Skip to main content
Log in

Lipophilic Defenses From Alcyonium Soft Corals of Antarctica

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Alcyonacean soft corals lack physical or skeletal defenses and their nematocyst system is weak, leading to the conclusion that soft corals mainly rely on chemistry for protection from predators and microbes. Defensive chemicals of primary and secondary metabolic origin are exuded in the mucus surface layer, explaining the general lack of heavy fouling and predation in corals. In Antarctic ecosystems, where generalist predation is intense and mainly driven by invertebrate consumers, the genus Alcyonium is represented by eight species. Our goal was to investigate the understudied chemical ecology of Antarctic Alcyonium soft corals. We obtained six samples belonging to five species: A. antarcticum, A. grandis, A. haddoni, A. paucilobulatum, and A. roseum, and assessed the lipid-soluble fractions for the presence of defensive agents in these specimens. Ethyl ether extracts were tested in feeding bioassays with the sea star Odontaster validus and the amphipod Cheirimedon femoratus as putative sympatric predators. Repellent activities were observed towards both consumers in all but one of the samples assessed. Moreover, three of the extracts caused inhibition to a sympatric marine bacterium. The ether extracts afforded characteristic illudalane sesquiterpenoids in two of the samples, as well as particular wax esters subfractions in all the colonies analyzed. Both kinds of metabolites displayed significant deterrent activities demonstrating their likely defensive role. These results suggest that lipophilic chemicals are a first line protection strategy in Antarctic Alcyonium soft corals against predation and bacterial fouling.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Arnaud, P. M. 1977. Adaptations within the Antarctic marine ecosystem, pp. 135–158, in: Llano GA, (ed.). Adaptations within Antarctic ecosystems. Houston: Proc 3rd SCAR Symp Antarct Biol.

  • Atwater, W. O., and Benedict, F.G. 1902. Experiments on the metabolism of matter and energy in the human body, 1898–1900. In: Stations UOoE, editor. Washington, DC: Government Printing Office.

  • Avila, C., Kelman, D., Kashman, Y., and Benayahu, Y. 1999. An association between a dendronotid nudibranch (Mollusca, Opisthobranchia) and a soft coral (Octocorallia, Alcyonaria) from the red sea. J. Nat. Hist. 33:1433–1449.

    Article  Google Scholar 

  • Avila, C., Taboada, S., and Núñez-Pons, L. 2008. Marine Antarctic chemical ecology: What is next? Mar. Ecol. 29:1–70.

    Article  CAS  Google Scholar 

  • Benson, A. A., Patton, J. S., and Field, C. E. 1975. Wax digestion in a crown-of-thorns starfish. Comp. Biochem. Physiol. B 52:339–340.

    Article  PubMed  CAS  Google Scholar 

  • Blunt, J. W., Copp, B. R., Keyzers, R. A., Munro, M. H. G., and Prinsep, M. R. 2012. Marine natural products. Nat. Prod. Rep. 29:144–222.

    Article  PubMed  CAS  Google Scholar 

  • Bregazzi, P. K. 1972. Life cycles and seasonal movements of Cheirimedon femoratus and Tryphosella kergueleni crustacea amphipoda. Brit. Antarct. Surv. B. 30:1–34.

    Google Scholar 

  • Brown, B. E. and Bythell, J. C. 2005. Perspectives on mucus secretion in reef corals. Mar. Ecol. Prog. Ser. 296:291–309.

    Article  CAS  Google Scholar 

  • Brusca, R. C., and Brusca, G. J. 2003. Invertebrates. Madrid: McGraw-Hill Interamericana en España, SAU. 895 p.

  • Carbone, M., Nunez-Pons, L., Castelluccio, F., Avila, C., and Gavagnin, M. 2009. Illudalane sesquiterpenoids of the alcyopterosin series from the Antarctic marine soft coral Alcyonium grandis. J. Nat. Prod. 72:1357–1360.

    Article  PubMed  CAS  Google Scholar 

  • Casas, C., Ramil, F., and van Ofwegen, L. P. 1997. Octocorallia (Cnidaria: Anthozoa) from the Scotia Arc, South Atlantic Ocean. I. The genus Alcyonium Linnaeus, 1758. Zool. Med. (Leiden) 71:299–311.

    Google Scholar 

  • Coll, J. C., Bowden, B. F., and Tapiolas, D. M. 1982. In situ isolation of allelochemicals released from soft corals (Coelenterata : Octocorallia): A totally submersible sampling apparatus. J. Exp. Mar. Biol. Ecol. 60:293–299.

    Article  CAS  Google Scholar 

  • Coll, J. C., Price, I. R., Konig, G. M., and Bowden, B. F. 1987. Algal overgrowth of alcyonacean soft corals. Mar. Biol. 96:129–135.

    Article  Google Scholar 

  • Dayton, P. K., Robillia, G. A., Paine, R. T., and Dayton, L. B. 1974. Biological accommodation in benthic community at McMurdo Sound Antarctica. Ecol. Monogr. 44:105–128.

    Article  Google Scholar 

  • De Broyer, C., Lowry, J. K., JAzdzewski, K., and Robert, H. 2007. Catalogue of the gammaridean and corophiidean Amphipoda of the Southern Ocean, with distribution and ecological data pp. 1–325, in: De Broyer C, (ed.). Census of Antarctic Marine Life: Synopsis of the Amphipoda of the Southern Ocean: Bulletin de l’Institut Royal des Sciences Naturelles de Belgique, Biologie, 77, supplement 1.

  • Ducklow, H. W. and Mitchell, R. 1979. Bacterial-populations and adaptations in the mucus layers on living corals. Limnol. Oceanogr. 24:715–725.

    Article  Google Scholar 

  • Finkielsztein, L. M., Bruno, A. M., Renou, S. G., and Iglesias, G. Y. M. 2006. Design, synthesis, and biological evaluation of alcyopterosin A and illudalane derivatives as anticancer agents. Bioorgan. Med. Chem. 14:1863–1870.

    Article  CAS  Google Scholar 

  • Fleury, B. G., Coll, J. C., Sammarco, P. W., Tentori, E., and Duquesne, S. 2004. Complementary (secondary) metabolites in an octocoral competing with a scleractinian coral: effects of varying nutrient regimes. J. Exp. Mar. Biol. Ecol. 303:115–131.

    Article  CAS  Google Scholar 

  • Fleury, B. G., Lages, B. G., Barbosa, J. P., Kaiser, C. R., and Pinto, A. C. 2008. New hemiketal steroid from the introduced soft coral Chromonephthea braziliensis is a chemical defense against predatory fishes. J. Chem. Ecol. 34:987–993.

    Article  PubMed  CAS  Google Scholar 

  • Gribble, G. W. 1996. Naturally occurring organohalogen compounds - a comprehensive survey. Fort. Chem. Org. Nat. 68:1–423.

    CAS  Google Scholar 

  • Gutt, J., Sirenko, B. I., Arntz, W. E., Smirnov, I. S., and de Broyer, C. 2000. Biodiversity of the Weddell Sea: macrozoobenthic species (demersal fish included) sampled during the expedition ANT XIII/3 (EASIZ I) with RV ‘Polarstern’. Ber. Polarforsch. 372:1–118.

    Google Scholar 

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

    Article  Google Scholar 

  • Harvell, C. D., Fenical, W., Roussis, V., Ruesink, J. L., Griggs, C. C., and Greene, C. H. 1993. Local and geographic variation in the defensive chemistry of a West-Indian gorgonian coral (Briareum asbestinum). Mar. Ecol. Prog. Ser. 93:165–173.

    Article  CAS  Google Scholar 

  • Kelecom, A. 2002. Secondary metabolites from marine microorganisms. An. Acad. Bras. Cienc. 74:151–170.

    Article  PubMed  CAS  Google Scholar 

  • Kelman, D., Kushmaro, A., Loya, Y., Kashman, Y., and Benayahu, Y. 1998. Antimicrobial activity of a Red Sea soft coral, Parerythropodium fulvum fulvum: Reproductive and developmental considerations. Mar. Ecol. Prog. Ser. 169:87–95.

    Article  Google Scholar 

  • Kelman, D., Benayahu, Y., and Kashman, Y. 1999. Chemical defence of the soft coral Parerythropadium fulvum fulvum (Forskal) in the Red Sea against generalist reef fish. J. Exp. Mar. Biol. Ecol. 238:127–137.

    Article  CAS  Google Scholar 

  • la Barre, S. C., Coll, J. C., and Sammarco, P. W. 1986a. Competitive strategies of soft corals (Coelenterata: Octocorallia): III. Spacing and aggressive interactions between alcyonaceans. Mar. Ecol. Prog. Ser. 28:147–156.

    Article  Google Scholar 

  • la Barre, S. C., Coll, J. C., and Sammarco, P. W. 1986b. Defensive strategies of soft corals (Coelenterata, Octocorallia) of the Great-Barrier-Reef.2. The relationship between toxicity and feeding deterrence. Biol. Bull. 171:565–576.

    Article  Google Scholar 

  • Mahon, A. R., Amsler, C. D., McClintock, J. B., Amsler, M. O., and Baker, B. J. 2003. Tissue-specific palatability and chemical defenses against macropredators and pathogens in the common articulate brachiopod Liothyrella uva from the Antarctic Peninsula. J. Exp. Mar. Biol. Ecol. 290:197–210.

    Article  CAS  Google Scholar 

  • Manzo, E., Ciavatta, M. L., Nuzzo, G., and Gavagnin, M. 2009. Terpenoid content of the Antarctic soft coral Alcyonium antarcticum. Nat. Prod. Commun. 4:1615–1619.

    PubMed  CAS  Google Scholar 

  • McClintock, J. B. 1994. Trophic biology of Antarctic echinoderms. Mar. Ecol. Prog. Ser. 111:191–202.

    Article  Google Scholar 

  • McFarland, J. 1907. The nephelometer:an instrument for estimating the number of bacteria in suspensions used for calculating the opsonic index and for vaccines. M.D. JAMA. XLIX:1176–1178.

    Article  Google Scholar 

  • Miyamoto, T., Yamada, K., Ikeda, N., Komori, T., and Higuchi, R. 1994. Bioactive terpenoids from Octocorallia.1. Bioactive diterpenoids – litophynol A and litophynol B from the mucus of the soft coral Litophyton sp. J. Nat. Prod. 57:1212–1219.

    Article  PubMed  CAS  Google Scholar 

  • Núñez-Pons, L., Carbone, M., Paris, D., Melck, D., Ríos, P., Cristobo, J., Castelluccio, F., Gavagnin, M., and Avila, C. 2012a. Chemo-ecological studies on hexactinellid sponges from the Southern Ocean. Naturwissenschaften 99:353–368.

    Article  PubMed  Google Scholar 

  • Núñez-Pons, L., Rodríguez-Arias, M., Gómez-Garreta, A., Ribera-Siguán, A., and Avila, C. 2012b. Feeding deterrency in Antarctic marine organisms: bioassays with an omnivorous lyssianasid amphipod. Mar. Ecol. Prog. Ser. 462:163–174.

    Article  Google Scholar 

  • O'Neal, W. and Pawlik, J. R. 2002. A reappraisal of the chemical and physical defenses of Caribbean gorgonian corals against predatory fishes. Mar. Ecol. Prog. Ser. 240:117–126.

    Article  Google Scholar 

  • Palermo, J. A., Brasco, M., Spagnuolo, C., and Seldes, A. M. 2000. Illudalane sesquiterpenoids from the soft coral Alcyonium paessleri: The first natural nitrate esters. J. Org. Chem. 65:4482–4486.

    Article  PubMed  CAS  Google Scholar 

  • Pass, M. A., Capra, M. F., Carlisle, C. H., Lawn, I., and Coll, J. C. 1989. Stimulation of contractions in the polyps of the soft coral Xenia elongata by compounds extracted from other alcyonacean soft corals. Comp. Biochem. Phys. C 94(2):677–681.

    Article  Google Scholar 

  • Paul, V. J. 1992. Ecological roles of marine natural products. Comstock Publications Association, New York.

    Google Scholar 

  • Peterson, C. H. and Renaud, P. E. 1989. Analysis of feeding preference experiments. Oecologia 80:82–86.

    Article  PubMed  CAS  Google Scholar 

  • Rhoades, D. F. and Cates, R. G. 1976. Toward a general theory of plant antiherbivore chemistry. Rec. Adv. Phytochem. 10:168–213.

    CAS  Google Scholar 

  • Ritchie, K. B. 2006. Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar. Ecol. Prog. Ser. 322:1–14.

    Article  CAS  Google Scholar 

  • Rodríguez-Brasco, M. F. R., Seldes, A. M., and Palermo, J. A. 2001. Paesslerins A and B: Novel tricyclic sesquiterpenoids from the soft coral Alcyonium paessleri. Org. Lett. 3:1415–1417.

    Article  PubMed  Google Scholar 

  • Sammarco, P. W. and Coll, J. C. 1992. Chemical adaptations in the octocorallia - evolutionary considerations. Mar. Ecol. Prog. Ser. 88:93–104.

    Article  CAS  Google Scholar 

  • Sargent, J. R., Gatten, R. R., and Mcintosh, R. 1977. Wax esters in marine-environment - their occurrence, formation, transformation and ultimate fates. Mar. Chem. 5:573–584.

    Article  CAS  Google Scholar 

  • Schmidt, H. 1974. On evolution in the anthozoa. Proc. Int. Coral Reef Symp. 2:533–560.

    Google Scholar 

  • Slattery, M. and McClintock, J. B. 1995. Population structure and feeding deterrence in three shallow-water Antarctic soft corals. Mar. Biol. 122:461–470.

    Article  Google Scholar 

  • Slattery, M. and McClintock, J. B. 1997. An overview of the population biology and chemical ecology of three species of Antarctic soft corals, pp. 309–315, in B. Battaglila, J. Valencia, and D. W. H. Walton (eds.), Antarctic communities: species, structure and survival. Cambridge University Press, England.

    Google Scholar 

  • Slattery, M., McClintock, J. B., Heine, J., and Weston, J. 1990. The chemical ecology of the Antarctic soft coral Alcyonium paessleri. Am. Zool. 30:A130.

    Google Scholar 

  • Slattery, M., Hines, G. A., and Watts, S. A. 1994. Progesterone and androstenedione metabolism in Antarctic soft corals. Am. Zool. 34:21A.

    Google Scholar 

  • Slattery, M., McClintock, J. B., and Heine, J. N. 1995. Chemical defenses in Antarctic soft corals: Evidence for antifouling compounds. J. Exp. Mar. Biol. Ecol. 190:61–77.

    Article  CAS  Google Scholar 

  • Slattery, M., Hamann, M. T., McClintock, J. B., Perry, T. L., Puglisi, M. P., and Yoshida, W. Y. 1997a. Ecological roles for water-borne metabolites from Antarctic soft corals. Mar. Ecol. Prog. Ser. 161:133–144.

    Article  CAS  Google Scholar 

  • Slattery, M., Hines, G. A., and Watts, S. A. 1997b. Steroid metabolism in Antarctic soft corals. Polar Biol. 18:76–82.

    Article  Google Scholar 

  • Slattery, M., Avila, C., Starmer, J., and Paul, V. J. 1998. A sequestered soft coral diterpene in the aeolid nudibranch Phyllodesmium guamensis Avila, Ballesteros, Slattery, Starmer and Paul. J. Exp. Mar. Biol. Ecol. 226:33–49.

    Article  CAS  Google Scholar 

  • Slattery, M., Starmer, J., and Paul, V. J. 2001. Temporal and spatial variation in defensive metabolites of the tropical Pacific soft corals Sinularia maxima and S. polydactyla. Mar. Biol. 138:1183–1193.

    Article  CAS  Google Scholar 

  • Sokal, R. R. and Rohlf, F. J. 1995. Biometry: The principles and practice of statistics in biological research. Freeman, W. H. and Co, New York. 887 p.

    Google Scholar 

  • Suzuki, S., Murayama, T., and Shiono, Y. 2005. Illudalane sesquiterpenoids, echinolactones A and B, from a mycelial culture of Echinodontium japonicum. Phytochemistry 66:2329–2333.

    Article  PubMed  CAS  Google Scholar 

  • Tomaschko, K. H. 1994. Ecdysteroids from Pycnogonum litorale (Arthropoda, Pantopoda) act as chemical defense against Carcinus maenas (Crustacea, Decapoda). J. Chem. Ecol. 20:1445–1455.

    Article  CAS  Google Scholar 

  • van Alstyne, K. L., Wylie, C. R., Paul, V. J., and Meyer, K. 1992. Antipredator defenses in tropical pacific soft corals coelenterata Alcyonacea 1. Sclerites as defenses against generalist carnivorous fishes. Biol. Bull. 182:231–240.

    Article  Google Scholar 

  • van Alstyne, K. L., Wylie, C. R., and Paul, V. J. 1994. Antipredator defenses in tropical Pacific soft corals (Coelenterata, Alcyonacea).2. The relative importance of chemical and structural defenses in 3 species of Sinularia. J. Exp. Mar. Biol. Ecol. 178:17–34.

    Article  Google Scholar 

  • van Ofwegen, L. P., Häussermann, V., and Försterra, G. 2007. The genus Alcyonium (Octocorallia: Alcyonacea: Alcyoniidae) in Chile. Zootaxa 1607:1–19.

    Google Scholar 

  • Verseveldt, J. and van Ofwegen, L. P. 1992. New and redescribed species of Alcyonium Linnaeus, 1758 (Anthozoa: Alcyonacea). Zool. Med. (Leiden) 66:155–181.

    Google Scholar 

  • Wang, C., Liu, H., Shao, C., Wang, Y., Li, L., and Guan, H. 2008. Chemical defensive substances of soft corals and gorgonians. Acta Ecol. Sinica 28:2320–2328.

    Article  CAS  Google Scholar 

  • Wylie, C. R. and Paul, V. J. 1989. Chemical defenses in three species of Sinularia (Coelenterata, Alcyonacea): Effects against generalist predators and the butterflyfish Chaetodon unimaculatus Bloch. J. Exp. Mar. Biol. Ecol. 129:141–160.

    Article  Google Scholar 

Download references

Acknowledgements

We thank L. Ciavatta, F. Castelluccio, M. Rodríguez-Arias, M. Paone, S. Taboada, J. Cristobo, B. Figuerola, C. Angulo, and J. Moles for support and help in the lab. Thanks are due to S. Catazine for the artwork. Also we are grateful to W. Arntz and the crew of R/V Polarstern, UTM (CSIC), “Las Palmas” and BAE “Gabriel de Castilla” crews for logistic support. Funding was provided by the Ministry of Science and Innovation of Spain (CGL/2004-03356, ANT, CGL2007-65453/ANT and CGL2010-17415/ANT).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Laura Núñez-Pons.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Núñez-Pons, L., Carbone, M., Vázquez, J. et al. Lipophilic Defenses From Alcyonium Soft Corals of Antarctica. J Chem Ecol 39, 675–685 (2013). https://doi.org/10.1007/s10886-013-0276-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-013-0276-1

Keywords

Navigation