Cnidosac morphology in dendronotacean and aeolidacean nudibranch molluscs: from expulsion of nematocysts to use in defense?

Abstract

Nudibranchs (Mollusca, Gastropoda) feeding on tentacles and polyps of Cnidaria thereby ingest both latent and discharged nematocysts (NCs) along with the food mass. In eolid nudibranchs (Opisthobranchia, Aeolidacea), many of the undischarged NCs are transported to terminal cnidosacs in their body appendages (cerata) and incorporated as kleptocnidae for defense. In the present report, the occurrence and fate of NCs in the digestive tracts of eolids is compared with hydrozoan-feeding dendronotacean nudibranchs (Opisthobranchia, Dendronotacea), which may show more basic stages in the evolution of cnidosacs. Tomographic reconstructions of the distal tips of cerata were composed from series of semithin light microscopic sections, utilizing 3D-surface rendering software. Doto acuta (Dendronotacea, Dotidae) does not have cnidosacs; transmission electron micrographs show that the NCs are digested in lysosomes of digestive gland cells. In contrast, species of the genus Hancockia (Dendronotacea, Hancockiidae) have several small cnidosacs in each ceras; they accumulate NCs in the digestive cells, as well as in the cnidosacs. Many of the cnidosacs were found open to the exterior with NCs in the process of expulsion. These and other structural details suggest assigning a function of expelling the NCs to the Hancockia spp. cnidosacs. It is proposed that cnidosacs similar to those of Hancockia spp. provide a clue to understanding how the defensive function of eolid cnidosacs may have evolved.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Alejandrino A (2007) Phylogeny of Aeolidacea (Gastropoda: Nudibranchia). In: Jordaens K, Van Houtte N, Van Goethem J, Backeljau T (eds) World Congress of Malacology, Antwerp, Belgium, 15 July 2007, abstracts: 198

  2. Burghardt I, Stemmer K, Waegele H (2008) Symbiosis between Symbiodinium (Dinophyceae) and various taxa of Nudibranchia (Mollusca: Gastropoda), with analyses of long-term retention. Org Divers Evol 8:66–76. doi:https://doi.org/10.1016/j.ode.2007.01.001

    Article  Google Scholar 

  3. Day RM, Harris LG (1978) Selection and turnover of coelenterate nematocysts in some aeolid nudibranchs. Veliger 21:104–109

    Google Scholar 

  4. Edmunds M (1966) Protective mechanisms in the Eolidacea (Mollusca: Nudibranchia). J Linn Soc Zool 47:27–71. doi:https://doi.org/10.1111/j.1096-3642.1966.tb00082.x

    Article  Google Scholar 

  5. Glaser OC (1910) The nematocysts of eolids. J Exp Zool 9:117–142. doi:https://doi.org/10.1002/jez.1400090106

    Article  Google Scholar 

  6. Grande C, Templado J, Cervera JL, Zardoya R (2004) Molecular phylogeny of Euthyneura (Mollusca: Gastropoda). Mol Biol Evol 21:303–313. doi:https://doi.org/10.1093/molbev/msh016

    Article  CAS  Google Scholar 

  7. Greenwood PG, Mariscal RN (1984a) Immature nematocyst incorporation by the aeolid nudibranch Spurilla neapolitana. Mar Biol (Berl) 80:35–38. doi:https://doi.org/10.1007/BF00393124

    Article  Google Scholar 

  8. Greenwood PG, Mariscal RN (1984b) The utilization of cnidarian nematocysts by aeolid nudibranchs: nematocyst maintenance and release in Spurilla. Tissue Cell 16:719–730. doi:https://doi.org/10.1016/0040-8166(84)90005-3

    Article  CAS  Google Scholar 

  9. Grosvenor GH (1903) On the nematocysts of aeolids. Proc R Soc Lond 72:462–486. doi:https://doi.org/10.1098/rspl.1903.0075

    Google Scholar 

  10. Harris LG (1973) Nudibranch associations. In: Cheng TC (ed) Current topics in comparative pathobiology, vol II. Academic Press, New York, pp 213–315

    Google Scholar 

  11. Harris LG (1987) Aeolid nudibranchs as predators and prey. Am Malacol Bull 5:287–292

    Google Scholar 

  12. Herdman WA (1890) Some experiments on feeding fishes with nudibranchs. Nature 42:201–203. doi:https://doi.org/10.1038/042201a0

    Article  Google Scholar 

  13. Kälker H, Schmekel L (1976) Bau und Funktion des Cnidosacks der Aeolidoidea (Gastropoda: Nudibranchia). Zoomorphologie 86:41–60. doi:https://doi.org/10.1007/BF01006712

    Article  Google Scholar 

  14. Klussmann-Kolb A, Wägele H (2005) Opisthobranchia (Mollusca, Gastropoda)-more than just slimy slugs. Shell reduction and its implications on defence and foraging. Front Zool 2:3. doi:https://doi.org/10.1186/1742-9994-2-3

    Article  Google Scholar 

  15. MacFarland FM (1923) The morphology of the nudibranch genus Hancockia. J Morphol 38:65–104. doi:https://doi.org/10.1002/jmor.1050380104

    Article  Google Scholar 

  16. Martin R (2003) Management of nematocysts in the alimentary tract and in cnidosacs of the aeolid nudibranch gastropod Cratena peregrina. Mar Biol (Berl) 143:533–541. doi:https://doi.org/10.1007/s00227-003-1078-8

    Article  Google Scholar 

  17. Martin R, Walther P (2002) Effects of discharging nematocysts when an eolid nudibranch feeds on a hydroid. J Mar Biol Assoc UK 82:455–462. doi:https://doi.org/10.1017/S0025315402005714

    Article  Google Scholar 

  18. Martin R, Hild S, Walther P, Ploss K, Boland W, Tomaschko KH (2007a) Granular chitin in the epidermis of nudibranch molluscs. Biol Bull 213:307–315

    Article  CAS  Google Scholar 

  19. Martin R, Tomaschko KH, Walther P (2007b) Protective skin structures in shell-less marine gatropods. Mar Biol (Berl) 150:807–817. doi:https://doi.org/10.1007/s00227-006-0402-5

    Article  Google Scholar 

  20. Miller JA, Byrne M (2000) Ceratal autotomy and regeneration in the aeolid nudibranch Phidiana crassicornis and the role of predators. Invertebr Biol 119:167–176

    Article  Google Scholar 

  21. Morse MP (1971) Biology and life history of the nudibranch mollusc Coryphella stimpsoni (Verrill 1879). Biol Bull 140:84–94. doi:https://doi.org/10.2307/1540028

    Article  CAS  Google Scholar 

  22. Rousseau C (1935) Histophysiologie du foie des éolidiens. Étude de leurs xanthelles. Cytologie des cellules nématophages. Arch Anat Micr 31:305–395

    Google Scholar 

  23. Rudman WB (1981) Polyp mimicry in a new species of aeolid nudibranch mollusc. J Zool 193:421–427

    Article  Google Scholar 

  24. Schmekel L, Portmann A (1982) Opisthobranchia des Mittelmeeres. Nudibranchia und Saccoglossa. In: Fauna e Flora del Golfo di Napoli. 40 Monografia della Stazione Zoologica di Napoli. Springer, Berlin, pp 1–410

    Google Scholar 

  25. Schrödl M (1999) Hancockia schoeferti, spec. nov., a new dendronotoidean nudibranch species from central Chile. Spixiana 22:247–254

    Google Scholar 

  26. Streble H (1967) Bau und Bedeutung der Nesselsäcke von Aeolidia papillosa L., der breitwarzigen Fadenschnecke (Gastropoda, Opisthobranchia). Zool Anz 180:356–372

    Google Scholar 

  27. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), Version 4b. Sinauer Associates, Sunderland

    Google Scholar 

  28. Thompson TE (1972) Eastern Australian Dendronotoidea (Gastropoda, Opisthobranchia). Zool J Linn Soc 51:63–77. doi:https://doi.org/10.1111/j.1096-3642.1972.tb00773.x

    Article  Google Scholar 

  29. Wägele H, Willan RC (2000) Phylogeny of Nudibranchia. Zool J Linn Soc 130:83–181. doi:https://doi.org/10.1111/j.1096-3642.2000.tb02196.x

    Article  Google Scholar 

  30. Wolter H (1967) Beiträge zur Biologie, Histologie und Sinnesphysiologie (insbesondere der Chemorezeptoren) einiger Nudibranchier (Mollusca, Opisthobranchia) der Nordsee. Z Morphol Oekol Tiere 60:275–337. doi:https://doi.org/10.1007/BF00424637

    Article  Google Scholar 

  31. Wright, TS (1858–1861) On the cnidae or thread-cells of the Eolidae. Proc R Phys Soc Edinburgh, Sessions 1858–1861

Download references

Acknowledgments

Yuri Hooker (Lima) helped to collect specimens of Hancockia schoeferti. The fieldwork in Peru was supported by the GeoBioCenter (LMU) and the Deutsche Forschungsgemeinschaft (DFG SCHR 667/4 to MS). Claus Valentin provided excellent working conditions at the Institute of Marine Biology at Giglio. We would like to thank Prof. E. Koenig (Buffalo) for critically reading and revising the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Rainer Martin.

Additional information

Communicated by J.P. Grassle.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Phylogenetic relationships of cnidosac bearing nudibranch gastropods

. The morphological data set (47 characters; one hypothetical plesiomorphic group plus 2 pleurobranchoidean taxa as outgroups, and 29 nudibranch taxa) used to reveal the phylogeny of the Nudibranchia by Wägele & Willan (2000) herein was supplemented by Hancockia and reanalyzed (PAUP). All characters were treated as unweighted and unordered; the tree was unrooted. The strict consensus tree of 120 equally parsimonious trees (102 steps) is shown; numbers refer to bootstrap values (<50 not indicated), obtained by a separate analysis (1000 replications, PAUP) with the same settings; a clade of Protaeolidiella and Phyllodesmium (marked in grey) received some bootstrap support but is not represented in the strict consensus tree. Species possessing cnidosacs with kleptocnidae are in bold face; Protaeolidiella has cnidosacs but without containing kleptocnidae. While the monophyly or e.g. Nudibranchia, Anthobranchia, and Doridacea is supported by high bootstrap values (>90), none of the traditional major dexiarchian taxa Arminacea, Dendronotacea and Aeolidacea results monophyletic. The Arminidae from the sister clade to a polytomy composed of members all three groups. The dendronotacean Hancockia (with cnidosacs) and Doto (without cnidosacs) group together, nestling within cnidosac-possessing eolid taxa in the strict consensus tree; however, these relationships are not statistically supported. From this, due to limited taxon and character sampling, very preliminary phylogenetic point of view, the systematic position of Hancockia and the evolution of cnidosacs remain unresolved

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Martin, R., Heß, M., Schrödl, M. et al. Cnidosac morphology in dendronotacean and aeolidacean nudibranch molluscs: from expulsion of nematocysts to use in defense?. Mar Biol 156, 261–268 (2009). https://doi.org/10.1007/s00227-008-1080-2

Download citation

Keywords

  • Digestive Gland
  • Hydroid
  • Tomographic Reconstruction
  • Digestive Cell
  • Midgut Gland