Seasonal alternation of the ontogenetic development of the moon jellyfish Aurelia coerulea in Maizuru Bay, Japan

Autoři: Kentaro S. Suzuki aff001;  Keita W. Suzuki aff002;  Emi Kumakura aff003;  Kana Sato aff003;  Yutaro Oe aff004;  Tasuku Sato aff004;  Hideki Sawada aff002;  Reiji Masuda aff002;  Yasuyuki Nogata aff001
Působiště autorů: Environmental Science Research Laboratory, Central Research Institute of Electric Power Industry, Abiko, Chiba, Japan aff001;  Maizuru Fisheries Research Station, Field Science Education and Research Center, Kyoto University, Maizuru, Kyoto, Japan aff002;  CERES Inc., Abiko, Chiba, Japan aff003;  College of Bioresource Sciences, Nihon University, Fujisawa, Kanagawa, Japan aff004
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0225513


Outbreaks of moon jellyfish Aurelia spp. are frequently reported from many parts of the world’s coastal areas. Aurelia spp. canonically show a metagenetic life cycle in which planulae transform into sessile polyps, which can drastically increase in number through asexual reproduction. Therefore, their asexual reproduction has been recognized as one of the major causes of the outbreaks. Aurelia spp. also show direct development that lacks asexual reproduction during the polyp stage, which prevents us from understanding the mechanisms of its outbreaks. To clarify the seasonality of the metagenetic and direct-development life cycles of Aurelia sp. in Maizuru Bay, Japan, we conducted field observations and laboratory experiments throughout the year. Additionally, the two life cycle types were genetically analyzed to confirm that they belong to the single species Aurelia coerulea, which dominates in coastal waters in Japan. From July until October, Aurelia coerulea produced smaller eggs and planulae all of which developed into polyps. However, from December until May, larger eggs and planulae were produced and 90% of the planulae developed into planktonic ephyrae bypassing the sessile polyp stage. Our results demonstrated that a single species, A. coerulea, seasonally shifts between their two life cycle types at a water temperature threshold of 20°C in Maizuru Bay. The higher energy storage of larger planulae was suggested to enable the planulae to develop into ephyrae without external energy input through feeding during the polyp stage. The adaptive significances of the two life cycle types were also discussed.

Klíčová slova:

Copepods – Life cycles – Oocytes – Ovaries – Predation – Salinity – Spawning – Asexual reproduction


1. Purcell JE, Uye S, Lo W-T. Anthropogenic causes of jellyfish blooms and their direct consequences for humans: A review. Mar Ecol Prog Ser. 2007;350: 153–174.

2. Richardson AJ, Bakun A, Hays GC, Gibbons MJ. The jellyfish joyride: causes, consequences and management responses to a more gelatinous future. Trends Ecol Evol. 2009;24: 312–322. doi: 10.1016/j.tree.2009.01.010 19324452

3. Robinson KL, Graham WM. Long-term change in the abundances of northern Gulf of Mexico scyphomedusae Chrysaora sp. and Aurelia spp. with links to climate variability. Limnol Oceanogr. 2013;58: 235–253.

4. Möller H. Reduction of a larval herring population by jellyfish predator. Science. 1984;224: 621–622. doi: 10.1126/science.224.4649.621 17838355

5. Uye S, Shimauchi H. Population biomass, feeding, respiration and growth rates, and carbon budget of the scyphomedusa Aurelia aurita in the Inland Sea of Japan. J Plankton Res. 2005;27: 237–248.

6. Dong Z, Liu D, Keesing JK. Jellyfish blooms in China: Dominant species, causes and consequences. Mar Pollut Bull. 2010;60: 954–963. doi: 10.1016/j.marpolbul.2010.04.022 20553695

7. Roughgarden J, Gaines S, Possingham H. Recruitment dynamics in complex life cycles. Science. 1988;241: 1460–1466. doi: 10.1126/science.11538249 11538249

8. Eckman JE. Closing the larval loop: Linking larval ecology to the population dynamics of marine benthic invertebrates. J Exp Mar Biol Ecol. 1996;200: 207–237.

9. Carrier TJ, Reitzel AM, Heyland A. Evolutionary Ecology of Marine Invertebrate Larvae. Oxford: Oxford University Press; 2018.

10. Arai MN. A functional biology of Scyphozoa. London: Chapman & Hall; 1997.

11. Kakinuma Y. On some factors for the differentiations of Cladonema uchidai and Aurelia aurita. Bull Mar Biol Stn Asamushi. 1962;11: 81–85.

12. Kakinuma Y. An experimental study of the life cycle and organ differentiation of Aurelia aurita Lamarck. Bull Mar Biol Stn Asamushi. 1975;15: 101–112.

13. Schiariti A, Morandini AC, Jarms G, von Glehn Paes R, Franke S, Mianzan H. Asexual reproduction strategies and blooming potential in Scyphozoa. Mar Ecol Prog Ser. 2014;510: 241–253.

14. Lucas CH, Graham WM, Widmer C. Jellyfish Life Histories: Role of Polyps in Forming and Maintaining Scyphomedusa Populations. Advances in Marine Biology. Amsterdam: Academic Press; 2012. p. 133–196. doi: 10.1016/B978-0-12-394282-1.00003-X 22877612

15. Han C-H, Uye S. Combined effects of food supply and temperature on asexual reproduction and somatic growth of polyps of the common jellyfish Aurelia aurita s.l. Plankton Benthos Res. 2010;5: 98–105.

16. Willcox S, Moltschaniwskyj NA, Crawford C. Asexual reproduction in scyphistomae of Aurelia sp.: Effects of temperature and salinity in an experimental study. J Exp Mar Biol Ecol. 2007;353: 107–114.

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

18. Thein H, Ikeda H, Uye S. The potential role of podocysts in perpetuation of the common jellyfish Aurelia aurita s.l. (Cnidaria: Scyphozoa) in anthropogenically perturbed coastal waters. Hydrobiologia. 2012;690: 157–167.

19. Yasuda T. Ecological studies on the jelly-fish, Aurelia aurita (Linné), in Urazoko Bay, Fukui Prefecture-XI. An observation on ephyra formation. Publ Seto Mar Biol Lab. 1975;22: 75–80.

20. Haeckel EHPA. Metagenesis und hypogenesis von Aurelia aurita. Jena: G. Fischer; 1881.

21. Hirai E. On the developmental cycles of Aurelia aurita and Dactylometra pacifica. Bull Mar Biol Stn Asamushi. 1958;9: 81.

22. Yasuda T. Jellyfish: UFO in the sea. Tokyo: Koseisha-koseikaku; 2003. (in Japanese)

23. Lucas CH. Reproduction and life history strategies of the common jellyfish, Aurelia aurita, in relation to its ambient environment. Hydrobiologia. 2001;451: 229–246.

24. Helm RR, Tiozzo S, Lilley MKS, Lombard F, Dunn CW. Comparative muscle development of scyphozoan jellyfish with simple and complex life cycles. EvoDevo. 2015;6: 11. doi: 10.1186/s13227-015-0005-7 25932322

25. Gröndahl F. Interactions between polyps of Aurelia aurita and planktonic larvae of scyphozoans: an experimental study. Mar Ecol Prog Ser. 1988;45: 87–93.

26. Conley K, Uye S. Effects of hyposalinity on survival and settlement of moon jelly fish (Aurelia aurita) planulae. J Exp Mar Biol Ecol. 2015;462: 14–19.

27. Yasuda T. Ecological studies on the jelly-fish, Aurelia aurita in Urazoko Bay, Fukui Prefecture–IV. Monthly change in the bell-length composition and breeding season. Bull. Japanese Soc. Sci. Fisheries. 1971;37: 364–370. (in Japanese with English abstract)

28. Dawson MN, Martin LE. Geographic variation and ecological adaptation in Aurelia (Scyphozoa, Semaeostomeae): Some implications from molecular phylogenetics. Hydrobiologia. 2001;451: 259–273.

29. Ki J-S, Hwang D-S, Shin K, Yoon WD, Lim D, Kang YS, et al. Recent moon jelly (Aurelia sp.1) blooms in Korean coastal waters suggest global expansion: examples inferred from mitochondrial COI and nuclear ITS-5.8S rDNA sequences. ICES J Mar Sci. 2008;65: 443–452.

30. Chiaverano LM, Bayha KW, Graham WM. Local versus generalized phenotypes in two sympatric Aurelia species: Understanding jellyfish ecology using genetics and morphometrics. PLoS One. 2016;11: e0156588. doi: 10.1371/journal.pone.0156588 27332545

31. Scorrano S, Aglieri G, Boero F, Dawson MN, Piraino S. Unmasking Aurelia species in the Mediterranean Sea: An integrative morphometric and molecular approach. Zool J Linn Soc. 2017;180: 243–267.

32. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2016. Available from:

33. Schneider G. Larvae production of the common jellyfish Aurelia aurita in the western Baltic 1982–1984. Kiel Meeresforsch. 1988;6: 295–300.

34. Lucas CH. Population dynamics of Aurelia aurita (Scyphozoa) from an isolated brackish lake, with particular reference to sexual reproduction. J Plankton Res. 1996;18: 987–1007.

35. Lucas CH, Lawes S. Sexual reproduction of the scyphomedusa Aurelia aurita in relation to temperature and variable food supply. Mar Biol. 1998;131: 629–638.

36. D’Ambra I, Graham WM, Carmichael RH, Hernandez FJ. Dietary overlap between jellyfish and forage fish in the northern Gulf of Mexico. Mar Ecol Prog Ser. 2018;587: 31–40.

37. Ishii H, Tanaka F. Food and feeding of Aurelia aurita in Tokyo Bay with an analysis of stomach contents and a measurement of digestion times. Hydrobiologia. 2001;451: 311–320.

38. Uye S. Length-weight relationships of important zooplankton from the Inland Sea of Japan. J Oceanogr Soc Jpn. 1982;38: 149–158.

39. Straehler-Pohl I, Jarms G. Identification key for young ephyrae: A first step for early detection of jellyfish blooms. Hydrobiologia. 2010;645: 3–21.

40. Dawson MN, Jacobs DK. Molecular evidence for cryptic species of Aurelia aurita (Cnidaria, Scyphozoa). Biol Bull. 2001;200: 92–96. doi: 10.2307/1543089 11249217

41. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994;3: 294–299. 7881515

42. Matsumura K, Kamiya K, Yamashita K, Hayashi F, Watanabe I, Murao Y, et al. Genetic polymorphism of the adult medusae invading an electric power station and wild polyps of Aurelia aurita in Wakasa Bay, Japan. J Mar Biol Assoc U K. 2005;85: 563–568.

43. Larkin MA, Blackshields G, Brown NP, Chenna R, Mcgettigan PA, McWilliam H, et al. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23: 2947–2948. doi: 10.1093/bioinformatics/btm404 17846036

44. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35: 1547–1549. doi: 10.1093/molbev/msy096 29722887

45. Kimura M. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980;16: 111–120. doi: 10.1007/bf01731581 7463489

46. Endo N, Nogata Y, Sato K, Yoshimura E, Matsumura K, Sakaguchi I, et al. Genetic relationship of moon jellyfish Aurelia aurita s.l. in Tokyo Bay and Ise Bay based on nucleotide sequences of mitochondrial DNA. Bull Plankton Soc Japan. 2011;58: 1–11. (in Japanese with English abstract)

47. Dawson MN, Sen Gupta A, England MH. Coupled biophysical global ocean model and molecular genetic analyses identify multiple introductions of cryptogenic species. Proc Natl Acad Sci U S A. 2005;102: 11968–11973. doi: 10.1073/pnas.0503811102 16103373

48. Marshall DJ, Krug PJ, Kupriyanova EK, Byrne M, Emlet RB. The biogeography of marine invertebrate life histories. Annu Rev Ecol Evol Syst. 2012;43: 97–114.

49. Chia F-S, Gibson G, Qian P-Y. Poecilogony as a reproductive strategy of marine invertebrates. Oceanol Acta. 1996;19: 203–208.

50. Vendetti JE, Trowbridge CD, Krug PJ. Poecilogony and population genetic structure in Elysia pusilla (Heterobranchia: Sacoglossa), and reproductive data for five sacoglossans that express dimorphisms in larval development. Integr Comp Biol. 2012;52: 138–150. doi: 10.1093/icb/ics077 22659202

51. Han C-H, Kawahara M, Uye S. Seasonal variations in the trophic relationship between the scyphomedusa Aurelia aurita s.l. and mesozooplankton in a eutrophic brackish-water lake, Japan. Plankton Benthos Res. 2009;4: 14–22.

52. Makabe R, Kurihara T, Uye S. Spatio-temporal distribution and seasonal population dynamics of the jellyfish Aurelia aurita s.l. studied with Dual-frequency IDentification SONar (DIDSON). J Plankton Res. 2012;34: 936–950.

53. Miyake H, Iwao K, Kakinuma Y. Life history and environment of Aurelia aurita. South Pac Study. 1997;17: 273–285.

54. Makabe R, Furukawa R, Takao M, Uye S. Marine artificial structures as amplifiers of Aurelia aurita s.l. blooms: A case study of a newly installed floating pier. J Oceanogr. 2014;70: 447–455.

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

56. Kim YS, Moon TS. Filtering rate with effect of water temperature and size of two farming ascidians Styela clava and S. plicata, and a farming mussel Mytilus edulis. J Korean Fish Soc. 1998;31: 272–277. (in Korean with English abstract)

57. Ishii H, Katsukoshi K. Seasonal and vertical distribution of Aurelia aurita polyps on a pylon in the innermost part of Tokyo Bay. J Oceanogr. 2010;66: 329–336.

58. Marshall DJ, Keough MJ. The evolutionary ecology of offspring size in marine invertebrates. Adv Mar Biol. 2007;53: 1–60. doi: 10.1016/S0065-2881(07)53001-4 17936135

59. Thatje S, Hall S. The effect of temperature on the evolution of per offspring investment in a globally distributed family of marine invertebrates (Crustacea: Decapoda: Lithodidae). Mar Biol. 2016;163: 1–9.

60. Bagenal TB. The interrelation of the size of fish eggs, the date of spawning and the production cycle. J Fish Biol. 1971;3: 207–219.

61. Suzuki KS, Yasuda A, Murata Y, Kumakura E, Yamada S, Endo N, et al. Quantitative effects of pycnocline and dissolved oxygen on vertical distribution of moon jellyfish Aurelia aurita s.l.: A case study of Mikawa Bay, Japan. Hydrobiologia. 2016;766: 151–163.

62. Suzuki KS, Kumakura E, Endo N, Ishii H, Nogata Y. Effects of water mass structure on vertical distribution of moon jellyfish Aurelia aurita s.l. within aggregations in four Japanese coastal areas. Bull Plankton Soc Japan. 2017;64: 114–123. (in Japanese with English abstract)

63. Itoh H, Tachibana A, Nomura H, Tanaka Y, Furota T, Ishimaru T. Vertical distribution of planktonic copepods in Tokyo Bay in summer. Plankton Benthos Res. 2011;6: 129–134.

64. Schneider G, Weisse T. Metabolism measurements of Aurelia aurita planulae larvae, and calculation of maximal survival period of the free swimming stage. Helgol Meeresunters. 1985;39: 43–47.

65. Kamiyama T. Planktonic ciliates as food for the scyphozoan Aurelia coerulea: feeding and growth responses of ephyra and metephyra stages. J Oceanogr. 2017; 1–11.

66. Berrill NJ. Developmental analysis of scyphomedusae. Biol Rev. 1949;24: 393–409. doi: 10.1111/j.1469-185x.1949.tb00581.x 24536313

67. Parker GA, Begon M. Optimal egg size and clutch size: Effects of environment and maternal phenotype. Am Nat. 1986;128: 573–592.

68. Smith CC, Fretwell SD. The optimal balance between size and number of offspring. Am Nat. 1974;108: 499–506.

69. Thorson G. Reproductive and larval ecology of marine bottom invertebrates. Biol Rev. 1950;25: 1–45. doi: 10.1111/j.1469-185x.1950.tb00585.x 24537188

70. Komai T. On Stephanoscyphus and Nausithoe. Mem Coll Sci Kyoto Imp Univ Ser B. 1935;10: 290–339.

71. Morandini AC, Da Silveira FL. Sexual reproduction of Nausithoe aurea (Scyphozoa, Coronatae). Gametogenesis, egg release, embryonic development, and gastrulation. Sci Mar. 2001;65: 139–149.

72. Metschnikoff E. Embryologische Studien an Medusen, Ein Beitrag zur Genealogie der Primitiv-Organe. Hölder A, editor. Vienna; 1886.

73. Conklin EG. The habits and early development of Linerges mercurius. Publs Carnegie Instn. 1908;103: 155–170.

74. Jarms G, Båmstedt U, Tiemann H, Martinussen MB, Fosså JH. The holopelagic life cycle of the deep-sea medusa Periphylla periphylla (Scyphozoa, Coronatae). Sarsia. 1999;84: 55–65.

75. Uchida T. The anatomy and development of rhizostome medusa, Mastigias papua L. Agassiz with observation on the phylogeny of Rhizostomae. J Fac Sci Imp Univ Tokyo, Sect IV, Zool. 1926;1: 45–95.

76. Goette A. Entwicklungsgeschichte der Aurelia aurita und Cotylorhiza tuberculata. Hamburg und Leipzig: Leopold Voss; 1887.

77. Ikeda H, Ohtsu K, Uye S. Structural changes of gonads during artificially induced gametogenesis and spawning in the giant jellyfish Nemopilema nomurai (Scyphozoa: Rhizostomeae). J Mar Biol Assoc U K. 2011;91: 215–227.

78. Hyde IH. Entwickelungsgeschichte einiger Scyphomedusen. Zeitschrift für Wissenschaftliche Zool. 1894;58: 531–564.

79. Goette A. Vergleichende Entwicklungsgeschichte von Pelagia noctiluca Pér. Z wiss Zool. 1893;55: 645–695.

80. Hadzi J. Über die Podozysten der Scyphopolypen. Biol Zentralb. 1912;32: 52–60.

81. Teissier G. La croissance embryonnaire de Chrysaora hysoscella (L.). Arch Zool Exp Gen. 1929;69: 137–178.

82. Littleford RA. The life cycle of Dactylometra quinquecirrha, L. Agassiz in the Chesapeake Bay. Biol Bull. 1939;77: 368–381.

83. Hargitt CW, Hargitt GT. Studies on the development of scyphomedusae. J Morphol. 1910;21: 217–262.

84. Suzuki KS, Kumakura E, Nogata Y. Incidental consumption of ephyrae of moon jellyfish Aurelia aurita s.l. by three filter-feeding sessile organisms: laboratory experiments. Fish Sci. 2016;82: 923–930.

85. Iguchi N. Spatial/temporal variations in zooplankton biomass and ecological characteristics of major species in the southern part of the Japan Sea: A review. Prog Oceanogr. 2004;61: 213–225.

86. Ishii H, Kojima S, Tanaka Y. Survivorship and production of Aurelia aurita ephyrae in the innermost part of Tokyo Bay, Japan. Plankton Biol Ecol. 2004;51: 26–35.

87. Lamb PD, Hunter E, Pinnegar JK, van der Kooij J, Creer S, Taylor MI. Cryptic diets of forage fish: jellyfish consumption observed in the Celtic Sea and western English Channel. J Fish Biol. 2019;94: 1026–1032. doi: 10.1111/jfb.13926 30746684

88. Miyajima-Taga Y, Masuda R, Morimitsu R, Ishii H, Nakajima K, Yamashita Y. Ontogenetic changes in the predator–prey interactions between threadsail filefish and moon jellyfish. Hydrobiologia. 2016;772: 175–187.

89. Feng S, Wang S, Zhang G, Sun S, Zhang F. Selective suppression of in situ proliferation of scyphozoan polyps by biofouling. Mar Pollut Bull. 2017;114: 1046–1056. doi: 10.1016/j.marpolbul.2016.10.062 27890264

90. Hoover RA, Armour R, Dow I, Purcell JE. Nudibranch predation and dietary preference for the polyps of Aurelia labiata (Cnidaria: Scyphozoa). Hydrobiologia. 2012;690: 199–213.

91. Takao M, Okawachi H, Uye S. Natural predators of polyps of Aurelia aurita s.l. (Cnidaria: Scyphozoa: Semaeostomeae) and their predation rates. Plankton Benthos Res. 2014;9: 105–113.

92. Hernroth L, Gröndahl F. On the biology of Aurelia aurita (L.) 3. Predation by Coryphella verrucosa (Gastropoda, Opisthobranchia), a major factor regulationg the development of Aurelia populations in the Gullmar Fjord, western Sweden. Ophelia. 1985;24: 37–45.

93. Isomura N, Nishihira M. Size variation of planulae and its effect on the lifetime of planulae in three pocilloporid corals. Coral Reefs. 2001;20: 309–315.

94. O’Connor MI, Bruno JF, Gaines SD, Halpern BS, Lester SE, Kinlan BP, et al. Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation. Proc Natl Acad Sci U S A. 2007;104: 1266–1271. doi: 10.1073/pnas.0603422104 17213327

95. Ishii H, Watanabe T. Experimental study of growth and asexual reproduction in Aurelia aurita polyps. Sessile Org. 2003;20: 69–73.

Článek vyšel v časopise


2019 Číslo 11