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Chemical Ecology of Three Antarctic Gastropods JAMES B (Eds.), Paleoecology, biostratigraphy, paleoceanography and tax- Sparck, R. 1933. Contributions to the animal ecology of the Franz onomy of agglutinated foraminifera (NATO ASI Series, C360). Joseph Fjord and adjacent East Greenland waters I-II. Meddelelser Dortrecht: Kluwer. om Grønland, 100(1), 5-38. Linke, P., and G.F. Lutze. 1993. Microhabitat preferences of benthic Stephen, A.C. 1923. Preliminary survey of the Scottish waters of the foraminifera—A static concept or a dynamic adaptation to opti- North Sea by Peterson Grab. Fishery Board for Scotland, Scientific mize food acquisition? Marine Micropaleontology, 20(3-4), Investigations, 1922, No. III. 215-234. Tendal, O.S., and R.R. Hessler. 1977. An introduction to the biology Lutze, G.F., and A.V. Altenbach. 1988. Rupertina stabilis (Wallich), a and systematics of Komokiacea. Galathea Report, 14, 165-194. highly adapted, suspension feeding foraminifer. Meyniana, 40, Thies, A. 1990. The ecology, distribution and taxonomy of Crithionina 55-69. hispida Flint, 1889. In C. Hemleben, M.A. Kaminski, W. Kuhnt, and McIntyre, A.D. 1961. Quantitative differences in the fauna of boreal D.B. Scott (Eds.), Paleoecology, biostratigraphy, paleoceanography mud association. Journal of the Marine Biological Association of and taxonomy of agglutinated foraminifera (NATO ASI Series, the United Kingdom, 41(3), 599-616. C360). Dortrecht: Kluwer. Snider, L.J., B.R. Burnett, and R.R. Hessler. 1984. The composition Thorson, G. 1934. Contributions to the animal ecology of the Scores- and distribution meiofauna in a central North pacific deep-sea by Sound Fjord complex (East Greenland). Meddelelser om Grøn- area. Deep-Sea Research, 31(10), 1225-1249. land, 100(3), 5-68. Chemical ecology of three antarctic gastropods JAMES B. MCCLINTOCK, PATRICK J. BRYAN, and MARC SLATTERY, Department of Biology, University ofAlabama, Birmingham, Alabama 35294-1170 BILL J. BAKER, WESLEY Y. YOSHIDA, and MARK HAMANN, Department of Chemistry, Florida Institute of Technology, Melbourne, Florida 32901 JOHN N. HEINE, Moss Landing Marine Laboratories, Moss Landing, California 95039-3304 t depths below the effects of anchor ice and ice scour the prosobranch M. mollis has a vestigial shell imbedded A(Dayton et al. 1969, 1970, pp. 244-258), the antarctic ben- within the mantle tissues. Although these results indicated thos is thought to be structured primarily by biological factors that these antarctic gastropods were noxious to ecologically such as predation and competition (Dayton et al. 1974). Such relevant predators, the secondary metabolites responsible for "biological accommodation" coupled with an extensive geo- this bioactivity were unknown. In this paper, we review the logical history characterized by relatively static environmen- nature of the bioactive compounds and discuss their possible tal conditions (approximately 20 million years; Dayton et al. dietary derivation. 1994) has provided ample time for the evolution of chemical The common pteropod C. antarctica was collected using means of defense in gastropods and other antarctic marine plankton nets near Hut Point and Cape Armitage in Novem- invertebrates (McClintock el al. 1990, 1991, 1992a, 1994a; ber and December 1993. Pteropods were sequentially extract- Baker et al. 1993). Water-column-dwelling gastropods, such ed in hexane, chloroform, methanol, and aqueous methanol. as pteropods, have likely been subjected to intense predation The antarctic fish P. borchgrevinki and Pseudo trematom us pressure from pelagic fish. Moreover, although benthic gas- bernacchii showed feeding deterrence to 2 percent alginate tropods do not appear to be the preferred food of most bot- pellets containing 2 percent dried krill and tissue-level con- tom-dwelling fish (Eastman 1993), they are likely prey of the centrations of the hexane extract [P.1. Bryan, W.Y. Yoshida, abundant seastars (Dearborn 1977, pp. 293-326; McClintock J.B. McClintock, and B.J. Baker, unpublished manuscript: An 1994). ecological role for pteroenone, a novel antifeedant from the As part of our multidisciplinary program investigating conspicuous antarctic pteropod C. antarctica (Gymnosomata: aspects of the chemical ecology of antarctic marine inverte- Gastropoda)]. No feeding deterrence was observed in brates, we have undertaken studies to investigate antarctic response to pellets containing the other extracts or krill alone. gastropods which are likely to possess chemical means of Using flash column chromatography, we further separated defense. Previous studies (McClintock and Janssen 1990; the hexane fraction, and using high pressure liquid chro- McClintock et al. 1992b) have revealed that whole-body tis- matography, we isolated five pure compounds. These com- sues of the antarctic pteropod Clione antarctica or mantle tis- pounds were imbedded in alginate pellets and offered to both sues of the prosobranch mollusk Marseniopsis mollis and the antarctic fish. One of the compounds caused rapid rejection nudibranch Tritoniella belli are rejected by antarctic fish of the krill pellets, and when we used 1- and 2-dimensional (either Pagothenia borchgi-evinkii or Trematomus bernacchii). proton and carbon-13 nuclear magnetic resonance (NMR), Moreover, mantle tissue homogenates of M. mollis and T. we determined the compound to be a linear -hydroxyketone belli caused significant sensory tubefoot retractions in five (C14H2402) and named it "pteroenone" (figure 1; Bryan et al., species of antarctic seastars (McClintock et al. 1992b). All of unpublished manuscript, previously cited; Yoshida et al. in these gastropods lack an external shell for defense, although preparation). The primary prey of C. antarctica, the shelled ANTARCTIC JOURNAL - REVIEW 1994 151 pteropod Limacina helicina (Gilmer and Lalli 1990), did not contain pteroenone suggesting that this defensive compound o OH is likely synthesized de novo. The prosobranch M. mollis and the dorid nudibranch T. belli, as well as their respective primary prey, the tunicate Cnemidocarpa verrucosa and the soft coral Clavularia frankliniana (Dayton et al. 1974), were collected from Octo- ber through December 1993 from approximately 30 meters of water near Hut Point, Cape Armitage, or Danger Slopes, near McMurdo Station. Multiple individuals (more than 10) of T. belli and C. frankliniana were lyophilized and tissues pooled. Pteroenone The mantle, viscera, and foot of three M. mollis and the tunic Figure 1. Chemical structure of the compound pteroenone, a linear of three C. verrucosa were lyophilized and pooled. Dried tis- hydroxyketone with fish antifeedant properties isolated from the tis- sues were extracted in organic solvents. An amino acid deriv- sues of the antarctic pteropod C/lone antarctica. ative was obtained by reverse-phase chromatography eluted with water from the mantle, visceral, and foot tissues of ethanolic extracts of M mollis (McClintock et al. 1994b). A H "14^ NMR spectral analysis indicated the presence of homarine (figure 2), which was confirmed by high-pressure liquid chro- matography (HPLC) analysis. Shrimp-treated filter paper disks loaded with tissue-level concentrations of homarine and presented to the omnivorous antarctic seastar Odontaster EM ON validus caused significant feeding deterrence (McClintock et al. 1994b). No homarine was detected in the tunic of C. verru- -N CO2.. cosa. Nonetheless, subsequent HPLC analysis of the epibionts (bryozoans and hydroids) on the surface of the tunic revealed I the presence of homarine suggesting that M. mollis may in fact derive its defensive chemistry from these epizooites. CH3 The dorid nudibranch T. belli was extracted in acetone and the concentrate partitioned between ethyl acetate and water. Employing normal phase HPLC, the ethyl acetate solu- Homarine ble portion yielded three gylcerol ethers, including chimyl alcohol (McClintock et al. in press; figure 3), a known antimi- Figure 2. Chemical structure of the amino acid derivative homarine, a seastar antifeedant isolated from the foot, mantle, and visceral tissues crobial and fish antifeedant (Gustafson and Anderson 1985). of the antarctic prosobranch mollusk Marseniopsis molls. Shrimp-treated filter paper disks loaded with one of three log concentrations of chimyl alcohol (bracketing tissue level con- centration) caused significant feeding deterrence in the OH OH OCH3 HOO HOO omnivorous antarctic seastar 0. validus when compared to (CH2)12CH3 rejection rates for control shrimp disks (McClintock et al. in Chimyl Alcohol press). An ethyl acetate/hexane fraction of the soft coral T. belli was subjected to normal phase HPLC to yield among other fatty acid derivatives, chimyl alcohol. The isolated OH HOO chimyl alcohol was characterized by comparison with com- (CH2)19CH3 mercially available material and by H NMR spectroscopy. The verification of chimyl alcohol in the tissues of the soft Figure 3. Chemical structures of three glycerol ethers isolated from coral C. frankliniana suggests that the dorid T. belli may be whole-body tissues of the antarctic dorid nudibranch Tritoniella be/li. deriving its defensive chemistry from its diet. This needs to be Chimyl alcohol was found to cause feeding inhibition in the omnivo- confirmed by future radioisotope studies. rous antarctic seastar Odontaster validus. We thank Mike Davies-Coleman and John D. Faulkner for providing data on the secondary metabolite chemistry of T. References belli. We also wish to thank the Antarctic Support Associates, the Antarctic Support Services of the National Science Foun- Baker, B.J.,
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