Harmful dinoflagellate blooms caused by Cochlodinium sp.: Global expansion and ecological strategies facilitating bloom formation

Harmful Algae

Volumn 14, Issue , 2012, Pages 71-86

  Kudela, Raphael M ^a   Gobler, Christopher J ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

Cochlodinium fulvescens; Cochlodinium polykrikoides; Ecophysiology; Food web interactions; Harmful algal bloom; Mitigation

Indexed keywords

ALGAE; COCHLODINIUM; COCHLODINIUM POLYKRIKOIDES; DINOPHYCEAE;

EID: 84856083100     PISSN: 15689883     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.hal.2011.10.015     Document Type: Article

References (196)

1. Abreu M.H., Varela D.A., Henríquez L., Villarroel A., Yarish C., Sousa-Pinto I., Buschmann A.H. Traditional vs. integrated multi-trophic aquaculture of Gracilaria chilensis C. J. Bird, J. McLachlan & E. C. Oliveira: productivity and physiological performance. Aquaculture 2009, 293:211-220.
2. Adam A., Mohammad-Noor N., Anton A., Saleh E., Saad S., Raehanah S., Shaleh M. Temporal and spatial distribution of harmful algal bloom (HAB) species in coastal waters of Kota Kinabalu, Sabah, Malaysia. Harmful Algae 2011, 10:495-502.
3. Ahn Y.-H., Shanmugam P., Chang K.-I., Moon J.-E., Ryu J.-H. Spatial and temporal aspects of phytoplankton blooms in complex ecosystems off the Korean coast from satellite ocean color observations. Ocean Sci. J. 2005, 40:67-78.
4. Ahn Y.-H., Shanmugam P., Ryu J.-H., Jeong J.-C. Satellite detection of harmful algal bloom occurrences in Korean waters. Harmful Algae 2006, 5:213-231.
5. Alamsjah M., Hirao S., Ishibashi F., Oda T., Fujita Y. Algicidal activity of polyunsaturated fatty acids derived from Ulva fasciata and U. pertusa (Ulvaceae, Chlorophyta) on phytoplankton. J. Appl. Phycol. 2008, 20:713-720.
6. Anderson D.M. Toxic algal blooms and red tides: a global perspective. Red Tides: Biology, Environmental Science, and Toxicology 1989, 11-16. Elsevier Science, New York. T. Okaichi, D.M. Anderson, T. Nemoto (Eds.).
7. Anderson D.M., Glibert P.M., Burkholder J.M. Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 2002, 25:704-726.
8. Anderson D.M., Pitcher G.C., Estrada M. The comparative systems approach to HAB research. Oceanography 2005, 18:148-157.
9. Anton A., Teoh P.L., Mohd-Shaleh S.R., Mohammad-Noor N. First occurrence of Cochlodinium blooms in Sabah, Malaysia. Harmful Algae 2008, 7:331-336.
10. Azanza R.V., David L.T., Borja R.T., Baula I.U., Fukuyo Y. An extensive Cochlodinium bloom along the western coast of Palawan, Philippines. Harmful Algae 2008, 7:324-330.
11. Babin M., Cullen J., Roesler C., Donaghay P., Doucette G., Kahru M., Mr L., Scholin C., Sieracki M., Sosik H. New approaches and technologies for observing harmful algal blooms. Oceanography 2005, 18:210-227.
12. Bauman A.G., Burt J.A., Feary D.A., Marquis E., Usseglio P. Tropical harmful algal blooms: an emerging threat to coral reef communities?. Mar. Pollut. Bull. 2010, 60:2117-2122.
13. Bhat S.R., Matondkar S.B.P. Algal blooms in the seas around India - networking for research and outreach. Curr. Sci. 2004, 87:1079-1083.
14. Bok T.-H., Paeng D.-G., Kim E., Na J., Kang D. Ultrasound backscattered power from Cochlodinium polykrikoides, the main red tide species in the Southern Sea of Korea. J. Plankton Res. 2010, 32:503-514.
15. Bolton J., Robertson-Andersson D., Shuuluka D., Kandjengo L. Growing Ulva (Chlorophyta) in integrated systems as a commercial crop for abalone feed in South Africa: a SWOT analysis. J. Appl. Phycol. 2009, 21:575-583.
16. Burkholder J.A.M., Glibert P.M., Skelton H.M. Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 2008, 8:77-93.
17. Burkholder J.M., Glibert P.M. The importance of intraspecific variability in harmful algae - preface to a collection of topical papers. Harmful Algae 2009, 8:744-745.
18. Carriker M.R., John N.K., Michael C. Functional morphology and behavior of shelled veligers and early juveniles. Developments in Aquaculture and Fisheries Science 2001, vol. 31. Elsevier, pp. 283-303 (Chapter 7).
19. Cho E., Costas E. Rapid monitoring for the potentially ichthyotoxic dinoflagellate Cochlodinium polykrikoides in Korean coastal waters using fluorescent probe tools. J. Plankton Res. 2004, 26:175-180.
20. Cho E.S. Cluster analysis on the lectin binding patterns of marine microalgae. J. Plankton Res. 2002, 25:309-315.
21. Cho E.S., Seo G.M., Lee S.G., Kim H.G., Lee S.J., Rhodes L.L., Hong Y.K. Application of FITC-conjugated lectin probes for the recognition and differentiation of some Korean coastal red tide microalgae. J. Fish. Sci. Technol. 1998, 1:250-254.
22. Costas E., Rodas V.L. Identification of marine dinoflagellates using fluorescent lectins. J. Phycol. 1994, 30:987-990.
23. Cullen J.J., Horrigan S.G. Effects of nitrate on the diurnal vertical migration, carbon to nitrogen ratio, and the photosynthetic capacity of the dinoflagellate Gymnodinium splendens. Mar. Biol. 1981, 62:81-89.
24. Curtiss C.C., Langlois G.W., Busse L.B., Mazzillo F., Silver M.W. The emergence of Cochlodinium along the California Coast (USA). Harmful Algae 2008, 7:337-346.
25. Del Carmen Cortes Lara M., Altamarino R.C., Sierra-Beltran A.P. Presence of Cochlodinium catenatum (Gymnodiniales: Gymnodiniaceae) in red tides of Bahia de Banderas, Mexican Pacific. Rev. Biol. Trop. 2004, 52(Suppl. 1):35-50.
26. Dierssen H., Kudela R., Ryan J., Zimmerman R. Red and black tides: quantitative analysis of water-leaving radiance and perceived color for phytoplankton, colored dissolved organic matter, and suspended sediments. Limnol. Oceanogr. 2006, 51:2646-2659.
27. Dorantes-Aranda J.J., Garcia-De La Parra L.M., Alonso-Rodriguez R., Morquecho L. Hemolytic activity and fatty acids composition in the ichthyotoxic dinoflagellate Cochlodinium polykrikoides isolated from Bahia de La Paz, Gulf of California. Mar. Pollut. Bull. 2009, 58:1401-1405.
28. Du Q., Huang Y., Wang X. Toxic dinoflagellate red tide by a Cochlodinium sp. along the coast of Fujian, China. Toxic Phytoplankton Blooms in the Sea 1993, 235-238. Elsevier, New York. T.J. Smayda, Y. Shimizu (Eds.).
29. Eppley R.W., Holm-Hansen O. Some observations on the vertical migration of dinoflagellates. J. Phycol. 1968, 4:333-340.
30. Fraga S., Gallager S.M., Anderson D.M. Chain-forming dinoflagellates: an adaptation to red tides. Red Tides: Biology, Environmental Science and Toxicology 1989, 281-284. Elsevier, New York. T. Okaichi, D. Anderson, T. Nemoto (Eds.).
31. Gárate-Lizárraga I., Bustillos-Guzmaón J., Morquecho J., Lechuga-Déveze C. First outbreak of Cochlodinium polykrikoides in the Gulf of California 2000, Harmful Algae News, Intergovernmental Oceanographic Commission of UNESCO, 21, 7 pp.
32. Gárate-Lizárraga I., López-Corets J.J., Bustillos-Guzmán J.J., Hernández-Sandoval F. Blooms of Cochlodinium polykrikoides (Gymnodiniaceae) in the Gulf of California, Mexico. Rev. Biol. Trop. 2004, 52.
33. Glibert P., Anderson D., Gentien P., Granéli E., Sellner K. The global, complex phenomena of harmful algal blooms. Oceanography 2005, 18:136-147.
34. Gobler C.J., Berry D.L., Anderson O.R., Burson A., Koch F., Rodgers B.S., Moore L.K., Goleski J.A., Allam B., Bowser P., Tang Y.Z., Nuzzi R. Characterization, dynamics, and ecological impacts of harmful Cochlodinium polykrikoides blooms on eastern Long Island, NY, USA. Harmful Algae 2008, 7:293-307.
35. Gobler, C.J., Burson, A.M., Tang, Y.Z., Mulholland, M.R. The role of nitrogenous nutrients in the occurrence of the harmful dinoflagellate blooms caused by Cochlodinium polykrikoides in New York estuaries. Harmful Algae, submitted for publication.
36. Gobler C.J., Renaghan M.J., Buck N.J. Impacts of nutrients and grazing mortality on the abundance of Aureococcus anophagefferens during a New York brown tide bloom. Limnol. Oceanogr. 2002, 47:129-141.
37. Gomez-Villarreal M.C., Martinez-Gaxiola M.D., Peña-Manjarrez J.L. Algal blooms at Banderas, Bay, Mexico (2000-2001), from SeaWiFS-sensor-data. Rev. Biol. Trop. 2008, 56:1653-1664.
38. Gower J., King S. An Antarctic ice-related " superbloom" observed with the MERIS satellite imager. Geophys. Res. Lett. 2007, 34:L15501. doi:15510.11029/12007GL029638.
39. Gower J., King S., Borstad G., Brown L. Detection of intense plankton blooms using the 709nm band of the MERIS imaging spectrometer. Int. J. Remote Sens. 2005, 26:2005-2012.
40. Guiry M.D., Guiry G.M. AlgaeBase. World-wide Electronic Publication 2011, National University of Ireland, Galway. http://www.algaebase.org/.
41. Guzmán H.M., Cortes J., Glynn P.W., Richmond R.H. Coral mortality associated with dinoflagellate blooms in the eastern Pacific (Costa Rica and Panama). Mar. Ecol. Prog. Ser. 1990, 60:299-303.
42. Hallegraef G.M. A review of harmful algal blooms and their apparent global increase. Phycologia 1993, 32:79-99.
43. Hallegraeff G.M. Harmful algal blooms in the Australian region. Mar. Pollut. Bull. 1992, 25:186-190.
44. Hallegraeff G.M. Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge. J. Phycol. 2010, 46:220-235.
45. Han H.-K., Kim Y.-M., Lim S.-J., Hong S.-S., Jung S.-G., Cho H., Lee W., Jin E. Enhanced efficacy of TD53, a novel algicidal agent, against the harmful algae via the liposomal delivery system. Int. J. Pharm. 2010, 405:137-141.
46. Hansen P.J. The role of photosynthesis and food uptake for the growth of marine mixotrophic dinoflagellates. J. Eukaryot. Microbiol. 2011, 58(3):203-214.
47. Hargraves P.E., Maranda L. Potentially toxic or harmful microalgae from the northeast coast. Northeastern Nat. 2002, 9:81-120.
48. Heisler J., Glibert P., Burkholder J., Anderson D., Cochlan W., Dennison W., Dortch Q., Gobler C., Heil C., Humphries E., Lewitus A., Magnien R., Marshall H., Sellner K., Stockwell D., Stoecker D., Suddleson M. Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae 2008, 8:3-13.
49. Ho M.S., Zubkoff P.L. The effects of a Cochlodinium heterolobactum bloom on the survival and calcium uptake by larvae of the American oyster Crassostrea virginica. Toxic Dinoflagellate Blooms 1979, Elsevier, North Holland, New York. F. Taylor, H. Seliger (Eds.).
50. Holliday D.V., Pieper R.E., Kleppel G.S. Determination of zooplankton size and distribution with multifrequency acoustic technology. J. Cons. Int. Explor. Mer. 1989, 46:52-61.
51. Holmes R., William P., Eppley R. Red water in La Jolla Bay, 1964-1966. Limnol. Oceanogr. 1967, 12:503-512.
52. Honda A., Ishida K., Miyamura S. III. Yatsushiro Kaiiki, Yatsushiro Kai-1. Fisheries Agency, Suisan Shikenjhou 1980, 108-123. Kyushu Seiganiki Akashiwo Yosatsu Chosa Houkokusho, (in Japanese). S.S. Fukuokaken, S.S. Sagaken, S.S. Nakgasaki, S.S. Kumamoto, S.S. Kagoshima (Eds.).
53. Howard, M.D.A., Jones, A.C., Schnetzer, A., Countway, P.D., Tomas, C.R., Kudela, R.M., Hayashi, K., Chia, P., Caron, D.A. Quantitative real-time PCR for Cochlodinium fulvescens (Dinophyceae), a potentially harmful dinoflagellate from California coastal waters. J. Phycol., in press.
54. Huang C., Dong Q. Taxonomic and biological studies on causative organisms from a large-scale red tide occurring in Pearl River Estuary in the spring, 1998. Oceanol. Limnol. Sin./Haiyang Yu Huzhao 2000, 31:233-238.
55. Humbert J.F., Quiblier C., Gugger M. Molecular approaches for monitoring potentially toxic marine and freshwater phytoplankton species. Anal. Bioanal. Chem. 2010, 397:1723-1732.
56. Imai I., Kimura S. Resistance of the fish-killing dinoflagellate Cochlodinium polykrikoides against algicidal bacteria isolated from the coastal sea of Japan. Harmful Algae 2008, 7:360-367.
57. Imai I., Yamaguchi M., Hori Y. Eutrophication and occurrences of harmful algal blooms in the Seto Inland Sea, Japan. Plankton Benthos Res. 2006, 1:71-84.
58. Iwataki M., Hansen G., Moestrup O., Matsuoka K. Ultrastructure of the harmful unarmored dinoflagellate Cochlodinium polykrikoides (Dinophyceae) with reference to the apical groove and flagellar apparatus. J. Eukaryot. Microbiol. 2010, 57:308-321.
59. Iwataki M., Kawami H., Matsuoka K. Cochlodinium fulvescens sp. nov. (Gymnodiniales, Dinophyceae), a new chain-forming unarmored dinoflagellate from Asian coasts. Phycol. Res. 2007, 55:231-239.
60. Iwataki M., Kawami H., Mizushima K., Mikulski C.M., Doucette G.J., Relox J.R., Anton A., Fukuyo Y., Matsuoka K. Phylogenetic relationships in the harmful dinoflagellate Cochlodinium polykrikoides (Gymnodiniales, Dinophyceae) inferred from LSU rDNA sequences. Harmful Algae 2008, 7:271-277.
61. Jeong H.J., Kim H.R., Kim K.I., Kim K.Y., Park K.H., Kim S.T., Yoo Y.D., Song J.Y., Kim J.S., Seong K.A., Yih W.H., Pae S.J., Lee C.H., Huh M.D., Lee S.H. NaOCl produced by electrolysis of natural seawater as a potential method to control marine red-tide dinoflagellates. Phycologia 2002, 41:643-656.
62. Jeong H.J., Kim J.S., Yoo Y.D., Kim S.T., Song J.Y., Kim T.H., Seong K.A., Kang N.S., Kim M.S., Kim J.H., Kim S., Ryu J., Lee H.M., Yih W.H. Control of the harmful alga Cochlodinium polykrikoides by the naked ciliate Strombidinopsis jeokjo in mesocosm enclosures. Harmful Algae 2008, 7:368-377.
63. Jeong H.J., Shim J.H., Kim J.S., Lee Y.P.J., Lee Y.C.W. Feeding by the mixotrophic thecate dinoflagellate Fragilidium cf. mexicanum on red-tide and toxic dinoflagellates. Mar. Ecol. Prog. Ser. 1999, 176:263-277.
64. Jeong H.J., Yoo Y.D., Kim J.S., Kim T.H., Kim J.H., Kang N.S., Yih W. Mixotrophy in the phototrophic harmful alga Cochlodinium polykrikoides (Dinophyceae): prey species, the effects of prey concentration, and grazing impact. J. Eukaryot. Microbiol. 2004, 51:563-569.
65. Jeong H.J., Yoo Y.D., Park J.Y., Song J.Y., Kim S.T., Lee S.H., Kim K.Y., Yih W.H. Feeding by phototrophic red-tide dinoflagellates: five species newly revealed and six species previously known to be mixotrophic. Aquat. Microb. Ecol. 2005, 40:133-150.
66. Jeong J.-H., Jin H.-J., Sohn C., Suh K.-H., Hong Y.-K. Algicidal activity of the seaweed Corallina pilulifera against red tide microalgae. J. Appl. Phycol. 2000, 12:37-43.
67. Jeong S.-Y., Ishida K., Ito Y., Okada S., Murakami M. Bacillamide, a novel algicide from the marine bacterium, Bacillus sp. SY-1, against the harmful dinoflagellate, Cochlodinium polykrikoides. Tetrahedron Lett. 2003, 44:8005-8007.
68. Jiang X., Tang Y., Lonsdale D.J., Gobler C.J. Deleterious consequences of a red tide dinoflagellate Cochlodinium polykrikoides for the calanoid copepod Acartia tonsa. Mar. Ecol. Prog. Ser. 2009, 390:105-116.
69. Jiang X.D., Lonsdale D.J., Gobler C.J. Density-dependent nutritional value of the dinoflagellate Cochlodinium polykrikoides to the copepod Acartia tonsa. Limnol. Oceanogr. 2010, 55:1643-1652.
70. Jiang X.D., Lonsdale D.J., Gobler C.J. Grazers and vitamins shape chain formation in a bloom-forming dinoflagellate, Cochlodinium polykrikoides. Oecologia 2010, 164:455-464.
71. Jochens A.E., Malone T.C., Stumpf R.P., Hickey B.M., Carter M., Morrison R., Dyble J., Jones B., Trainer V.L. Integrated ocean observing system in support of forecasting harmful algal blooms. Mar. Technol. Soc. J. 2010, 44:99-121.
72. Ki J.S., Han M.S. Implications of complete nuclear large subunit ribosomal RNA molecules from the harmful unarmored dinoflagellate Cochlodinium polykrikoides (Dinophyceae) and relatives. Biochem. Syst. Ecol. 2008, 36:573-583.
73. Kim C.-H., Cho H.-J., Shin J.-B., Moon C.-H., Matsuoka K. Regeneration from hyaline cysts of Cochlodinium polykrikoides (Gymnodiniales, Dinophyceae), a red tide organism along the Korean coast. Phycologia 2002, 41:667-669.
74. Kim C.-J., Kim H.-G., Kim C.-H., Oh H.-M. Life cycle of the ichthyotoxic dinoflagellate Cochlodinium polykrikoides in Korean coastal waters. Harmful Algae 2007, 6:104-111.
75. Kim C.S., Lee S.G., Lee C.K., Kim H.G., Jung J. Reactive oxygen species as causative agents in the ichthyotoxicity of the red tide dinoflagellate Cochlodinium polykrikoides. J. Plankton Res. 1999, 21:2105-2115.
76. Kim D., Kim J.F., Yim J.H., Kwon S.K., Lee C.H., Lee C.K. Red to red - the marine bacterium Hahella chejuensis and its product prodigiosin for mitigation of harmful algal blooms. J. Microbiol. Biotechnol. 2008, 18:1621-1629.
77. Kim D., Oda T., Muramatsu T., Kim D., Matsuyama Y., Honjo T. Possible factors responsible for the toxicity of Cochlodinium polykrikoides, a red tide phytoplankton. Comp. Biochem. Physiol. C 2002, 132:415-423.
78. Kim D.-I., Matsuyama Y., Nagasoe S., Yamaguchi M., Yoon Y.-H., Oshima Y., Imada N., Honjo T. Effects of temperature, salinity, and irradiance on the growth of the harmful red tide dinoflagellate Cochlodinium polykrikoides Margalef (Dinophyceae). J. Plankton Res. 2004, 26:61-66.
79. Kim E., Lee H., Na J.W.C., Kang D. 5-MHz acoustic-backscatter measurements of Cochlodinium polykrikoides blooms in Korean coastal waters. ICES J. Mar. Sci. 2010, 67:1759-1765.
80. Kim H., Kim D., Lee D., Park C., Kim H. Limiting nutrients of Cochlodinium polykrikoides red tide in Saryang Island coast by algal growth potential (AGP) assay. J. Korean Fish. Soc. 2001, 34:457-464.
81. Kim H., Lee C., Lee S., Kim H., Park C. Physico-chemical factors on the growth of Cochlodinium polykrikoides and nutrient utilization. J. Korean Fish. Soc. 2001, 34:445-456.
82. Kim H.G. Harmful algal blooms in Korean coastal waters focused on three fish killing dinoflagellates. Harmful Algal Blooms in Korea and China 1998, NFRDI, Pusan, Korea. H. Lee, S. Lee, C. Lee (Eds.).
83. Kim H.G. Recent harmful algal blooms and mitigation strategies in Korea. Ocean Res. (Seoul) 1997, 19:185-192.
84. Kim J.-S., Kim J.-C., Lee S., Lee B.-H., Cho K.Y. Biological activity of l-2-azetidinecarboxylic acid, isolated from Polygonatum odoratum var. pluriflorum, against several algae. Aquat. Bot. 2006, 85:1-6.
85. Kim M.J., Jeong S.Y., Lee S.J. Isolation, identification, and algicidal activity of marine bacteria against Cochlodinium polykrikoides. J. Appl. Phycol. 2008, 20:1069-1078.
86. Kim S., Lee H., Lee Y., Yim J. Mutant selection of Hahella chejuensis KCTC 2396 and statistical optimization of medium components for prodigiosin yield-up. J. Microbiol. 2008, 46:183-188.
87. Kim Y., Byun Y., Kim Y., Eo Y. Detection of Cochlodinium polykrikoides red tide based on two-stage filtering using MODIS data. Desalination 2009, 249:1171-1179.
88. Kim Y.S., Jeong C.S., Seong G.T., Han I.S., Lee Y.S. Diurnal vertical migration Cochlodinium polykrikoides during the red tide in Korean coastal sea waters. J. Environ. Biol. 2010, 31:687-693.
89. Kofoid C.A., Swezy O. The Free Living Unarmoured Dinoflagellata 1921, Memoirs of the Univeristy of California, Berkeley.
90. Kraemer G.P., Carmona R., Chopin T., Neefus C., Tang X., Yarish C. Evaluation of the bioremediatory potential of several species of the red alga Porphyra using short-term measurements of nitrogen uptake as a rapid bioassay. J. Appl. Phycol. 2004, 16:489-497.
91. Kudela R., Ryan J., Blakely M., Lane J., Peterson T. Linking the physiology and ecology of Cochlodinium to better understand harmful algal bloom events: a comparative approach. Harmful Algae 2008, 7:278-292.
92. Kudela R.M., Seeyave S., Cochlan W.P. The role of nutrients in regulation and promotion of harmful algal blooms in upwelling systems. Prog. Oceanogr. 2010, 85:122-135.
93. Landsberg J.H. The effects of harmful algal blooms on aquatic organisms. Rev. Fish. Sci. 2002, 10:113-390.
94. Larsen J., Sournia A. Diversity of heterotrophic dinoflagellates. The Biology of Free-living Heterotrophic Dinoflagellates 1991, 313-332. Clarendon Press, Oxford. D.J. Patterson, J. Larsen (Eds.).
95. Lee B.-K., Katano T., Kitamura S.-I., Oh M.-J., Han M.-S. Monitoring of algicidal bacterium, Alteromonas sp. Strain A14 in its application to natural Cochlodinium polykrikoides blooming seawater using fluorescence in situ hybridization. J. Microbiol. 2008, 46:274-282.
96. Lee C.K., Kim H.C., Lee S.-G., Jung C.S., Kim H.G., Lim W.A. Abundance of harmful algae, Cochlodinium polykrikoides, Gyrodinium impudicum and Gymnodinium catenatum in the coastal area of South Sea of Korea and their effects of temperature, salinity, irradiance and nutrient on the growth in culture. J. Korean Fish. Soc. 2001, 34:536-544.
97. Lee D.-K. Cochlodinium polykrikoides blooms and eco-physiological conditions in the South Sea of Korea. Harmful Algae 2008, 7:318-323.
98. Lee J.S. Bioactive components from red tide plankton Cochlodinium polykrikoides. J. Korean Fish. Soc. 1996, 29:165-173.
99. Lee M., Kim B., Kwon Y., Kim J. Characteristics of the marine environment and algal blooms in Gamak Bay. Fish. Sci. 2009, 75:401-411.
100. Lee M.O., Choi J.H., Park I.H. Outbreak conditions for Cochlodinium polykrikoides blooms in the southern coastal waters of Korea. Mar. Environ. Res. 2010, 70:227-238.
101. Lee Y.-J., Choi J.-K., Kim E.-K., Youn S.-H., Yang E.-J. Field experiments on mitigation of harmful algal blooms using a Sophorolipid - yellow clay mixture and effects on marine plankton. Harmful Algae 2008, 7:154-162.
102. Lee Y.S., Kim J.D., Lim W.A., Lee S.G. Survival and growth of Cochlodinium polykrikoides red tide after addition of yellow loess. J. Environ. Biol. 2009, 30:929-932.
103. Lee Y.S., Lee S.Y. Factors affecting outbreaks of Cochlodinium polykrikoides blooms in coastal areas of Korea. Mar. Pollut. Bull. 2006, 52:626-634.
104. Mague T.H., Friberg E., Hughes D.J., Morris I. Extracellular release of carbon by marine phytoplankton: a physiological approach. Limnol. Oceanogr. 1980, 25:262-279.
105. Maldonado, D.J.C., 2008. Spectral properties and population dynamics of the harmful dinoflagellate Cochlodinium polykrikoides (Margalef) in southwestern Puerto Rico. Ph.D. Thesis. University of Puerto Rico, Mayagüez, Puerto Rico, 166 pp.
106. Margalef R. Hidrografia y fitoplancton de un area marina de la costa meridional de Puerto Rico. Inv. Pesq. 1961, 18:76-78.
107. Marshall H.G. Phytoplankton of the York River. J. Coast. Res. 2009, 57:59-65.
108. Marshall H.G., Egerton T.A., Burchardt L., Cerbin S., Kokocinski M. Long term monitoring results of harmful algal populations in Chesapeake Bay and its major tributaries in Virginia, U.S.A. Ocean. Hydrobiol. Stud. 2005, 34(3):35-41.
109. Matsuoka K., Fukuyo Y. Technical Guide for Modern Dinoflagellate Cyst Study 2000, IOC/WESTPAC-HAB, the University of Tokyo, Tokyo, 29 pp., 22 pls.
110. Matsuoka K., Fukuyo Y. Technical guide for modern dinoflagellate cyst study. WESTPAC-HAB/WEATPAC/IOC 2002, Japanese Society for the Promotion of Science, p. 29.
111. Matsuoka K., Iwataki M., Kawami H. Morphology and taxonomy of chain-forming species of the genus Cochlodinium (Dinophyceae). Harmful Algae 2008, 7:261-270.
112. Matsuoka K., Mizuno A., Iwataki M., Takano Y., Toshifumi Y., Yoon Y.H., Lee J.B. Seed populations of a harmful unarmored dinoflagellate Cochlodinium polykrikoides Margalef in the East China Sea. Harmful Algae 2010, 9:548-556.
113. Mikulski C., Park Y., Jones K., Lee C., Lim W., Lee Y., Scholin C., Doucette G. Development and field application of rRNA-targeted probes for the detection of Cochlodinium polykrikoides Margalef in Korean coastal waters using whole cell and sandwich hybridiization formats. Harmful Algae 2008, 7:347-359.
114. Montero M.V., Bustamante E.F., Guzman J.C., Vargas J.C. Harmful blooms by noxious dinoflagellates in the Pacific coast of Costa Rica. Hydrobiologica 2008, 18:15-23.
115. Morales-Blake A., Cavazos-Guerra C., Hernandez-Becerril D. Unusual HABs in Manzanillo Bay, Colima, Mexico. Harmful Algae News 2001, 22:6.
116. Morse R.E., Shen J., Blanco-Garcia J.L., Hunley W.S., Fentress S., Wiggins M., Mulholland M.R. Environmental and physical controls on the formation and transport of blooms of the dinoflagellate Cochlodinium polykrikoides Margalef in the lower Chesapeake Bay and its tributaries. Estuar. Coast 2011.
117. Mulholland M.R., Morse R.E., Boneillo G.E., Bernhardt P.W., Filippino K.C., Procise L.A., Blanco-Garcia J.L., Marshall H.G., Egerton T.A., Hunley W.S., Moore K.A., Berry D.L., Gobler C.J. Understanding causes and impacts of the dinoflagellate, Cochlodinium polykrikoides, blooms in the Chesapeake Bay. Estuar. Coast 2009, 32:734-747.
118. Nagai S., Nishitani G., Sakamoto S., Sugaya T., Lee C.K., Kim C.H., Itakura S., Yamaguchi M. Genetic structuring and transfer of marine dinoflagellate Cochlodinium polykrikoides in Japanese and Korean coastal waters revealed by microsatellites. Mol. Ecol. 2009, 18:2337-2352.
119. Nagayama K., Shibata T., Fujimoto K., Honjo T., Nakamura T. Algicidal effect of phlorotannins from the brown alga Ecklonia kurome on red tide microalgae. Aquaculture 2003, 218:601-611.
120. Neori A., Chopin T., Troell M., Buschmann A.H., Kraemer G.P., Halling C., Shpigel M., Yarish C. Integrated aquaculture: rationale, evolution and state of the art emphasizing seaweed biofiltration in modern mariculture. Aquaculture 2004, 231:361-391.
121. National Fisheries Research Development Institute (NFRDI) Recent Red Tides in Korea Coastal Waters 1998, National Fisheries Research and Development Institute, Pusan, Republic of Korea, 292 pp. (in Korean). 2nd Ed.
122. Officer C.B., Smayda T.J., Mann R. Benthic filter feeding: a natural eutrophication control. Mar. Ecol. Prog. Ser. 1982, 9:203-210.
123. Oh M.Y., Lee S.B., Jin D.H., Hong Y.K., Jin H.J. Isolation of algicidal compounds from the red alga Corallina pilulifera against red tide microalgae. J. Appl. Phycol. 2010, 22:453-458.
124. Oh S.J., Yoon Y.H., Kim D.-I., Shimasaki Y., Oshima Y., Honjo T. Effect of light quantity and quality on the growth of the harmful dinoflagellate Cochlodinium polykrikoides Margalef (Dinophyceae). Algae 2006, 21:311-316.
125. Okamura K. Akashio ni Tsuite. Suisan Koushu Sikenjo Kenkyu Hokoku 1916, 12:26-41.
126. Onitsuka G., Miyahara K., Hirose N., Watanabe S., Semura H., Hori R., Nishikawa T., Miyaji K., Yamaguchi M. Large-scale transport of Cochlodinium polykrikoides blooms by the Tsushima Warm Current in the southwest Sea of Japan. Harmful Algae 2010, 9:390-397.
127. Onoue Y., Nozawa K. Separation of toxins from harmful red tides occurring along the coast of Kagoshima Prefecture. Red Tides, Biology, Environmental Science and Toxicology 1989, 371-374. Elsevier, New York. T. Okaichi, D.M. Anderson, T. Nemoto (Eds.).
128. Onoue Y., Nozawa K. Zinc-bound PSP toxins separated from Cochlodinium red tide. Mycotoxins and Phycotoxins'88 1989, 359-366. Elsevier, Amsterdam. S. Natori, K. Hashimoto, Y. Ueno (Eds.).
129. Onoue Y., Nozawa K., Kumanda K., Takeda K., Aramaki T. Toxicity of Cochlodinium'78 Yatsushiro occurring in Yatsushiro Sea. Nippon Suisan Gakkaishi 1985, 51:147-151.
130. Orlova T.Y., Morozova T.V., Gribble K.E., Kulis D.M., Anderson D.M. Dinoflagellate cysts in recent marine sediments from the east coast of Russia. Bot. Mar. 2004, 47:184-201.
131. Orlova T.Y., Stonik I.V., Shevchenko O.G. Flora of planktonic microalgae of Amursky Bay, Sea of Japan. Planktonology 2009, 35:60-78.
132. Ou L.-J., Zhang Y.-Y., Li Y., Wang H.-J., Xie X.-D., Rong Z.-M., Lu S.-H., Qi Y.-Z. The outbreak of Cochlodinium geminatum bloom in Zhuhai, Guangdong. J. Trop. Oceanogr. 2010, 29:57-61.
133. Palanisamy S., Ahn Y.-H., Ryu J.-H., Moon J.-E. Application of optical remote sensing imagery for detection of red tide algal blooms in Korean waters. IEEE International, IGARSS'05, vol. 3 2005, 1912-1915.
134. Park G.-H., Lee K., Koo C.-M., Lee H.-W., Lee C.-K., Koo J.-S., Lee T., Ahn S.-H., Kim H.-G., Park B.-K. A sulfur hexafluoride-based Lagrangian study on initiation and accumulation of the red tide Cochlodinium polykrikoides in southern coastal waters of Korea. Limnol. Oceanogr. 2005, 50:578-586.
135. Park J.G., Jeong M.K., Lee J.A., Cho K.-J., Kwon O.-S. Diurnal vertical migration of a harmful dinoflagellate, Cochlodinium polykrikoides (Dinophyceae) during a red tide in coastal waters of Namhae Island, Korea. Phycologia 2001, 40:292-297.
136. Park T.-G., Park G.-H., Park Y.-T., Kang Y.-S., Bae H.-M., Kim C.-H., Jeong H.-J., Lee Y. Identification of the dinoflagellate community during Cochlodinium polykrikoides (Dinophyceae) blooms using amplified rDNA melting curve analysis and real-time PCR probes. Harmful Algae 2009, 8:430-440.
137. Park T.-G., Park Y.-T. Detection of Cochlodinium polykrikoides and Gymnodinium impudicum (Dinophyceae) in sediment samples. Harmful Algae 2010, 9:59-65.
138. Phlips E.J., Badylak S., Christman M., Wolny J., Brame J., Garland J., Hall L., Hart J., Landsberg J., Lasi M., Lockwood J., Paperno R., Scheidt D., Staples A., Steidinger K. Scales of temporal and spatial variability in the distribution of harmful algae species in the Indian River Lagoon, Florida, USA. Harmful Algae 2011, 10:277-290.
139. Qi D., Huang Y., Wang X. Toxic dinoflagellate red tide by a Cochlodinium sp. along the coast of Fujian, China. Toxic Phytoplankton Blooms in the Sea 1993, Elsevier, Amsterdam. T. Smayda, Y. Shimizu (Eds.).
140. Ramaiah N., Paul J.T., Fernandes V., Raveendran T., Raveendran O., Sundar D., Revichandran C., Shenoy D.M., Gauns M., Kurian S., Gerson V.J. The September 2004 stench off the southern Malabar coast - a consequence of holococcolithophore bloom. Curr. Sci. 2005, 88:551-554.
141. Rashed-Un-Nabi M., Ee L.S., Hoque M.A., Sidik M.J., Saleh E., Anton A Effects of red tide on physico-chemical properties of water and phytoplankton assemblage in Sepanggar Bay, Sabah, Malaysia. Int. J. Ecol. Environ. Sci. 2010, 36:245-251.
142. Richlen M.L., Morton S.L., Jamali E.A., Rajan A., Anderson D.M. 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 2010, 9:163-172.
143. Roberts R.J. The parasitology of teleosts. Fish Pathology 2001, 254-296. Elsevier, New York. R.J. Roberts (Ed.).
144. Robertson-Andersson D., Potgieter M., Hansen J., Bolton J., Troell M., Anderson R., Halling C., Probyn T. Integrated seaweed cultivation on an abalone farm in South Africa. J. Appl. Phycol. 2008, 20:579-595.
145. Rosales-Loessener F., Matsuoka K., Fukuyo Y., Sanchez E.H. Cysts of harmful dinoflagellates found from Pacific coastal waters of Guatemala. Harmful and Toxic Algal Blooms 1996, International Oceanographic Commission of UNESCO, Paris. T. Yasumoto, Y. Oshima, Y. Fukuyo (Eds.).
146. Rubino F., Belmonte M., Caroppo C., Giacobbe M. Dinoflagellate cysts from surface sediments of Syracuse Bay (Western Ionian Sea, Mediterranean). Deep-Sea Res. II 2010, 57:243-247.
147. Ryan J., Fischer A., Kudela R., Gower J., King S., Marin Iii R., Chavez F. Influences of upwelling and downwelling winds on red tide bloom dynamics in Monterey Bay, California. Cont. Shelf Res. 2009, 29:785-795.
148. Samson J.C., Shumway S.E., Weis J.S. Effects of the toxic dinoflagellate, Alexandrium fundyense on three species of larval fish: a food-chain approach. J. Fish Biol. 2008, 72:168-188.
149. Sannio A., Luglie A., Sechi N. Potentially toxic dinoflagellates in Sardinia. Plant Biosyst. 1997, 131:73-78.
150. Saracino O.D., Rubino F. Phytoplankton composition and distribution along the Albanian coast, South Adriatic Sea. Nova Hedwigia 2006, 83:253-266.
151. Sasaki H., Tanaka A., Iwataki M., Touke Y., Siswanto E., Tan C.K., Ishizaka J. Optical properties of the red tide in Isahaya Bay, south-western Japan: influence of chlorophyll a concentration. J. Oceanogr. 2008, 64:511-523.
152. Saunders G.W., Hill D.A., Sexton J.P., Andersen R.A. Small-subunit ribosomal RNA sequences from selected dinoflagellates: testing classical evolutionary hypotheses with molecular systematic methods. Plant Syst. Evol. Suppl. 1997, 11:237-260.
153. Schütt, F., 1895. Peridineen der Plankton-Expedition. Ergebn. Plankton--Expedition der Humboldt-Stiftung 4 (M, a, A) 1-170, 127 pls.
154. Seaborn D.W., Marshall H.G. Dinoflagellate cysts within sediment collections from the southern Chesapeake Bay and tidal regions of the James, York, and Rappahannock rivers. J. Sci. 2008, 59:135-141.
155. Seong K.A., Jeong H.J., Kim S., Kim G.H., Kang J.H. Bacterivory by co-occurring red-tide algae, heterotrophic nanoflagellates, and ciliates. Mar. Ecol. Prog. Ser. 2006, 322:85-97.
156. Shanmugam P., Ahn S.-H., Ram P.S. SeaWiFS sensing of hazardous algal blooms and their underlying mechanisms in shelf-slope waters of the Northwest Pacific during summer. Remote Sens. Environ. 2008, 112:3248-3270.
157. Shao P., Chen Y.Q., Zhou H., Yuan J., Qu L.H., Zhao D., Lin Y.S. Genetic variability in Gymnodiniaceae ITS regions: implications for species identification and phylogenetic analysis. Mar. Biol. 2004, 144:215-224.
158. Shin K., Jang M.-C., Jang P.-K., Ju S.-J., Lee T.-K., Chang M. Influence of food quality on egg production and viability of the marine planktonic copepod Acartia omorii. Prog. Oceanogr. 2003, 57:265-277.
159. Silva E.S. Cochlodinium heterolobactum n. sp.: structure and some cytophysiological aspects. J. Protozool. 1967, 14:745-754.
160. Smayda T.J. Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol. Oceanogr. 1997, 42:1137-1153.
161. Smayda T.J. Reflections on the ballast water dispersal - harmful algal bloom paradigm. Harmful Algae 2007, 6:601-622.
162. Smayda T.J. Complexity in the eutrophication-harmful algal bloom relationship, with comment on the importance of grazing. Harmful Algae 2008, 8:140-151.
163. Sogawa K., Matsuda M., Okutani K. Induction of apoptosis by a marine microalgal polysaccharide in a human leukemic cell line. J. Mar. Biotechnol. 1998, 6:241-243.
164. Sogawa K., Sumida T., Hamakawa H., Yamada T., Matsumoto K., Matsuda M., Oda H., Miyake H., Tashiro S., Okutani K. Inhibitory effect of a marine microalgal polysaccharide on the telomerase activity in K562 cells. Res. Commun. Mol. Pathol. Pharmacol. 1998, 99:259-265.
165. Sohn M.H., Seo K.W., Choi Y.S., Lee S.J., Kang Y.S., Kang Y.S. Determination of the swimming trajectory and speed of chain-forming dinoflagellate Cochlodinium polykrikoides with digital holographic particle tracking velocimetry. Mar. Biol. 2011, 158:561-570.
166. Song Y.-C., Sivakumar S., Woo J.-H., Ko S.-J., Hwang E.-J., Jo Q. Removal of Cochlodinium polykrikoides by dredged sediment: a field study. Harmful Algae 2010, 9:227-232.
167. Stoecker D., Tillmann U., Granéli E. Phagotrophy in harmful algae. Ecology of Harmful Algae 2006, vol. 189:177-187. Springer-Verlag, Berlin.
168. Stumpf R.P., Tomlinson M.C. Remote sensing of harmful algal blooms. Remote Sens. Coast. Aquat. Environ. 2005, 7:277-296.
169. Suh Y.S., Kim J.H., Kim H.G. Relationship between sea surface temperature derived from NOAA satellites and Cochlodinium polykrikoides red tide occurrence in Korea coastal waters. J. Korean Environ. Sci. 2000, 9:215-221.
170. Sullivan J.M., Swift E., Donaghay P., Rines J.E.B. Small-scale turbulence affects the division rate and morphology of two red-tide dinoflagellates. Harmful Algae 2003, 2:183-199.
171. Sun X.-X., Choi J.-K., Kim E.-K. A preliminary study on the mechanism of harmful algal bloom mitigation by use of sophorolipid treatment. J. Exp. Mar. Biol. Ecol. 2004, 304:35-49.
172. Sun X.-X., Lee Y.-J., Choi J.-K., Kim E.-K. Synergistic effect of sophorolipid and loess combination in harmful algal blooms mitigation. Mar. Pollut. Bull. 2004, 48:863-872.
173. Sunda W.G., Graneli E., Gobler C.J. Positive feedback and the development and persistence of ecosystem disruptive algal blooms. J. Phycol. 2006, 42:963-974.
174. Tang Y.Z., Gobler C. Cochlodinium polykrikoides blooms and clonal isolates from the northwest Atlantic coast cause rapid mortality in larvae of multiple bivalve species. Mar. Biol. 2009, 156:2601-2611.
175. Tang Y.Z., Gobler C.J. Characterization of the toxicity of Cochlodinium polykrikoides isolates from Northeast US estuaries to finfish and shellfish. Harmful Algae 2009, 8:454-462.
176. Tang Y.Z., Gobler C.J. Allelopathic effects of Cochlodinium polykrikoides isolates and blooms from the estuaries of Long Island, New York, on co-occurring phytoplankton. Mar. Ecol. Prog. Ser. 2010, 406:19-31.
177. Tang Y.Z., Gobler C.J. The green macroalga, Ulva lactuca, inhibits the growth of seven common harmful algal bloom species via allelopathy. Harmful Algae 2011, 10:480-488.
178. Terenko L. New dinoflagellate (Dinoflagellata) species from the Odessa Bay of the Black Sea. Ocean. Hydrobiol. Stud. 2005, 34:205-216.
179. Tomas C.R., Smayda T.J. Red tide blooms of Cochlodinium polykrikoides in a coastal cove. Harmful Algae 2008, 7:308-317.
180. Tort M.J., Jennings-Bashore C., Wilson D., Wooster G.A., Bowser P.R. Assessing the effects of increasing hydrogen peroxide dosage on rainbow trout gills utilizing a digitized scoring methodology. J. Aquat. Anim. Health 2002, 14:95-103.
181. Trainer V.L., Pitcher G.C., Reguera B., Smayda T.J. The distribution and impacts of harmful algal bloom species in eastern boundary upwelling systems. Prog. Oceanogr. 2010, 85:33-52.
182. Vargas-Montero M., Freer E., Jimenez-Montealegre R., Guzman J. Extensive blooms due to Cochlodinium polykrikoides: new to Costa Rica. Harmful Algae News 2004, 26:7.
183. Vargas-Montero M., Freer E., Jimenez-Montealegre R., Guzman J.C. Occurrence and predominance of the fish killer Cochlodinium polykrikoides on the Pacific coast of Costa Rica. Afr. J. Mar. Sci. 2006, 28:215-217.
184. Verity P.G. Expansion of potentially harmful algal taxa in a Georgia Estuary (USA). Harmful Algae 2010, 9:144-152.
185. Vershinin A.O., Moruchkov A.A., Leighfield T., Sukanova I., Kamnev A.N., Pankov S., Morton S.L., Ramsdell J.S. Potential toxic algae in northeast Black Sea coastal phytoplankton in 2000-2002. Okeanologiya 2005, 45:240-248.
186. Vershinin A.O., Moruchkov A.A., Sukanova I., Kamnev A.N., Pankov S., Morton S.L., Ramsdell J.S. Seasonal changes in phytoplankton in the area of Cape Bolshoi Utrish off northern Caucasian coast in the Black Sea 2001-2002. Russ. Acad. Sci. Oceanol. 2004, 44:379-387.
187. Viques R., Hargraves P.E. Annual cycle of potentially harmful dinoflagellates in the Gulfo de Nicoya. Costa Rica Bull. Mar. Sci. 1995, 57:467-475.
188. Whyte J.N.C., Haigh N., Ginther N.G., Keddy L.J. First record of blooms of Cochlodinium sp. (Gymnodiniales, Dinophyceae) causing mortality to aquacultured salmon on the west coast of Canada. Phycologia 2001, 40:298-304.
189. Yamasaki Y., Nagasoe S., Matsubara T., Shikata T., Shimasaki Y., Oshima Y., Honjo T. Growth inhibition and formation of morphologically abnormal cells of Akashiwo sanguinea (Hirasaka) G. Hansen et Moestrup by cell contact with Cochlodinium polykrikoides Margalef. Mar. Biol. 2007, 152:157-163.
190. Yamatogi T., Maruta H. Occurrence of Cochlodinium polykrikoides red tide and its growth characteristics in Imari Bay in 1999. Bull. Nagasaki Prefect. Inst. Fish. 2002, 28:21-26.
191. Yamatogi T., Sakaguchi M., Iwataki M., Matsuoka K. Seasonal occurrence and growth characteristics of a harmful dinoflagellate Cochlodinium polykrikoides in Usuka Bay. Jpn. J. Phycol. 2005, 53:229-235.
192. Yamatogi T., Sakaguchi M., Iwataki M., Matsuoka K. Effects of temperature and salinity on the growth of four harmful red tide flagellates occurring in Isahaya Bay in Ariake Sound, Japan. Nippon Suisan Gakkaishi 2006, 72:160-168.
193. Yang Y.-F., Fei X.-G., Song J.-M., Hu H.-Y., Wang G.-C., Chung I.K. Growth of Gracilaria lemaneiformis under different cultivation conditions and its effects on nutrient removal in Chinese coastal waters. Aquaculture 2006, 254:248-255.
194. Yoo D.Y., Jeong H.J., Kim M.S., Kang N.S., Song J.Y., Shin W., Kim K.Y., Lee K. Feeding by phototrophic red-tide dinoflagellates on the ubiquitous marine diatom Skeletonema costatum. J. Eukaryot. Microbiol. 2009, 56:413-420.
195. Yuki K., Yoshimatsu S. Two fish-killing species of Cochlodinium from Harima-Nada, Seto Inland Sea Japan. Red Tides: Biology, Environmental Science, and Toxicology 1989, 451-454. Elsevier, New York. T. Okaichi, D. Anderson, T. Nemoto (Eds.).
196. Zhou Y., Yang H., Hu H., Liu Y., Mao Y., Zhou H., Xu X., Zhang F. Bioremediation potential of the macroalga Gracilaria lemaneiformis (Rhodophyta) integrated into fed fish culture in coastal waters of north China. Aquaculture 2006, 252:264-276.