DOI QR코드

DOI QR Code

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)
  • 투고 : 2017.09.29
  • 심사 : 2017.11.28
  • 발행 : 2017.12.15

초록

Cochlodinium polykrikoides red tides have caused great economic losses in the aquaculture industry in many countries. To investigate the roles of metazooplankton in red tide dynamics of C. polykrikoides in the South Sea of Korea, the abundance of metazooplankton was measured at 60 stations over 1- or 2-week intervals from May to November 2014. In addition, the grazing impacts of dominant metazooplankton on red tide species and their potential heterotrophic protistan grazers were estimated by combining field data on the abundance of red tide species, heterotrophic protist grazers, and dominant metazooplankton with data obtained from the literature concerning ingestion rates of the grazers on red tide species and heterotrophic protists. The mean abundance of total metazooplankton at each sampling time during the study was 297-1,119 individuals $m^{-3}$. The abundance of total metazooplankton was significantly positively correlated with that of phototrophic dinoflagellates (p < 0.01), but it was not significantly correlated with water temperature, salinity, and the abundance of diatoms, euglenophytes, cryptophytes, heterotrophic dinoflagellates, tintinnid ciliates, and naked ciliates (p > 0.1). Thus, dinoflagellate red tides may support high abundance of total metazooplankton. Copepods dominated metazooplankton assemblages at all sampling times except from Jul 11 to Aug 6 when cladocerans and hydrozoans dominated. The calculated maximum grazing coefficients attributable to calanoid copepods on C. polykrikoides and Prorocentrum spp. were 0.018 and $0.029d^{-1}$, respectively. Therefore, calanoid copepods may not control populations of C. polykrikoides or Prorocentrum spp. Furthermore, the maximum grazing coefficients attributable to calanoid copepods on the heterotrophic dinoflagellates Polykrikos spp. and Gyrodinium spp., which were grazers on C. polykrikoides and Prorocentrum spp., respectively, were 0.008 and $0.047d^{-1}$, respectively. Therefore, calanoid copepods may not reduce grazing impact by these heterotrophic dinoflagellate grazers on populations of the red tide dinoflagellates.

키워드

참고문헌

  1. 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.
  2. Anderson, D. M. 1997. Turning back the harmful red tide. Nature 388:513-514. https://doi.org/10.1038/41415
  3. 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. https://doi.org/10.1016/j.hal.2011.10.012
  4. American Public Health Association (APHA). 1995. Standard methods for the examination of water and wastewater. 19th ed. APHA, Washington, DC, 1100 pp.
  5. Calbet, A. 2001. Metazooplankton grazing effect on primary production: a global comparative analysis in marine ecosystems. Limnol. Oceanogr. 46:1824-1830. https://doi.org/10.4319/lo.2001.46.7.1824
  6. 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. https://doi.org/10.1093/plankt/23.3.319
  7. 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. https://doi.org/10.3354/meps259303
  8. 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. https://doi.org/10.3354/meps127213
  9. 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. https://doi.org/10.1093/plankt/fbm016
  10. Conover, W. J. 1980. Practical nonparametric statistics. 2nd ed. John Wiley and Sons, New York, NY, 493 pp.
  11. 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. https://doi.org/10.3354/meps289117
  12. 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. https://doi.org/10.3354/meps10047
  13. Fulton, R. S. 1984. Distribution and community structure of estuarine copepods. Estuaries 7:38-50. https://doi.org/10.2307/1351955
  14. Gallienne, C. P. & Robins, D. B. 2001. Is Oithona the most important copepod in the world's oceans? J. Plankton Res. 23:1421-1432. https://doi.org/10.1093/plankt/23.12.1421
  15. 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.
  16. 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. https://doi.org/10.1016/S0925-8574(00)00122-1
  17. Hallegraeff, G. M. 1993. A review of harmful algal blooms and their apparent global increase. Phycologia 32:79-99. https://doi.org/10.2216/i0031-8884-32-2-79.1
  18. Hansen, P. J., Bjornsen, P. K. & Hansen, B. W. 1997. Zooplankton grazing and growth: scaling within the 2-2,000-${\mu}m$ body size range. Limnol. Oceanogr. 42:687-704. https://doi.org/10.4319/lo.1997.42.4.0687
  19. Holmes, R. W., Williams, P. M. & Eppley, R. W. 1967. Red water in La Jolla Bay, 1964-1966. Limnol. Oceanogr. 12:503-512. https://doi.org/10.4319/lo.1967.12.3.0503
  20. 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. https://doi.org/10.3354/meps040069
  21. 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.
  22. 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. https://doi.org/10.1016/j.hal.2005.06.006
  23. Jeong, H. J. 1999. The ecological roles of heterotrophic dinoflagellates in marine planktonic community. J. Eukaryot. Microbiol. 46:390-396. https://doi.org/10.1111/j.1550-7408.1999.tb04618.x
  24. 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. https://doi.org/10.3354/meps218077
  25. 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. https://doi.org/10.3354/meps07094
  26. 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. https://doi.org/10.1111/j.1550-7408.2003.tb00134.x
  27. 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. https://doi.org/10.1016/j.hal.2007.12.004
  28. 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. https://doi.org/10.3354/meps106173
  29. 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. https://doi.org/10.1016/j.hal.2015.06.004
  30. 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. https://doi.org/10.4490/algae.2017.32.5.30
  31. 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. https://doi.org/10.1111/j.1550-7408.1999.tb04586.x
  32. 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. https://doi.org/10.1111/j.1550-7408.2004.tb00292.x
  33. 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. https://doi.org/10.1007/s12601-010-0007-2
  34. 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. https://doi.org/10.1016/j.hal.2013.10.008
  35. 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. https://doi.org/10.1016/j.hal.2013.10.011
  36. 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.
  37. Katechakis, A. & Stibor, H. 2004. Feeding selectivities of the marine cladocerans Penilia avirostris, Podon intermedius and Evadne nordmanni. Mar. Biol. 145:529-539.
  38. 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. https://doi.org/10.1093/plankt/fbh001
  39. 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. https://doi.org/10.3354/meps280085
  40. 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. https://doi.org/10.1016/j.hal.2013.10.010
  41. 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. https://doi.org/10.11626/KJEB.2013.31.4.275
  42. 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.
  43. 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. https://doi.org/10.3354/meps267071
  44. 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.
  45. 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. https://doi.org/10.1016/j.hal.2015.08.006
  46. 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. https://doi.org/10.1016/j.hal.2014.05.003
  47. 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. https://doi.org/10.4490/algae.2017.32.8.25
  48. 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. https://doi.org/10.11626/KJEB.2013.31.3.192
  49. 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. https://doi.org/10.4490/ALGAE.2006.21.3.311
  50. 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. https://doi.org/10.1016/j.hal.2013.10.012
  51. 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.
  52. 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. https://doi.org/10.1046/j.1439-0485.2003.03816.x
  53. Sanders, R. W. & Wickham, S. A. 1993. Planktonic protozoa and metazoan: predation, food quality and population control. Mar. Microb. Food Webs 7:197-223.
  54. 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.
  55. Smayda, T. J. 1997. What is a bloom? A commentary. Limnol. Oceanogr. 42:1132-1136. https://doi.org/10.4319/lo.1997.42.5_part_2.1132
  56. 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. https://doi.org/10.1006/ecss.2000.0788
  57. Stoecker, D. K. & Capuzzo, J. M. 1990. Predation on protozoa, its importance to zooplankton. J. Plankton Res. 12:891-908. https://doi.org/10.1093/plankt/12.5.891
  58. 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. https://doi.org/10.1016/j.csr.2004.06.018
  59. Tillmann, U. 2004. Interactions between planktonic microalgae and protozoan grazers. J. Eukaryot. Microbiol. 51:156-168. https://doi.org/10.1111/j.1550-7408.2004.tb00540.x
  60. 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.
  61. Turner, J. T. 2004. The importance of small planktonic copepods and their roles in pelagic marine food webs. Zool. Stud. 43:255-266.
  62. 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. https://doi.org/10.1016/j.dsr2.2005.06.011
  63. 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. https://doi.org/10.1016/0022-0981(92)90071-H
  64. Turner, J. T. & Tester, P. A. 1997. Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs. Limnol. Oceanogr. 42:1203-1213. https://doi.org/10.4319/lo.1997.42.5_part_2.1203
  65. 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. https://doi.org/10.4319/lo.1988.33.2.0245
  66. Uye, S. 1986. Impact of copepod grazing on the red-tides flagellate Chattonella antiqua. Mar. Biol. 92:35-43. https://doi.org/10.1007/BF00392743
  67. 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. https://doi.org/10.1016/S0924-7963(97)00052-3
  68. 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. https://doi.org/10.3354/meps07518
  69. 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. https://doi.org/10.3354/ame01401
  70. 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. https://doi.org/10.1016/j.hal.2013.10.009
  71. 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. https://doi.org/10.4490/algae.2015.30.4.281
  72. 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. https://doi.org/10.1111/jeu.12002
  73. 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.
  74. Zar, J. H. 1999. Biostatistical analysis. 4th ed. Prentice Hall, Upper Saddle River, NJ, 663 pp.

피인용 문헌

  1. (Dinophyceae), one of the fastest growing dinoflagellates vol.54, pp.5, 2018, https://doi.org/10.1111/jpy.12775
  2. First report of the photosynthetic dinoflagellate Heterocapsa minima in the Pacific Ocean: morphological and genetic characterizations and the nationwide distribution in Korea vol.34, pp.1, 2017, https://doi.org/10.4490/algae.2019.34.2.28