Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-16T03:24:23.616Z Has data issue: false hasContentIssue false
  • English
  • Français

Gonad morphology and gametogenesis in the deep-sea jellyfish Atolla wyvillei and Periphylla periphylla (Scyphozoa: Coronatae) collected from Cape Hatteras and the Gulf of Mexico

Published online by Cambridge University Press:  03 November 2009

Cathy H. Lucas  and
Adam J. Reed
Cathy H. Lucas*
Affiliation:
School of Ocean & Earth Science, University of Southampton, National Oceanography Centre, European Way, Southampton, SO14 3ZH, UK
Adam J. Reed
Affiliation:
School of Ocean & Earth Science, University of Southampton, National Oceanography Centre, European Way, Southampton, SO14 3ZH, UK
*
Correspondence should be addressed to: C.H. Lucas, School of Ocean & Earth Science, University of Southampton, National Oceanography Centre, European Way, Southampton, SO14 3ZH, UK email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Observations on gonad morphology and the structure of ovaries and testes of the coronate scyphozoans Atolla wyvillei and Periphylla periphylla are described based on samples collected from the Gulf of Mexico and Cape Hatteras (north-western Atlantic). In A. wyvillei, gonads of distinguishable sex were observed in medusae as small as 17 mm bell diameter (BD). Spermatogenesis occurred within follicles (average 366 × 254 μm) that were evenly distributed throughout the gonad. Oocytes in different stages of development were observed in all the females with gonads. Oocytes arise from the gastrodermis and migrate into the mesoglea to develop from early-mid to late vitellogenic oocytes characterized by a large nucleus and granular (organic-rich) cytoplasm. The largest oocytes measured were 543 μm and 263 μm from the Gulf of Mexico and Cape Hatteras respectively. Possible reasons for this difference are discussed. In P. periphylla gonads were also initially observed in medusae 17 mm BD, although not all larger medusae had obvious gonads. Unlike A. wyvillei sperm follicles were arranged in long convoluted rows normally only one follicle thick. The organization of ooytes in female P. periphylla was very similar to A. wyvillei, although the gonads were small and the number of oocytes present in each gonad very low (<22). The largest oocyte measured was 777 μm in a 53 mm BD medusa. Although medusae were collected from one time period only (September) in this study, our findings appear to be in agreement with literature evidence indicating that coronate jellyfish produce few eggs continuously over a long time period. Aspects of gonad development and gametogenesis are discussed with respect to potential differences in site productivity and species identification.

Keywords

jellyfishAtollaPeriphyllagametogenesisoocytessperm folliclescontinuous reproduction
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 90 , Special Issue 6: In Honour of Sir Frederick Stratten Russell, FRS , September 2010 , pp. 1095 - 1104
Copyright
Copyright © Marine Biological Association of the United Kingdom 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Arai, M.N. (1997) A functional biology of Scyphozoa. London: Chapman and Hall, 316 pp.Google Scholar
Berrill, N.J. (1949) Developmental analysis of scyphomedusae. Biological Review Cambridge 24, 393–410.CrossRefGoogle ScholarPubMed
Campbell, R.D. (1974) Cnidaria. In Giese, A.C. and Pearse, J.S. (eds) Reproduction of marine invertebrates, Volume I, Acoelomate and pseuocoelomate metazoans. New York: Academic Press, pp. 133–199.CrossRefGoogle Scholar
Claus, C. (1883) Untersuchungen über die Organisation und Entwicklung der Medusen. Leipzig: Prag.CrossRefGoogle Scholar
Dalpadado, P., Ellersten, B., Melle, W. and Skjoldal, H.R. (1998) Summer distribution patterns and biomass estimates of macrozooplankton and micronekton in Nordic seas. Sarsia 83, 103–116.CrossRefGoogle Scholar
Dawson, M.N. and Jacobs, D.K. (2001) Molecular evidence for cryptic species of Aurelia aurita (Cnidaria, Scyphozoa). Biological Bulletin. Marine Biological Laboratory, Woods Hole 200, 92–96.CrossRefGoogle ScholarPubMed
Donnelly, J., Sutton, T.T. and Torres, J.J. (2006) Distribution and abundance of micronekton and macrozooplankton in the NW Weddell Sea: relation to a spring ice-edge bloom. Polar Biology 29, 280–293.CrossRefGoogle Scholar
Eckelbarger, K.J. (1994) Oocyte nutrition in the lower Metazoa: the Scyphozoa. In Wilson, W.H., Stricker, S.A. and Shinn, G.L. (eds) Reproduction and development of marine invertebrates. Baltimore: Johns Hopkins University Press, pp. 15–28.Google Scholar
Eckelbarger, K.J. and Larson, R.J. (1988) Ovarian morphology and oogenesis in Aurelia aurita (Scyphozoa: Semaeostomae): ultrastructural evidence of heterosynthetic yolk formation in a primitive metazoan. Marine Biology 100, 103–115.CrossRefGoogle Scholar
Eckelbarger, K.J. and Larson, R.J. (1992) Ultrastructure of the ovary and oogenesis in the jellyfish Linuche unguiculata and Stomolophus meleagris, with a review of ovarian structure in the Scyphozoa. Marine Biology 114, 633–643.CrossRefGoogle Scholar
Gershwin, L. and Zeidler, W. (2008) Some new and previously unrecorded Scyphomedusae (Cnidaria: Scyphozoa) from southern Australian coastal waters. Zootaxa 1744, 1–18.CrossRefGoogle Scholar
Haeckel, E. (1882) Report on the deep-sea medusae dredged by H.M.S. Challenger during the years of 1873–1876. Report on the scientific results of the voyage of H.M.S. Challenger during the years 1873–1876. Zoology, IV (part II), i-cv, pp. 1–154.Google Scholar
Jarms, G., Båmstedt, U., Tiemann, H., Martinussen, M.B. and Fosså, J.H. (1999) The holopelagic life cycle of the deep-sea medusa Periphylla periphylla (Scyphozoa, Coronatae). Sarsia 84, 55–65.CrossRefGoogle Scholar
Jarms, G., Tiemann, H. and Båmstedt, U. (2002) Development and biology of Periphylla periphylla (Scyphozoa: Coronatae) in a Norwegian fjord. Marine Biology 141, 647–657.Google Scholar
Kaartvedt, S., Klevjer, T.A., Torgersen, T., Sørnes, T.A. and Rostad, A. (2007) Diel vertical migration of individual jellyfish (Periphylla periphylla). Limnology and Oceanography 52, 975–983.CrossRefGoogle Scholar
Kikinger, R. (1992) Cotylorhiza tuberculata (Cnidaria: Scyphozoa)—life history of a stationary population. PSZNI: Marine Ecology 13, 333–362.Google Scholar
Kramp, P.L. (1961) Synopsis of the medusae of the world. Journal of the Marine Biological Association of the United Kingdom 40, 1–469.CrossRefGoogle Scholar
Larson, R.J. (1986) Pelagic Scyphomedusae (Scyphoza: Coronatae and Semeaostomae) of the Southern Ocean. In Kornicker, L.S. (ed.) Biology of the Antarctic Seas, XVI. Antarctic Research Series 41, 59–165.CrossRefGoogle Scholar
Larson, R.J., Mills, C.E. and Harbison, G.R. (1991) Western Atlantic midwater hydrozoan and scyphozoan medusae: in situ studies using manned submersibles. Hydrobiologia 216/217, 311–317.CrossRefGoogle Scholar
Lesh-Laurie, G.E. and Suchy, P.E. (1991) Cnidaria: Scyphozoa and Cubozoa. In Harrison, F.W. and Westfall, J.A. (eds) Microscopic anatomy of invertebrates. New York: Wiley-Liss, pp. 185–266.Google Scholar
Lindsay, D.J., Furushima, Y., Miyake, H., Kitamura, M. and Hunt, J.C. (2004) The scyphomedusan fauna of the Japan Trench: preliminary results from a remotely-operated vehicle. Hydrobiologia 530/531, 537–547.Google Scholar
Lucas, C.H. (1996) Population dynamics of Aurelia aurita (Scyphozoa) from an isolated brackish lake, with particular reference to sexual reproduction. Journal of Plankton Research 18, 987–1007.CrossRefGoogle Scholar
Lucas, C.H. (2001) Reproduction and life history strategies of the common jellyfish, Aurelia aurita, in relation to its ambient environment. Hydrobiologia 451, 229–246.CrossRefGoogle Scholar
Lucas, C.H. (2009) Biochemical composition of the mesopelagic coronate jellyfish Periphylla periphylla from the Gulf of Mexico. Journal of the Marine Biological Association of the United Kingdom 89, 77–81.CrossRefGoogle Scholar
Lucas, C.H. and Reed, A.J. (2009) Observations on the life histories of the narcomedusae Aeginura grimaldii, Cunina peregrina and Solmissus incisa from the western North Atlantic. Marine Biology 156, 373–379.CrossRefGoogle Scholar
Maas, O. (1897) Reports on an exploration off the coasts of Mexico, Central and South America, and off the Galapagos Islands, in charge of Alexander Agassiz, by the U.S. Fish Commission Steamer ‘Albatross’, during 1891, Lieut. Commander Z.L. Tanner, U.S.N., commanding. XXI. Die medusen. Memoirs of the Museum of Comparative Zoology at Harvard College, 23, 1–92.Google Scholar
Martin, L.E. (1999) Population biology and ecology of Aurelia sp. (Scyphozoa: Semaeostomeae) in a tropical meromictic marine lake in Palau, Micronesia. PhD thesis. University of California. 250 pp.Google Scholar
Mauchline, J. and Harvey, P.F. (1983) The scyphomedusae of the Rockall Trough, northeastern Atlantic ocean. Journal of Plankton Research 5, 881–890.CrossRefGoogle Scholar
Mianzan, H.W. and Cornelius, P.F.S. (1999) Cubomedusae and Scyphomedusae. In Boltovskoy, D. (ed.) South Atlantic zooplankton, Volume 1. Leiden: Backhuys Publishers, pp. 513–559.Google Scholar
Morandini, A.C. and da Silveira, F.L. (2001) Sexual reproduction of Nausithoe aurea (Scyphozia, Coronatae). Gametogenesis, egg release, embryonic development, and gastrulation. Scientia Marina 65, 139–149.CrossRefGoogle Scholar
Osborn, D.A. (2000) Cnidarian ‘parasites’ on Solmissus incisa, a narcomedusa. Scientia Marina 64, 157–163.CrossRefGoogle Scholar
Osborn, D.A., Silver, M.W., Castro, C.G., Bros, S.M. and Chavez, F.P. (2007) The habitat of mesopelagic scyphomedusae in Monterey Bay, California. Deep-Sea Research I 54, 1241–1255.CrossRefGoogle Scholar
Pagès, F., White, M.G. and Rodhouse, P.G. (1996) Abundance of gelatinous carnivores in the nekton community of the Antarctic Polar Frontal Zone in summer 1994. Marine Ecology Progress Series 141, 139–147.CrossRefGoogle Scholar
Pitt, K.A. and Kingsford, M.J. (2000) Reproductive biology of the edible jellyfish Catostylus mosaicus (Rhizostomeae). Marine Biology 137, 791–799.CrossRefGoogle Scholar
Raskoff, K.A., Purcell, J.E. and Hopcroft, R.R. (2005) Gelatinous zooplankton of the Arctic Ocean: in situ observations under the ice. Polar Biology 28, 207–217.CrossRefGoogle Scholar
Riemann, L., Titelman, J. and Båmstedt, U. (2006) Links between jellyfish and microbes in a jellyfish dominated fjord. Marine Ecology Progress Series 325, 29–42.CrossRefGoogle Scholar
Rottini-Sandrini, L. and Avian, M. (1991) Reproduction of Pelagia noctiluca in the central and northern Adriatic. Hydrobiologia 216/217, 197–202.CrossRefGoogle Scholar
Russell, F.S. (1953) The medusae of the British Isles Volume I: Anthomedusae, Leptomedusae, Limnomedusae, Trachymedusae and Narcomedusae. London: Cambridge University Press, 530 pp.Google Scholar
Russell, F.S. (1959) Some observations on the scyphomedusa Atolla. Journal of the Marine Biological Association of the United Kingdom 38, 33–40.CrossRefGoogle Scholar
Russell, F.S. (1970) The medusae of the British Isles Volume II: Pelagic Scyphozoa with a supplement to the first volume on hydromedusae. London: Cambridge University Press, 284 pp.Google Scholar
Soetje, I., Tiemann, H. and Båmstedt, U. (2007) Trophic ecology and the related functional ecology of the deepwater medusa Periphylla periphylla (Scyphozoa, Coronata). Marine Biology 150, 329–343.CrossRefGoogle Scholar
Sørnes, T.A., Hosio, A., Båmstedt, U. and Aksnes, D.L. (2008) Swimming and feeding in Periphylla periphylla (Scyphozoa, Coronatae). Marine Biology 153, 653–659.CrossRefGoogle ScholarPubMed
Vanhöffen, E. (1902) Die Acraspeden Medusen der deutschen Tiefsee-expedition 1898–1899. Wissenschaftliche Ergebnisse der Deutschen Tiefsee-expedition auf dem dampfer Valdivia 1898–1899 3, 3–52.Google Scholar
Widersten, B. (1965) Genital organs and fertilization in some Scyphozoa. Zoologiska Bidrag från Uppsala 37, 45–58.Google Scholar
Youngbluth, M.J. and Båmstedt, U. (2001) Distribution, abundance, behaviour and metabolism of Periphylla periphylla, a mesopelagic coronate medusa in a Norwegian fjord. Hydrobiologia 451, 321–333.CrossRefGoogle Scholar
Youngbluth, M., Sørnes, T., Hosia, A. and Stemmann, L. (2008) Vertical distribution and relative abundance of gelatinous zooplankton, in situ observations near the Mid-Atlantic Ridge. Deep-Sea Research II 55, 119–125.CrossRefGoogle Scholar