Skip to main content

Advertisement

Log in

Human forcing of the copepod–fish–jellyfish triangular trophic relationship

  • COPEPODA: BIOLOGY AND ECOLOGY
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Copepods, the most abundant planktonic metazoans, constitute an intermediate trophic position between phytoplankton and higher trophic-level animals such as fish and jellyfish. Fish and jellyfish are adversaries because they often compete for prey copepods and also can be prey of each other. The classical food chain represented by phytoplankton–copepod–fish is the main process leading to efficient and sustainable production of fish as human food. At present, more than 75% of world fish stocks are fully or over exploited. On the other hand, jellyfish populations have increased world-wide, particularly in waters under significant human influences. Two such cases are seen in East Asian waters, where massive blooms of moon jellyfish (Aurelia aurita s.l.) and giant jellyfish (Nemopilema nomurai) have repeatedly occurred in recent decades, causing severe damage to local fisheries. In this article, I will review the pivotal role of copepods in marine ecosystems, particularly in the Inland Sea of Japan, where the annual fish catch per unit area is among the world’s highest. Then, I will describe an ongoing ecosystem shift from dominance by fish to dominance by jellyfish as a consequence of human forcing. Finally, I will propose to create “sato-umi”, a coastal sea with high productivity and biodiversity with wise human interaction, where copepod production would most efficiently transforms into food for humans.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Aoyama, M., S. Uye & H. Takeoka, 2005. Annual variations in the occurrence of the scyphomedusae Aurelia aurita population in Uwa Sea, western Shikoku, and their predation impact on mesozooplankton. Bulletin of Plankton Society of Japan 52: 21–25. (in Japanese with English abstract).

    Google Scholar 

  • Arai, M. N., 2001. Pelagic coelenterates and eutrophication: a review. Hydrobiologia 451: 69–87.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Azam, F., T. Fenchel, J. G. Field, J. S. Gray, L. A. Meyer-Reil & F. Thingstad, 1983. The ecological role of water-column microbes in the sea. Marine Ecology Progress Series 10: 257–263.

    Article  Google Scholar 

  • Bernard, C. & F. Rassoulzadegan, 1990. Bacteria or microflagellates as a major food source for marine ciliates: possible implications for the microzooplankton. Marine Ecology Progress Series 64: 147–155.

    Article  Google Scholar 

  • Brewer, R. H., 1978. Larval settlement behavior in the jellyfish Aurelia aurita (Linnaeus) (Scyphozoa: Semaeostomeae). Estuaries 1: 120–122.

    Article  Google Scholar 

  • Brodeur, R. D., H. Sugisaki & G. L. Hunt Jr., 2002. Increases in jellyfish biomass in the Bering Sea: implication for the ecosystem. Marine Ecology Progress Series 233: 89–103.

    Article  Google Scholar 

  • Brodeur, R. D., M. B. Decker, L. Ciannelli, J. E. Purcell, N. A. Bond, P. J. Stabeno, G. L. Hunt Jr. & E. Acuna, 2008. Rise and fall of jellyfish in the Bering Sea in relation to climate regime shifts. Progress of Oceanography 77: 103–111.

    Article  Google Scholar 

  • Chang, P. H. & A. Isobe, 2003. A numerical study on the Changjiang diluted water in the Yellow and East China Seas. Journal of Geophysical Research C 108: 3299.

    Article  Google Scholar 

  • Condon, R. H., M. B. Decker & J. E. Purcell, 2001. Effects of low dissolved oxygen on survival and asexual reproduction of scyphozoan polyps (Chrysaora quinquecirrha). Hydrobiologia 451: 89–95.

    Article  Google Scholar 

  • Cushing, D. H., 1976. Biology of fisheries in the pelagic community. In Cusing, D. H. & J. J. Walsh (eds), The Ecology of the Sea. Blackwell, Oxford: 317–340.

    Google Scholar 

  • Endo, T., 1970. On primary production in the Seto Inland Sea. Journal of Faculty of Fisheries and Animal Husbandry, Hiroshima University 9: 177–221. (in Japanese with English abstract).

    Google Scholar 

  • Graham, W. M., 2001. Numerical increase and distribution shifts of Chrysaora quinquecirrha (Desor) and Aurelia aurita (Linné) (Cnidaria: Scyphozoa) in the northern Gulf of Mexico. Hydrobiologia 451: 97–111.

    Article  Google Scholar 

  • Hardy, A. C., 1956. The Open Sea, its Natural History: The World of Plankton. Collins, London.

    Google Scholar 

  • Humborg, C., V. Ittekkot, A. Cociasu & B. Bodungen, 1997. Effects of Danube River dam on Black Sea biogeochemistry and ecosystem structure. Nature 386: 385–388.

    Article  CAS  Google Scholar 

  • Ishii, H., 2001. The influence of environmental changes upon the coastal plankton ecosystems, with special reference to mass occurrence of jellyfish. Bulletin of the Plankton Society Japan 48: 55–61. (in Japanese with English abstract).

    Google Scholar 

  • Ishii, H., T. Ohba & T. Kobayashi, 2008. Effects of low dissolved oxygen on planura settlement, polyp growth and asexual reproduction of Aurelia aurita. Plankton and Benthos Research 3(Suppl.): 107–113.

    Article  Google Scholar 

  • Kawahara, M., S. Uye, K. Ohtsu & H. Iizumi, 2006. Unusual population explosion of the giant jellyfish Nemopilema nomurai (Scyphozoa: Rhizostomeae) in East Asian waters. Marine Ecology Progress Series 307: 161–173.

    Article  Google Scholar 

  • Ketchum, B. H. (ed.), 1983. Estuaries and Enclosed Seas. Elsevier, Amsterdam.

    Google Scholar 

  • Ki, J.-S., D.-S. Hwang, K. Shin, W. D. Yoon, D. Lim, Y. S. Kang, Y. Lee & J.-S. Lee, 2008. Recent moon jelly (Aurelia sp. 1) blooms in Korean coastal waters suggest global expansion: examples inferred from mitochondrial COI and nuclear ITS-5/8S rNDA sequences. ICES Journal of Marine Science 65: 443–452.

    Article  Google Scholar 

  • Kishinouye, K., 1922. Echizen kurage (Nemopilema nomurai). Dobutsugaku Zasshi 34: 343–345. (in Japanese).

    Google Scholar 

  • Kuwabara, R., S. Sato & N. Noguchi, 1969. Ecological studies on the medusa, Aurelia aurita. 1. Distribution of Aurelia patches in the north-eastern region of Tokyo Bay in summer of 1966 and 1967. Bulletin of the Japanese Society of Scientific Fisheries 35: 156–162. (in Japanese with English abstract).

    Google Scholar 

  • Liang, D. & S. Uye, 1996a. Population dynamics and production of the planktonic copepods in a eutrophic inlet of the Inland Sea of Japan. II. Acartia omorii. Marine Biology 125: 109–117.

    Article  Google Scholar 

  • Liang, D. & S. Uye, 1996b. 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.

    Article  Google Scholar 

  • Liang, D. & S. Uye, 1997a. Seasonal reproductive biology of the egg-carrying calanoid copepod Pseudodiaptomus marinus in a eutrophic inlet of the Inland Sea of Japan. Marine Biology 128: 409–414.

    Article  Google Scholar 

  • Liang, D. & S. Uye, 1997b. Population dynamics and production of the planktonic copepods in a eutrophic inlet of the Inland Sea of Japan. IV. Pseudodiaptomus marinus, the egg-carrying calanoid. Marine Biology 128: 415–421.

    Article  Google Scholar 

  • Liang, D., S. Uye & T. Onbe, 1996. Population dynamics and production of the planktonic copepods in a eutrophic inlet of the Inland Sea of Japan. I. Centropages abdominalis. Marine Biology 124: 527–536.

    Article  Google Scholar 

  • Lin, C., J. Ning, J. Su, Y. Lin & B. Xu, 2005. Environmental changes and the responses of the ecosystem of the Yellow Sea during 1976–2000. Journal of Marine Systems 55: 223–234.

    Article  Google Scholar 

  • Lynam, C. P., S. J. Hay & A. S. Brierley, 2004. Interannual variability in abundance of North Sea jellyfish and links to the North Atlantic Oscillation. Limnology and Oceanography 49: 637–643.

    Article  Google Scholar 

  • Lynam, C. P., M. J. Gibbon, B. E. Axelsen, C. A. J. Sparks, J. Coetzee, B. G. Heywood & A. S. Brierley, 2006. Jellyfish overtake fish in a heavily fished ecosystem. Current Biology 16: R492–R493.

    Article  PubMed  CAS  Google Scholar 

  • Okaichi, T. & T. Yanagi, 1997. Sustainable Development in the Seto Inland Sea, Japan: From the Viewpoint of Fisheries. Terrapub, Tokyo.

    Google Scholar 

  • Omori, M. & M. Kitamura, 2004. Taxonomic review of three Japanese species of edible jellyfish (Schyphozoa: Rhizostomeae). Plankton Biology and Ecology 51: 36–51.

    Google Scholar 

  • Omori, M., H. Ishii & A. Fujinaga, 1995. Life history strategy of Aurelia aurita (Cnidaria, Scyphomedusae) and its impact on the zooplankton community of Tokyo Bay. ICES Journal of Marine Science 52: 597–603.

    Article  Google Scholar 

  • Pagés, F., 2001. Past and present anthropogenic factors promoting the invasion, colonization and dominance by jellyfish of a Spanish coastal lagoon. In Gelatinous Zooplankton Outbreaks: Theory and Practice. IESM Workshop Series 14, Monaco: 69–71.

  • Parsons, T. R. & C. M. Lalli, 2002. Jellyfish population explosions: Revisiting a hypothesis of possible causes. La Mer 40: 111–121.

    Google Scholar 

  • Pomeroy, L. R., 1974. The ocean’s food web, a changing paradigm. BioScience 24: 499–504.

    Article  Google Scholar 

  • Postma, H. & J. J. Zijlstra (eds), 1988. Continental Shelves. Elsevier, Amsterdam.

    Google Scholar 

  • Purcell, J. E., 2005. Climate effects on formation of jellyfish and ctenophore blooms. Journal of Marine Biological Association of the United Kingdom 85: 461–476.

    Article  Google Scholar 

  • Purcell, J. E., S. 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.

    Article  Google Scholar 

  • Rabalais, N. N. & R. E. Turner (eds), 1998. Coastal Hypoxia: Consequences for Living Resources and Ecosystems. American Geophysical Union, Washington, DC.

    Google Scholar 

  • Reizen, N. & A. Isobe, 2006. Numerical tracer experiments representing behavior of the giant jellyfish, Nemopilema nomurai, in the Yellow and East China Seas. Oceanography in Japan 15: 425–436. (in Japanese with English abstract).

    Google Scholar 

  • Rutherford Jr., L. D. & E. V. Thusen, 2005. Metabolic performance and survival of medusae in estuarine hypoxia. Marine Ecology Progress Series 294: 189–200.

    Article  Google Scholar 

  • Ryther, J. H., 1969. Photosynthesis and fish production in the sea. The production of organic matter and its conversion to higher forms of life vary throughout the world ocean. Science 166: 72–76.

    Article  PubMed  CAS  Google Scholar 

  • Sanders, R. W., D. A. Caron & U.-G. Berninger, 1992. Relationship between bacteria and heterotrophic nanoplankton in marine and fresh waters: an inter-ecosystem comparison. Marine Ecology Progress Series 86: 1–14.

    Article  Google Scholar 

  • Shimomura, T., 1959. On the unprecedented flourishing of ‘Echizen Kurage’ Stomolophus nomurai (Kishinouye), in the Tsushima Current regions in autumn, 1958. Bulletin of the Japan Sea Regional Fisheries Research Laboratory 7: 85–107. (In Japanese with English abstract).

    Google Scholar 

  • Shoji, J., R. Masuda, Y. Yamashita & M. Tanaka, 2005. Effects of low dissolved oxygen concentrations on behavior and predation rate on fish larvae by moon jellyfish Aurelia aurita and by juvenile Spanish mackerel Scomberomorus niphonius. Marine Biology 147: 863–868.

    Article  Google Scholar 

  • Takahashi, S. & S. Seiki, 2004. Long-term change of water temperature in the Seto Inland Sea. Sea and Sky 80: 11–16. (in Japanese with English abstract).

    Google Scholar 

  • Takeoka, H., 1997. Comparison of the Seto Inland Sea with other enclosed seas from around the world. In Okaichi, T. & T. Yanagi (eds), Sustainable Development in the Seto Inland Sea, Japan: From the Viewpoint of Fisheries. Terrapub, Tokyo: 223–247.

    Google Scholar 

  • Takikawa, T., J. H. Yoon & K. D. Cho, 2005. The Tsushima warm current through Tsushima Straits estimated from ferryboat ADCP data. Journal of Physical Oceanography 35: 1154–1168.

    Article  Google Scholar 

  • Tang, Q., X. Jin, J. Wang, Z. Zhuang, Y. Cui & T. Meng, 2003. Decadal-scale variations of ecosystem productivity and control mechanisms in the Bohai Sea. Fisheries Oceanography 12: 223–233.

    Article  Google Scholar 

  • Toyokawa, M., T. Furota & M. Terazaki, 2000. Life history and seasonal abundance of Aurelia aurita medusae in Tokyo Bay, Japan. Plankton Biology and Ecology 47: 48–58.

    Google Scholar 

  • Turner, J. T. & P. A. Tester, 1997. Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs. Limnology and Oceanography 42: 1203–1214.

    Article  Google Scholar 

  • Unoki, S. & M. Kishino, 1977. Average ocean condition and water exchange in Tokyo Bay. Technical Report of Physical Oceanography Laboratory, Institute of Physics and Chemistry Research 1: 1–89. (in Japanese).

  • Uotani, I., A. Izuha & K. Asai, 1978. Food habits and selective feeding of anchovy larvae (Engraulis japonicus). Bulletin of the Japanese Society of Scientific Fisheries 44: 427–434. (in Japanese with English abstract).

    Google Scholar 

  • Uye, S., 1982. Length-weight relationships of important zooplankton from the Inland Sea of Japan. Journal of Oceanographic Society of Japan 38: 149–158.

    Article  Google Scholar 

  • Uye, S., 1988. Temperature-dependent development and growth of Calanus sinicus (Copepoda: Calanoida) in the laboratory. Hydrobiologia 167(168): 285–293.

    Article  Google Scholar 

  • Uye, S., 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.

  • Uye, S., 1994. Replacement of large copepods by small ones with eutrophication of embayments: cause and consequence. Hydrobiologia 292(293): 513–519.

    Article  Google Scholar 

  • Uye, S., 2005a. Recent jellyfish bloom in the coastal waters of the East Asia: cause and consequence. Bulletin of Coastal Oceanography 43: 13–17. (in Japanese with English abstract).

    Google Scholar 

  • Uye, S., 2005b. Growth and production of planktonic copepods: a key component to support fish production. In Nagasawa, K. (ed.), Introduction to Copepodology. Tokai University Press, Tokyo: 72–85. in Japanese.

    Google Scholar 

  • Uye, S., 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(Suppl): 125–131.

    Article  Google Scholar 

  • Uye, S. & K. Sano, 1995. Seasonal reproductive biology of the small cyclopoid copepod Oithona davisae in a temperate eutrophic inlet. Marine Ecology Progress Series 118: 121–128.

    Article  Google Scholar 

  • Uye, S. & K. Sano, 1998. Seasonal variations in biomass, growth rate and production rate of the small cyclopoid copepod Oithona davisae in a temperate eutrophic inlet. Marine Ecology Progress Series 163: 37–44.

    Article  Google Scholar 

  • Uye, S. & H. Shimauchi, 2005. Population biomass, feeding, respiration and growth rates, and carbon budge of the scyphomedusa Aurelia aurita in the Inland Sea of Japan. Journal of Plankton Research 27: 237–248.

    Article  CAS  Google Scholar 

  • Uye, S. & T. Shimazu, 1997. Geographical and seasonal variations in abundance, biomass and estimated production rates of meso- and macrozooplankton in the Inland Sea of Japan. Journal of Oceanography 53: 529–538.

    Google Scholar 

  • Uye, S. & K. Takamatsu, 1990. Feeding interactions between planktonic copepods and red-tide flagellates from Japanese coastal waters. Marine Ecology Progress Series 59: 97–107.

    Article  Google Scholar 

  • Uye, S. & Y. Ueta, 2004. Recent increase of jellyfish populations and their nuisance to fisheries in the Inland Sea of Japan. Bulletin of Japanese Society of Fisheries Oceanography 68: 9–19. (in Japanese with English abstract).

    Google Scholar 

  • Uye, S., N. Nagano & H. Tamaki, 1996. Geographical and seasonal variations in abundance, biomass and estimated production rates of microzooplankton in the Inland Sea of Japan. Journal of Oceanography 52: 689–703.

    Article  Google Scholar 

  • Uye, S., N. Iwamoto, T. Ueda, H. Tamaki & K. Nakahira, 1999. Geographical variations in the trophic structure of the plankton community along a eutrophic–mesotrophic–oligotrophic transect. Fisheries Oceanography 8: 227–237.

    Article  Google Scholar 

  • Uye, S., N. Fujii & H. Takeoka, 2003. Unusual aggregations of the scyphomedusa Aurelia aurita in coastal waters along western Shikoku, Japan. Plankton Biology and Ecology 50: 17–21.

    Google Scholar 

  • Wang, B., 2006. Cultural eutrophication in the Changjiang (Yangtze River) plume: history and perspective. Estuarine Coastal and Shelf Science 69: 471–477.

    Article  Google Scholar 

  • Watanabe, T. & H. Ishii, 2001. In situ estimation of ephyrae liberated from polyps of Aurelia aurita using settling plates in Tokyo Bay, Japan. Hydrobiologia 451: 247–258.

    Article  Google Scholar 

  • Yanagi, T., 2007. Sato-Umi: A New Concept for Coastal Sea Management. Terrapub, Tokyo.

    Google Scholar 

  • Yasuda, T., 2004. On the unusual occurrence of the giant medusa Nemopilema nomurai in Japanese waters. Nippon Suisan Gakkaishi 70: 380–386. (in Japanese).

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Zaitsev, Y. P., 1992. Recent changes in the trophic structure of the Black Sea. Fisheries Oceanography 2: 108–189.

    Google Scholar 

Download references

Acknowledgments

I entered the world of copepodology (e.g., on copepod resting eggs) by guidance of Dr. T. Onbe when I was a senior of Hiroshima University, and was enabled to widen my interest in biological oceanography (e.g., copepod production ecology) by advice of late Drs. A. Fleminger and M. M. Mullin when I was a visiting student at Scripps Institution of Oceanography. Since I became a faculty member of Hiroshima University, so many people have supported my work. I thank the captain and crew of the T&R/V Toyoshio Maru, Hiroshima University, for their tireless support at sea. My gratitude is extended to staff and students of my laboratory for assistance and collaboration. My jellyfish study was partially supported by research grants from the Japan Society for the Promotion of Science and from the Ministry of Agriculture, Forestry and Fisheries. This article was presented as Maxilliped Lecture at the 10th International Conference on Copepoda in Pattaya, Thailand, July 2008. English of the early manuscript was edited by Sea Pen Scientific Writing, LLC. Constructive comments from three anonymous reviewers are greatly appreciated.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shin-ichi Uye.

Additional information

Guest editors: L. Sanoamuang & J. S. Hwang / Copepoda: Biology and Ecology

Electronic supplementary material

Below is the link to the electronic supplementary material.

10750_2010_208_MOESM1_ESM.pdf

Appendix 1. Bird-eye view of white carpet-like aggregation of Aurelia aurita in Uwa Sea, western Shikoku, in August, 2000 (from Uye et al., 2003) (111 kb)

10750_2010_208_MOESM2_ESM.pdf

Appendix 2. Medusae of Nemopilema nomurai trapped in a set-net in Iwate Prefecture in December, 2005 (from Uye, 2008) (857 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Uye, Si. Human forcing of the copepod–fish–jellyfish triangular trophic relationship. Hydrobiologia 666, 71–83 (2011). https://doi.org/10.1007/s10750-010-0208-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-010-0208-9

Keywords

Navigation