Natural predators of polyps of three scyphozoans: Nemopilema nomurai, Aurelia coerulea, and Rhopilema esculentum -- Journal of Oceanology and Limnology,2021,39(2):598-608

	Cite this paper:
	Changsheng TANG, Song SUN, Fang ZHANG. Natural predators of polyps of three scyphozoans: Nemopilema nomurai, Aurelia coerulea, and Rhopilema esculentum[J]. Journal of Oceanology and Limnology, 2021, 39(2): 598-608

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

Changsheng TANG^1,2,3,4, Song SUN^1,2,3,4,5, Fang ZHANG^1,2,3,4

1 Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
2 Laboratory of Marine Ecology and Environmental Sciences, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China;
3 University of Chinese Academy of Sciences, Beijing 100049, China;
4 Center for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao 266071, China;
5 Jiaozhou Bay Marine Ecosystem Research Station, Chinese Academy of Sciences, Qingdao 266071, China

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.

Key words: jellyfish bloom|polyps|predation rate|predators

Received: 2020-07-24 Revised: 2020-08-20

Tools

PDF (1307 KB) Free

Print this page

Add to favorites

Email this article to others

Authors

Articles by Changsheng TANG

Articles by Song SUN

Articles by Fang ZHANG

References:
Arai M N. 1997. A Functional Biology of Scyphozoa. Springer, Netherlands. p.203-223, https://doi.org/10.1007/978-94-009-1497-1.
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.
Arim M, Marquet P A. 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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Hoover R A, Purcell J E. 2009. Substrate preferences of scyphozoan Aurelia labiata polyps among common dockbuilding materials. Hydrobiologia, 616(1):259-267, https://doi.org/10.1007/s10750-008-9595-6.
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 FishCulturist, 48(2):154-155, https://doi.org/10.1577/1548-8640(1986)48<154:CQ>2.0.CO;2.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Thiel H. 1962. Untersuchungen über die Strobilisation von Aurelia aurita LAM. an einer Population der Kieler Förde. Kieler Meeresforschungen, 18:198-230.
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.
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.
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.
von Salvini-Plawen L. 1972. Cnidaria as food-sources for marine invertebrates. Cahiers de Biologie Marine, 13(3):385-400.
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.
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.