Hydrobiologia

, Volume 754, Issue 1, pp 43–58 | Cite as

Distribution pattern of zooplankton functional groups in the Yellow Sea in June: a possible cause for geographical separation of giant jellyfish species

  • Yong-Qiang Shi
  • Song Sun
  • Guang-Tao Zhang
  • Shi-Wei Wang
  • Chao-Lun Li
CHINA JELLYFISH PROJECT
First Online:
Received:
Revised:
Accepted:

Abstract

Because jellyfish are sensitive to the availability of prey, their distribution likely is linked to the distribution pattern of zooplankton functional groups. We studied the regional and interannual variations of zooplankton functional groups in the Yellow Sea using data from six cruises conducted in June between 2000 and 2009. We compared these data to previously collected data on giant jellyfish distribution and biomass. Our results indicate that different zooplankton functional groups have their own relatively fixed distribution patterns and that the distribution of zooplankton can affect the distribution of the jellyfish community. Giant crustaceans and large copepods were found to be mainly distributed offshore, small copepods and small jellyfish tended to be located in the coastal region, and chaetognaths were mainly sampled along the 50 m isobath. Sea bottom temperature and salinity, determined by the Yellow Sea Cold Water Mass, are shown to have been major factors affecting the distribution of zooplankton functional groups. Among zooplankton functional groups, small copepods and giant jellyfish show similar distribution patterns, suggesting that the abundance of small copepods is feeding that of giant jellyfish. The observed interannual biomass of small copepod was positively related to temperature, and we suggest that this relationship may explain the rarity of giant jellyfish outbreaks in cold years.

Keywords

Zooplankton Functional groups Jellyfish Yellow Sea Cold Water Mass Distribution 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

We greatly thank Dr. D. Huang and Dr. H. Wei for contributing CTD data, and Dr. F. Zhang for providing giant jellyfish data. We are grateful to the captain and crew of the RV “Beidou” for their efforts in the field, P. Ji and other people who provided support during our sampling efforts, and B. Yang for identification of zooplankton. This study was supported by the State Key Program of National Natural Science Foundation of China (41230963), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA11020305), the National Basic Research Program of China (2011CB403601), the National Public S&T Research Funds Projects of the Ocean (201005018), and the National Natural Science Foundation of China (41306155).

References

  1. Andersen, V., 1985. Filtration and ingestion rates of Salpa fusiformis Cuvier (Tunicata: Thaliacea): effects of size, individual weight and algal concentration. Journal of Experimental Marine Biology and Ecology 87: 13–29.CrossRefGoogle Scholar
  2. Anon, 1977. Study on plankton in China Seas. In Anon, (ed.), Scientific Reports of ‘Comprehensive Oceanography Expedition in China Seas’, Vol. 8. Ocean Research Office Press, Tianjin: 1–159. (in Chinese).Google Scholar
  3. Attrill, M. J., J. Wright & M. Edwards, 2007. Climate-related increases in jellyfish frequency suggest a more gelatinous future for the North Sea. Limnology and Oceanography 52: 480–485.CrossRefGoogle Scholar
  4. Bai, H., D. X. Hu, Y. L. Chen & Q. Y. Wang, 2004. Statistic characteristics of thermal structure in the southern Yellow Sea in summer. Chinese Journal of Oceanology and Limnology 22: 237–243.CrossRefGoogle Scholar
  5. Brodeur, R. D., C. E. Mills, J. E. Overland, G. E. Walters & J. D. Schumacher, 1999. Evidence for a substantial increase in gelatinous zooplankton in the Bering Sea, with possible links to climate change. Fisheries Oceanography 8: 296–306.CrossRefGoogle Scholar
  6. Brodeur, R. D., M. B. Decker, L. Ciannelli, J. E. Purcell, N. A. Bond, P. J. Stabeno, E. Acuna & G. L. Hunt Jr, 2008. Rise and fall of jellyfish in the eastern Bering Sea in relation to climate regime shifts. Progress in Oceanography 77: 103–111.CrossRefGoogle Scholar
  7. Brotz, L., W. W. Cheung, K. Kleisner, E. Pakhomov & D. Pauly, 2012. Increasing jellyfish populations: trends in Large Marine Ecosystems. Hydrobiologia 690: 3–20.CrossRefGoogle Scholar
  8. Chae, J., H. W. Choi, W. J. Lee, D. Kim & J. H. Lee, 2008. Distribution of a pelagic tunicate, Salpa fusiformis in warm surface current of the eastern Korean waters and its impingement on cooling water intakes of Uljin nuclear power plant. Journal of Environmental Biology 29: 585–590.PubMedGoogle Scholar
  9. Chen, Q. C. & S. Z. Zhang, 1965. The planktonic copepods of the Yellow Sea and the East China Sea. I. Calanoida. Studia Marina Sinica 7: 20–131. (In Chinese, with English Abstr.).Google Scholar
  10. Chen, Q. C., S. Z. Zhang & C. S. Zhu, 1974. On planktonic copepods of the Yellow Sea and the East China Sea. II. Cyclopoida and Harpacticoida. Studia Marina Sinica 9: 27–100. (In Chinese, with English Abstr.).Google Scholar
  11. Chiaverano, L. M., B. S. Holland, G. L. Crow, L. Blair & A. A. Yanagihara, 2013. Long-Term fluctuations in circalunar Beach aggregations of the box jellyfish Alatina moseri in Hawaii, with links to environmental variability. PLoS One 8: e77039.CrossRefPubMedCentralPubMedGoogle Scholar
  12. Condon, R. H., C. M. Duarte, K. A. Pitt, K. L. Robinson, C. H. Lucas, K. R. Sutherland, H. W. Mianzan, M. Bogeberg, J. E. Purcell, M. B. Decker, S. I. Uye, L. P. Madin, R. D. Brodeur, S. H. D. Haddock, A. Malej, G. D. Parry, E. Eriksen, J. Quiñones, M. Acha, M. Harvey, J. M. Arthur & W. M. Graham, 2013. Recurrent jellyfish blooms are a consequence of global oscillations. Proceedings of the National Academy of Sciences of the United States of America 110: 1000–1005.Google Scholar
  13. Dong, Z. J., D. Y. Liu & J. K. Keesing, 2010. Jellyfish blooms in China: dominant species, causes and consequences. Marine Pollution Bulletin 60: 954–963.CrossRefPubMedGoogle Scholar
  14. Endo, Y. & F. Yamano, 2006. Diel vertical migration of Euphausia pacifica (Crustacea, Euphausiacea) in relation to molt and reproductive processes, and feeding activity. Journal of Oceanography 62: 693–703.CrossRefGoogle Scholar
  15. Gómez-Gutiérrez, J., L. R. Feinberg, T. C. Shaw & W. T. Peterson, 2007. Interannual and geographical variability of the brood size of the euphausiids Euphausia pacifica and Thysanoessa spinifera along the Oregon coast (1999–2004). Deep-Sea Research Part I 54: 2145–2169.CrossRefGoogle Scholar
  16. Gibbons, M. J. & A. J. Richardson, 2009. Patterns of jellyfish abundance in the North Atlantic. Hydrobiologia 616: 51–65.CrossRefGoogle Scholar
  17. Hopcroft, R. R., J. C. Roff & F. P. Chavez, 2001. Size paradigms in copepod communities: a re-examination. Hydrobiologia 453(454): 133–141.CrossRefGoogle Scholar
  18. Hu, D. X. & Q. Y. Wang, 2004. Interannual variability of the southern Yellow Sea Cold Water Mass. Chinese Journal of Oceanology and Limnology 22: 231–236.CrossRefGoogle Scholar
  19. Huang, C., S. I. Uye & T. Onbé, 1993. Geographic distribution, seasonal life cycle, biomass and production of a planktonic copepod Calanus sinicus in the Inland Sea of Japan and its neighboring Pacific Ocean. Journal of Plankton Research 15: 1229–1246.CrossRefGoogle Scholar
  20. Huang, J. Q. & Z. Zheng, 1986. The effects of temperature and salinity on the survival of some copepods from Xiamen Harbour. Oceanologia et Limnologia Sinica 17: 161–167. (In Chinese, with English Abstr.).Google Scholar
  21. Iguchi, N. & T. Ikeda, 1994. Experimental study on brood size, egg hatchability and early development of a Euphausiid Euphausia pacifica from Toyama Bay, Southern Japan Sea. Bulletin Japan Sea National Fishery Research Institute 44: 49–57.Google Scholar
  22. Iguchi, N. & T. Ikeda, 1995. Growth, metabolism and growth efficiency of a euphausiid crustacean Euphausia pacifica in the southern Japan Sea, as influenced by temperature. Journal of Plankton Research 17: 1757–1769.CrossRefGoogle Scholar
  23. Jin, X. S., X. J. Shan, X. S. Li, J. Wang, Y. Cui & T. Zuo, 2013. Long-term changes in the fishery ecosystem structure of Laizhou Bay, China. Science China Earth Sciences 56: 366–374.CrossRefGoogle Scholar
  24. Kang, J. H. & W. S. Kim, 2008. Spring dominant copepods and their distribution pattern in the Yellow Sea. Ocean Science Journal 43: 67–79.CrossRefGoogle Scholar
  25. Kang, J. H., W. S. Kim, H. J. Jeong, K. Shin & M. Chang, 2007. Why did the copepod Calanus sinicus increase during the 1990s in the Yellow Sea? Marine Environmental Research 63: 82–90.CrossRefPubMedGoogle Scholar
  26. Li, C. L., S. Sun, R. Wang & X. Wang, 2004. Feeding and respiration rates of a planktonic copepod (Calanus sinicus) oversummering in Yellow Sea Cold Bottom Waters. Marine Biology 145: 149–157.CrossRefGoogle Scholar
  27. Li, S. J., 1963. Studies on the comparative morphology of Calanus pacificus off Fukien coast. Journal of Xiamen University (Natural Science) 10: 57–81. (In Chinese, with English Abstr.).Google Scholar
  28. Liang, D. & S. I. Uye, 1996. Population dynamics and production of the planktonic copepods in a eutrophic inlet of the Inland Sea of Japan. III. Paracalanus sp. Marine Biology 127: 219–227.CrossRefGoogle Scholar
  29. Liu, H. L. & S. Sun, 2010. Diel vertical distribution and migration of a euphausiid Euphausia pacifica in the Southern Yellow Sea. Deep-Sea Research Part II 57: 594–605.CrossRefGoogle Scholar
  30. Liu, Y. Q., S. Sun & G. T. Zhang, 2012. Seasonal variation in abundance, diel vertical migration and body size of pelagic tunicate Salpa fusiformis in the Southern Yellow Sea. Chinese Journal of Oceanology and Limnology 30: 92–104.CrossRefGoogle Scholar
  31. Mann, K. H., 1993. Physical oceanography, food chains, and fish stocks: a review. ICES Journal of Marine Science 50: 105–119.CrossRefGoogle Scholar
  32. Miglietta, M. P., M. Rossi & R. Collin, 2008. Hydromedusa blooms and upwelling events in the Bay of Panama, Tropical East Pacific. Journal of Plankton Research 30: 783–793.CrossRefGoogle Scholar
  33. Mills, C. E., 2001. Jellyfish blooms: are populations increasing globally in response to changing ocean conditions? Hydrobiologia 451: 55–68.CrossRefGoogle Scholar
  34. Nagasawa, S., 1984. Laboratory feeding and egg production in the Chaetognath Sagitta crassa Tokioka. Journal of Experimental Marine Biology and Ecology 76: 51–65.CrossRefGoogle Scholar
  35. Nagasawa, S. & R. Marumo, 1972. Feeding of a pelagic chaetognath, Sagitta nagae Alvariño in Suruga Bay, central Japan. Journal of the Oceanographical Society of Japan 28: 181–186.CrossRefGoogle Scholar
  36. Nagasawa, S. & R. Marumo, 1978. Reproduction and life history of the Chaetognath Sagitta nagae Alvariño in Suruga Bay. Bulletin of the Plankton Society of Japan 25: 67–84. (In Japanese, with English Abstr.).Google Scholar
  37. Nagasawa, S. & R. Marumo, 1984. Feeding habits and copulation of the chaetognath Sagitta crassa. La mer 22: 8–14.Google Scholar
  38. Nomura, H., K. Aihara & T. Ishimaru, 2007. Feeding of the chaetognath Sagitta crassa Tokioka in heavily eutrophicated Tokyo Bay, Japan. Plankton and Benthos Research 2: 120–127.CrossRefGoogle Scholar
  39. Olesen, N. J., 1995. Clearance potential of jellyfish Aurelia aurita, and predation impact on zooplankton in a shallow cove. Marine Ecology Progress Series 124: 63–72.CrossRefGoogle Scholar
  40. Omori, M., 1969. Weight and chemical composition of some important oceanic zooplankton in the North Pacific Ocean. Marine Biology 3: 4–10.CrossRefGoogle Scholar
  41. Park, S., P. C. Chu & J. H. Lee, 2011. Interannual-to-interdecadal variability of the Yellow Sea Cold Water Mass in 1967–2008: characteristics and seasonal forcings. Journal of Marine Systems 87: 177–193.CrossRefGoogle Scholar
  42. Pinchuk, A. I. & R. R. Hopcroft, 2006. Egg production and early development of Thysanoessa inermis and Euphausia pacifica (Crustacea: Euphausiacea) in the northern Gulf of Alaska. Journal of Experimental Marine Biology and Ecology 332: 206–215.CrossRefGoogle Scholar
  43. Pinchuk, A. I. & R. R. Hopcroft, 2007. Seasonal variations in the growth rates of euphausiids (Thysanoessa inermis, T. spinifera, and Euphausia pacifica) from the northern Gulf of Alaska. Marine Biology 151: 257–269.CrossRefGoogle Scholar
  44. Pu, X. M., S. Sun, B. Yang, G. T. Zhang & F. Zhang, 2004. Life history strategies of Calanus sinicus in the southern Yellow Sea in summer. Journal of Plankton Research 26: 1059–1068.CrossRefGoogle Scholar
  45. Purcell, J. E., 2003. Predation on zooplankton by large jellyfish, Aurelia labiata, Cyanea capillata and Aequorea aequorea, in Prince William Sound, Alaska. Marine Ecology Progress Series 246: 137–152.CrossRefGoogle Scholar
  46. Purcell, J. E., 2005. Climate effects on formation of jellyfish and ctenophore blooms: a review. Journal of the Marine Biological Association of the United Kingdom 85: 461–476.CrossRefGoogle Scholar
  47. Purcell, J. E., S. I. Uye & W. T. Lo, 2007. Anthropogenic causes of jellyfish blooms and their direct consequences for humans: a review. Marine Ecology Progress Series 350: 153–174.CrossRefGoogle Scholar
  48. Richardson, A. J., A. Bakun, G. C. Hays & M. J. Gibbons, 2009. The jellyfish joyride: causes, consequences and management responses to a more gelatinous future. Trends in Ecology & Evolution 24: 312–322.CrossRefGoogle Scholar
  49. Riisgård, H. U., C. Barth-Jensen & C. V. Madsen, 2010. High abundance of the jellyfish Aurelia aurita excludes the invasive ctenophore Mnemiopsis leidyi to establish in a shallow cove (Kertinge Nor, Denmark). Aquatic Invasions 5: 347–356.CrossRefGoogle Scholar
  50. Riisgård, H. U., C. V. Madsen, C. Barth-Jensen & J. E. Purcell, 2012. Population dynamics and zooplankton-predation impact of the indigenous scyphozoan Aurelia aurita and the invasive ctenophore Mnemiopsis leidyi in Limfjorden (Denmark). Aquatic Invasions 7: 147–162.CrossRefGoogle Scholar
  51. Rose, K., J. C. Roff & R. R. Hopcroft, 2004. Production of Penilia avirostris in Kingston Harbour, Jamaica. Journal of Plankton Research 26: 605–615.CrossRefGoogle Scholar
  52. Sørnes, T. A., D. L. Aksnes, U. Båmstedt & M. J. Youngbluth, 2007. Causes for mass occurrences of the jellyfish Periphylla periphylla: a hypothesis that involves optically conditioned retention. Journal of Plankton Research 29: 157–167.CrossRefGoogle Scholar
  53. Su, Y. S. & X. C. Weng, 1994. Water masses in China seas. In Zhou, D., Y. B. Liang & C. K. Zeng (eds), Oceanology of China Seas, Vol. 1. Kluwer Academic, Dordrecht/Boston/London: 3–16.Google Scholar
  54. Sun, S., Y. Z. Huo & B. Yang, 2010. Zooplankton functional groups on the continental shelf of the yellow sea. Deep-Sea Research Part II 57: 1006–1016.CrossRefGoogle Scholar
  55. Sun, S., Z. C. Tao, C. L. Li & H. L. Liu, 2011. Spatial distribution and population structure of Euphausia pacifica in the Yellow Sea (2006–2007). Journal of Plankton Research 33: 873–889.CrossRefGoogle Scholar
  56. Turner, J. T., 2004. The importance of small planktonic copepods and their roles in pelagic marine food webs. Zoological Studies 43: 255–266.Google Scholar
  57. Uye, S. I., 1982. Length-weight relationships of important zooplankton from the Inland Sea of Japan. Journal of the Oceanographical Society of Japan 38: 149–158.CrossRefGoogle Scholar
  58. Uye, S. I., 1988. Temperature-dependent development and growth of Calanus sinicus (Copepoda: Calanoida) in the laboratory. Hydrobiologia 167(168): 285–293.CrossRefGoogle Scholar
  59. Uye, S. I., 1991. Temperature-dependent development and growth of the planktonic copepod Paracalanus sp. in the laboratory. Bulletin of the Plankton Society of Japan Special Volume: 627–636.Google Scholar
  60. Uye, S. I., 2000. Why does Calanus sinicus prosper in the shelf ecosystem of the Northwest Pacific Ocean? ICES Journal of Marine Science 57: 1850–1855.CrossRefGoogle Scholar
  61. Uye, S. I., 2008. Blooms of the giant jellyfish Nemopilema nomurai: a threat to the fisheries sustainability of the East Asian Marginal Seas. Plankton and Benthos Research 3: 125–131.CrossRefGoogle Scholar
  62. Uye, S. I. & S. Ichino, 1995. Seasonal variations in abundance, size composition, biomass and production rate of Oikopleura dioica (Fol) (Tunicata: Appendicularia) in a temperate eutrophic inlet. Journal of Experimental Marine Biology and Ecology 189: 1–11.CrossRefGoogle Scholar
  63. Uye, S. I. & N. Shibuno, 1992. Reproductive biology of the planktonic copepod Paracalanus sp. in the Inland Sea of Japan. Journal of Plankton Research 14: 343–358.CrossRefGoogle Scholar
  64. Wang, R. & K. Wang, 2003. Field test of capture capabilities of two plankton nets. Journal of Fisheries of China 27: 98–102. (In Chinese, with English Abstr.).Google Scholar
  65. Wang, R. & T. Zuo, 2004. The Yellow Sea Warm Current and the Yellow Sea Cold Bottom Water, their impact on the distribution of zooplankton in the southern Yellow Sea. Journal of the Korean Society of Oceanography 39: 1–13.Google Scholar
  66. Wang, R., T. Zuo & K. Wang, 2003. The Yellow Sea Cold Bottom Water—an oversummering site for Calanus sinicus (Copepoda, Crustacea). Journal of Plankton Research 25: 169–183.CrossRefGoogle Scholar
  67. Wang, S. W., C. L. Li, S. Sun, X. R. Ning & W. C. Zhang, 2009. Spring and autumn reproduction of Calanus sinicus in the Yellow Sea. Marine Ecology Progress Series 379: 123–133.CrossRefGoogle Scholar
  68. Xu, Y., J. Ishizaka, H. Yamaguchi, E. Siswanto & S. Wang, 2013. Relationships of interannual variability in SST and phytoplankton blooms with giant jellyfish (Nemopilema nomurai) outbreaks in the Yellow Sea and East China Sea. Journal of Oceanography 69: 511–526.CrossRefGoogle Scholar
  69. Yan, L. P., S. F. Li & F. Y. Ding, 2004. The preliminary studies on the dynamics of macro-jellyfish resources and their relationship with fisheries in the East China Sea and Yellow Sea. Marine Fisheries 26: 9–12. (In Chinese, with English Abstr.).Google Scholar
  70. Yoon, W. D., J. Y. Yang, M. B. Shim & H. K. Kang, 2008. Physical processes influencing the occurrence of the giant jellyfish Nemopilema nomurai (Scyphozoa: Rhizostomeae) around Jeju Island, Korea. Journal of Plankton Research 30: 251–260.CrossRefGoogle Scholar
  71. Yu, F., Z. X. Zhang, X. Y. Diao, J. S. Guo & Y. X. Tang, 2006. Analysis of evolution of the Huanghai Sea Cold Water Mass and its relationship with adjacent water masses. Acta Oceanologica Sinica 28: 26–34. (In Chinese, with English Abstr.).Google Scholar
  72. Zhang, B., Q. S. Tang & X. S. Jin, 2007. Decadal-scale variations of trophic levels at high trophic levels in the Yellow Sea and the Bohai Sea ecosystem. Journal of Marine Systems 67: 304–311.CrossRefGoogle Scholar
  73. Zhang, F., S. Sun, X. S. Jin & C. L. Li, 2012. Associations of large jellyfish distributions with temperature and salinity in the Yellow Sea and East China Sea. Hydrobiologia 690: 81–96.CrossRefGoogle Scholar
  74. Zhang, G. T., S. Sun & F. Zhang, 2005. Seasonal variation of reproduction rates and body size of Calanus sinicus in the Southern Yellow Sea, China. Journal of Plankton Research 27: 135–143.CrossRefGoogle Scholar
  75. Zhang, Q. L., X. C. Weng & Y. L. Yang, 1996. Analysis of water masses in the south Yellow Sea in spring. Oceanologia et Limnologia Sinica 27: 421–428. (In Chinese, with English Abstr.).Google Scholar
  76. Zheng, Z., S. Q. Li & Z. Z. Xu, 1984. Marine Planktology. China Ocean Press, Beijing. (In Chinese).Google Scholar
  77. Zuo, T., K. Wang & C. L. Li, 2003. Length-dry weight relationship of Calanus sinicus in the southern part of the Yellow Sea. Journal of Fisheries of China 27: 103–107. (In Chinese, with English Abstr.).Google Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Yong-Qiang Shi
    • 1
    • 2
  • Song Sun
    • 1
    • 3
  • Guang-Tao Zhang
    • 3
  • Shi-Wei Wang
    • 3
  • Chao-Lun Li
    • 1
  1. 1.Key Laboratory of Marine Ecology and Environmental Sciences, Institute of OceanologyChinese Academy of SciencesQingdaoPeople’s Republic of China
  2. 2.University of Chinese Academy of SciencesBeijingPeople’s Republic of China
  3. 3.Jiaozhou Bay Marine Ecosystem Research StationChinese Ecosystem Research NetworkQingdaoPeople’s Republic of China

Personalised recommendations