Journal of Chemical Ecology

, Volume 27, Issue 11, pp 2287–2299 | Cite as

Chemical Defenses of the Sacoglossan Mollusk Elysia rufescens and Its Host Alga Bryopsis sp.

  • Mikel A. Becerro
  • Gilles Goetz
  • Valerie J. Paul
  • Paul J. Scheuer


Sacoglossans are a group of opisthobranch mollusks that have been the source of numerous secondary metabolites; however, there are few examples where a defensive ecological role for these compounds has been demonstrated experimentally. We investigated the deterrent properties of the sacoglossan Elysia rufescens and its food alga Bryopsis sp. against natural fish predators. Bryopsis sp. produces kahalalide F, a major depsipeptide that is accumulated by the sacoglossan and that shows in vitro cytotoxicity against several cancer cell lines. Our data show that both Bryopsis sp. and Elysia rufescens are chemically protected against fish predators, as indicated by the deterrent properties of their extracts at naturally occurring concentrations. Following bioassay-guided fractionation, we observed that the antipredatory compounds of Bryopsis sp. were present in the butanol and chloroform fractions, both containing the depsipeptide kahalalide F. Antipredatory compounds of Elysia rufescens were exclusively present in the dichloromethane fraction. Further bioassay-guided fractionation led to the isolation of kahalalide F as the only compound responsible for the deterrent properties of the sacoglossan. Our data show that kahalalide F protects both Bryopsis sp. and Elysia rufescens from fish predation. This is the first report of a diet-derived depsipeptide used as a chemical defense in a sacoglossan.

Antipredatory role herbivore–prey relationship depsipeptides kahalalide F sacoglossan mollusks green algae Elysia rufescens Bryopsis sp. 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. AVILA, C. 1995. Natural products from opisthobranch mollusks: A biological review. Oceanogr. Mar. Biol. Annu. Rev. 33:487–559.Google Scholar
  2. BECERRO, M. A., PAUL, V. J., and STARMER, J. 1998. Intraspecimen variation in chemical defenses of the sponge Cacospongia sp. and its consequences on generalist fish predators and the specialist nudibranch predator Glossodoris pallida. Mar. Ecol. Prog. Ser. 168:187–196.Google Scholar
  3. BISKUPIAK, J. E. and IRELAND, C. M. 1983. Pectinatone, a new antibiotic from the mollusk Siphonaria pectinata. Tetrahedron Lett. 24:3055–3058.Google Scholar
  4. CIMINO, G. and GHISELIN, M. T. 1998. Chemical defence and evolution in the Sacoglossa (Mollusca: Gastropoda: Opisthobranchia). Chemoecology 8:51–60.Google Scholar
  5. CIMINO, G. and SODANO, G. 1993. Biosynthesis of secondary metabolites in marine mollusks, pp. 78–115, in P. J. Scheuer (ed.). Topics in Current Chemistry 167. Springer, Berlin, Germany.Google Scholar
  6. CLARK, K. B., JENSEN, K. R., and STIRTS, H. M. 1990. Survey for functional kleptoplasy among Atlantic Ascoglossa (DSacoglossa) (Mollusca: Opisthobranchia). The Veliger 33:339–345.Google Scholar
  7. DAWE, R. D. and WRIGHT, J. L. C. 1986. The major polypropionate metabolites from the sacoglossan mollusk, Elysia chlorotica. Tetrahedron Lett. 27:2559–2562.Google Scholar
  8. DI MARZO, V., VARDARO, R. R., DE PETROCELLIS, L., VILLANI, G., MINEI, R., and CIMINO, G. 1991. Cyercenes, novel pyrones from the ascoglossan mollusk Cyerce cristallina. Tissue distribution, biosynthesis and possible involvement in defense and regenerative processes. Experientia 47:1221–1227.Google Scholar
  9. DOTY, M. S. and AGUILAR-SANTOS, G. 1970. Transfer of toxic algal substances in marine food chains. Pac. Sci. 24:351–355.Google Scholar
  10. DUFFY, J. E. and HAY, M. E. 1994. Herbivore resistance to seaweed chemical defense: The roles of mobility and predator risk. Ecology 75:1304–1319.Google Scholar
  11. FAULKNER, D. J. 1992. Chemical defenses of marine mollusks, pp. 119–163, in V. J. Paul (ed.). Ecological Roles of Marine Natural Products. Comstock Publishing Associates, Ithaca, New York.Google Scholar
  12. GAVAGNIN, M., MARIN, A., CASTELLUCCIO, F., VILLANI, G., and CIMINO, G. 1994a. Defensive relationships between Caulerpa prolifera and its shelled sacoglossan predators. J. Exp. Mar. Biol. Ecol. 175:197–210.Google Scholar
  13. GAVAGNIN, M., SPINELLA, A., CASTELLUCCIO, F., CIMINO, G., and MARIN, A. 1994b. Polypropionates from the Mediterranean mollusk Elysia timida. J. Nat. Prod. 57:298–304.Google Scholar
  14. GAVAGNIN, M., MOLLO, E., CIMINO, G., and ORTEA, J. 1996. A new γ-Dihydropyrone propionate from the Caribbean sacoglossan Tridachia crispata. Tetrahedron Lett. 37:4259–4262.Google Scholar
  15. GAVAGNIN, M., MOLLO, E., MONTARANO, D., ORTEA, J., and CIMINO, G. 2000. Chemical studies of Caribbean sacoglossans: Dietary relationships with green algae and ecological implications. J. Chem. Ecol. 26:1563–1578.Google Scholar
  16. GOETZ, G., NAKAO,Y., and SCHEUER, P. J. 1997. Two acyclic kahalalides from the sacoglossan mollusk Elysia rufescens. J. Nat. Prod. 60:562–567.Google Scholar
  17. HAMMAN, M. T. and SCHEUER, P. J. 1993. Kahalalide F: A bioactive depsipeptide from the sacoglossan mollusk Elysia rufescens and the green alga Bryopsis sp. J. Am Chem. Soc. 115: 5825–5826.Google Scholar
  18. HAMMAN, M. T., OTTO, C. S., SCHEUER, P. J., and DUNBAR, D. C. 1996. Kahalalides: Bioactive peptides from a marine mollusk Elysia rufescens and its algal diet Bryopsis sp. J. Org. Chem. 61:6594–6600.Google Scholar
  19. HAY, M. E. 1992. The role of seaweed chemical defenses in the evolution of feeding specialization and in the mediation of complex interactions, pp. 93–118, in V. J. Paul (ed.). Ecological Roles of Marine Natural Products. Comstock Publishing Associates, Ithaca, New York.Google Scholar
  20. HAY, M. E., PAWLIK, J. R., DUFFY, J. E., and FENICAL, W. 1989. Seaweed-herbivore-predator interactions: Host-plant specialization reduces predation on small herbivores. Oecologia 81:418–427.Google Scholar
  21. HAY, M. E., DUFFY, J. E., PAUL, V. J., RENAUD, P. E., and FENICAL, W. 1990. Specialist herbivores reduce their susceptibility to predation by feeding on the chemically defended seaweed Avrainvillea longicaulis. Limnol. Oceanogr. 35:1734–1743.Google Scholar
  22. IRELAND, C. and FAULKNER, D. J. 1981. The metabolites of the marine mollusks Tridachiella diomedea and Tridachnia crispata. Tetrahedron 37(suppl. 1):233–240.Google Scholar
  23. IRELAND, C. and SCHEUER, P. J. 1979. Photosynthetic marine mollusks: In vivo 14C incorporation into metabolites of the sacoglossan Placobranchus ocellatus. Science 205:922–923.Google Scholar
  24. JENSEN, K. R. 1984. Defensive behavior and toxicity if ascoglossan opisthobranch Mourgana germaineae Marcus. J. Chem. Ecol. 10:475–486.Google Scholar
  25. KAN, Y., FUJITA, T., SAKAMOTO, B., HOKAMA, Y., and NAGAI, H. 1999. Kahalalide K. A new cyclic depsipeptide from the Hawaiian green alga Bryopsis species. J. Nat. Prod. 68:1169–1172.Google Scholar
  26. KSEBATI, M. B. and SCHMITZ, F. J. 1985. Tridachiapyrones: Propionate-derived metabolites from the sacoglossan mollusk Tridachia crispata. J. Org. Chem. 50:5637–5642.Google Scholar
  27. LEWIN, R. A. 1970. Toxin secretion and tail autonomy by irritated Oxynoe panamensis (Opisthobranchiata; Sacoglossa). Pac. Sci. 24:356–358.Google Scholar
  28. LUBCHENCO, J. and GAINES, S. D. 1981. A unified approach to marine plant-herbivore interactions. I. Populations and communities. Annu. Rev. Ecol. Syst. 12:405–437.Google Scholar
  29. PAUL, V. J. 1987. Feeding deterrent effects of algal natural products. Bull. Mar. Sci. 41:514–522.Google Scholar
  30. PAUL, V. J. and VAN ALSTYNE, K. L. 1988. Use of ingested algal diterpenoids by Elysia halimeade Macnae (Opisthobranchia: Ascoglossa) as antipredator defenses. J. Exp. Mar. Biol. Ecol. 119:15–29.Google Scholar
  31. PAWLIK, J. R, CHANAS, B., TOONEN, R. J., and FENICAL, W. 1995. Defenses of Caribbean sponges against predatory reef fish. I. Chemical deterrency. Mar. Ecol. Prog. Ser. 127:183–194.Google Scholar
  32. ROUSSIS, V., PAWLIK, J. R., HAY, M. E., and FENICAL, W. 1990. Secondary metabolites of the chemically rich ascoglossan Cyerce nigricans. Experientia 49:327–329.Google Scholar
  33. THACKER, R. W., BECERRO, M. A., LUMBANG, W. A., and PAUL, V. J. 1998. Allelopathic interactions between sponges in a tropical reef community. Ecology 79:1740–1750.Google Scholar
  34. TROWBRIDGE, C. D. 1994. Defensive responses and palatability of specialist herbivores: Predation on NE Pacific ascoglossan gastropods. Mar. Ecol. Prog. Ser. 105:61–70.Google Scholar
  35. VARDARO, R. R., DI MARZO, V., CRISPINO, A., and CIMINO, G. 1991.Cyercenes, novel polypropionate pryrones from the autotomizing Mediterranean mollusk Cyerce cristallina. Tetrahedron 47:5569–5576.Google Scholar
  36. WILLIAMS, S. I. and WALKER, D. I. 1999. Mesoherbivore-macroalgal interactions: Feeding ecology of sacoglossan sea slugs (Mollusca, Opisthobranchia) and their effects on their food algae. Oceanogr. Mar. Biol. Annu. Rev. 37:87–128.Google Scholar
  37. WYLIE, C. R. and PAUL, V. J. 1988. Feeding preferences of the surgeonfish Zebrasoma flavenses in relation to chemical defenses of tropical algae. Mar. Ecol. Prog. Ser. 45:23–32.Google Scholar

Copyright information

© Plenum Publishing Corporation 2001

Authors and Affiliations

  • Mikel A. Becerro
    • 1
    • 2
  • Gilles Goetz
    • 1
  • Valerie J. Paul
    • 2
  • Paul J. Scheuer
    • 1
  1. 1.Department of ChemistryUniversity of Hawaii at ManoaHonolulu
  2. 2.University of Guam Marine LaboratoryMangilaoGuam

Personalised recommendations