Skip to main content
Log in

Ecological role for pteroenone, a novel antifeedant from the conspicuous antarctic pteropod Clione antarctica (Gymnosomata: Gastropoda)

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Dense populations of the antarctic pteropod Clione antarctica (Smith) offer a rich source of potential nutrients and energy to planktivorous predators. Nonetheless, antarctic fish do not prey on C. antarctica. Employing flash and high-pressure liquid chromatographic techniques, a linear β-hydroxyketone, pteroenone (C14H24O2) was isolated from whole tissues of C. antarctica. When embedded in alginate food pellets at ecologically relevant concentrations, pteroenone caused significant feeding deterrence in Pagothenia borchgrevinki and Pseudotrematomas bernacchii, two antarctic fish known to feed on planktonic organisms. Concentrations of pteroenone were variable between pteropods (0.056 to 4.5 mg ml-1 tissue), but even those individuals with the lowest natural concentration contained levels five-fold greater than the lowest effective feeding-deterrent concentration (0.012 mg ml-1 alginate). Chemical analysis indicated that the primary dietary item of the carnivorous C. antarctica, the shelled pteropod Limacina helicina, does not contain pteroenone. This suggests that C. antarctica does not derive this defensive compound from its diet. This is the first example of a defensive secondary metabolite in a pelagic gastropod.

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

Access this article

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

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein using the principle of protein-dye binding. Analyt Biochem 72:248–254

    Article  PubMed  Google Scholar 

  • Brody S (1945) Bioenergetics and growth. Hafner Publishing Co, New York

    Google Scholar 

  • Conover RJ (1966) Factors affecting the assimilation of organic matter by zooplankton and the question of superfluous feeding. Limnol Oceanogr 11:346–354

    Google Scholar 

  • DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith R (1953) Colorimetric determination of sugars and related substances. Analyt Chem 28:350–356

    Google Scholar 

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

    Google Scholar 

  • Faulkner DJ (1993) Marine natural products. Nat Product Rep 10:497–539

    Article  Google Scholar 

  • Foster BA (1987) Composition and abundance of zooplankton under the spring sea-ice of McMurdo Sound, Antarctica. Polar Biol 8:41–48

    Google Scholar 

  • Foster BA, Carghill JM, Montgomery JC (1987) Planktivory in Pagothenia borchgrevinki (Pisces: Nototheniidae) in McMurdo Sound, Antarctica. Polar Biol 8:49–54

    Google Scholar 

  • Freeman NK, Lindgren FT, Ng YC, Nichols AV (1957) Infrared spectra of some lipoproteins and related lipids. J biol Chem 203:293–304

    Google Scholar 

  • Gerwick WH, Whatley G (1989) Aplysia sea hare assimilation of secondary metabolites from brown seaweed, Stypopodium zonale. J chem Ecol 15:677–683

    Google Scholar 

  • Gilmer RW, Lalli CM (1990) Bipolar variation in Clione, a gymmosomatous pteropod. Am malac Bull 8:67–75

    Google Scholar 

  • Gittleman JL, Harvey PH, Greenwood PJ (1980) The evolution of conspicuous coloration: some experiments in bad taste. Anim Behav 28:897–899

    Google Scholar 

  • Guilford T (1988) The evolution of conspicuous coloration. In: Brower LP (ed) Mimicry and the evolutionary process. University of Chicago Press, Chicago, pp 7–21

    Google Scholar 

  • Guilford T, Cuthill I (1991) The evolution of aposematism in marine gastropods. Evolution 45:449–451

    Google Scholar 

  • Harvell CD, Fenical W (1989) Chemical and structural defenses of Caribbean gorgonians (Pseudopterogorgia spp.): intracolony localization of defense. Limnol Oceanogr 32:382–389

    Google Scholar 

  • Harvell CD, Fenical W, Green CH (1988) Chemical and structural defenses of Caribbean gorgonians (Pseudopterogorgia spp.). I. Development of an in situ feeding assay. Mar Ecol Prog Ser 49:287–294

    Google Scholar 

  • Hay ME, Fenical W (1988) Marine plant-herbivore interactions: the ecology of chemical defense. A Rev Ecol Syst 19:111–145

    Google Scholar 

  • Karuso P (1987) Chemical ecology of the nudibranchs. In: Scheuer PJ (ed) Bioorganic marine chemistry. Springer Verlag, New York, pp 31–60

    Google Scholar 

  • Kerfoot WC (1982) A question of taste: crypsis and warning coloration in freshwater zooplankton communities. Ecology 63:538–554

    Google Scholar 

  • Larson RJ, Harbison GR (1990) Medusae from McMurdo Sound, Ross Sea including the descriptions of two new species, Leuckartiara brownei and Benthocodon hyalinus. Polar Biol 11:19–25

    Google Scholar 

  • Lawrence JM, Kafri J (1979) Numbers, biomass, and caloric content of the echinoderm fauna of the rocky shores of Barbados. Mar Biol 52:87–91

    Google Scholar 

  • Lindquist N, Hay ME, Fenical W (1992) Chemical defenses of ascidians and their conspicuous larvae. Ecol Monogr 62:547–568

    Google Scholar 

  • McClintock JB (1986) On estimating energetic values of prey: implications in optimal diet models. Oecologia 70:161–162

    Google Scholar 

  • McClintock JB (1987) Investigation of the relationship between invertebrate predation and biochemical composition, energy content, spicule armament and toxicity of benthic sponges at McMurdo Sound, Antarctica. Mar Biol 94:479–487

    Google Scholar 

  • McClintock JB (1989) Toxicity of shallow-water antarctic echinoderms. Polar Biol 9:461–465

    Google Scholar 

  • McClintock JB, 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 

  • McClintock JB, Janssen J (1990) Pteropod abduction as a chemical defense in a pelagic amphipod. Nature, Lond 346:462–464

    Google Scholar 

  • McClintock JB, Slattery M, Heine J, Weston J (1992) Chemical defense, biochemical composition and energy content of three shallow-water antarctic gastropods. Polar Biol 11:623–629

    Article  Google Scholar 

  • Michaels AF, Silver MW (1988) Primary production, sinking flux and the microbial food web. Deep-Sea Res 35:473–490

    Article  Google Scholar 

  • Montgomery JC, MacDonald JA (1987) Sensory tuning of lateral line receptors in antarctic fish to the movements of planktonic prey. Nature, Lond 235:195–196

    Google Scholar 

  • Montgomery JC, MacDonald JA, Housley GD (1988) Lateral line function in an antarctic fish related to the signal produced by planktonic prey. J comp Physiol (Sect A) 163:827–833

    Google Scholar 

  • Montgomery JC, Pankhurst NW, Foster BA (1989) Limitations on visual food-location in the planktivorous antarctic fish Pagothenia borchgrevinki. Experientia 45:395–397

    Google Scholar 

  • Moreno CA (1980) Observations on food and reproduction in Trematomas bernacchii (Pisces: Nototheniidae) from the Palmer Archipelago, Antarctica. Copeia 1:171–173

    Google Scholar 

  • Pankhurst NW, Montgomery JC (1989) Visual function in four antarctic nototheniid fishes. J exp Biol 142:311–324

    Google Scholar 

  • Paul VJ (1992) Ecological roles of marine natural products, Comstock Publishing Associates, Ithaca, New York

    Google Scholar 

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

    Article  Google Scholar 

  • Paul VJ, Van Alstyne KL (1992) Activation of chemical defenses in the tropical green algae Halimeda spp. J exp mar Biol Ecol 160:191–203

    Article  Google Scholar 

  • Pawlik JR (1993) Marine invertebrate chemical defenses. Chem Rev 93:1911–1922

    Google Scholar 

  • Pawlik JR, Albizati KF, Faulkner DJ (1986) Evidence of a defensive role for limatulone, a novel triterpene from the intertidal limpet Collisella limatula. Mar Ecol Prog Ser 30:251–260

    Google Scholar 

  • Pawlik JR, Kernan MR, Molinski TF, Harper MK, Faulkner DJ (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

    Article  Google Scholar 

  • Rivkin R (1991) Seasonal patterns of planktonic production in McMurdo Sound, Antarctica. Am Zool 31:5–16

    Google Scholar 

  • Still WC, Kahn M, Mitra A (1978) Rapid chromatographic technique for preparative separations with moderate resolution. J org Chem 43:2923–2925

    Google Scholar 

  • Thompson TE (1960) Defensive adaptation in opisthobranchs. J mar biol Ass UK 39:123–134

    Google Scholar 

  • Van Alstyne KL (1988) Herbivore grazing increases polyphenolic defenses in the intertidal brown algae Fuscus distichus. Ecology 69:655–663

    Google Scholar 

  • Yoshida WY, Bryan PJ, Baker BJ, McClintock JB (1995) Pteroenone: a defensive metabolite of the abducted antarctic pteropod Clione antarctica. J org Chem (in press)

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by N. H. Marcus, Tallahassee

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bryan, P.J., Yoshida, W.Y., McClintock, J.B. et al. Ecological role for pteroenone, a novel antifeedant from the conspicuous antarctic pteropod Clione antarctica (Gymnosomata: Gastropoda). Marine Biology 122, 271–277 (1995). https://doi.org/10.1007/BF00348940

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00348940

Keywords

Navigation