Advertisement

Marine Biology

, Volume 157, Issue 3, pp 527–535 | Cite as

Organ-like gonads, complex oocyte formation, and long-term spawning in Periphylla periphylla (Cnidaria, Scyphozoa, Coronatae)

  • Henry Tiemann
  • Gerhard Jarms
Original Paper

Abstract

An account is given about the development of the gametes of the holopelagic coronate scyphomedusa Periphylla periphylla (Péron and Lesueur 1809). The gonads of the species are complex and differ from those thus far described in Scyphozoa in having this characteristic composition of trophocytes, follicle cells, gamete-releasing pores, mucus cells, and resorption cells. Our results differ from those of previous coronate studies with respect to the contact of the oocytes with the gonad tissue throughout the duration of development. Among the Medusozoa, follicle cells have thus far been considered as an apomorphy for the Staurozoa, but their presence in the Scyphozoa casts some doubts on this assumption. From morphological structure and examination of the gonads and gametes, it can be deduced that P. periphylla has true organs and that gamete release is continuous. These results supplement our knowledge of the reproductive biology of this mesopelagic species.

Keywords

Follicle Cell Mature Oocyte Gonad Tissue Female Gonad Male Gonad 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank the crews of R/V Håkon Mosby and R/V Hans Brattström for superior working facilities. Support from the TMR (Training and Mobility of Researchers) Programme from the European Union, through Contract No. ERBFMGECT950013, is acknowledged. We are grateful to Dietmar Keyser and Renate Walter for technical assistance with electron microscopy. We are thankful to Ilka Sötje for discussions and assistance in preparing the figures and the manuscript. For discussions and improvement of the language we are thankful to Paul F.S. Cornelius and Blair D. Johnston.

References

  1. Adam H, Czihak G (1964) Arbeitsmethoden der makroskopischen und mikroskopischen Anatomie. Fischer, StuttgartGoogle Scholar
  2. Afzelius BA, Franzén A (1971) The spermatozoon of the jellyfish Nausithoe. J Ultrastr Res 37:186–199CrossRefGoogle Scholar
  3. Arai MN (1997) A functional biology of Scyphozoa. Chapman and Hall, LondonGoogle Scholar
  4. Avian M, Rottini-Sandrini LR (1991) Oocyte development in four species of scyphomedusa in northern Adriatic Sea. Hydrobiologia 216(21):189–195CrossRefGoogle Scholar
  5. Beams HW, Kessel RG (1983) Cnidaria. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates. Volume I: oogenesis, oviposition and Oosorption. Wiley, New York, pp 31–66Google Scholar
  6. Campbell R (1974) Cnidaria. In: Giese AC, Pearse S (eds) Reproduction of marine invertebrates. 1: Acoelomate and pseudocoelomate metazoans. Academic Press, New York, pp 133–199Google Scholar
  7. Collins AG (2002) Phylogeny of Medusozoa and the evolution of cnidarian life cycles. J Evol Biol 15:418–432CrossRefGoogle Scholar
  8. Collins AG, Schuchert P, Marques AC, Jankowski T, Medina M, Schierwater B (2006) Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models. Syst Biol 55(1):97–115CrossRefPubMedGoogle Scholar
  9. Eckelbarger KJ, Larson RL (1988) Ovarian morphology and oogenesis in Aurelia aurita (Scyphozoa: Semaeostomae): ultrastructural evidence of heterosynthetic yolk formation in a primitive metazoan. Mar Biol 100:103–115CrossRefGoogle Scholar
  10. Eckelbarger KJ, Larson R (1992) Ultrastructure of the ovary and oogenesis in the jellyfish Linuche unguiculata and Stomolophus meleagris, with a review of ovarian structure in the Scyphozoa. Mar Biol 114:633–643CrossRefGoogle Scholar
  11. Eckelbarger KJ, Larson RL (1993) Ultrastructural study of the ovary of the sessile scyphozoan, Haliclystus octoradiatus (Cnidaria: Stauromedusae). J Morphol 218:225–236CrossRefGoogle Scholar
  12. Eckelbarger KJ, Hand C, Uhlinger KR (2008) Ultrastructural features of the trophonema and oogenesis in the starlet sea anemone, Nematostella vectensis (Edwarsiidae). Invert Biol 12:381–395CrossRefGoogle Scholar
  13. Fosså JH (1992) Mass occurrence of Periphylla periphylla (Scyphozoa, Coronatae) in a Norwegian fjord. Sarsia 77:237–251Google Scholar
  14. Fraser JH (1968) Standardization of zooplankton sampling methods at sea. Part II. In: Zooplankton Sampling. The UNESCO Press: ParisGoogle Scholar
  15. Hinsch GW (1974) Comparative ultrastructure of cnidarian sperm. Am Zool 14:457–465Google Scholar
  16. 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 84:55–65Google Scholar
  17. Jarms G, Tiemann H, Båmstedt U (2002) Development and biology of Periphylla periphylla (Scyphozoa: Coronatae) in a Norwegian fjord. Mar Biol 141:647–657CrossRefGoogle Scholar
  18. Kikinger R (1992) Cotylorhiza tuberculata (Cnidaria: Scyphozoa)—Life History of a Stationary Population. Mar Ecol 13(4):333–362CrossRefGoogle Scholar
  19. Komai T (1935) On Stephanoscyphus and Nausithoe. Mem Coll Sci Kyoto (B) 10(5):289–339Google Scholar
  20. Larkman A (1980) Ultrastructural aspects of gametogenesis in Actinia equina L. In: Tardent PR (ed) Developmental and cellular biology of coelenterates—proceedings of the 4th international coelenterate conference held in Interlaken, Switzerland, 4–8 September, 1979. Elsevier, Amsterdam, pp 61–66Google Scholar
  21. Larkman AU, Carter MA (1982) Preliminary ultrastructural and autoradiographic evidence that the trophonema of the sea anemone Actinia fragacea (Cnidaria, Anthozoa) has a nutritive function. Int J Invert Reprod Dev 4:375–379Google Scholar
  22. Maas O (1897) Reports on an exploration of the west coasts of Mexico, Central and South America, and of the Galapagos Islands. 21. Die Medusen. Mem Mus Comp Zool Harv 23(1):9–92Google Scholar
  23. Marques AC, Collins AG (2004) Cladistic analysis of Medusozoa and cnidarian evolution. Invert Biol 123(1):23–42Google Scholar
  24. Morandini AC, de Silveira FL (2001) Sexual reproduction of Nausithoe aurea (Scyphozoa, Coronatae). Gametogensis, egg release, embryonic development, and gastrulation. Sci Mar 65(2):139–149CrossRefGoogle Scholar
  25. Pitt KA, Kingford MJ (2000) Reproductive biology of the edible jellyfish Catostylus mosaicus (Rhizostomae). Mar Biol 137:791–799CrossRefGoogle Scholar
  26. Robinson DG, Ehlers U, Herken R, Herrmann B, Mayer F, Schürmann F-W (1985) Präparations- methodik in der Elektronenmikroskopie. Springer, BerlinGoogle Scholar
  27. Rottini Sandrini L, Bratina F, Avian M (1986) Apsetti ultrastratturali della gametogensi in Discomedusa lobata (Claus). Nova Thalassia 8:59–66Google Scholar
  28. Rottini-Sandrini L, Avian M, Axiak M, Malej A (1983) The breeding period of Pelagia noctiluca (Scyphozoa, Semaeostomeae) in the Adriatic and central Mediterranean Sea. Nova Thalassia 6:65–75Google Scholar
  29. Schaxel (1910) Die Oogenese von Pelagia noctiluca Pér. et Less. mit besonderer Berücksichtigung der Chromidien und Nucleolen. Zool Anz 35(12/13):407–414Google Scholar
  30. Schmidt H, Schäfer WG (1980) The anthozoan egg: trophic mechanisms and oocyte surfaces. In: Tardent P, Tardent R (eds) Developmental and cellular biology of coelenterates. Elsevier, Amsterdam, pp 41–46Google Scholar
  31. Sötje I (2003) Untersuchung zur reduzierten Metagenese von Thecoscyphus zibrowii Werner, 1984 (Cnidaria, Scyphozoa). Dissertation, Universität HamburgGoogle Scholar
  32. Sötje I, Tiemann H, Båmstedt U (2007) Trophic ecology and the related functional morphology of the deepwater medusa Periphylla periphylla (Scyphozoa, Coronata). Mar Biol 150(3):329–343CrossRefGoogle Scholar
  33. Thomas MB, Edwards NC (1991) Cnidaria: Hydrozoa. In: Harrison FW, Westfall JA (eds) Microscopic anatomy of invertebrates, Vol 2: placozoa, porifera, cnidaria, and ctenophora. Wiley, New York, pp 91–183Google Scholar
  34. Tiemann H, Sötje I, Johnston BD, Flood PR, Båmstedt U (2009) Documentation of potential courtship-behaviour in Periphylla periphylla (Cnidaria, Scyphozoa). JMBA 89(1):63–66CrossRefGoogle Scholar
  35. Tsakaguchi R (1914) Über die feinere Struktur des Ovarialeies von Aurelia aurita L. Arch mikrosk Anat 85:114–123CrossRefGoogle Scholar
  36. Werner B (1970) Contribution to the evolution in the genus Stephanoscyphus (Scyphozoa Coronatae) and ecology and regeneration qualities of Stephanoscyphus racemosus Komai. Publ Seto Mar Biol Lab 18(1):1–20Google Scholar
  37. Werner B (1984) Stamm cnidaria, nesseltiere. In: Kaestner A (ed) Lehrbuch der speziellen Zoologie I./2. Fischer, Stuttgart, pp 11–305Google Scholar
  38. Widersten B (1965) Genital organs and fertilization in some Scyphozoa. Zool Bidr Upps 37:45–58Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Biozentrum Grindel und Zoologisches MuseumUniversität HamburgHamburgGermany

Personalised recommendations