Advertisement

Ecological aspects of early life stages of Cotylorhiza tuberculata (Scyphozoa: Rhizostomae) affecting its pelagic population success

  • Diana Astorga
  • Javier Ruiz
  • Laura PrietoEmail author
Chapter
  • 659 Downloads
Part of the Developments in Hydrobiology book series (DIHY, volume 220)

Abstract

Cotylorhiza tuberculata is a common symbiotic scyphozoan in the Mediterranean Sea. The medusae occur in extremely high abundances in enclosed coastal areas in the Mediterranean Sea. Previous laboratory experiments identified thermal control on its early life stages as the driver of medusa blooms. In the present study, new ecological aspects were tested in laboratory experiments that support the pelagic population success of this zooxanthellate jellyfish. We hypothesized that planulae larvae would have no settlement preference among substrates and that temperature would affect ephyra development, ingestion rates and daily ration. The polyp budding rate and the onset of symbiosis with zooxanthellae also were investigated. Transmission electron microscopy revealed that zooxanthella infection occurred by the polyp stage. Our results showing no substrate selectivity by planulae and high polyp budding rates in high temperatures suggest increased benthic polyp populations, which would lead to higher medusa abundances. Rates of transition from ephyrae to medusae and the feeding of early medusa stages also increased with temperature. Continuing changes in coastal ecosystems such as future climate warming and marine construction may lead to increased populations of jellyfish to the detriment of fish globally.

Keywords

Jellyfish Mediterranean sea Planulae settlement Zooxanthellae Feeding Growth Reproduction 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgments

The authors thank A. Moreno, F. Rey and J. Pampín for their support on medusa sampling; Dr. A. García and O. Aliseda for assistance with electronic microscopy; Dr. A. Medina and A. Santos for their support and advice regarding microscopic preparations; and the reviewers and editor for helpful suggestions. This work was financially supported by projects PERSEUS (FP7-287600), JELLY-PHYS (CTM2011-22856), Junta de Andalucía (P07-RNM-02976), and Observatorio del Estrecho. A research grant to L. Prieto from Ramon y Cajal Programme of Spanish MIC, and an I3P-CSIC (partly funded by the European Social Fund, ESF) pre-doctoral fellowship to D. Astorga, are also acknowledged.

References

  1. Achituv, Y., Y. Benayahu & J. Hanania, 1992. Planulae brooding and acquisition of zooxanthellae in Xenia macrospiculata (Cnidaria: Octocorallia). Helgoländer Meeresuntersuchungen 46: 301–310.CrossRefGoogle Scholar
  2. Arai, M. N., 1997. A Functional Biology of Scyphozoa. Chapman and Hall, London.Google Scholar
  3. Arai, M. N., 2001. Pelagic coelenterates and eutrophication: a review. Hydrobiologia 451: 69–87.CrossRefGoogle Scholar
  4. Attrill, M. J., J. Wright & M. Edwards, 2007. Climate-related increases in jellyfish frequency suggest a more gelatinous future for the North Sea. Limnology and Oceanography 52: 480–485.CrossRefGoogle Scholar
  5. Båmstedt, U., 1990. Trophodynamics of the scyphomedusae Aurelia aurita. Predation rate in relation to abundance, size and type of prey organism. Journal of Plankton Research 12: 215–229.CrossRefGoogle Scholar
  6. Båmstedt, U., J. Lane & M. B. Martinussen, 1999. Bioenergetics of ephyrae larvae of the scyphozoan jellyfish Aurelia aurita in relation to temperature and salinity. Marine Biology 135: 89–98.CrossRefGoogle Scholar
  7. Båmstedt, U., B. Wild & M. B. Martinussen, 2001. Significance of food type for growth of ephyrae Aurelia aurita (Scyphozoa). Marine Biology 139: 641–650.CrossRefGoogle Scholar
  8. Belkin, I. M., 2009. Rapid warming of Large Marine Ecosystems. Progress in Oceanography 81: 207–213.CrossRefGoogle Scholar
  9. Brewer, R. H., 1989. The annual pattern of feeding, growth, and sexual reproduction in Cyanea (Cnidaria: Scyphozoa) in the Niantic River Estuary, Connecticut. Biological Bulletin 176: 272–281.CrossRefGoogle Scholar
  10. Brodeur, R. D., C. L. Suchman, D. C. Reese, T. W. Miller & E. A. Daly, 2008. Spatial overlap and trophic interactions between pelagic fish and large jellyfish in the northern California Current. Marine Biology 154: 649–659.CrossRefGoogle Scholar
  11. Calvín, J. C., I. Franco Navarro, A. Marín, A. M. Martínez Inglés, A. Belmonte Ríos, J. M. Ruiz Fernández, A. Belando Franco, M. Vicente Albaladejo & J. M. Rocamora Tomás, 1999. El Litoral Sumergido de la Región de Murcia. Cartografía Bionómica y Valores Ambientales. Consejería de Medio Ambiente, Agricultura y Agua, Región de Murcia.Google Scholar
  12. Carli, A., V. Pane, T. Valente & S. Cotta, 1991. Lipid and protein content of jellyfish from the Ligurian Sea. First results. In Jellyfish Blooms in the Mediterranean. Proceedings of the II Workshop on Jellyfish in the Mediterranean Sea. MAP Technical Report Series 47 UNEP, Athens: 236–240.Google Scholar
  13. Cevik, C., O. B. Derici, F. Cevik & L. Cavas, 2011. First record of Phyllorhiza punctata von Lendenfeld, 1884 (Scyphozoa: Rhizostomeae: Mastigiidae) from Turkey. Aquatic Invasions 6: S27–S28.CrossRefGoogle Scholar
  14. Claus, C., 1890. Über die Entwicklung des Scyphostoma von Cotylorhiza, Aurelia, und Chrysaora, sowie ueber die systematische Stellung der Scyphomedusen. I Arbeiten aus den Zoologischen Instituten der Universität Wien 9: 85–128.Google Scholar
  15. Claus, C., 1893. Über die Entwicklung des Scyphostoma von Cotylorhiza, Aurelia, und Chrysaora, sowie ueber die systematische Stellung der Scyphomedusen. II Arbeiten aus den Zoologischen Instituten der Universität Wien 10: 1–70.Google Scholar
  16. Daly Yahia, M. N., J. Goy & O. Daly Yahia-Kéfi, 2003. Distribution et écologie des Méduses (Cnidaria) du golfe de Tunis (Méditerranée sud occidentale). Oceanologica Acta 26: 645–655.CrossRefGoogle Scholar
  17. Fuentes, V. L., D. L. Angel, K. M. Bayha, D. Atienza, D. Edelist, C. Bordehore, J. M. Gili & J. E. Purcell, 2010. Blooms of the invasive ctenophore, Mnemiopsis leidyi, span the Mediterranean Sea in 2009. Hydrobiologia 645: 23–37.CrossRefGoogle Scholar
  18. Galil, B. S., L. Shoval & M. Goren, 2009. Phyllorhiza punctata von Lendenfeld, 1884 (Scyphozoa: Rhizostomeae: Mastigiidae) reappeared off the Mediterranean coast of Israel. Aquatic Invasions 4: 481–483.CrossRefGoogle Scholar
  19. Gibbons, M. J. & A. J. Richardson, 2009. Patterns of jellyfish abundance in the North Atlantic. Hydrobiologia 616: 51–65.CrossRefGoogle Scholar
  20. Gröndahl, F. & L. Hernroth, 1987. Release and growth of Cyanea capillata (L.) ephyrae in the Gullmar Fjord, western Sweden. Journal of Experimental Marine Biology and Ecology 106: 91–101.CrossRefGoogle Scholar
  21. Gülsahin, N. & A. N. Tarkan, 2011. A familiar organism in Mugla Region Cotylorhiza tuberculata (Macri, 1778). In Turan, C. & B. Öztürk (eds), First National Workshop on Jellyfish and Other Gelatinous Species in Turkish Marine Waters. Turkish Marine Research Foundation 35, Istanbul: 53–57.Google Scholar
  22. 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.PubMedCrossRefGoogle Scholar
  23. Hamner, W. M. & M. N. Dawson, 2009. A review and synthesis on the systematics and evolution of jellyfish blooms: advantageous aggregations and adaptive assemblages. Hydrobiologia 616: 161–191.CrossRefGoogle Scholar
  24. Hay, S., 2006. Marine ecology: gelatinous bells may ring change in marine ecosystems. Current Biology 16: 679–682.CrossRefGoogle Scholar
  25. Hiromi, J., T. Kasuya & H. Ishii, 2005. Impacts of massive occurrence of jellyfish on pelagic ecosystem. Bulletin of Plankton Society of Japan 52: 82–90.Google Scholar
  26. Hofmann, D. K. & G. Crow, 2002. Induction of larval metamorphosis in the tropical scyphozoan Mastigias papua: striking similarity with upside down-jellyfish Cassiopea spp. (with notes on related species). Vie et Milieu 52: 141–147.Google Scholar
  27. Hofmann, D. K., R. Neuman & K. Henne, 1978. Strobilation, budding and initiation of scyphistoma morphogenesis in the rhizostome Cassiopea andromeda (Cnidaria: Scyphozoa). Marine Biology 47: 161–176.CrossRefGoogle Scholar
  28. Holst, S. & G. Jarms, 2007. Substrate choice and settlement preferences of planula larvae of 453 five Scyphozoa (Cnidaria) from German Bight, North Sea. Marine Biology 151: 863–871.CrossRefGoogle Scholar
  29. Holst, S., I. Sötje, H. Tiemann & G. Jarms, 2007. Life cycle of the rhizostome jellyfish Rhizostoma octopus (L.) (Scyphozoa, Rhizostomeae), with studies on cnidocysts and statoliths. Marine Biology 151: 1695–1710.CrossRefGoogle Scholar
  30. Hoover, R. A. & J. E. Purcell, 2009. Substrate preferences of scyphozoan Aurelia labiata polyps among common dock-building materials. Hydrobiologia 616: 259–267.CrossRefGoogle Scholar
  31. IPCC, 2007. Climate Change 2007: Synthesis Report. In Core Writing Team, Pachauri, R. K. & Reisinger, A. (eds), Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva.Google Scholar
  32. Issel, R., 1922. Nuove indagini sul plankton nelle aquae di Rovigno. Memorie R. Comitato Talassografico Italiano 102: 1–36.Google Scholar
  33. Kikinger, R., 1992. Cotylorhiza tuberculata (Cnidaria: Scyphozoa)- life history of a stationary population. PSZNI Marine Ecology 13: 333–362.CrossRefGoogle Scholar
  34. Kogovsek, T., B. Bogunovic & A. Malej, 2010. Recurrence of bloom-forming scyphomedusae: wavelet analysis of a 200-year time series. Hydrobiologia 645: 81–96.CrossRefGoogle Scholar
  35. Kroiher, M. & S. Berking, 1999. On natural metamorphosis inducers of the cnidarian Hydractinia echinata (Hydrozoa) and Aurelia aurita (Scyphozoa). Helgoland Marine Research 53: 118–121.CrossRefGoogle Scholar
  36. Lakkis, S., 1991. Aggregations of the scyphomedusa Rhizostoma pulmo in the Lebanese coastal waters during the summer of 1986. In Jellyfish Blooms in the Mediterranean. Proceedings of the II Workshop on Jellyfish in the Mediterranean Sea. MAP Technical Report Series 47. UNEP, Athens: 119–127.Google Scholar
  37. Lo, W. T. & I. L. Chen, 2008. Population succession and feeding of scyphomedusae Aurelia aurita in a eutrophic tropical lagoon in Taiwan. Estuarine, Coastal and Shelf Science 76: 227–238.CrossRefGoogle Scholar
  38. Lucas, C. H., 2001. Reproduction and life history strategies of the common jellyfish, Aurelia aurita, in relation to its ambient environment. Hydrobiologia 451: 55–68.CrossRefGoogle Scholar
  39. Ludwig, F. D., 1969. Die Zooxanthellen bei Cassiopea andromeda, Eschscholtz 1829 (Polyp Stadium) und Ihre Bedeutung für die Strobilation. Zoologische Jahrbbucher-Abteilung für Anatomie und Ontogenie der Tiere 86: 238–277.Google Scholar
  40. Lynam, C. P., S. J. Hay & A. S. Brierley, 2005. Jellyfish abundance and climatic variation: contrasting responses in oceanographically distinct regions of the North Sea, and possible implications for fisheries. Journal of the Marine Biological Association of the United Kingdom 85: 435–450.CrossRefGoogle Scholar
  41. Ma, X. & J. E. Purcell, 2005. Temperature, salinity, and prey effects on polyp versus medusa bud production by the invasive hydrozoan Moerisia lyonsi. Marine Biology 147: 225–234.CrossRefGoogle Scholar
  42. Mas, J., 1999. Estudio de la dinámica de poblaciones de las medusas Cotylohiza tuberculata, Rhizostoma pulmo y Aurelia aurita en el Mar Menor y su problemática asociada. Instituto Español de Oceanografía, La Coruña, Internal Report.Google Scholar
  43. Mills, C. E., 1995. Medusae, siphonophores, and ctenophores as planktivorous predators in changing global ecosystems. ICES Journal of Marine Science 52: 575–581.CrossRefGoogle Scholar
  44. Mills, C. E., 2001. Jellyfish blooms: are populations increasing globally in response to changing ocean conditions? Hydrobiologia 451: 55–68.CrossRefGoogle Scholar
  45. Möller, H., 1980. Population dynamics of Aurelia aurita medusae in the Kiel Bight, Germany (FRG). Marine Biology 60: 123–128.CrossRefGoogle Scholar
  46. Montgomery, M. K. & P. M. Kremer, 1995. Transmission of symbiotic dinoflagellates through the sexual cycle of the host scyphozoan Linuche unguiculata. Marine Biology 124: 147–155.CrossRefGoogle Scholar
  47. Nawroth, J. C., K. E. Feitl, S. P. Colin, J. H. Costello & J. O. Dabiri, 2010. Phenotypic plasticity in juvenile jellyfish medusae facilitates effective animal-fluid interaction. Biology Letters 6: 389–393.PubMedCrossRefGoogle Scholar
  48. Pagès, F., 2001. Past and present anthropogenic factors promoting the invasion, colonization and dominance by jellyfish of a Spanish coastal lagoon. In CIESM Gelatinous Zooplankton Outbreaks: Theory and Practice 14. CIESM Workshop Series, Monaco: 69–71.Google Scholar
  49. Parsons, T. R. & C. M. Lalli, 2002. Jellyfish population explosions: revisiting a hypothesis of possible causes. La Mer 40: 111–121.Google Scholar
  50. Pauly, D., V. Christensen, S. Guénette, T. J. Pitcher, U. R. Sumaila, C. J. Walters, R. Watson & D. Zeller, 2002. Towards sustainability in world fisheries. Nature 418: 695–986.CrossRefGoogle Scholar
  51. Pérez-Ruzafa, A. & C. Marcos, 1992. Colonization rates and dispersal as essential parameters in the confinement theory to explain the structure and horizontal zonation of lagoon benthic assemblages. Rapports et Proces-Verbaux des Reunions Commission Internationale pour l’Exploration Scientifique de la Mer Mediterranee 33: 100.Google Scholar
  52. Pérez-Ruzafa, A., C. Marcos, M. Pérez-Ruzafa & J. D. Ros, 1987. Evolución de las características ambientales y los poblamientos del Mar Menor (Murcia, SE de España). Anales de Biología 12(Biología Ambiental 3): 53–65.Google Scholar
  53. Pérez-Ruzafa, A., C. Marcos-Diego & J. D. Ros, 1991. Environmental and biological changes related to recent human activities in the Mar Menor (SE of Spain). Marine Pollution Bulletin 23: 747–751.CrossRefGoogle Scholar
  54. Pérez-Ruzafa, A., J. Gilabert, J. M. Gutiérrez, A. I. Fernández, C. Marcos & S. Sabah, 2002. Evidence of a planktonic food web response to changes in nutrient input dynamics in the Mar Menor coastal lagoon, Spain. Hydrobiologia 475–476: 359–369.CrossRefGoogle Scholar
  55. Pérez-Ruzafa, A., M. I. Hegazi, I. M. Pérez-Ruzafa & C. Marcos, 2008. Differences in spatial and seasonal patterns of macrophyte assemblages between a coastal lagoon and the open sea. Marine Environmental Research 65: 291–314.PubMedCrossRefGoogle Scholar
  56. Pierce, J., 2005. A system for mass culture of upside-down jellyfish Cassiopea spp. as a potential food item for medusivores in captivity. International Zoo Yearbook 39: 62–69.CrossRefGoogle Scholar
  57. Pitt, K. A., 2000. Life history and settlement preferences of the edible jellyfish Catostylus mosaicus (Scyphozoa: Rhizostomeae). Marine Biology 136: 269–279.CrossRefGoogle Scholar
  58. Pitt, K. A. & J. E. Purcell (eds), 2009. Jellyfish blooms: causes, consequences, and recent advances, Hydrobiologia, Vol. 616. Springer, Dordrecht.Google Scholar
  59. Pitt, K. A., K. Koop & D. Rissik, 2005. Contrasting contributions to inorganic nutrient recycling by the co-occurring jellyfishes, Catostylus mosaicus and Phyllorhiza punctata (Scyphozoa, Rhizostomeae). Journal of Experimental Marine Biology and Ecology 315: 71–86.CrossRefGoogle Scholar
  60. Prieto, L., D. Astorga, G. Navarro & J. Ruiz, 2010. Environmental control of phase transition and polyp survival of a massive-outbreaker jellyfish. PLoS ONE 5: e13793.PubMedCrossRefGoogle Scholar
  61. Purcell, J. E., 2005. Climate effects on formation of jellyfish and ctenophore blooms: a review. Journal of the Marine Biological Association of the United Kingdom 85: 461–476.CrossRefGoogle Scholar
  62. Purcell, J. E., 2012. Jellyfish and ctenophore blooms coincide with human proliferations and environmental perturbations. Annual Review of Marine Science 4: 209–235.PubMedCrossRefGoogle Scholar
  63. Purcell, J. E. & M. V. Sturdevant, 2001. Prey selection and dietary overlap among zooplanktivorous jellyfish and juvenile fishes in Prince William Sound, Alaska. Marine Ecology Progress Series 210: 67–83.CrossRefGoogle Scholar
  64. Purcell, J. E., T. A. Shiganova, M. B. Decker & E. D. Houde, 2001. The ctenophore Mnemiopsis in native and exotic habitats: US estuaries versus the Black Sea basin. Hydrobiologia 451: 145–176.CrossRefGoogle Scholar
  65. Purcell, J. E., S. I. Uye & W. T. Lo, 2007. Anthropogenic causes of jellyfish blooms and direct consequences for humans: a review. Marine Ecology Progress Series 350: 153–174.CrossRefGoogle Scholar
  66. Purcell, J. E., D. Atienza, V. Fuentes, A. Olariaga, U. Tilves, C. Colahan, J.-M. Gili, 2012. Temperature effects on asexual reproduction rates of Scyphozoan species from the northwest Mediterranean Sea. Hydrobiologia. doi: 10.1007/s10750-012-1047-7.
  67. Rahat, M. & O. Adar, 1980. Effect of symbiotic zooxanthellae and temperature on budding and strobilation in Cassiopea andromeda (Eschscholtz). Biological Bulletin 159: 394–401.CrossRefGoogle Scholar
  68. Richardson, A. J., A. Bakun, G. C. Hays & M. J. Gibbons, 2009. The jellyfish joyride: causes, consequences and management to a more gelatinous future. Trends in Ecology & Evolution 24(6): 312–322.CrossRefGoogle Scholar
  69. Rippingale, R. J. & S. J. Kelly, 1995. Reproduction and survival of Phyllorhiza punctata (Cnidaria: Rhizostomeae) in a seasonally fluctuating salinity regime in Western Australia. Marine Freshwater Research 46: 1145–1151.CrossRefGoogle Scholar
  70. Schiriati, A., M. Kawahara, S. Uye & H. W. Mianzan, 2008. Life cycle of the jellyfish Lychnorhiza lucerna (Scyphozoa: Rhizostomeae). Marine Biology 156: 1–12.CrossRefGoogle Scholar
  71. Schwarz, J. A., D. A. Krupp & V. M. Weis, 1999. Late larval development and onset of symbiosis in the scleractinian coral Fungia scutaria. Biological Bulletin 196: 70–79.CrossRefGoogle Scholar
  72. Shiganova, T. A., Z. A. Mirzoyan & E. A. Studenikina, 2001. Population development of the invader ctenophore Mnemiopsis leidyi, in the Black Sea and in other seas of the Mediterranean basin. Marine Biology 139: 431–445.CrossRefGoogle Scholar
  73. Straehler-Pohl, I. & G. Jarms, 2010. Identification key for young ephyrae: a first step for early detection of jellyfish blooms. Hydrobiologia 645: 3–21.CrossRefGoogle Scholar
  74. Sugiura, Y., 1964. On the life-history of rhizostome medusae. II. Indispensability of zooxanthellae for strobilation in Mastigias papua. Embryologia 8: 223–233.CrossRefGoogle Scholar
  75. Sugiura, Y., 1965. On the life–history of rhizostomae medusae. III On the effects of temperature on the strobilation of Mastigias papua. Biological Bulletin 28: 493–496.CrossRefGoogle Scholar
  76. Thornhill, D. J., M. W. Daniel & T. C. LaJeunesse, 2006. Natural infections of aposymbiotic Cassiopea xamachana scyphistomae from environmental pools of Symbiodinium. Journal of Experimental Marine Biology and Ecology 338: 50–56.CrossRefGoogle Scholar
  77. Uye, S. & Y. Ueta, 2004. Recent increase of jellyfish populations and their nuisance to fisheries in the Inland Sea of Japan. Bulletin of the Japanese Society of Fisheries and Oceanography 68: 9–19.Google Scholar
  78. Vinogradov, M. E. & E. A. Shushkina, 1992. Temporal changes in community structure in the open Black Sea. Oceanology 32: 485–491.Google Scholar
  79. Widmer, C. L., 2005. Effects of temperature on growth of north-east Pacific moon jellyfish ephyrae, Aurelia labiata (Cnidaria: Scyphozoa). Journal of the Marine Biological Association of the United Kingdom 85: 569–573.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Instituto de Ciencias Marinas de Andalucía (CSIC)Puerto RealSpain

Personalised recommendations