Ichthyotoxic Cochlodinium polykrikoides red tides offshore in the South Sea, Korea in 2014: III. Metazooplankton and their grazing impacts on red-tide organisms and heterotrophic protists |
Lee, Moo Joon
(Department of Marine Biotechnology, Anyang University)
Jeong, Hae Jin (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) Kim, Jae Seong (Water and Eco-Bio Corporation, Kunsan National University) Jang, Keon Kang (Water and Eco-Bio Corporation, Kunsan National University) Kang, Nam Seon (Marine Biodiversity Institute of Korea) Jang, Se Hyeon (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) Lee, Hak Bin (School of Marine Life and Applied Sciences, Kunsan National University) Lee, Sang Beom (School of Marine Life and Applied Sciences, Kunsan National University) Kim, Hyung Seop (School of Marine Life and Applied Sciences, Kunsan National University) Choi, Choong Hyeon (School of Marine Life and Applied Sciences, Kunsan National University) |
1 | Griffin, S. L., Herzfeld, M. & Hamilton, D. P. 2001. Modelling the impact of zooplankton grazing on phytoplankton biomass during a dinoflagellate bloom in the Swan River Estuary, Western Australia. Ecol. Eng. 16:373-394. DOI |
2 | Jeong, H. J., Yoo, Y. D., Kim, J. S., Kim, T. H., Kim, J. H., Kang, N. S. & Yih, W. 2004. Mixotrophy in the phototrophic harmful alga Cochlodinium polykrikoides (Dinophycean): prey species, the effects of prey concentration, and grazing impact. J. Eukaryot. Microbiol. 51:563-569. DOI |
3 | 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 Sci. J. 45:65-91. DOI |
4 | Kim, J. S., Jeong, H. J., Yoo, Y. D., Kang, N. S., Kim, S. K., Song, J. Y., Lee, M. J., Kim, S. T., Kang, J. H., Seong, K. A. & Yih, W. H. 2013a. Red tides in Masan Bay, Korea, in 2004-2005: III. Daily variations in the abundance of metazooplankton and their grazing impacts on red-tides organisms. Harmful Algae 30(Suppl.):S102-S113. DOI |
5 | Kim, M. J., Youn, S. H., Kim, J. Y. & Oh, C. W. 2013b. Feeding characteristics of the Japanese anchovy, Engraulis japonicus according to the distribution of zooplankton in the coastal waters of southern Korea. Korean J. Environ. Biol. 31:275-287. DOI |
6 | Kim, S. T. 2005. The interactions between dominant copepod Acartia spp. and red-tides organisms and protozoans in the coastal waters in the west and south coast in Korea, egg production rates and grazing impact in the coastal waters off the Saemankeum and Kwangyang Bay. Kunsan National University, Gunsan, 157 pp. |
7 | Kimmel, D. G. & Roman, M. R. 2004. Long-term trends in mesozooplankton abundance in Chesapeake Bay, USA: influence of freshwater input. Mar. Ecol. Prog. Ser. 267:71-83. DOI |
8 | Lazareva, V. I. & Kopylov, A. I. 2011. Zooplankton productivity at the height of eutrophication of a plain reservoir ecosystem: the role of invertebrate predators. Usp. Sovrem. Biol. 131:300-310. |
9 | Jeong, H. J., Kim, J. S., Yoo, Y. D., Kim, S. T., Kim, T. H., Park, M. G., Lee, C. H., Seong, K. A., Kang, N. S. & Shim, J. H. 2003. Feeding by the heterotrophic dinoflagellate Oxyrrhis marina on the red-tide raphidophyte Heterosigma akashiwo: a potential biological method to control red tides using mass-cultured grazers. J. Eukaryot. Microbiol. 50:274-282. DOI |
10 | 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. 2008. Control of the harmful alga Cochlodinium polykrikoides by the naked ciliate Strombidinopsis jeokjo in mesocosm enclosures. Harmful Algae 7:368-377. DOI |
11 | Jeong, H. J. & Latz, M. I. 1994. Growth and grazing rates of the heterotrophic dinoflagellate Protoperidinium spp. on red tide dinoflagellates. Mar. Ecol. Prog. Ser. 106:173-185. DOI |
12 | Jeong, H. J., Lim, A. S., Franks, P. J. S., Lee, K. H., Kim, J. H., Kang, N. S., Lee, M. J., Jang, S. H., Lee, S. Y., Yoon, E. Y., Park, J. Y., Yoo, Y. D., Seong, K. A., Kwon, J. E. & Jang, T. Y. 2015. A hierarchy of conceptual models of red-tides generation: nutrition, behavior, and biological interactions. Harmful Algae 47:97-115. DOI |
13 | Jeong, H. J., Yoo, Y. D., Lee, K. H., Kim, T. H., Seong, K. A., Kang, N. S., Lee, S. Y., Kim, J. S., Kim, S. & Yih, W. H. 2013. Red tidess in Masan Bay, Korea in 2004-2005: I. Daily variations in the abundance of red-tides organisms and environmental factors. Harmful Algae 30(Suppl. 1):S75-S88. DOI |
14 | Kang, N. S., Lee, K. H., Jeong, H. J., Yoo, Y. D., Seong, K. A., Potvin, e., Hwang, Y. J. & Yoon, E. Y. 2013. Red tides in Shiwha Bay, western Korea: a huge dike and tidal power plant established in a semi-enclosed embayment system. Harmful Algae 30(Suppl. 1):S114-S130. DOI |
15 | Kang, Y. S., Park, J. S., Lee, S. S., Kim, H. G. & Lee, P. Y. 1996. Zooplankton community and distributions of copepods in relation to eutrophic evaluation in Chinhae Bay. Korean J. Fish. Aquat. Sci. 29:415-430. |
16 | Katechakis, A. & Stibor, H. 2004. Feeding selectivities of the marine cladocerans Penilia avirostris, Podon intermedius and Evadne nordmanni. Mar. Biol. 145:529-539. |
17 | Kim, D. I., Matsuyama, Y., Nagasoe, S., Yamaguchi, M., Yoon, Y. H., Oshima, Y., Imada, N. & Honjo, T. 2004. Effects of temperature, salinity and irradiance on the growth of the harmful red tide dinoflagellate Cochlodinium polykrikoides Margalef (Dinophyceae). J. Plankton Res. 26:61-66. DOI |
18 | Kim, J. S. & Jeong, H. J. 2004. Feeding by the heterotrophic dinoflagellates Gyrodinium dominans and G. spirale on the red-tides dinoflagellate Prorocentrum minimum. Mar. Ecol. Prog. Ser. 280:85-94. DOI |
19 | Lee, M. J., Jeong, H. J., Lee, K. H., Jang, S. H., Kim, J. H. & Kim, K. Y. 2015. Mixotrophy in the nematocyst–taeniocyst complex-bearing phototrophic dinoflagellate Polykrikos hartmannii. Harmful Algae 49:124-134. DOI |
20 | Lim, A. S., Jeong, H. J., Jang, T. Y., Jang, S. H. & Franks, P. J. S. 2014. Inhibition of growth rate and swimming speed of the harmful dinoflagellate Cochlodinium polykrikoides by diatoms: implications for red tide formation. Harmful Algae 37:53-61. DOI |
21 | Jeong, H. J., Lim, A. S., Lee, K., Lee, M. J., Seong, K. A., Kang, N. S., Jang, S. H., Lee, K. H., Lee, S. Y., Kim, M. O., Kim, J. H., Kwon, J. E., Kang, H. C., Kim, J. S., Yih, W., Shin, K., Jang, P. K., Ryu, J. H., Kim, S. Y., Park, J. Y. & Kim, K. W. 2017. Ichthyotoxic Cochlodinium polykrikoides red tides offshore in the South Sea, Korea in 2014: I. Temporal variations in three-dimensional distributions of red-tide organisms and environmental factors. Algae 32:101-130. DOI |
22 | Jeong, H. J., Shim, J. H., Lee, C. W., Kim, J. S. & Koh, S. M. 1999. Growth and grazing rates of the marine planktonic ciliate Strombidinopsis sp. on red-tide and toxic dinoflagellates. J. Eukaryot. Microbiol. 46:69-76. DOI |
23 | Uye, S. 1986. Impact of copepod grazing on the red-tides flagellate Chattonella antiqua. Mar. Biol. 92:35-43. DOI |
24 | Uye, S. & Liang, D. 1998. Copepods attain high abundance, biomass and production in the absence of large predators but suffer cannibalistic loss. J. Mar. Syst. 15:495-501. DOI |
25 | Waggett, R. J., Tester, P. A. & Place, A. R. 2008. Anti-grazing properties of the toxic dinoflagellate Karlodinium veneficum during predator-prey interactions with the copepod Acartia tonsa. Mar. Ecol. Prog. Ser. 366:31-42. DOI |
26 | Yoo, Y. D., Jeong, H. J., Kang, N. S., Kim, J. S., Kim, T. H. & Yoon, E. Y. 2010. Ecology of Gymnodinium aureolum. II. Predation by common heterotrophic dinoflagellates and a ciliate. Aqut. Microb. Ecol. 59:257-272. DOI |
27 | Yoo, Y. D., Jeong, H. J., Kim, J. S., Kim, T. H., Kim, J. H., Seong, K. A., Lee, S. H., Kang, N. S., Park, J. W., Park, J., Yoon, E. Y. & Yih, W. H. 2013a. Red tides in Masan Bay, Korea in 2004-2005: II. Daily variations in the abundance of heterotrophic protists and their grazing impact on red-tide organisms. Harmful Algae 30(Suppl. 1):S89-S101. DOI |
28 | Lim, A. S., Jeong, H. J., Seong, K. A., Lee, M. J., Kang, N. S., Jang, S. H., Lee, K. H., Park, J. Y., Jang, T. Y. & Yoo, Y. D. 2017. Ichthyotoxic Cochlodinium polykrikoides red tides offshore in the South Sea, Korea in 2014: II. Heterotrophic protists and their grazing impacts on red-tide organisms. Algae 32:199-222. DOI |
29 | Oh, H. J., Moon, S. Y. & Soh, H. Y. 2013. Seasonal changes of zooplankton communities along the coast of Geumo Archipelago, Yeosu. Korean J. Environ. Biol. 31:192-203. DOI |
30 | Oh, S. J., Yoon, Y. H., Kim, D. I., Shimasaki, Y., Oshima, Y. & Honjo, T. 2006. Effects of light quantity and quality on the growth of the harmful dinoflagellate, Cochlodinium polykrikoides Margalef (Dinophyceae). Algae 21:311-316. DOI |
31 | Park, T. G., Lim, W. A., Park, Y. T., Lee, C. K. & Jeong, H. J. 2013. Economic impact, management and mitigation of red tidess in Korea. Harmful Algae 30(Suppl. 1):S131-S143. DOI |
32 | Porter, K. G., Sherr, E. B., Sherr, B. F., Pace, M. & Sanders, R. W. 1985. Protozoa in planktonic food webs. J. Eukaryot. Microbiol. 32:409-415. |
33 | Sordo, I., Barton, E. D., Cotos, J. M. & Pazos, Y. 2001. An inshore poleward current in the NW of the Iberian Peninsula detected from satellite images, and its relation with G. catenatum and D. acuminata blooms in the Galican Rias. Estuar. Coast. Shelf Sci. 53:787-799. DOI |
34 | Stoecker, D. K. & Capuzzo, J. M. 1990. Predation on protozoa, its importance to zooplankton. J. Plankton Res. 12:891-908. DOI |
35 | Tan, Y., Huang, L., Chen, Q. & Huang, X. 2004. Seasonal variation in zooplankton composition and grazing impact on phytoplankton standing stock in the Pearl River Estuary, China. Cont. Shelf Res. 24:1949-1968. DOI |
36 | Tillmann, U. 2004. Interactions between planktonic microalgae and protozoan grazers. J. Eukaryot. Microbiol. 51:156-168. DOI |
37 | Tseng, L. C., Dahms, H. U., Chen, Q. C. & Hwang, J. S. 2009. Copepod feeding study in the upper layer of the tropical South China Sea. Helgol. Mar. Res. 62:327-337. |
38 | Turner, J. T. 2004. The importance of small planktonic copepods and their roles in pelagic marine food webs. Zool. Stud. 43:255-266. |
39 | Turner, J. T. & Borkman, D. G. 2005. Impact of zooplankton grazing on Alexandrium blooms in the offshore Gulf of Maine. Deep Sea Res. Part II Top. Stud. Oceanogr. 52:2801-2816. DOI |
40 | Turner, J. T. & Graneli, E. 1992. Zooplankton feeding ecology: grazing during enclosure studies of phytoplankton blooms from the west coast of Sweden. J. Exp. Mar. Biol. Ecol. 157:19-31. DOI |
41 | Turner, J. T. & Tester, P. A. 1997. Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs. Limnol. Oceanogr. 42:1203-1213. DOI |
42 | Turner, J. T., Tester, P. A. & Ferguson, R. L. 1988. The marine cladoceran Penilia avirostris and the "microbial loop" of pelagic food webs. Limnol. Oceanogr. 33:245-255. DOI |
43 | Yoo, Y. D., Seong, K. A., Myung, G., Kim, H. S., Jeong, H. J., Palenik, B. & Yih, W. 2015. Ingestion of the unicellular cyanobacterium Synechococcus by the mixotrophic red tide ciliate Mesodinium rubrum. Algae 30:281-290. DOI |
44 | Yoo, Y. D., Yoon, E. Y., Jeong, H. J., Lee, K. H., Hwang, Y. J., Seong, K. A., Kim, J. S. & Park, J. Y. 2013b. The newly described heterotrophic dinoflagellate Gyrodinium moestrupii, an effective protistan grazer of toxic dinoflagellates. J. Eukaryot. Microbiol. 60:13-24. DOI |
45 | Youn, S. H., Oh, G. S. & Chung, M. H. 2010. Zooplankton community structure and copepod production in the Seomjin River Estuary. J. Korean Soc. Mar. Environ. Saf. 16:369-379. |
46 | Zar, J. H. 1999. Biostatistical analysis. 4th ed. Prentice Hall, Upper Saddle River, NJ, 663 pp. |
47 | Aktan, Y. & Keskin, C. 2017. Second habitat record of Polykrikos hartmannii W. Zimm. (Dinophyceae) in the South Aegean Sea, Eastern Mediterranean. Turk. J. Fish. Aquatic Sci. 17:1077-1081. |
48 | Anderson, D. M. 1997. Turning back the harmful red tide. Nature 388:513-514. DOI |
49 | Anderson, D. M., Alpermann, T. J., Cembella, A. D., Collos, Y., Masseret, E. & Montresor, M. 2012. The globally distributed genus Alexandrium: multifaceted roles in marine ecosystems and impacts on human health. Harmful Algae 14:10-35. DOI |
50 | American Public Health Association (APHA). 1995. Standard methods for the examination of water and wastewater. 19th ed. APHA, Washington, DC, 1100 pp. |
51 | Calbet, A. 2001. Metazooplankton grazing effect on primary production: a global comparative analysis in marine ecosystems. Limnol. Oceanogr. 46:1824-1830. DOI |
52 | Calbet, A., Garrido, S., Saiz, E., Alcaraz, M. & Duarte, C. M. 2001. Annual zooplankton succession in coastal NW Mediterranean waters: the importance of the smaller size fractions. J. Plankton Res. 23:319-331. DOI |
53 | Puelles, M. F., Gras, D. & Hernandez-Leon, S. 2003. Annual cycle of zooplankton biomass, abundance and species composition in the neritic area of the Balearic Sea, Western Mediterranean. Mar. Ecol. 24:123-139. DOI |
54 | Sanders, R. W. & Wickham, S. A. 1993. Planktonic protozoa and metazoan: predation, food quality and population control. Mar. Microb. Food Webs 7:197-223. |
55 | Smayda, T. J. 1990. Novel and nuisance phytoplankton blooms in the sea: evidence for a global epidemic. RWS-North Sea Directorate, Rijswijk, pp. 29-40. |
56 | Smayda, T. J. 1997. What is a bloom? A commentary. Limnol. Oceanogr. 42:1132-1136. DOI |
57 | Hallegraeff, G. M. 1993. A review of harmful algal blooms and their apparent global increase. Phycologia 32:79-99. DOI |
58 |
Hansen, P. J., Bjornsen, P. K. & Hansen, B. W. 1997. Zooplankton grazing and growth: scaling within the 2-2,000- |
59 | Holmes, R. W., Williams, P. M. & Eppley, R. W. 1967. Red water in La Jolla Bay, 1964-1966. Limnol. Oceanogr. 12:503-512. DOI |
60 | Houde, S. E. L. & Roman, M. R. 1987. Effects of food quality on the functional ingestion response of the copepod Acartia tonsa. Mar. Ecol. Prog. Ser. 40:69-77. DOI |
61 | Hue, H. K., Kim, D. H. & Ahn, S. H. 2002. Community structure and distributions of zooplankton in Gangjin Bay in 1999. Koean J. Environ. Biol. 20:46-54. |
62 | Jansen, S., Riser, C. W., Wassmann, P. & Bathmann, U. 2006. Copepod feeding behaviour and egg production during a dinoflagellate bloom in the North Sea. Harmful Algae 5:102-112. DOI |
63 | Jeong, H. J. 1999. The ecological roles of heterotrophic dinoflagellates in marine planktonic community. J. Eukaryot. Microbiol. 46:390-396. DOI |
64 | Jeong, H. J., Kang, H., Shim, J. H., Park, J. K., Kim, J. S., Song, J. Y. & Choi, H. J. 2001. Interactions among the toxic dinoflagellate Amphidinium carterae, the heterotrophic dinoflagellate Oxyrrhis marina, and the calanoid copepods Acartia spp. Mar. Ecol. Prog. Ser. 218:77-86. DOI |
65 | Jeong, H. J., Kim, J. S., Song, J. Y., Kim, J. H., Kim, T. H., Kim, S. K. & Kang, N. S. 2007. Feeding by heterotrophic protists and copepods on the heterotrophic dinoflagellates Pfiesteria piscicida, Stoeckeria algicida, and Luciella masanensis. Mar. Ecol. Prog. Ser. 349:199-211. DOI |
66 | Calbet, A., Vaque, D., Felipe, J., Vila, M., Sala, M. M., Alcaraz, M. & Estrada, M. 2003. Relative grazing impact of microzooplankton and metazooplankton on a bloom of the toxic dinoflagellate Alexandrium minutum. Mar. Ecol. Prog. Ser. 259:303-309. DOI |
67 | Carlsson, P., Graneli, E., Tester, P. & Boni, L. 1995. Influences of riverine humic substances on bacteria, protozoa, phytoplankton, and copepods in a coastal plankton community. Mar. Ecol. Prog. Ser. 127:213-221. DOI |
68 | Cohen, J. H., Tester, P. A. & Forward, R. B. Jr. 2007. Sublethal effects of the toxic dinoflagellate Karenia brevis on marine copepod behavior. J. Plankton Res. 29:301-315. DOI |
69 | Conover, W. J. 1980. Practical nonparametric statistics. 2nd ed. John Wiley and Sons, New York, NY, 493 pp. |
70 | Croll, D. A., Marinovic, B., Benson, S., Chavez, F. P., Black, N., Ternullo, R. & Tershy, B. R. 2005. From wind to whales: trophic links in a coastal upwelling system. Mar. Ecol. Prog. Ser. 289:117-130. DOI |
71 | Fu, F. X., Tatters, A. O. & Hutchins, D. A. 2012. Global change and the future of harmful algal blooms in the ocean. Mar. Ecol. Prog. Ser. 470:207-233. DOI |
72 | Fulton, R. S. 1984. Distribution and community structure of estuarine copepods. Estuaries 7:38-50. DOI |
73 | Gallienne, C. P. & Robins, D. B. 2001. Is Oithona the most important copepod in the world's oceans? J. Plankton Res. 23:1421-1432. DOI |
74 | Glibert, P. M., Anderson, D. M., Gentien, P., Graneli, E. & Sellner, K. G. 2005. The global, complex phenomena of harmful algal blooms. Oceanography 18:136-147. |
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