Advertisement

Effects of duration at low temperature on asexual reproduction in polyps of the scyphozoan Nemopilema nomurai (Scyphozoa: Rhizostomeae)

Abstract

In recent decades, massive outbreaks of the giant jellyfish, Nemopilema nomurai have been appearing frequently in coastal seas of China. In the life cycle of N. nomurai, asexual reproduction by its benthic polyps may largely determine the jellyfish population size, and it was thought that asexual reproduction leading to medusae might be affected by differences in the duration at low winter temperature on different parts of the coast. To test this hypothesis, polyps were first stored at low temperature for two different durations, 5°C for either 40 or 117 days. They were then maintained at seven temperatures, (maintained at 5°C, and separately elevated to 10, 13, 16, 19, 22, 27°C) reached by raising the temperature 1°C every 2 days from 5°C, as well as a control temperature: 5°C. Polyps were fed with three frequencies (once per 5 days, once per 10 days, and unfed, prey concentration, 0.1 mgC l−1, being supplied once). The percentages of polyps strobilating, strobilation duration, ephyra and podocyst production were recorded. The results showed that longer duration at low temperature accelerated strobila formation at warmer temperature, as well as significantly enhancing podocyst production, but not for the strobilation percentage or ephyra production. Temperature had a marked influence on strobilation percentage, as well as on ephyra and podocyst production. The optimum temperature for strobilation by N. nomurai polyps ranged from 10 to 13°C. The maximum numbers of ephyrae appeared after polyps had been stored at longer low temperature then warmed to 10°C and fed once per 5 days, while the maximum production of podocysts occurred in polyps warmed to 27°C and fed once per 5 days. We conclude that longer duration at low temperature in winter, a continuous 10–13°C period in spring, and increasing food supply all accelerate the strobila formation, increase jellyfish production and are tend to increase blooms of N. nomurai medusae.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Arai, M. N., 1997. A Functional Biology of Scyphozoa. Chapman & Hall, London. 316 pp.

  2. Arai, M. N., 2009. The potential importance of podocysts to the formation of scyphozoan blooms: a review. Hydrobiologia 616: 241–246.

  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.

  4. Chen, J. K. & G. W. Ding, 1983. Effect of temperature on the strobilation of jellyfish (Rhopilema esculentum Kishinouye, Rhizostomeae). Acta Zoologica Sinica 29: 195–206 (in Chinese with English abstract).

  5. Chen, D. X., X. P. Sun, Y. X. Pu, L. C. Ba, X. Q. Niu, B. T. Li, B. L. Li, Y. Y. Chen, F. J. Zhang, G. M. Lin, C. F. Lin, Y. N. Xu, S. D. Jia, S. L. Qin, H. K. Huang & W. B., Yan. 1993. Marine Atlas of Bohai Sea Yellow Sea East China Sea: Hydrology. China Ocean Press, Beijing: 19–96.

  6. 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. Uye, L. P. Madin, R. D. Brodeur, S. H. D. Haddock, A. Malej, G. D. Parry, E. Eriksen, J. Quinones, 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.

  7. Ding, F. Y. & J. H. Cheng, 2005. The analysis on fish stock characteristics in the distribution areas of large jellyfish during summer and autumn in the East China Sea region. Marine Fisheries 27: 120–128 (in Chinese with English abstract).

  8. Ding, F. Y. & J. H. Cheng, 2007. Dynamic distribution of Stomolophus meleagris in the East China Sea Region. Journal of Fishery Sciences of China 14: 83–89 (in Chinese with English abstract).

  9. Dong, J., M. Sun, Y. Zhao, B. Wang, X. Z. Liu, X. G. Yu & C.Y. Li, 2012. Comparasion of Nemopilema nomurai and other jellyfish in reproductive biological characteristics and morphology. Oceanologia Et Limnologia Sinica 43(3): 550–555 (in Chinese with English abstract).

  10. Holst, S., 2012. Effects of climate warming on strobilation and ephyra production of North Sea scyphozoan jellyfish. Hydrobiologia 690: 127–140.

  11. IPCC, 2007. Summary for policymakers. In Solomon, S., D. Qin, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M. Tignor & H. L. Miller (eds), Climate Change 2007: The Physical Science Basis., Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change Cambridge University Press, Cambridge.

  12. Kamiyama, T., 2013. Planktonic ciliates as food for the scyphozoan Aurelia aurita (s.l.): effects on asexual reproduction of the polyp stage. Journal of Experimental Marine Biology and Ecology 445: 21–28.

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

  14. Kawahara, M., K. Ohtsu & S. Uye, 2013. Bloom or non-bloom in the giant jellyfish Nemopilema nomurai (Scyphozoa: Rhizostomeae): roles of dormant podocysts. Journal of Plankton Research 35: 213–217.

  15. Kishinouye, K., 1922. Echizenkurage (Nemopilema nomurai) DobutsugakuZasshi. Hydrobiologia 34: 343–345. (In Japanese with English abstract).

  16. Kogovšek, T., B. Bogunović & A. Malej, 2010. Recurrence of bloom-forming scyphomedusae: wavelet analysis of a 200-year time series. Hydrobiologia 645: 81–96.

  17. Liu, W.-C., W.-T. Lo, J. E. Purcell & H.-H. Chang, 2009. Effects of temperature and light intensity on asexual reproduction of the scyphozoan, Aurelia aurita (L.) in Taiwan. Hydrobiologia 616: 247–258.

  18. Lu, N., S. Jiang & J. K. Chen, 1997. Effect of temperature, salinity and light on the podocyst generation of Rhopilema esculentum Kishinouye. Fisheries Science 16: 3–8 (in Chinese with English abstract).

  19. 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 Oceanology 49: 637–643.

  20. Lynam, C. P., M. J. Attrill & M. D. Skogen, 2010. Climatic and oceanic influences on the abundance of gelatinous zooplankton in the North Sea. Journal of the Marine Biological Association of the United Kingdom 90: 1153–1159.

  21. Lynam, C. P., M. K. S. Lilley, T. Bastian, T. K. Doyle, S. E. Beggs & G. C. Hays, 2011. Have jellyfish in the Irish sea benefited from climate change and overfishing? Global Change Biology 17: 767–782.

  22. Purcell, J. E., 2005. Climate effects on jellyfish populations. Journal of the Marine Biological Association United Kingdom 85: 461–476.

  23. Purcell, J. E., 2007. Environmental effects on asexual reproduction rates of the scyphozoan, Aurelia labiata. Marine Ecology Progress Series 348: 183–196.

  24. Purcell, J. E., 2012. Jellyfish and ctenophore blooms coincide with human proliferations and environmental perturbations. Annual Review of Marine Science 4: 209–235.

  25. 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.

  26. Purcell, J. E., D. Atienza, V. Fuentes, A. Olariaga, U. Tilves, C. Colahan & J.-M. Gili, 2012. Temperature effects on asexual reproduction rates of scyphozoan species from the northwest Mediterranean Sea. Hydrobiologia 690: 169–180.

  27. 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.

  28. Russell, F. S., 1970. The Medusae of the British Isles II. Pelagic Scyphozoa with a Supplement to the First Volume on Hydromedusae. Cambridge University Press, Cambridge.

  29. Schiariti, A., A. C. Morandini, G. Jarms, R. V. G. Paes, S. Franke & H. Mianzan, 2014. Asexual reproduction strategies and blooming potential in Scyphozoa. Marine Ecology Progress Series 501: 241–253.

  30. Suchman, C. L., R. D. Brodeur, R. L. Emmett & E. A. Daly, 2012. Large medusae in surface waters of the Northern California Current: variability in relation to environmental conditions. Hydrobiologia 690: 113–125.

  31. Sun, M., J. Dong, Y. Chai & Y. L. Li, 2013. Effect of temperature and feeding frequency on asexual reproduction and polyp growth of the scyphozoan Cyanea nozakii Kishinouye. Acta Ecologica Sinica 33: 3222–3232 (in Chinese with English abstract).

  32. Sun, S., F. Zhang, C. L. Li, S. W. Wang, Z. C. Tao, Y. T. Wang, Submitted. Breeding place, population development and distribution pattern of the giant jellyfish Nemopilema nomurai (Scyphozoa: Rhizostomeae) in the Yellow Sea and East China Sea. Hydrobiologia.

  33. Thein, H., H. Ikeda & S. Uye, 2013. Ecophysiological characteristics of podocysts in Chrysaora pacifica (Goette) and Cyanea nozakii Kishinouye (Cnidaria: Scyphozoa: Semaeostomeae): effects of environmental factors on their production, dormancy and excystment. Journal of Experimental Marine Biology and Ecology 446: 151–158.

  34. 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(Suppl): 125–131.

  35. Uye, S. I., 2011. Human forcing of the copepod-fish-jellyfish triangular trophic relationship. Hydrobiologia 666: 71–83.

  36. Wang, N. & C. L. Li, 2014. The effect of temperature and food supply on the growth and ontogeny of Aurelia sp. 1 ephyrae. Hydrobiologia. doi:10.1007/s10750-014-1981-7.

  37. Wang, Y.-T., S. Sun, C.-L. Li & F. Zhang, 2012. Effect of temperature and food on asexual reproduction of the scyphozoan, Aurelia sp. 1. Oceanologia et Limnologia Sinica 43: 900–904 (in Chinese with English abstract).

  38. Wang, B., Y. B. Qi, J. Dong, Y. L. Li, W. B. Wang, Y. P. Li, M. Sun & C. Y. Liu, 2013. Dynamic distribution of Nemopilema nomurai in inshore waters of the northern Liaodong Bay, Bohai Sea. Acta Ecologica Sinica 33: 1701–1712.

  39. Wang, Y.-T., S. Zheng, S. Sun & F. Zhang, 2014. Effect of temperature and food type on asexual reproduction in Aurelia sp.1 polyps. Hydrobiologia. doi:10.1007/s10750-014-2020-4.

  40. Willcox, S., N. Moltschaniwskyj & C. Crawford, 2007. Asexual reproduction in scyphistomae of Aurelia sp.: effects of temperature and salinity in an experimental study. Journal of Experimental Marine Biology and Ecology 353: 107–114.

  41. Xu, Y. J., J. Ishizaka, H. Yamaguchi, E. Siswanto & S. Q. 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.

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

  43. 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.

  44. Zhou, M. J., Z. L. Shen & R. C. Yu, 2005. Responses of a coastal phytoplankton community to increased nutrient input from the Changjiang (Yangtze) River. Continental Shelf Research 28: 1483–1489.

  45. Zhu, Z. Y., Y. Wu, J. Zhang, J. Z. Du & G. S. Zhang, 2014. Reconstruction of anthropogenic eutrophication in the region off the Changjiang Estuary and central Yellow Sea: from decades to centuries. Continental Shelf Research 72: 152–162.

Download references

Acknowledgments

We thank Miss Zhenghua Zhang and Dr. Mengtan Liu for caring for the polyps for several days. We are grateful to the fishermen of the ship ‘Lulao Yu 2030’ for their efforts in sampling Nemopilema nomurai adults for fertilization in the field, also to the people who provided support and help in our experiments and samplings. This research was provided by National Key Fundamental Developing Project No. 2011CB403601, the Strategic Priority Research Program of the Chinese Academy of Sciences XDA11020305, and NSFC project (41230963) to S. Sun, and NSFC (40606036) to F. Zhang. Song Feng and Fang Zhang contributed equally to this work and should be considered co-first authors. We are grateful to two anonymous referees for suggesting important improvements.

Author information

Correspondence to Song Sun.

Additional information

Song Feng and Fang Zhang contributed equally to this work and should be considered co-first authors.

Guest editors: Song Sun, Xiaoxia Sun & Ian Jenkinson / Giant Jellyfish Blooms and Ecosystem Change

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Feng, S., Zhang, F., Sun, S. et al. Effects of duration at low temperature on asexual reproduction in polyps of the scyphozoan Nemopilema nomurai (Scyphozoa: Rhizostomeae). Hydrobiologia 754, 97–111 (2015). https://doi.org/10.1007/s10750-015-2173-9

Download citation

Keywords

  • Jellyfish bloom
  • Podocyst
  • Strobilation
  • Feeding frequency