Skip to main content
SpringerLink
Log in

Sequestration of dietary secondary metabolites by three species of sea hares: location, specificity and dynamics

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

We examined the location of squuestered secondary metabolites in three species of sea hares, Stylocheilus longicauda, Dolabella auricularia, and Aplysia californica (Opisthobranchia: Anaspidea). The sea hares ate a natural diet or were fed an artificial diet containing secondary metabolites in the laboratory. In all three species, sequestered secondary metabolites were located almost exclusively in the digestive gland, an internal organ, rather than in the exterior parts of the body, in eggs, or in ink (released when sea hares are disturbed). S. longicauda, a specialist sea hare, was able to sequester measur-able amounts of all six algal metabolites offered (caulerpenyne, halimedatetraacetate, pachydictyol A, malyingamides A and B, and ochtodene) and two (luffariellolide and Dysidea spp. brominated diphenyl ether) of three sponge metabolites offered (chondrillin was not sequestered). Malyngamides A and B, found in the host plant of S. longicauda, were sequestered at high, but not unique concentrations. D. auricularia, a generalist sea hare, was fed caulerpenyne, pachydictyol A and malyngamide B; patterns of sequestration of these three compounds did not differ markedly between S. longicauda and D. auricularia. S. longicauda did not lose measurable amounts of malyngamides after 18 d on a malyngamide-free diet. These results suggest that sea hares have generic mechanisms for sequestering algal metabolites rather than mechanisms that are tightly linked to particular compounds, that these mechanisms do not differ dramatically between species, and that sequestered secondary metabolites are not located optimally for defense.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Albizati, K. F., Holman, T., Faulkner, D. J., Glaser, K. B., Jacobs, R. S. (1987). Luffariellolide, an anti-inflammatory sesterterpene from the marine sponge Luffariella sp. Experientia 43: 949–950

    Google Scholar 

  • Ambrose, H. W., Givens, R. P., Chen, R., Ambrose, K. P. (1979). Distastefulness as a defense mechanism in Aplysia brasiliana (Mollusca: Gastropoda). Mar. Behav. Physiol. 6: 57–64

    Google Scholar 

  • Audesirk, T. E. (1979) A field study of growth and reproduction in Aplysia californica. Biol. Bull. mar. biol. Lab., Woods Hole 157: 407–421

    Google Scholar 

  • Avila, C., Ballesteros, M., Cimino, G., Crispino, A., Bavagnin, M., Sodano, G. (1990) Biosynthetic origin and anatomical distribution of the main secondary metabolites in the nudibranch molluse Doris verrucosa. Comp. Biochem. Physiol. 97B: 363–368

    Google Scholar 

  • Avila, C., Cimino, G., Fontana, A., Gavagnin, M., Ortea, J., Trivellone, E. (1991). Defensive strategy of two Hypselodoris nudibranchs from Italian and Spanish coasts. J. chem. Ecol. 17: 625–636

    Google Scholar 

  • Barbosa, P. (1988) Some thoughts on “the evolution of host range”. Ecology 69: 912–915

    Google Scholar 

  • Beitler, M. K., Liston, J. (1990). Uptake and tissue distribution of PSP toxins in butter clams. In: Graneli, E., Sundstrom, B., Edler, L., Anderson, D. M. (eds.) Toxic marine phytoplankton. Elsevier, New York, p. 257–262

    Google Scholar 

  • Bernays, E. (1991). Relationship between deterrence and toxicity of plant secondary compounds for the grasshopper Schistocerca americana. J. chem. Ecol. 17: 2519–2526

    Google Scholar 

  • Bernays, E., Graham, M. (1988). On the evolution of host specificity in phytophagous arthropods. Ecology 69: 886–892

    Google Scholar 

  • Bleiler, J. A., Rosenthal, G. A., Janzen, D. H. (1988). Biochemical ecology of canavanine-eating seed predators. Ecology 69: 427–433

    Google Scholar 

  • Brodie, G. (1984). Nudibranchs: molluses without shells. Fiji Shell Club Mag. 1984: 37–44

    Google Scholar 

  • Brower, L. P., Glazier, S. C. (1975). Localization of heart poisons in the monarch butterfly. Science, N. Y. 188: 19–25

    Google Scholar 

  • Brower, L. P., Nelson, C. J., Seiber, J. N., Fink, L. S., Bond, C. (1988). Exaptation as an alternative to coevolution in the cardenolide-based chemical defense of monarch butterflies (Danaus plexippus L.) against avian predators. In: Spencer, K. C. (ed.) Chemical mediation of coevolution. Academic Press, San Diego, p. 447–476

    Google Scholar 

  • Brown, K. S., Jr. (1984). Adult-obtained pyrrolizidine alkaloids defend ithomiine butterflies against a spider predator. Nature, Lond. 309: 707–709

    Google Scholar 

  • Cardellina, II, J. H., Marner, F.-J., Moore, R. E. (1979) Malyngamide A, a novel chlorinated metabolite of the marine cyanophyte Lyngby majuscula. J. Am. chem. Soc. 101: 240–241

    Google Scholar 

  • Carefoot, T. H. (1987). Aplysia: its biology and ecology. Oceanogr. mar. Biol. A. Rev. 25: 167–284

    Google Scholar 

  • Carte, B., Faulkner, D. J. (1981). Polybrominated diphenyl ethers from Dysidea herbacea, Dysidea chlorea and Phyllospongia foliascens. Tetrahedron Lett. 37: p. 2335

    Google Scholar 

  • Cimino G., De Rosa, S., De Stefano, S., Sodano, G. (1982) The chemical defense of four mediterranean nudibranchs. Comp. Biochem. Physiol. 73B: 471–474

    Google Scholar 

  • Daly, J. W., Brown, G. B., Mensah-Dwumah, M. (1978). Classification of skin alkaloids from neotropical poison-dart frogs (Dendrobatidae). Toxicon 16: 163–188

    Google Scholar 

  • De Vore, D. E., Brodie, E. D. (1982). Palatability of the tissues of the holothurian Thyone briareus (Lesueur) to fish. J. exp. mar. Biol. Ecol. 61: 279–285

    Google Scholar 

  • Dethier, V. G. (1954) Evolution of feeding preferences in phytophagous insects. Evolution 8: 35–54

    Google Scholar 

  • DiMatteo, T. (1981). The inking behavior of Aplysia dactylomela (Gastropoda: Opischobranchia): evidence for distastefulness. Mar. Behav. Physiol. 7: 285–290

    Google Scholar 

  • DiMatteo, T. (1982). The ink of Aplysia dactylomela (Rang, 1828) (Gastropoda: Opisthobranchia) and its role as a defensive mechanism. J. exp. mar. Biol. Ecol. 57: 169–180

    Google Scholar 

  • Duffy, J. E., Paul, V. J. (1992). Prey nutritional quality and the effectiveness of chemical defenses against tropical reef fishes. Oecologia 90: 333–339

    Google Scholar 

  • Egelhaaf, A., Colln, K., Schmitz, B., Buck, M. (1990). Organ specific storage of dietary pyrrolizidine alkaloids in the arctiid moth Creatonotos transiens. Z. Naturf. 45c: 115–120

    Google Scholar 

  • Ehrlich, P. R., Murphy, D. D. (1988). Plant chemistry and host range in insect herbivores. Ecology 69: 908–909

    Google Scholar 

  • Ehrlich, P. R., Raven, P. H. (1964). Butterflies and plants: a study in coevolution. Evolution 18: 586–608

    Google Scholar 

  • Faulkner, D. J. (1984). Marine natural products: metabolites of marine algae and herbivorous marine molluscs. Nat. Product. Rep. 1: 251–280

    Google Scholar 

  • Faulkner, D. J. (1988). Feeding deterrents in molluscs. Mem. Calif. Acad. Sci. 13: 29–36

    Google Scholar 

  • Faulkner, D. J. (1992). Chemical defenses of marine molluscs. In: Paul, V. J. (ed.) Ecological roles of marine secondary metabolites. Cornell University Press, Ithaca, New York, p. 119–163

    Google Scholar 

  • Harvell, C. D., Fenical, W. (1989). Chemical and structural defenses of Caribbean gorgonians (Pseudopterogorgia spp.): intracolony localization of defense. Limnol. Oceanogr. 34: 382–389

    Google Scholar 

  • Hay, M. E., Duffy, J. E., Fenical, W. (1989a). Seaweed chemical defenses: among-compound and among-herbivore variance. Proc. 6th int. coral Reef Symp. 3: 43–48. [Choat, J. H. et al. (eds.) Sixth International Coral Reef Symposium Executive Committee, Townsville]

    Google Scholar 

  • Hay, M. E., Duffy, J. E., Fenical, W. (1990). Host-plant specialization decreases predation on a marine amphipod: an herbivore in plant's clothing. Ecology 71: 733–743

    Google Scholar 

  • Hay, M. E., Duffy, J. E., Pfister, C. A., Fenical, W. (1987a). Chemical defense against different marine herbivores: are amphipods insect equivalents? Ecology 68: 1567–1580

    Google Scholar 

  • Hay, M. E., Fenical, W., Gustafson, K. (1987b). Chemical defense against diverse coral-reef herbivores. Ecology 68: 1581–1591

    Google Scholar 

  • Hay, M. E., Pawlik, J. R., Duffy, J. E., Fenical, W. (1989b). Seaweedherbivore-predator interactions: host-plant specialization reduces predation on small hervivores. Oecologia 81: 418–427

    Google Scholar 

  • Hay, M. E., Renaud, P. E., Fenical, W. (1988). Large mobile versus small sedentary herbivores and their resistance to seaweed chemical defense. Oecologia 75: 233–245

    Google Scholar 

  • Hay, M. E., Steinberg, P. D. (1992). The chemical ecology of plantherbivore interactions in marine versus terrestrial communities. In: Rosenthal, G. A., Berenbaum, M. R. (eds.) Herbivores: their interactions with secondary plant metabolites. 2E. Vol. II: evolutionary and ecological processes. Academic Press, New York, p. 371–413

    Google Scholar 

  • Ireland, C., Stallard, M. O., Faulkner, D. J. (1976). Some chemical constituents of the digestive gland of the sea hare Aplysia californica. J. org. Chem 41: 2461–2465

    Google Scholar 

  • Kato, Y., Scheuer, P. J. (1974). Aplysiatoxin and debromoaplysiatoxin, constitutents of the marine mollusk Stylocheilus longicauda (Quoy and Gaimard, 1824). J. Am. chem. Soc. 96: 2245–2246

    Google Scholar 

  • Kvitek, R. G., DeGange, A. R., Beitler, M. K. (1991). Paralytic shellfish poisoning toxins mediate feeding behavior of sea otters. Limnol. Oceanogr. 36: 393–404

    Google Scholar 

  • McClintock, J. B., Heine, J., Slattery, M., Weston, J. (1991). Biochemical and energetic composition, population biology, and chemical defense of the antarctic ascidian Cnemidocarpa verrucosa Lesson. J. exp. mar. Biol. Ecol. 147: 163–175

    Google Scholar 

  • Meyer, K. D., Paul, V. J. (1992). Intraplant variation in secondary metabolite concentration in three species of Caulerpa (Chlorophyta: Caulerpales) and its effects on herbivorous fishes. Mar. Ecol. Prog. Ser. 82: 249–257

    Google Scholar 

  • Moore, R. E. (1981). Constituents of blue-green algae. In: Scheuer, P. J. (ed.) Marine natural products. Vol. 4. Academic Press, New York, p. 1–52

    Google Scholar 

  • Mynderse, J. S., Moore, R. E., Kashigawi, M., Norton, T. R. (1977). Antileukemia activity in the Oscillatoriaceae: isolation of debromoaplysiatoxin from Lyngbya. Science, N. Y. 196: 538–539

    Google Scholar 

  • Nickisch-Rosenegk, E., von, Detzel, A., Wink, M. (1990a). Carriermediated uptake of digoxin by larvae of the cardenolide sequestering moth, Syntomeida epilais. Naturwissenschaften 77: 336–338

    Google Scholar 

  • Nickisch-Rosenegk, E., von, Schneider, D., Wink, M. (1990 b). Time-course of pyrrolizidine alkaloid processing in the alkaloid exploiting arctiid moth, Creatonotos transiens. Z. Naturf. 45c: 881–894

    Google Scholar 

  • Parsons, J. A. (1965). A digitalis-like toxin in the monarch butterfly Danaus plexippus L. J. Physiol. 178: 290–304

    Google Scholar 

  • Pasteels, J. M., Gregoire, J.-C. (1983). The chemical ecology of defense in arthropods. A. Rev. Ent. 28: 263–289

    Google Scholar 

  • Paul, V. J., Fenical, W. (1986). Chemical defense in tropical green algae, order Caulerpales. Mar. Ecol. Prog. Ser. 34: 157–169

    Google Scholar 

  • Paul, V. J., Hay, M. E., Duffy, J. E., Fenical, W., Gustafson, K. (1987). Chemical defense in the seaweed Ochtodes secundiramea (Montagne) Howe (Rhodophyta): effects of its monoterpenoid components upon diverse coral-reef herbivores. J. exp. mar. Biol. Ecol. 114: 249–260

    Google Scholar 

  • Paul, V. J., Lindquist, N., Fenical, W. (1990). Chemical defenses of the tropical ascidian Atapozoa sp. and its nudibranch predators Nembrotha spp. Mar. Ecol. Prog. Ser. 59: 109–118

    Google Scholar 

  • Paul, V. J., Pennings, S. C. (1991). Diet-derived chemical defenses in the sea hare Stylocheilus longicauda (Quoy et Gaimard, 1824). J. exp. mar. Biol. Ecol. 151: 227–243

    Google Scholar 

  • Paul, V. J., Van Alstyne, K. L. (1988). Chemical defense and chemical variation in some tropical Pacific species of Halimeda (Halimedaceae; Chlorophyta). Coral Reefs 6: 263–269

    Google Scholar 

  • Paul, V. J., Van Alstyne, K. L. (1989). Antiherbivore defenses in Halimeda. Proc. 6th int. coral Reef Symp. 3: 133–138. [Choat, J. H., et al. (eds.) Sixth International Coral Reef Symposium Executive Committee, Townsville]

    Google Scholar 

  • Pawlik, J. R., Kernan, M. R., Molinski, T. F., Harper, M. K., Faulkner, D. J. (1988). Defensive chemicals of the spanish dancer nudibranch Hexabranchus sanguineus and its egg ribbons: macrolides derived from a sponge diet. J. exp. mar. Biol. Ecol. 119: 99–109

    Google Scholar 

  • Pennings, S. C. (1990a). Multiple factors promoting narrow host range in the sea hare, Aplysia californica. Oecologia 82: 192–200

    Google Scholar 

  • Pennings, S. C. (1990 b). Size-related shifts in herbivory: specialization in the sea hare Aplysia californica Cooper. J. exp. mar. Biol. Ecol. 142: 43–61

    Google Scholar 

  • Pennings, S. C. (1991). Spatial and temporal variation in recruitment of Aplysia californica Cooper: patterns, mechanisms and consequences. J. exp. mar. Biol. Ecol. 146: 253–274

    Google Scholar 

  • Pennings, S. C., Nadeau, T. M., Paul, V. J. (1993). Selectivity and growth of the generalist herbivore Dolabella auricularia feeding upon complementary resources. Ecology 74: 879–890

    Google Scholar 

  • Pennings, S. C., Paul, V. J. (1992). Effect of plant toughness, calcification and chemistry on herbivory by Dolabella auricularia. Ecology 73: 1606–1619

    Google Scholar 

  • Pennings, S. C., Paul, V. J. (1993). Secondary chemistry does not limit host range of the specialist sea hare Stylocheilus longicauda. J. exp. mar. Biol. Ecol. (in press)

  • Rose, A. F., Scheuer, P. J., Springer, J. P., Clardy, J. (1978). Stylocheilamide, an unusual constituent of the sea hare Stylocheilus longicauda. J. Am. chem. Soc. 100: 7665–7670

    Google Scholar 

  • Rothschild, M., rowan, M. G., Fairbairn, J. W. (1977). Storage of cannabinoids by Arctia caja and Zonocerus elegans fed on chemically distinct strains of Cannabis sativa. Nature, Lond. 266: 650–651

    Google Scholar 

  • Sakemi, S., Higa, T., Anthoni, U., Christophersen, C. (1987). Antitumor cyclic peroxides from the sponge Plakortis lita. Tetrahedron 43: 263–268

    Google Scholar 

  • Schultz, J. C. (1988). Many factors influence the evolution of herbivore diets, but plant chemistry is central. Ecology 69: 896–897

    Google Scholar 

  • Sorokin, M. (1988). Human poisoning by ingestion of a sea hare (Dolabella auricularia). Toxicon 26: 1095–1097

    Google Scholar 

  • Stallard, M. O., Faulkner, D. J. (1974). Chemical constituents of the digestive gland of the sea hare Aplysia california. I. Importance of diet. Comp. Biochem. Physiol. 49B: 25–35

    Google Scholar 

  • Switzer-Dunlap, M, Hadfield, M. G. (1977). Observations on development, larval growth and metamorphosis of four species of Aplysiidae (Gastropoda: Opisthobranchia) in laboratory culture. J. exp. mar. Biol. Ecol. 29: 245–261

    Google Scholar 

  • Switzer-Dunlap, M., Hadfield, M. G. (1979). Reproductive patterns of Hawaiian aplysiid gastropods. In: Stancyk, S. E. (ed.) Reproductive ductive ecology of marine invertebrates. University of South Carolina Press, Columbia, South Carolina, p. 199–210

    Google Scholar 

  • Thompson, J. E., Murphy, P. T., Bergquist, P. R., Evans, E. A. (1987). Environmentally induced variation in diterpene composition of the marine sponge Rhopaloiedes odorablile. Biochem. System. Ecol. 15: 595–606

    Google Scholar 

  • Thompson, J. E., Walker, R. P., Wratten, S. J., Faulkner, D. J. (1982). A chemical defense mechanism for the nudibranch Cadlina luteomarginata. Tetrahedron 38: 1865–1873

    Google Scholar 

  • Vermeij, G. J. (1987). Evolution and escalation. Princeton University Press, Princeton, New Jersey

    Google Scholar 

  • Wells, R. J. (1976). A novel peroxyketal from a sponge. Tetrahedron Lett. 30: 2637–2638

    Google Scholar 

  • Wink, M., Montllor, C. B., Bernays, E. A., Witte, L. (1991). Uresiphita reversalis (Lepidoptera: Pyralidae): carrier-mediated uptake and sequestration of quinolizidine alkaloids obtained from the host plant Teline monspessulana. Z. Naturf. 45 c: 1080–1088

    Google Scholar 

  • Winkler, L. R. (1969). Distribution of organic bromine compounds in Aplysia californica Cooper, 1863. Veliger 11: 268–271

    Google Scholar 

  • Young, D. N., Howard, B. M., Fenical, W. (1980). Subcellular localization of brominated secondary metabolites in the red alga Laurencia snyderae. J. Phycol. 16: 182–185

    Google Scholar 

  • Zangerl, A. R., Bazzaz, F. A. (1992). Theory and pattern in plant defense allocation. In: Fritz, R. S., Simms, E. L. (eds.) Plant resistance to herbivores and pathogens. University of Chicago Press, Chicago, p. 363–391

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Marine Laboratory, University of Guam, 96923, Mangilao, Guam, USA

    S. C. Pennings & V. J. Paul

Authors
  1. S. C. Pennings
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. J. Paul
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by M. G. Hadfield, Honolulu

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pennings, S.C., Paul, V.J. Sequestration of dietary secondary metabolites by three species of sea hares: location, specificity and dynamics. Marine Biology 117, 535–546 (1993). https://doi.org/10.1007/BF00349763

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00349763

Keywords

Search

Navigation