Hernandez-Sandoval. 2004. Blooms of Cochlodinium polykrikoides (Gymnodiniaceae) in the Gulf of California, Mexico. Revista de Biología Tropical 52: 51–58.
Glibert, P.M., R. Magnien, M.W. Lomas, J. Alexander, C. Fan, E. Haramoto, M. Trice, and T.M. Kana. 2001. Harmful algal blooms in the Chesapeake and Coastal Bays of Maryland, USA: Comparison of 1997, 1998, and 1999 events. Estuaries 24: 875–883. doi:10.2307/1353178.
Gobler, C.J., M.J. Renaghan, and N.J. Buck. 2002. Impacts of nutrients and grazing mortality on the abundance of Aureococcus anophagefferens during a New York brown tide bloom. Limnology and Oceanography 47: 129–141.
Gobler, C.J., D.L. Berry, O.R. Anderson, A. Burson, F. Koch, B.S. Rodgers, L.K. Moore, J.A. Goleski, B. Allam, P. Bowser, Y. Tang, and R. Nuzzi. 2008. Characterization, dynamics, and ecological impacts of harmful Cochlodinium polykrikoides blooms on eastern Long Island, NY, USA. Harmful Algae 7: 293–307. doi:10.1016/j.hal.2007.12.006.
Guzmán, H.M., J. Cortes, P.W. Glynn, and R.H. Richmond. 1990. Coral mortality associated with dinoflagellate blooms in the eastern Pacific (Costa Rica and Panama). Marine Ecology Progress Series 60: 299–303. doi:10.3354/meps060299.
Ho, M.S., and P.L. Zubkoff. 1979. The effects of a Cochlodinium heterolobatum bloom on the survival and calcium uptake by larvae of the American oyster, Crassostrea virginica. In Toxic dinoflagellate blooms, ed. D.L. Taylor, and H.H. Seliger, 409–412. New York: Elsevier.
Iwataki, M., H. Kawami, and K. Matsuoka. 2007. Cochlodinium fulvescens sp. nov. (Gymnodiniales, Dinophyceae), a new chain-forming unarmored dinoflagellate from Asian coasts. Phycological Research 55: 231–239. doi:10.1111/j.1440-1835.2007.00466.x.
Iwataki, M., H. Kawami, K. Mizushima, C.M. Mikulski, G.J. Doucette, J.R. Relox Jr., A. Antone, Y. Fukuyo, and K. Matsuoka. 2008. Phylogenetic relationships in the harmful dinoflagellate Cochlodinium polykrikoides (Gymnodiniales, Dinophyceae) inferred from LSU rDNA sequences. Harmful Algae 73: 271–277. doi:10.1016/j.hal.2007.12.003.
Jeong, H.J., Y.D. Yoo, J.S. Kim, T.H. Kim, J.H. Kim, N.S. Kang, and W. Yih. 2004. Mixotrophy in the phototrophic harmful alga Cochlodinium polykrikoides (Dinophycean): Prey species, the effects of prey concentration, and grazing impact. Journal of Eukaryotic Microbiology 51: 563–569. doi:10.1111/j.1550-7408.2004.tb00292.x.
Jeong, H.J., J.Y. Park, J.H. Nho, M.O. Park, J.H. Ha, K.A. Seong, C. Jeng, C.N. Seong, K.Y. Lee, and W.H. Yih. 2005. Feeding by red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquatic Microbial Ecology 41: 131–143. doi:10.3354/ame041131.
Kim, H.G. 1998. Cochlodinium polykrikoides blooms in Korean coastal waters and their mitigation. In Harmful algae, ed. B. Reguera, J. Blanco, M.L. Fernandez, and T. Wyatt, 227–228. Galicia: Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO.
Kim, C.S., S.G. Lee, H.G. Kim, and J. Jung. 1999. Reactive oxygen species as causative agents in the ichthyotoxicity of the red tide dinoflagellate Cochlodinium polykrikoides. Journal of Plankton Research 21: 2105–2115. doi:10.1093/plankt/21.11.2105.
Kim, C.H., H.J. Cho, J.B. Shin, C.H. Moon, and K. Matsuo. 2002. Regeneration from hyaline cysts of Cochlodinium polykrikoides (Gymnodiniales, Dinophyceae), a red tide organism along the Korean coast. Phycologia 41: 667–669.
Kim, C.J., H.G. Kim, C.H. Kim, and H.M. Oh. 2007. Life cycle of the ichthyotoxic dinoflagellate Cochlodinium polykrikoides in Korean coastal waters. Harmful Algae 6: 104–111. doi:10.1016/j.hal.2006.07.004.
Kudela, R.M., J.P. Ryan, M.D. Blakely, J.Q. Lane, and T.D. Peterson. 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.
Larsen, J., and A. Sournia. 1991. Diversity of heterotrophic dinoflagellates. In The biology of free-living heterotrophic dinoflagellates, ed. D.J. Patterson, and J. Larsen, 313–332. Oxford: Clarendon.
Mackiernan, G. B. 1968. Seasonal distribution of dinoflagellates in the lower York River, Virginia. M.A. Thesis. College of William and Mary, Williamsburg, VA, 104 pp.
Malone, T.C., D.J. Conley, T.R. Fisher, P.M. Glibert, L.W. Harding, and K.G. Sellner. 1996. Scales of nutrient-limited phytoplankton productivity in Chesapeake Bay. Estuaries 19(2B): 371–385. doi:10.2307/1352457.
Marshall, H.G. 1995a. Autotrophic picoplankton distribution and abundance in the Chesapeake Bay, U.S.A. Maine Nature 4: 33–42.
Marshall, H.G. 1995b. Succession of dinoflagellate blooms in the Chesapeake Bay, U. S. A. In Harmful marine algal blooms, ed. P.G. Lassus, E. Arzul, E. Erard, P. Gentien, and C. Marcaillou, 615–620. Paris: Lavoisier, Intercept. Technique et Documentation.
Marshall, H.G., and K.K. Nesius. 1996. Phytoplankton composition in relation to primary production in Chesapeake Bay. Marine Biology 125: 611–617.
Marshall, H.G., T.A. Egerton, L. Burchardt, S. Cerbin, and M. Kokocinski. 2005. Long term monitoring results of harmful algal populations in Chesapeake Bay and its major tributaries in Virginia, U.S.A. Oceanological and hydrobiological studies 34(Suppl. 3): 35–41.
Marshall, H.G., R. Lacouture, C. Buchanan, and J. Johnson. 2006. Phytoplankton assemblages associated with water quality and salinity regions in Chesapeake Bay, USA. Estuarine, Coastal and Shelf Science 69: 10–18. doi:10.1016/j.ecss.2006.03.019.
Matsuoka, K., and Y. Fukuyo. 2000. Technical guide for modern dinoflagellate cyst study. Tokyo: WESTPAC-HAB/WESTPAC/IOC.
Matsuyama, Y., H. Usuki, T. Uchida, and Y. Kotani. 2001. Effects of harmful algae on the early planktonic larvae of the oyster Crassostrea gigas. In Proceedings of the Ninth International Conference on Harmful Algal Blooms, ed. G.M. Hallegraeff, S.I. Blackburn, C.J. Bolch, and R.J. Lewis, 411–414. Paris: IOC of UNESCO.
Mikulski, C.M., S.L. Morton, and G.J. Doucette. 2005. Development and application of LSU rRNA probes for Karenia brevis in the Gulf of Mexico, USA. Harmful Algae 4: 49–60. doi:10.1016/j.hal.2003.11.001.
Mulholland, M.R., C.J. Gobler, and C. Lee. 2002. Peptide hydrolysis, amino acid oxidation and N uptake in communities seasonally dominated by Aureococcus anophagefferens. Limnology and Oceanography 47: 1094–1108.
Mulholland, M.R., P.M. Glibert, and C. Lee. 2003. Peptide hydrolysis, amino acid oxidation and N uptake along a nutrient and salinity gradient in the Pocomoke River, Maryland. Marine Ecology Progress Series 258: 3–17. doi:10.3354/meps258003.
Mulholland, M.R., C.A. Heil, D.A. Bronk, J.M. O’Neil, and P.W. Bernhardt. 2006. Nitrogen fixation and regeneration in the Gulf of Mexico. Limnology and Oceanography 51: 1762–1776.
Mulholland, M.R., G.E. Boneillo, P.W. Bernhardt, and E.C. Minor. 2009. Comparison of nutrient and microbial dynamics over a seasonal cycle in a mid-Atlantic coastal lagoon prone to Aureococcus anophagefferens (brown tide) blooms. Estuaries and Coasts (submitted).
Onoue, Y., K. Nozawa, K. Kumanda, K. Takeda, and T. Aramaki. 1985. Toxicity of Cochlodinium ’78 Yatsushiro occurring in Yatsushiro Sea. Nippon Suisan Gakkaishi 51: 147–151.
Parsons, T.R., Y. Maita, and C.M. Lalli. 1984. A manual of chemical and biological methods for seawater analysis. Oxford: Pergamon.
Pyke, C.R., R. Najjar, M.B. Adams, D. Breitburg, C. Hershner, M.W. Kemp, R. Howarth, M.R. Mulholland, M. Paolisso, D. Secor, K. Sellner, D. Wardrop, and R. Wood. 2008. Climate change and the Chesapeake Bay: State-of-the-science review and recommendations. Edgewater: STAC. STAC Publication 08-001.
Qi, D., Y. Huang, and X. Wang. 1993. Toxic dinoflagellate red tide by a Cochlodinium sp. along the coast of Fujian, China. In Toxic phytoplankton blooms in the sea, ed. T.J. Smayda, and Y. Shimizu, 235–238. Amsterdam: Elsevier.
Rosales-Loessener, F., K. Matsuoka, Y. Fukuyo, and E.H. Sanchez. 1996. Cysts of harmful dinoflagellates found from Pacific coastal waters of Guatemala. In Harmful and toxic algal blooms, ed. T. Yasumoto, Y. Oshima, and Y. Fukuyo, 193–195. Paris: Intergovernmental Oceanographic Commission of UNESCO of 1996.
Seaborn, D.W., and H.G. Marshall. 2008. Dinoflagellate cysts within sediment collections from the southern Chesapeake Bay and tidal regions of the James, York, and Rappahannock rivers. Virginia Journal of Science 59: 135–141.
Seong, K.A., H.J. Jeong, S. Kim, G.H. Kim, and J.H. Kang. 2006. Bactivory by co-occurring red-tide algae, heterotrophic nanoflagellates, and ciliates on marine bacteria in the Korean waters. Marine Ecology Progress Series 322: 85–97. doi:10.3354/meps322085.
Shin, K., M.C. Jang, P.K. Jang, S.J. Ju, T.K. Lee, and M. Chang. 2003. Influence of food quality on egg production and viability of the marine planktonic copepod Acartia omorii. Progress in Oceanography 57: 265–277. doi:10.1016/S0079-6611(03)00101-0.
Solarzano, L. 1969. Determination of ammonia in natural waters by the phenol hypochlorite method. Limnology and Oceanography 14: 16–23.
Stoecker, D.K. 1999. Mixotrophy among dinoflagellates. Journal of Eukaryotic Microbiology 46: 397–401. doi:10.1111/j.1550-7408.1999.tb04619.x.
Tyler, M.A., D.W. Coats, and S.M. Anderson. 1982. Encystment in a dynamic environment: Deposition of dinoflagellate cysts by a frontal convergence. Marine Ecology Progress Series 7: 163–178. doi:10.3354/meps007163.
Valderrama, J. 1981. The simultaneous analysis of total nitrogen and total phosphorous in natural waters. Marine Chemistry 10: 109–122. doi:10.1016/0304-4203(81)90027-X.
Welschmeyer, N.A. 1994. Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnology and Oceanography 39: 1985–1992.
Whyte, J.N.C.I., N. Haigh, N.G. Ginther, and L.J. Keddy. 2001. First record of blooms of Cochlodinium sp (Gymnodiniales, Dinophyceae) causing mortality to aquacultured salmon on the west coast of Canada. Phycologia 40: 298–304.
Yuki, K., and S. Yoshimatsu. 1989. Two fish-killing species of Cochlodinium from Harima-Nada, Seto Inland Sea, Japan. In Red tides: Biology, environmental science, and toxicology, ed. T. Okaichi, D.M. Anderson, and T. Nemoto, 451–454. New York: Elsevier.
Acknowledgements
Funding was provided by the National Oceanic and Atmospheric Administration, Center for Sponsored Coastal Ocean Research Event Response Program. We thank the Hampton Roads Sanitation District and Virginia Department of Environmental Quality for supporting DATAFLOW mapping and shallow-water continuous monitoring efforts. This work was also funded through grants from the Virginia Environmental Endowment to MRM.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mulholland, M.R., Morse, R.E., Boneillo, G.E. et al. Understanding Causes and Impacts of the Dinoflagellate, Cochlodinium polykrikoides, Blooms in the Chesapeake Bay. Estuaries and Coasts 32, 734–747 (2009). https://doi.org/10.1007/s12237-009-9169-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12237-009-9169-5