Abstract
Scyphozoans display a high level of developmental plasticity, including asexual reproductive strategies in their polyps. Irrespective of the alternating medusa-polyp life cycle, life stages or even complete generations can be omitted, occasionally or consistently, in some species. For example, ephyrae can be produced directly by planulae, leaving out the polyp generation, and polyps can produce free-swimming planula-like propagules, thus bypassing the medusa generation. Here, we raised Chrysaora plocamia polyps under unusually high, naturally occurring temperatures, which resulted in these polyps being unable to strobilate but able to form podocysts. Early excysts that hatched from these podocysts produced ephyrae in a premature type of strobilation. This developmental shortcut, previously unknown in scyphozoan life cycles, is described in the present report.
This is a preview of subscription content, log in via an institution to check access.
References
Adler L, Jarms G (2009) New insights into reproductive traits of scyphozoans: special methods of propagation in Sanderia malayensis GOETTE, 1886 (Pelagiidae, Semaeostomeae) enable establishing a new classification of asexual reproduction in the class Scyphozoa. Mar Biol 156:1411–1420. https://doi.org/10.1007/s00227-009-1181-6
Arai MN (1997) A functional biology of Scyphozoa. Chapman & Hall, London
Arai MN (2009) The potential importance of podocysts to the formation of scyphozoan blooms: a review. Hydrobiologia 616:241–246. https://doi.org/10.1007/s10750-008-9588-5
Berrill N (1949) Developmental analysis of scyphomedusae. Biol Rev 24:393–409. https://doi.org/10.1111/j.1469-185X.1949.tb00581.x
Bouillon J, Boero F, Fraschetti S (1991) The life cycle of Laodicea indica (Laodiceidae, Leptomedusae, Cnidaria). Hydrobiologia 216:151–157
Ceh J, Gonzalez J, Pacheco AS, Riascos JM (2015) The elusive life cycle of scyphozoan jellyfish – metagenesis revisited. Sci Rep 5:12037. https://doi.org/10.1038/srep12037
Daryanabard R, Dawson MN (2008) Jellyfish blooms: Crambionella orsini (Scyphozoa: Rhizostomeae) in the Gulf of Oman, Iran, 2002–2003. J Mar Biol Assoc UK 88:477–483. https://doi.org/10.1017/S0025315408000945
Dawson M, Martin L (2001) Geographic variation and ecological adaptation in Aurelia (Scyphozoa, Semaeostomeae): some implications from molecular phylogenetics. Hydrobiologia 451:259–273. https://doi.org/10.1023/A:1011869215330
Fuchs B, Wang W, Graspeuntner S, Li Y, Insua S, Herbst EM, Dirksen P, Böhm AM, Hemmrich G, Sommer F, Domazet-Lošo T, Klostermeier UC, Anton-Erxleben F, Rosenstiel P, Bosch TCG, Khalturin K (2014) Regulation of polyp-to-jellyfish transition in Aurelia aurita. Curr Biol 24:263–273. https://doi.org/10.1016/j.cub.2013.12.003
Hadži J (1909) Rückgängig gemachte Entwicklung einer Scyphomeduse. Zool Anz 34:94–100
Han CH, Uye SI (2010) Combined effects of food supply and temperature on asexual reproduction and somatic growth of polyps of the common jellyfish Aurelia aurita sl. Plankt Benth Res 5:98–105. https://doi.org/10.3800/pbr.5.98
He J, Zheng L, Zhang W, Lin Y (2015) Life cycle reversal in Aurelia sp. 1 (Cnidaria, Scyphozoa). PLoS ONE 10:e0145314. https://doi.org/10.1371/journal.pone.0145314
Helm RR (2018) Evolution and development of scyphozoan jellyfish. Biol Rev 93:1228–1250. https://doi.org/10.1111/brv.12393
Hofmann DK, Neumann R, Henne K (1978) Strobilation, budding and initiation of scyphistoma morphogenesis in the rhizostome Cassiopea andromeda (Cnidaria: Scyphozoa). Mar Biol 47:161–176. https://doi.org/10.1007/BF00395637
Jarms G, Båmstedt U, Tiemann H, Martinussen MB, Fosså JH (1999) The holopelagic life cycle of the deep-sea medusa Periphylla periphylla (Scyphozoa, Coronatae). Sarsia 84:55–65. https://doi.org/10.1080/00364827.1999.10420451
Jarms G (2010) The early life history of Scyphozoa with emphasis on Coronatae. Verh Naturwiss Ver Hamburg 45:17–31
Loeb MJ (1972) Strobilation in the Chesapeake Bay sea nettle Chrysaora quinquecirrha. I. The effects of environmental temperature changes on strobilation and growth. J Exp Zool 180:279–292. https://doi.org/10.1002/jez.1401800214
Loeb MJ (1974) Strobilation in the Chesapeake Bay sea nettle Chrysaora quinquecirrha - III. Dissociation of the neck-inducing factor from strobilating polyps. Comp Biochem Physiol 49A:423–432. https://doi.org/10.1016/0300-9629(74)90558-1
Lucas CH, Graham WM, Widmer C (2012) Jellyfish life histories: role of polyps in forming and maintaining scyphomedusa populations. Adv Mar Biol 63:133–196. https://doi.org/10.1016/B978-0-12-394282-1.00003-X
Morandini AC, Marques AC (2010) Revision of the genus Chrysaora Péron & Lesueur, 1810 (Cnidaria: Scyphozoa). Zootaxa 2464:1–97. https://doi.org/10.11646/zootaxa.2464.1.1
Piraino S, De Vito D, Schmich J, Bouillon J, Boero F (2004) Reverse development in Cnidaria. Can J Zool 82:1748–1754. https://doi.org/10.1139/z04-174
Riascos JM, Paredes L, González K, Cáceres I, Pacheco AS (2013) The larval and benthic stages of the scyphozoan medusa Chrysaora plocamia under El Niño–La Niña thermal regimes. J Exp Mar Biol Ecol 446:95–101. https://doi.org/10.1016/j.jembe.2013.05.006
Riascos JM, Villegas V, Pacheco AS (2014) Diet composition of the large scyphozoan jellyfish Chrysaora plocamia in a highly productive upwelling centre off northern Chile. Mar Biol Res 10:791–798. https://doi.org/10.1080/17451000.2013.863353
Rottini Sandrini L, Avian M (1983) Biological cycle of Pelagia noctiluca: morphological aspects of the development from planula to ephyra. Mar Biol 74:169–174. https://doi.org/10.1007/BF00413920
Schiariti A, Morandini AC, Jarms G, Paes R, Franke S, Mianzan H (2014) Asexual reproduction strategies and blooming potential in Scyphozoa. Mar Ecol Prog Ser 510:241–253. https://doi.org/10.3354/meps10798
Silveira FLD, Jarms G, Morandini AC (2003) Experiments in nature and laboratory observations with Nausithoe aurea (Scyphozoa: Coronatae) support the concept of perennation by tissue saving and confirm dormancy. Biota Neotrop 2:1–25. https://doi.org/10.1590/S1676-06032002000200009
Spangenberg DB (1967) Iodine induction of metamorphosis in Aurelia. J Exp Zool 165:441–450. https://doi.org/10.1002/jez.1401650312
Vagelli A (2007) New observations on the asexual reproduction of Aurelia aurita (Cnidaria, Scyphozoa) with comments on its life cycle and adaptive significance. Invertebr Zool 4:111–127
Widmer CL (2008) Life cycle of Chrysaora fuscescens (Cnidaria: Scyphozoa) and a key to sympatric ephyrae. Pac Sci 62:71–82. https://doi.org/10.2984/1534-6188(2008)62[71:LCOCFC]2.0.CO;2
Yasuda T (1975) 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 22:75–80. https://doi.org/10.5134/175889
Acknowledgements
The authors thank Felipe Docmac and Claudia Infante for assisting with photography and for providing their stereoscope and camera, respectively. We thank the three anonymous reviewers for their insightful comments and suggestions.
Funding
JC was a recipient of a CONICYT/FONDECYT Grant (Number 11140353).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This study was approved by the Comité de Ética de Investigación Científica, University of Antofagasta. All applicable international, national, and/or institutional guidelines for animal testing, animal care, and use of animals were followed by the authors.
Sampling and field studies
All necessary permits for sampling have been obtained by the authors from the competent authorities. The study is compliant with CBD and Nagoya protocols.
Data availability
All data generated during this study are included in this published article.
Author contribution statement
LC, KG, and JC did the lab work. JC did the field work. JC wrote the manuscript. LC contributed to the writing. LC and JC contributed equally to this work. All authors read and approved the manuscript.
Additional information
Communicated by B. W. Hoeksema
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Campos, L., González, K. & Ceh, J. First report of a precocious form of strobilation in a jellyfish, the South American Pacific sea nettle Chrysaora plocamia. Mar. Biodivers. 50, 85 (2020). https://doi.org/10.1007/s12526-020-01106-3
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12526-020-01106-3