Marine Biology

, Volume 143, Issue 3, pp 533–541 | Cite as

Management of nematocysts in the alimentary tract and in cnidosacs of the aeolid nudibranch gastropod Cratena peregrina

Article

Abstract

The nudibranch gastropod Cratena peregrina (Opisthobranchia: Aeolidaceae), when feeding on polyps of the hydrozoan Eudendrium racemosum (Cnidaria: Anthoathecata), devours masses of small microbasic eurytele and holotrichous isorhiza nematocysts. Large proportions of these nematocysts were found undischarged in the alimentary tracts of the snails. Feeding experiments in this study tracked the fate of nematocysts as they passed through the alimentary canal to the digestive gland in the dorsal appendages, the cerata, to the cnidosacs, and finally in the faeces. In digestive cells, many structurally intact nematocysts were present in large phagosomes that remained unaffected even after 2 days fasting, and phagosomes containing nematocysts were found in the faeces. Thus, it is inferred that fusion of nematocyst-containing phagosomes with lysosomes and subsequent digestion of nematocysts is blocked. Masses of exposed, undigested and structurally intact nematocysts were discarded in the faeces. In the tips of the cerata, other nematocysts were phagocytosed by cnidophages and stored in the cnidosacs. After release, in contact with seawater, cnidosac nematocysts were able to discharge. When cnidophore tentacles of E. racemosum with only holotrichous isorhizas were fed to the snails, the isorhizas arrived in the cnidosacs about 2 h after feeding and mixed with existing small euryteles. Some cnidosacs also contained very large microbasic eurytele or large macrobasic eurytele nematocysts, possibly from Eudendrium ramosum and Eudendrium glomeratum, respectively. This indicates that the various types of nematocysts from food were all incorporated into the cnidosacs. Evidence for a selection process or digestion of a certain nematocyst type in the cnidophages was not obtained. It is concluded that a large proportion of the nematocysts ingested with the food are not digested, but are eliminated, structurally and functionally intact, via the alimentary canal and the tips of the cerata.

Notes

Acknowledgements

Support by the Deutsche Forschungsgemeinschaft (Ma 259/16-3) is gratefully acknowledged. I would like to thank P. Walther for hospitality in the laboratory at Ulm and help with high pressure freezing, E. Koenig (University at Buffalo) for revision of the text, two anonymous and a non-anonymous colleague for criticisms of the manuscript, and M. Hagedorn (Ulm) for help with the computer work. C. Valentin and his staff provided excellent working conditions at the field station at Giglio. The experiments comply with the current laws of Italy and Germany.

References

  1. Conklin EJ, Mariscal RN (1977) Feeding behavior, ceras structure, and nematocyst storage in the aeolid nudibranch, Spurilla neapolitana (Mollusca). Bull Mar Sci 27:658–667Google Scholar
  2. Day RM, Harris LG (1978) Selection and turnover of coelenterate nematocysts in some aeolid nudibranchs. Veliger 21:104–109Google Scholar
  3. Edmunds M (1966) Protective mechanisms in the Eolidacea (Mollusca: Nudibranchia). J Linn Soc Zool 47:27–71Google Scholar
  4. Ericsson JLE, Trump BF (1965) Observations on the application of electron microscopy of the lead phosphate technique for the demonstration of acid phosphatase. Histochemistry 4:470–487PubMedGoogle Scholar
  5. Glaser OC (1910) The nematocysts of eolids. J Exp Zool 9:117–142Google Scholar
  6. Graham A (1938) The structure and function of the alimentary canal of aeolid molluscs, with a special discussion on their nematocysts. Trans R Soc Edinb 59:267–307Google Scholar
  7. Greenwood PG, Mariscal RN (1984a) Immature nematocyst incorporation by the aeolid nudibranch Spurilla neapolitana. Mar Biol 80:35–38Google Scholar
  8. Greenwood PG, Mariscal RN (1984b) The utilization of cnidarian nematocysts by aeolid nudibranchs: nematocyst maintenance and release in Spurilla. Tissue Cell 16:719–730PubMedGoogle Scholar
  9. Griebel R (1993) Fine structure of the three cell types found in the digestive gland of Elysia viridis (Opisthobranchia: Sacoglossa). Veliger 36:107–114Google Scholar
  10. Grosvenor GH (1903) On the nematocysts of aeolids. Proc R Soc London 72:462–486Google Scholar
  11. Harris LG (1973) Nudibranch associations. In: Cheng TC (ed) Current topics in comparative pathobiology, vol II. Academic, New York, pp 213–315Google Scholar
  12. Herdman WA (1890) Some experiments on feeding fishes with nudibranchs. Nature 42:201–203Google Scholar
  13. Hörstadius S (1933) Einige Untersuchungen über die Eiweißverdauung bei Gastropoden. Biol Zentralbl 53:645–650Google Scholar
  14. Kepner WA (1943) The manipulation of the nematocysts of Pennaria tiarella by Aeolis pilata. J Morphol 73:297–311Google Scholar
  15. Kress A, Schmekel L, Nott JA (1994) Ultrastructure of the digestive gland in the opisthobranch mollusk, Runcina. Veliger 37:358–373Google Scholar
  16. Kühnel MP, Goethe R, Habermann A, Müller E, Rohde M, Griffiths G, Valentin-Weigand P (2001) Characterization of the intracellular survival of Mycobacterium avium ssp. paratuberculosis: phagosomal pH and fusogenicity in J774 macrophages compared with other mycobacteria. Cell Microbiol 3:551–566CrossRefPubMedGoogle Scholar
  17. Martin R, Walther P (2002a) Effects of discharging nematocysts when an eolid nudibranch feeds on a hydroid. J Mar Biol Assoc UK 82:455–462CrossRefGoogle Scholar
  18. Martin R, Walther P (2002b) Protective mechanisms against the action of nematocysts in the epidermis of Cratena peregrina and Flabellina affinis (Gastropoda, Nudibranchia). Zoomorphology 122:25–35Google Scholar
  19. Miller JA, Byrne M (2000) Ceratal autotomy and regeneration in the aeolid nudibranch Phidiana crassicornis and the role of predators. Invertebr Biol 119:167–176Google Scholar
  20. Moreteau JC (1977) Étude sur l'alimentation d'Aeolidia papillosa L. Cah Biol Mar 18:369–383Google Scholar
  21. Naville A (1926) Notes sur les Éolidiens. Un Éolidien d'eau saumâtre. Zooxanthelles et homochromie. Rev Suisse Zool 33:251–286Google Scholar
  22. Östman C (1997) Abundance, feeding behavior and nematocysts of scyphopolyps (Cnidaria) and nematocysts in their predator, the nudibranch Coryphella verrucosa (Mollusca). Hydrobiologia 355:21–28CrossRefGoogle Scholar
  23. Rosin R (1970) On Aeolidoidea, Coelenterata and nematocysts. Argamon, Israel J Malacol 1:43–50Google Scholar
  24. Salvini-Plawen L von (1972) Cnidaria as food sources for marine invertebrates. Cah Biol Mar 13:385–400Google Scholar
  25. Schmekel L, Portmann A (1982) Opisthobranchia des Mittelmeeres. Nudibranchia und Saccoglossa. Springer, Berlin Heidelberg New YorkGoogle Scholar
  26. Schmekel L, Wechsler W (1968a) Feinstruktur der Mitteldarmdrüse (Leber) von Trinchesia granosa (Gastropoda, Opisthobranchia). Z Zellforsch Mikrosk Anat 84:238–268PubMedGoogle Scholar
  27. Schmekel L, Wechsler W (1968b) Beobachtungen zur Nahrungsaufnahme und -verarbeitung in der Mitteldarmdrüse von Nudibranchiern (Gastropoda, Opisthobranchia). Anat Anz 121[Suppl]:535–543Google Scholar
  28. Schuchert P (2003) Cnidaria, Klasse Hydrozoa. In: Hofrichter R (ed) Das Mittelmeer, vol 2. Spektrum, HeidelbergGoogle Scholar
  29. Streble H (1967) Bau und Bedeutung der Nesselsäcke von Aeolidia papillosa L., der breitwarzigen Fadenschnecke (Gastropoda: Opisthobranchia). Zool Anz 180:356–372Google Scholar
  30. Tardy J (1964) Comportment prédateur de Eolidiella alderi (mollusque: nudibranche). CR Acad Sci Ser III Sci Vie 258:2190–2192Google Scholar
  31. Taylor DL (1968) Chloroplasts as symbiotic organelles in the digestive gland of Elysia viridis (Gastropoda: Opisthobranchia). J Mar Biol Assoc UK 48:1–15Google Scholar
  32. Thompson TE, Bennett I (1969) Physalia nematocysts: utilized by molluscs for defense. Science 166:1532–1533Google Scholar
  33. Trench RK (1969) Chloroplasts as functional endosymbionts in the mollusc Tridachia crispata (Bergh) (Opisthobranchia, Sacoglossa). Nature 222:1071–1072Google Scholar
  34. Wolter H (1967) Beiträge zur Biologie, Histologie und Sinnesphysiologie (insbesondere der Chemorezeption) einiger Nudibranchier (Mollusca, Opisthobranchia) der Nordsee. Z Morphol Oekol Tiere 60:275–337Google Scholar
  35. Wright TS (1863) On the cnidae or thread cells of the Eolidae. Proc R Soc Edinb, sessions 1858–1859, 1859–1860, 1860–1861Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Zentrale Einrichtung ElektronenmikroskopieUniversität UlmUlmGermany

Personalised recommendations