Natural predators of polyps of three scyphozoans: Nemopilema nomurai, Aurelia coerulea, and Rhopilema esculentum

Abstract

Jellyfish blooms have become a hot research topic in recent decades because they pose a serious threat to fisheries, coastal industries, tourism, and the marine ecosystem. The life cycle of scyphozoan jellyfish consists of a pelagic medusa stage and a benthic polyp stage, where asexual reproduction and strobilation of the polyps directly affect the abundance of ephyra and subsequently medusa abundance. The dynamics of polyps are affected by both environmental and biological factors, and predation by natural predators is one of the most important biological factors. Nemopilema nomurai, Aurelia coerulea, and Rhopilema esculentum are three scyphozoan species that are commonly found in Chinese coastal waters, and previous studies reported that the survivorship of polyps differs among the three species when they are exposed to the same benthic community. To identify potential natural predators of polyps of these three species in Chinese coastal waters and to determine whether the predation rates on polyps of the three species differ, we collected 39 species of macrozoobenthos from the Bohai Sea, Yellow Sea, and East China Sea from May 2014 to June 2016 and conducted predation tests and predation rate measurements. We found that the nudibranchs Pleurobranchaea novaezealandiae, Okenia plana, and Chromodoris tinctoria and the sea anemones Paracalliactis sinica, Calliactis japonica, Anthopleura incerta, and Anthopleura midori could prey on the polyps of all three scyphozoan species. The predation rates increased with the body length of the predators. The predations rates were also related to the polyp species, although the different predators showed no consistent preference for a particular species of polyp. Our results indicate that introducing predators to locations inhabited by polyps might be a way to control the benthic polyp populations and prevent subsequent jellyfish blooms.

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References

  1. Arai M N. 1997. A Functional Biology of Scyphozoa. Springer, Netherlands. p.203–223, https://doi.org/10.1007/978-94-009-1497-1.

    Google Scholar 

  2. Arai M N. 2009. The potential importance of podocysts to the formation of scyphozoan blooms: a review. Hydrobiologia, 616(1): 241–246, https://doi.org/10.1007/s10750-008-9588-5.

    Article  Google Scholar 

  3. Arim M, Marquet PA. 2004. Intraguild predation: a widespread interaction related to species biology. Ecology Letters, 7(7): 557–564, https://doi.org/10.1111/j.1461-0248.2004.00613.x.

    Article  Google Scholar 

  4. Bertsch H. 1984. Book Review: Opisthobranchia des Mittelmeeres: Nudibranchia und Saccoglossa. L. Schmekel, A. Portmann. Quarterly Review of Biology, 59(1): 79–80, https://doi.org/10.1086/413719.

    Article  Google Scholar 

  5. Cattaneo-Vietti R, Burlando B, Senes L. 1993. Life history and diet of Pleurobranchaea meckelii (Opisthobranchia: Notaspidea). Journal of Molluscan Studies, 59(3): 309–313, https://doi.org/10.1093/mollus/59.3.309.

    Article  Google Scholar 

  6. Condon R H, Decker M B, Purcell J E. 2001. Effects of low dissolved oxygen on survival and asexual reproduction of scyphozoan polyps (Chrysaora quinquecirrha). Hydrobiologia, 451: 89–95, https://doi.org/10.1023/A:1011892107211.

    Article  Google Scholar 

  7. Condon R H, Duarte C M, Pitt K A, Robinson K L, Lucas C H, Sutherland K R, Mianzan H W, Bogeberg M, Purcell J E, Decker M B, Uye S I, Madin L P, Brodeur R D, Haddock S H D, Malej A, Parry G D, Eriksen E, Quiñones J, Acha M, Harvey M, Arthur J M, Graham W M. 2013. Recurrent jellyfish blooms are a consequence of global oscillations. Proceedings of the National Academy of Sciences, 110(3): 1 000–1 005, https://doi.org/10.1073/pnas.1210920110.

    Article  Google Scholar 

  8. Conklin E J, Mariscal R N. 1977. Feeding behavior, ceras structure, and nematocyst storage in the aeolid nudibranch, Spurilla neapolitana (Mollusca). Bulletin of Marine Science, 27(4): 658–667.

    Google Scholar 

  9. de Lafontaine Y, Leggett W C. 1988. Predation by Jellyfish on larval fish: an experimental evaluation employing in situ enclosures. Canadian Journal of Fisheries and Aquatic Sciences, 45(7): 1 173–1 190, https://doi.org/10.1139/f88-140.

    Article  Google Scholar 

  10. Dong J, Jiang L X, Tan K F, Liu H Y, Purcell J E, Li P J, Ye C C. 2009. Stock enhancement of the edible jellyfish (Rhopilema esculentum Kishinouye) in Liaodong Bay, China: a review. Hydrobiologia, 616(1): 113–118, https://doi.org/10.1007/s10750-008-9592-9.

    Article  Google Scholar 

  11. Dong Z J, Liu D Y, Keesing J K. 2010. Jellyfish blooms in China: dominant species, causes and consequences. Marine Pollution Bulletin, 60(7): 954–963, https://doi.org/10.1016/j.marpolbul.2010.04.022.

    Article  Google Scholar 

  12. Dong Z J, Liu D Y, Keesing J K. 2014. Contrasting trends in populations of Rhopilema esculentum and Aurelia aurita in Chinese waters. In: Pitt K, Lucas C eds. Jellyfish Blooms. Springer, Dordrecht. p.207–218, https://doi.org/10.1007/978-94-007-7015-7_9.

    Google Scholar 

  13. Dong Z J, Wang F H, Peng S J, Chen G F, Sun S. 2019. Effects of copper and reduced salinity on the early life stages of the moon jellyfish Aurelia coerulea. Journal of Experimental Marine Biology and Ecology, 513: 42–46, https://doi.org/10.1016/j.jembe.2019.02.005.

    Article  Google Scholar 

  14. Feng S, Wang S W, Sun S, Zhang F, Zhang G T, Liu M T, Uye S. 2018. Strobilation of three scyphozoans (Aurelia coelurea, Nemopilema nomurai, and Rhopilema esculentum) in the field at Jiaozhou Bay, China. Marine Ecology Progress Series, 591: 141–153, https://doi.org/10.3354/meps12276.

    Article  Google Scholar 

  15. Feng S, Wang S W, Zhang G T, Sun S, Zhang F. 2017. Selective suppression of in situ proliferation of scyphozoan polyps by biofouling. Marine Pollution Bulletin, 114(2): 1 046–1 056, https://doi.org/10.1016/j.marpolbul.2016.10.062.

    Article  Google Scholar 

  16. Feng S, Zhang G T, Sun S, Zhang F, Wang S W, Liu M T. 2015. Effects of temperature regime and food supply on asexual reproduction in Cyanea nozakii and Nemopilema nomurai. Hydrobiologia, 754(1): 201–214, https://doi.org/10.1007/s10750-015-2279-0.

    Article  Google Scholar 

  17. Fenner P J, Lippmann J, Gershwin L A. 2010. Fatal and nonfatal severe jellyfish stings in Thai waters. Journal of Travel Medicine, 17(2): 133–138, https://doi.org/10.1111/j.1708-8305.2009.00390.x.

    Article  Google Scholar 

  18. Greenwood P G. 2009. Acquisition and use of nematocysts by cnidarian predators. Toxicon, 54(8): 1 065–1 070, https://doi.org/10.1016/j.toxicon.2009.02.029.

    Article  Google Scholar 

  19. Han C H, Uye S I. 2010. Combined effects of food supply and temperature on asexual reproduction and somatic growth of polyps of the common jellyfish Aurelia aurita s.l. Plankton and Benthos Research, 5(3): 98–105, https://doi.org/10.3800/pbr.5.98.

    Article  Google Scholar 

  20. Hernroth L, Gröndahl F. 1985. On the biology of Aurelia aurita (L.) 3. Predation by Coryphella verrucosa (Gastropoda, Opisthobranchia), a major factor regulating the development of Aurelia populations in the Gullmar Fjord, western Sweden. Ophelia, 24(1): 37–45, https://doi.org/10.1080/00785236.1985.10426617.

    Article  Google Scholar 

  21. Holst S, Jarms G. 2007. Substrate choice and settlement preferences of planula larvae of five Scyphozoa (Cnidaria) from German Bight, North Sea. Marine Biology, 151(3): 863–871, https://doi.org/10.1007/s00227-006-0530-y.

    Article  Google Scholar 

  22. Holst S. 2012. Effects of climate warming on strobilation and ephyra production of North Sea scyphozoan jellyfish. Hydrobiologia, 690(1): 127–140, https://doi.org/10.1007/s10750-012-1043-y.

    Article  Google Scholar 

  23. Hoover R A, Armour R, Dow I, Purcell J E. 2012. Nudibranch predation and dietary preference for the polyps of Aurelia labiata (Cnidaria: Scyphozoa). Hydrobiologia, 690(1): 199–213, https://doi.org/10.1007/s10750-012-1044-x.

    Article  Google Scholar 

  24. Hoover R A, Purcell J E. 2009. Substrate preferences of scyphozoan Aurelia labiata polyps among common dock-building materials. Hydrobiologia, 616(1): 259–267, https://doi.org/10.1007/s10750-008-9595-6.

    Article  Google Scholar 

  25. Hutton C H, Delisle P F, Roberts M H, Hepworth D A. 1986. Chrysaora quinquecirrha: a predator on mysids (Mysidopsis bahia) in culture. The Progressive Fish-Culturist, 48(2): 154–155, https://doi.org/10.1577/1548-8640(1986)48<154:CQ>2.0.CO;2.

    Article  Google Scholar 

  26. Kawahara M, Uye S I, Ohtsu K, Iizumi H. 2006. Unusual population explosion of the giant jellyfish Nemopilema nomurai (Scyphozoa: Rhizostomeae) in East Asian waters. Marine Ecology Progress Series, 307: 161–173, https://doi.org/10.3354/meps307161.

    Article  Google Scholar 

  27. Laurie-Lesh G E, Corriel R. 1973. Scyphistoma regeneration from isolated tentacles in Aurelia aurita. Journal of the Marine Biological Association of the United Kingdom, 53(4): 885–894, https://doi.org/10.1017/S0025315400022542.

    Article  Google Scholar 

  28. Lee H E, Han C H, Kim B, Yoon W D. 2017. Effects of temperature and salinity on the asexual reproduction of Nemopilema nomurai (Scyphozoa: Rhizostomeae). Ocean Science Journal, 52(4): 573–579, https://doi.org/10.1007/s12601-017-0040-5.

    Article  Google Scholar 

  29. Lucas C H, Graham W M, Widmer C. 2012. Jellyfish life histories: role of polyps in forming and maintaining scyphomedusa populations. Advances in Marine Biology, 63: 133–196, https://doi.org/10.1016/B978-0-12-394282-1.00003-X.

    Article  Google Scholar 

  30. Lucas C H. 2001. Reproduction and life history strategies of the common jellyfish, Aurelia aurita, in relation to its ambient environment. Hydrobiologia, 451(1): 229–246, https://doi.org/10.1023/A:1011836326717.

    Article  Google Scholar 

  31. Martin R. 2003. Management of nematocysts in the alimentary tract and in cnidosacs of the aeolid nudibranch gastropod Cratena peregrina. Marine Biology, 143(3): 533–541, https://doi.org/10.1007/s00227-003-1078-8.

    Article  Google Scholar 

  32. Miller J A, Byrne M. 2000. Ceratal autotomy and regeneration in the aeolid nudibranch Phidiana crassicornis and the role of predators. Invertebrate Biology, 119(2): 167–176, https://doi.org/10.1111/j.1744-7410.2000.tb00005.x.

    Article  Google Scholar 

  33. Mills C E. 2001. Jellyfish blooms: are populations increasing globally in response to changing ocean conditions? Hydrobiologia, 451(1–3): 55–68, https://doi.org/10.1023/A:1011888006302.

    Article  Google Scholar 

  34. Miyajima-Taga Y, Masuda R, Morimitsu R, Ishii H, Nakajima K, Yamashita Y. 2016. Ontogenetic changes in the predator-prey interactions between threadsail filefish and moon jellyfish. Hydrobiologia, 772(1): 175–187, https://doi.org/10.1007/s10750-016-2658-1.

    Article  Google Scholar 

  35. Oakes M, Haven D S. 1971. Some predators of polyps of Chrysaora quinquecirrha (Scyphozoa, Semaeostmae) in the Chesapeake Bay. Virginia Journal of Science, 22: 45–46.

    Google Scholar 

  36. Okanishi M, Sentoku A, Fujimoto S, Jimi N, Nakayama R, Yamana Y, Yamauchi H, Hayate T, Kato T, Kashio S, Uyeno D, Yamamoto K, Miyazaki K, Asakura A. 2016. Marine benthic community in Shirahama, southwestern Kii Peninsula, central Japan. Publications of the Seto Marine Biological Laboratory, 44: 7–52, https://doi.org/10.5134/217458.

    Article  Google Scholar 

  37. Peng S Y, Li X Z, Wang H F, Zhang B L. 2014. Macrobenthic community structure and species composition in the Yellow Sea and East China Sea in jellyfish bloom. Chinese Journal of Oceanology and Limnology, 32(3): 576–594, https://doi.org/10.1007/s00343-014-3068-8.

    Article  Google Scholar 

  38. Polis G A, Holt R D. 1992. Intraguild predation: the dynamics of complex trophic interactions. Trends in Ecology and Evolution, 7(5): 151–154, https://doi.org/10.1016/0169-5347(92)90208-S.

    Article  Google Scholar 

  39. Purcell J E, Bondyale-Juez D R, Romero-Kutzner V, Martínez I, Caprioli R, Tames-Espinosa M, Almunia J, Alonso E, Packard T T, Gómez M. 2019. Food supply effects on the asexual reproduction and respiratory metabolism of Aurelia aurita polyps. Hydrobiologia, 846(1): 135–146, https://doi.org/10.1007/s10750-019-04057-4.

    Article  Google Scholar 

  40. Purcell J E, Uye S I, Lo W T. 2007. Anthropogenic causes of jellyfish blooms and their direct consequences for humans: a review. Marine Ecology Progress Series, 350: 153–174, https://doi.org/10.3354/meps07093.

    Article  Google Scholar 

  41. Purcell J E. 2012. Jellyfish and ctenophore blooms coincide with human proliferations and environmental perturbations. Annual Review of Marine Science, 4: 209–235, https://doi.org/10.1146/annurev-marine-120709-142751.

    Article  Google Scholar 

  42. Shoji J, Kudoh T, Takatsuji H, Kawaguchi O, Kasai A. 2010. Distribution of moon jellyfish Aurelia aurita in relation to summer hypoxia in Hiroshima Bay, Seto Inland Sea. Estuarine, Coastal and Shelf Science, 86(3): 485–490, https://doi.org/10.1016/j.ecss.2009.03.001.

    Article  Google Scholar 

  43. Sun S, Sun X X, Jenkinson I R. 2015a. Preface: Giant jellyfish blooms in Chinese waters. Hydrobiologia, 754(1): 1–11, https://doi.org/10.1007/s10750-015-2320-3.

    Article  Google Scholar 

  44. Sun S, Zhang F, Li C L, Wang S W, Wang M X, Tao Z C, Wang Y T, Zhang G T, Sun X X. 2015b. 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(1): 59–74, https://doi.org/10.1007/s10750-015-2266-5.

    Article  Google Scholar 

  45. Suzuki K S, Kumakura E, Nogata Y. 2016. Incidental consumption of ephyrae of moon jellyfish Aurelia aurita s.l. by three filter-feeding sessile organisms: laboratory experiments. Fisheries Science, 82(6): 923–930, https://doi.org/10.1007/s12562-016-1034-4.

    Article  Google Scholar 

  46. Takao M, Okawachi H, Uye S I. 2014. Natural predators of polyps of Aurelia aurita s.l. (Cnidaria: Scyphozoa: Semaeostomeae) and their predation rates. Plankton and Benthos Research, 9(2): 105–113, https://doi.org/10.3800/pbr.9.105.

    Article  Google Scholar 

  47. Tang C S, Sun S, Zhang F. 2020. Intraguild predation by polyps of three scyphozoan jellyfish: Nemopilema nomurai, Aurelia coerulea, and Rhopilema esculentum. Journal of Oceanology and Limnology, 38(6): 1 755–1 761, https://doi.org/10.1007/s00343-019-9079-8.

    Article  Google Scholar 

  48. Thein H, Ikeda H, Uye S I. 2012. The potential role of podocysts in perpetuation of the common jellyfish Aurelia aurita s.l. (Cnidaria: Scyphozoa) in anthropogenically perturbed coastal waters. Hydrobiologia, 690: 157–167, https://doi.org/10.1007/s10750-012-1045-9.

    Article  Google Scholar 

  49. Thiel H. 1962. Untersuchungen über die Strobilisation von Aurelia aurita LAM. an einer Population der Kieler Förde. Kieler Meeresforschungen, 18: 198–230.

    Google Scholar 

  50. Uchida T, Hanaoka K I. 1933. On the morphology of a stalked medusa, Thaumatoscyphus distinctus kishinouye. Journal of the Faculty of Science, Hokkaido Imperial University, Series VI. Zoology, 2(3): 135–153.

    Google Scholar 

  51. Uye S I. 2011. Human forcing of the copepod-fish-jellyfish triangular trophic relationship. Hydrobiologia, 666(1): 71–83, https://doi.org/10.1007/s10750-010-0208-9.

    Article  Google Scholar 

  52. Uye S I. 2014. The giant jellyfish Nemopilema nomurai in East Asian marginal seas. In: Pitt K, Lucas C eds. Jellyfish Blooms. Springer, Dordrecht. p.185–205, https://doi.org/10.1007/978-94-007-7015-7_8.

    Google Scholar 

  53. von Salvini-Plawen L. 1972. Cnidaria as food-sources for marine invertebrates. Cahiers de Biologie Marine, 13(3): 385–400.

    Google Scholar 

  54. Watanabe T, Ishii H. 2001. In situ estimation of ephyrae liberated from polyps of Aurelia aurita using settling plates in Tokyo Bay, Japan. Hydrobiologia, 451(1): 247–258, https://doi.org/10.1023/A:1011856929443.

    Article  Google Scholar 

  55. Zhang F, Sun S, Jin X S, Li C L. 2012. Associations of large jellyfish distributions with temperature and salinity in the Yellow Sea and East China Sea. Hydrobiologia, 690(1): 81–96, https://doi.org/10.1007/s10750-012-1057-5.

    Article  Google Scholar 

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Correspondence to Song Sun.

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All data generated and/or analyzed during this study are available upon request by contacting with the corresponding author.

Supported by the National Key Research and Development Program of China (No. 2017YFC1404405), the Mount Tai Scholar Climbing Plan to Song SUN, the Shandong Joint Fund for Marine Ecology and Environmental Sciences (No. U1606404), and the Aoshan Science and Technology Innovation Project (No. 2016ASKJ02-2)

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Tang, C., Sun, S. & Zhang, F. Natural predators of polyps of three scyphozoans: Nemopilema nomurai, Aurelia coerulea, and Rhopilema esculentum. J. Ocean. Limnol. (2021). https://doi.org/10.1007/s00343-020-0284-2

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Keyword

  • jellyfish bloom
  • polyps
  • predation rate
  • predators