Skip to main content
SpringerLink
Log in

Effects of low salinity on the physiological ecology of planulae and polyps of scyphozoans in the East Asian Marginal Seas: potential impacts of monsoon rainfall on medusa population size

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Salinity is hypothesized to influence the abundance of scyphozoan medusae in the East Asian Marginal Seas, as their spawning largely coincides with the summer monsoon season, and extreme rainfalls subject planulae to reduced salinity, presumably jeopardizing the recruitment of polyps. We examined the effects of different salinities (5, 10, 15, 20, 25, and 32) on body size, swimming speed, survivorship and settlement of planulae, and subsequent development of metamorphosed polyps of three bloom-forming scyphozoans: Chrysaora pacifica, Nemopilema nomurai, and Rhopilema esculentum. Their physiology and behaviors were affected by osmotic stress, but differed by species. At 5, planulae of all species died. At 10, C. pacifica could not settle but survived as plankton, whereas N. nomurai and R. esculentum could settle and develop into four-tentacle polyps, yet the former showing delayed development and tentacle abnormalities. The lowest salinities permitting normal recruitment of polyps were 10, 15, and 20 for R. esculentum, N. nomurai, and C. pacifica, respectively. Inter-annual variations in monsoon rainfall can alter hydrographic conditions in the polyp habitats, affecting medusa population sizes in the following year. The robustness to low salinity of R. esculentum and N. nomurai larvae may enable them to establish yet-to-be-identified polyp populations in brackish-water environments.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arai, M. N., 1997. A Functional Biology of Scyphozoa. Chapman & Hall, London.

    Google Scholar 

  • Bayha, K. M. & W. M. Graham, 2014. Nonindigenous marine jellyfish: invasiveness, invisibility, and impacts. In Pitt, K. P. & C. H. Lucas (eds), Jellyfish Blooms. Springer, Dordrecht: 45–77.

    Chapter  Google Scholar 

  • Boero, F., L. Brotz, M. J. Gibbons, A. Piraino & S. Zampardi, 2016. Impacts and effects of ocean warming on jellyfish. In Laffoley, D. & J. M. Baxter (eds), Explaining Ocean Qarming: Causes, Scale, Effects and Consequences. Full report. IUCN, Gland: 213–237.

    Google Scholar 

  • Brewer, R. H., 1976. Larval settling behavior in Cyanea capillata (Cnidaria: Scyphozoa). Biological Bulletin 150: 183–199.

    Article  Google Scholar 

  • Brotz, L., 2016. Jellyfish fisheries—a global assessment. In Pauly, D. & D. Zeller (eds), Global Atlas of Marine Fisheries: A Critical Appraisal of Catches and Ecosystem Impacts. Island Press, Washington, DC: 110–124.

    Google Scholar 

  • Brotz, L., W. W. L. Cheung, K. Kleisner, E. Pakhomov & D. Pauly, 2012. Increasing jellyfish populations: trends in large marine ecosystems. Hydrobiologia 690: 3–20.

    Article  Google Scholar 

  • Calder, D. R., 1982. Life history of the cannonball jellyfish, Stomolophus meleagris L. Agassiz, 1860 (Scyphozoa, Rhizostomida). Biological Bulletin 162: 149–162.

    Article  Google Scholar 

  • Cargo, D. G., 1979. Observations on the settling behavior of planular larvae of Chrysaora quinquecirrha. International Journal of Invertebrate Reproduction 1: 279–287.

    Article  Google Scholar 

  • Cartwright, P., S. L. Halgedahl, J. R. Hendricks, R. D. Jarrard, A. C. Marques, A. G. Collins & B. S. Lieberman, 2007. Exceptionally preserved jellyfishes from the Middle Cambrian. PLoS ONE 2: e1121.

    Article  PubMed Central  PubMed  Google Scholar 

  • Chen, T.-C., S.-Y. Wang, W.-R. Huang & M.-C. Yen, 2004. Variation of the East Asian summer monsoon rainfall. Journal of Climate 17: 744–762.

    Article  Google Scholar 

  • 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. Majej, 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 Science of the United States of America 110: 1000–1005.

  • Conley, K. & S. Uye, 2015. Effects of hyposalinity on survival and settlement of moon jellyfish (Aurelia aurita) planulae. Journal of Experimental Marine Biology and Ecology 462: 14–19.

    Article  CAS  Google Scholar 

  • Dawson, M. N., 2003. Macro-morphological variation among cryptic species of the moon jellyfish, Aurelia (Cnidaria: Scyphozoa). Marine Biology 143: 369–379.

    Article  Google Scholar 

  • Ding, Y. & J. C. L. Chan, 2005. The East Asian summer monsoon: an overview. Meteorology & Atmospheric Physics 89: 117–142.

    Article  Google Scholar 

  • Dolmer, P. & I. Suane, 1993. Settlement pattern of the scyphozoan Cyanea capllata (L.). Effects of established scyphistomae and water flow. Ophelia 38: 117–126.

    Article  Google Scholar 

  • Dong, J., B. Wang, Y. Duan, W.-D. Yoon, A. Wang, X. Liu, Y. Li, M. Sun & Y. Chai, 2017. Initial occurrence, ontogenetic distribution-shifts and advection of Nemopilema nomurai (Scyphozoa: Rhizostomeae) in Liaodong Bay, China, from 2005–2015. Marine Ecology Progress Series. https://doi.org/10.3354/meps12272.

    Google Scholar 

  • Dong, Z., D. Liu & J. K. Keesing, 2014. Contrasting trends in populations of Rhopilema exculentum and Aurelia aurita in Chinese waters. In Pitt, K. A. & C. H. Lucas (eds), Jellyfish Blooms. Springer, Dordrecht: 207–218.

    Chapter  Google Scholar 

  • Duarte, C. M., K. Pitt, C. Lucas, J. E. Purcell, S. Uye, K. Robinson, L. Brotz, M. B. Decker, K. R. Sutherland, A. Malej, L. Madin, H. Mianzan, J. M. Gili, V. Fuentes, D. Atienza, F. Pagés, D. Breitburg, J. Malek, W. M. Graham & R. Condon, 2012. Is global ocean sprawl a cause of jellyfish blooms? Frontier in Ecology and the Environment 11: 91–97.

    Article  Google Scholar 

  • Feng, S., J. Lin, S. Sun, F. Zhang & C. Li, 2017a. Hyposalinity and incremental micro-zooplankton supply in early-developed Nemopilema nomurai polyp survival, growth, and podocyst reproduction. Marine Ecology Progress Series. https://doi.org/10.3354/meps12204.

    Google Scholar 

  • Feng, S., S. W. Wang, S. Sun, F. Zhang, G. T. Zhang, M. T. Liu & S. Uye, 2017b. Strobilation of three scyphozoans (Aurelia coerulea, Nemopilema nomurai and Rhopilema esculentum) in the field at Jiaozhou Bay, China. Marine Ecology Progress Series. https://doi.org/10.3354/meps12276.

    Google Scholar 

  • Gambill, M., S. L. McNaughton, M. Kreus & M. A. Peck, 2018. Temperature-dependent settlement of planula larvae of two scyphozoan jellyfish from the North Sea. Estuarine and Coastal Shelf Science 201: 64–71.

    Article  Google Scholar 

  • Graham, W. M., S. Gelcich, K. L. Robinson, C. M. Duarte, L. Brotz, J. E. Purcell, L. P. Madin, H. Mianzan, K. R. Sutherland, S. Uye, K. A. Pitt, C. H. Lucas, M. Bøgeberg, R. D. Brodeur & R. H. Condon, 2014. Linking human well-being and jellyfish: ecosystem services, impacts, and societal responses. Frontier in Ecology and the Environment 12: 515–523.

    Article  Google Scholar 

  • Gröndahl, F., 1989. Evidence of gregarious settlement of planula larvae of the scyphozoan Aurelia aurita: an experimental study. Marine Ecology Progress Series 56: 87–93.

    Article  Google Scholar 

  • Guo, X. & T. Yanagi, 1998. Three-dimensional structure of tidal current in the East China Sea and the Yellow Sea. Journal of Oceanography 54: 651–668.

    Article  Google Scholar 

  • Hagadorn, J. W., R. H. Dott & D. Damrow, 2002. Stranded on a Late Cambrian shoreline: medusae from central Wisconsin. Geology 30: 147–150.

    Article  Google Scholar 

  • Halpern, B. S., S. Walbridge, K. A. Selkoe, C. V. Kappel, F. Micheli, C. D’Agrosa, J. F. Bruno, K. S. Casey, C. Ebert, H. E. Fox, R. Fujita, D. Heinemann, H. S. Lenihan, E. M. P. Madin, M. T. Perry, E. R. Selig, M. Spalding, R. Steneck & R. Watson, 2008. A global map of human impact on marine ecosystems. Science 319: 948–952.

    Article  CAS  PubMed  Google Scholar 

  • Holst, S. & G. Jarms, 2007. Substrate choice and settlement preferences of planula larvae of five Scyphozoa (Cnidaria) from German Bight, North Sea. Marine Biology 151: 863–871.

    Article  Google Scholar 

  • Holst, S. & G. Jarms, 2010. Effect of low salinity on settlement and strobilation of scyphozoan (Cnidaria): is the lion’s mane Cyanea capillata (L.) able to reproduce in the brackish Baltic Bea? Hydrobiologia 645: 53–68.

    Article  CAS  Google Scholar 

  • Hsieh, Y.-H. P., F.-M. Leong & J. Rudloe, 2001. Jellyfish as food. Hydrobiologia 451: 11–17.

    Article  Google Scholar 

  • Ikeda, H., K. Ohtsu & S. Uye, 2011. Structural changes of gonads during artificially induced gamatogenesis and spawning in the giant jellyfish Nemopilema nomurai (Schphozoa: Rhizostomeae). Journal of Marine Biological Association of the United Kingdom 91: 215–227.

    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 

  • Keen, S. L., 1987. Recruitment of Aurelia aurita (Cnidaria: Scyhozoa) larvae is position-dependent, and independent of conspecific density, within a settling surface. Marine Ecology Progress Series 38: 151–160.

    Article  Google Scholar 

  • Kim, D. H., J. N. Seo, Y. N. Yoon & Y.-S. Suh, 2012. Estimating the economic damage caused by jellyfish to fisheries in Korea. Fisheries Science 78: 1147–1152.

    Article  CAS  Google Scholar 

  • Kinoshita, J., J. Hiromi & Y. Yamada, 2006. Abundance and biomass of scyphomedusae, Aurelia aurita and Chysaora melanaster, and ctenophore, Bolinopsis mikado, with estimates of their feeding impact on zooplankton in Tokyo Bay, Japan. Journal of Oceanography 62: 607–615.

    Article  Google Scholar 

  • Lucas, C. H., W. M. Graham & C. Widmer, 2012. Jellyfish life histories: role of polyps in forming and maintaining scyphomedusa populations. Advance in Marine Biology 63: 133–196.

    Article  Google Scholar 

  • Magni, P. & S. Montani, 2000. Water chemistry variability in the lower intertidal zone of an estuary in the Seto Inland Sea, Japan: seasonal patterns of nutrients and particulate compounds. Hydrobiologia 432: 9–23.

    Article  CAS  Google Scholar 

  • Makabe, R., R. Furukawa, M. Takao & S. Uye, 2014. Marine artificial structures as amplifiers of Aurelia aurita s.l. blooms: a case study of a newly installed floating pier. Journal of Oceanography 70: 447–455.

    Article  CAS  Google Scholar 

  • Makabe, R., H. Takeoka & S. Uye, 2015. Offshore dispersion of ephyrae and medusae of Aurelia aurita s.l. (Cnidaria: Scyphozoa) from port enclosures: Physical and biological factors. Journal of Marine Systems 152: 75–82.

    Article  Google Scholar 

  • Malej, A., T. Kogovšek & S. Uye, 2014. Medusae—Pest or resource for humans? Biologia Marina Mediterranea 21: 2–9.

    Google Scholar 

  • Manda, A., H. Nakamura, N. Asano, S. Iizuka, T. Miyama, Q. Moteki, M. K. Yoshioka, K. Nishii & T. Miyasaka, 2014. Impacts of a warming marginal sea on torrential rainfall organized under the Asian summer monsoon. Scientific Reports 4: 1–6.

    Google Scholar 

  • Matsuda, O., Y. Kishimoto & S. Hamasaki, 1990. Factors affecting seasonal variation of oceanographic conditions at Kure Port. Journal of Faculty of Applied Biological Science, Hiroshima University 29: 135–144. (in Japanese with English abstract).

    Google Scholar 

  • Miyake, H., K. Iwao & Y. Kakinuma, 1997. Life history and environment of Aurelia aurita. South Pacific Study 17: 273–285.

    Google Scholar 

  • Miyake, H., M. Terazaki & Y. Kakinuma, 2002. On the polyps of the common jellyfish Aurelia aurita in Kagoshima Bay. Journal of Oceanography 58: 451–459.

    Article  Google Scholar 

  • Ohtsu, K., M. Kawahara, H. Ikeda & S. Uye, 2007. Experimental induction of gonadal maturation and spawning in the giant jellyfish Nemopilema nomurai (Schyphozoa: Rhizostomeae). Marine Biology 152: 667–676.

    Article  Google Scholar 

  • Peneda, J., 2000. Linking larval settlement to larval transport: assumptions, potentials, and pitfalls. Oceanography of the Eastern Pacific 1: 84–105.

    Google Scholar 

  • Pitt, K. P. & C. H. Lucas (eds), 2014. Jellyfish Blooms. Springer, Dordrecht.

    Google Scholar 

  • Prieto, L., D. Astorga, G. Navarro & J. Ruiz, 2010. Environmental control of phase transition and polyp survival of massive-outbreaker jellyfish. PLoS ONE 5: e13793.

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Purcell, J. E., S. Uye & L. 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 

  • Purcell, J. E., R. A. Hoover & N. T. Schwarck, 2009. Interannual variation of strobilation by the scyphozoan Aurelia labiata in relation to polyp density, temperature, salinity, and light conditions in situ. Marine Ecology Progress Series 375: 139–149.

    Article  Google Scholar 

  • Riascos, J. M., L. Paredes, K. González, I. Cáceres & A. Pacheco, 2013. The larval and benthic stages of the scyphozoan medusa Chrysaora plocamia under El Niño-La Niña thermal regimes. Journal of Experimental Marine Biology and Ecology 446: 95–101.

    Article  Google Scholar 

  • 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 and Evolution 24: 312–322.

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Schneider, G. & T. Weisse, 1985. Metabolism measurements of Aurelia aurita planulae larvae, and calculation of maximal survival period of the free swimming stage. Helgoland Marine Research 39: 43–47.

    Google Scholar 

  • Scorrano, S., G. Aglieri, F. Boero, M. N. Dawson & S. Piraino, 2016. Unmasking Aurelia species in the Mediterranean Sea: an integrative morphometric and molecular approach. Zoological Journal of Linnean Society. https://doi.org/10.1111/zoj.12494.

    Google Scholar 

  • Song, S., F. Zhang, C. Li, S. Wang, M. Wang, Z. Tao, Y. Wang, G. Zhang & X. Sun, 2015. Breeding places, population dynamics, and distribution of the giant jellyfish Nemopilema nomurai (Scyphozoa: Rhizostomeae) in the Yellow Sea and the East China Sea. Hydrobiologia 754: 59–74.

    Article  Google Scholar 

  • Sun, Y. & Y. Ding, 2010. A projection of future changes in summer precipitation and monsoon in East Asia. Science China Earth Science 53: 284–300.

    Article  CAS  Google Scholar 

  • 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. Journao of Experimental Marine Biology and Ecology 446: 151–158.

    Article  Google Scholar 

  • Toyokawa, M., 2011. First record of wild polyps of Chrysaora pacifica (Goette, 1886) (Scyphozoa, Cnidaria). Plankton Benthos Research 6: 175–177.

    Article  Google Scholar 

  • Toyokawa, M., M. Shibata, J. H. Cheng, H. Y. Li, J. Z. Ling, N. Lin, Z. L. Liu, Y. Zhang, M. Shimizu & H. Akiyama, 2012. First record of wild ephyrae of the giant jellyfish Nemopilema nomurai. Fisheries Science 78: 1213–1218.

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Uye, S., 2014. The giant jellyfish Nemopilema nomurai in East Asian Marginal Seas. In Pitt, K. A. & C. H. Lucas (eds), Jellyfish Blooms. Springer, Dordrecht: 185–205.

    Chapter  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • Wang, Y. & L. Zhou, 2005. Observed trends in extreme precipitation events in China during 1961–2001 and the associated changes in large-scale circulation. Geophysical Reearchg Letters. https://doi.org/10.1029/2005GL022574.

    Google Scholar 

  • Webster, C. N. & C. H. Lucas, 2012. The effect of food and temperature on settlement of Aurelia aurita planula larvae ans subsequent somatic growth. Journal of Experimental Marine Biology and Ecology 436: 50–55.

    Article  Google Scholar 

  • Weiler, K. S. & R. E. Black, 1991. Immediate decrease in apparent translation rate caused by salinity change in scyphistomae of Aurelia aurita (Linnaeus). Comparative Biochemistry and Physiology A 99: 199–202.

    Article  Google Scholar 

  • Willcox, S., N. A. Moltschaniwskyj & C. M. Crawford, 2008. Population dynamics of natural colonies of Aurelia sp. scyphistomae in Tasmania. Australia. Marine Biology 154: 661–670.

    Article  Google Scholar 

  • Yoon, W. D., S. H. Choi, C. Han & W. G. Park, 2014. Rock preference of planulae of jellyfish Aurelia aurita (Linnaeus 1758) for settlement in the laboratory. Ocean Science 49: 163–166.

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Keats Conley for her valuable comments on an early version of the manuscript and Hideki Ikeda for his assistance in field sampling. We are also grateful to two anonymous reviewers for helpful comments. This work was partially supported by a Grant from the Agriculture, Forestry and Fisheries Research Council, Japan (Project name: STOPJELLY), and JSPS KAKENHI (No. 16K07826).

Author information

Authors and Affiliations

  1. Graduate School of Biosphere Science, Hiroshima University, 4-4 Kagamiyama 1 Chome, Higashi-Hiroshima, 739-8528, Japan

    Mariko Takao & Shin-ichi Uye

Authors
  1. Mariko Takao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shin-ichi Uye
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shin-ichi Uye.

Additional information

Handling editor: Juan Carlos Molinero

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Takao, M., Uye, Si. Effects of low salinity on the physiological ecology of planulae and polyps of scyphozoans in the East Asian Marginal Seas: potential impacts of monsoon rainfall on medusa population size. Hydrobiologia 815, 165–176 (2018). https://doi.org/10.1007/s10750-018-3558-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3558-3

Keywords

Search

Navigation