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Palatability of Macroalgae that Use Different Types of Chemical Defenses

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Abstract

This study compared algal palatability and chemical defenses from subtropical green algae that may use different types of defense systems that deter feeding by the rock-boring sea urchin Echinometra lucunter. The potential defense systems present include (1) the terpenoid caulerpenyne and its activated products from Caulerpa spp., and (2) dimethylsulfoniopropionate (DMSP)-related defenses in Ulva spp. Secondary metabolites from these chemical groups have been shown to deter feeding by various marine herbivores, including tropical and temperate sea urchins. Live algal multiple-choice feeding assays and assays incorporating algal extracts or isolated metabolites into an artificial diet were conducted. Several green algae, including Ulva lactuca, Caulerpa prolifera, and Cladophora sp., were unpalatable. Nonpolar extracts from U. lactuca deterred feeding, whereas nonpolar extracts from C. prolifera had no effect on feeding. Polar extracts from both species stimulated feeding. Caulerpenyne deterred feeding at approximately 4% dry mass; however, dimethyl sulfide and acrylic acid had no effect at natural and elevated concentrations. E. lucunter is more tolerant than other sea urchins to DMSP-related defenses and less tolerant to caulerpenyne than many reef fish. Understanding the chemical defenses of the algae tested in this study is important because they, and related species, frequently are invasive or form blooms, and can significantly modify marine ecosystems.

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References

  • Amade, P. and Lemee, R. 1998. Chemical defence of the Mediterranean alga Caulerpa taxifolia: Variations in caulerpenyne production. Aquat. Toxicol. 43:287–300.

    Article  CAS  Google Scholar 

  • Borowsky, R. and Borowsky, B. 1990. Feeding inhibition of the salt marsh amphipod Gammarus palustris Bousfield, 1969 by heat-labile substances in Ulva lactuca L. Crustaceana 59:299–301.

    Article  Google Scholar 

  • Carpenter, R. C. 1986. Partitioning herbivory and its effects on coral reef algal communities. Ecol. Monogr. 56:345–363.

    Article  Google Scholar 

  • Cimino, G., Crispino, A., Di Marzo, V., Gavagnin, M., and Ros, J. D. 1990. Oxytoxins, bioactive molecules produced by the marine opisthobranch mollusc Oxynoe olivacea from a diet-derived precursor. Experientia 46:767–770.

    Article  PubMed  CAS  Google Scholar 

  • Davis, A. R., Benkendorff, K., and Ward, D. W. 2005. Responses of common SE Australian herbivores to three suspected invasive Caulerpa spp. Mar. Biol. 146:859–868.

    Article  Google Scholar 

  • Duffy, J. E. and Hay, M. E. 1994. Herbivore resistance to seaweed chemical defense: The roles of mobility and predation risk. Ecology 75:1304–1319.

    Article  Google Scholar 

  • Dumay, O., Pergent, G., Pergent-Martini, C., and Amade, P. 2002. Variations in caulerpenyne contents in Caulerpa taxifolia and Caulerpa racemosa. J. Chem. Ecol. 28:343–352.

    Article  PubMed  CAS  Google Scholar 

  • Elenkov, I., Georgieva, T., Hadjieva, P., Dimitrova-Konaklieva, S., and Popov, S. 1995. Terpenoids and sterols in Cladophora vagabunda. Phytochemistry. 38:457–459.

    Article  CAS  Google Scholar 

  • Gavagnin, M., Marin, A., Castelluccio, F., Villani, G., and Cimino, G. 1994. Defensive relationships between Caulerpa prolifera and its shelled sacoglossan predators. J. Exp. Mar. Biol. Ecol. 175:197–210.

    Article  Google Scholar 

  • Granado, I. and Caballero, P. 2001. Feeding rates of Littorina striata and Osilinus atratus in relation to nutritional quality and chemical defenses of seaweeds. Mar. Biol. 138:1213–1224.

    Article  Google Scholar 

  • Guerriero, A. and D'Ambrosio, M. 1999. Epoxycaulerpenynes: Reactivity, and diastereoselective and highly regioselective synthesis by dimethyldioxirane oxidation of caulerpenyne. Eur. J. Org. Chem. 1999:1985–1990.

    Article  Google Scholar 

  • Guerriero, A., Marchetti, F., D'Ambrosio, M., Senesi, S., Dini, F., and Pietra, F. 1993. New ecotoxicologically and biogenetically relevant terpenes of the tropical green seaweed Caulerpa taxifolia which is invading the Mediterranean. Helv. Chim. Acta. 76:855–864.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hay, M. E., Stachowicz, J. J., Cruz-Rivera, E., Bullard, S., Deal, M. S., and Lindquist, N. 1998. Bioassays with marine and freshwater organisms, pp. 39–141, in K. F. Haynes and J. G. Millar (eds.). Methods in Chemical Ecology, vol. 2, Bioassay Methods. Chapman & Hall, New York, NY.

    Google Scholar 

  • Hendler, G., Miller, J. E., Pawsom, D. L., and Kier, P. M. 1995. Sea Stars, Sea Urchins, and Allies. Smithsonian Institution Press, Washington, DC.

    Google Scholar 

  • Jousson, O., Pawlowski, J., Zaninetti, L., Zechman, F. W., Din, F., Di Guiseppe, G., Woodfield, R., Millar, A., and Meinesz, A. 2000. Invasive alga reaches California—The alga has been identified that threatens to smother Californian coastal ecosystems. Nature 408:157–158.

    Article  PubMed  CAS  Google Scholar 

  • Jung, V. and Pohnert, G. 2001. Rapid wound-activated transformation of the green algal defensive metabolite caulerpenyne. Tetrahedron 57:7169–7172.

    Article  CAS  Google Scholar 

  • Jung, V., Thibaut, T., Meinesz, A., and Pohnert, G. 2002. Comparison of the wound—activated transformation of caulerpenyne by invasive and noninvasive Caulerpa species of the Mediterranean. J. Chem. Ecol. 28:2091–2105.

    Article  PubMed  CAS  Google Scholar 

  • Kamenarska, Z., Stefanov, K., Dimitrova-Konaklieva, S., Najdenski, H., Tsvetkova, I., and Popov, S. 2004. Chemical composition and biological activity of the brackish-water green alga Cladophora rivularis (L.) Hoek. Bot. Mar. 47:215–221.

    Article  CAS  Google Scholar 

  • Lemee, R., Pesando, D., Durand-Clement, M., Dubreuil, A., Meinesz, A., Guerriero, A., and Pietra, F. 1993. Preliminary survey of toxicity of the green alga Caulerpa taxifolia introduced into the Mediterranean. J. Appl. Phycol. 5:485–493.

    Article  CAS  Google Scholar 

  • Lemee, R., Boudouresque, C. F., Gobert, J., Malestroit, P., Mari, X., Meinesz, A., Menager, V., and Ruitton, S. 1996. Feeding behavior of Paracentrotus lividus in the presence of Caulerpa taxifolia introduced in the Mediterranean Sea. Oceanol. Acta 19:245–253.

    Google Scholar 

  • Littler, M. M., Taylor, P. R., and Littler, D. S. 1983. Algal resistance to herbivory on a Caribbean barrier reef. Coral Reefs 2:111–118.

    Article  Google Scholar 

  • Lockwood, J. R. 1998. On the statistical analysis of multiple-choice feeding preference experiments. Oecologia 116:475–481.

    Article  Google Scholar 

  • Lowe, E. F. 1974. Absorption efficiencies, feeding rates and food preference of Lytechinus variegatus (Echinodermata: Echinoidea) for selected marine plants. MS thesis. University of South Florida, Tampa, FL.

  • McConnell, O. J., Hughes, P. A., Targett, N. M., and Daley, J. 1982. Effects of secondary metabolites from marine algae on feeding by the sea urchin, Lytechinus variegatus. J. Chem. Ecol. 8:1437–1453.

    Article  CAS  Google Scholar 

  • Meinesz, A., De Vaugelas, J., Hesse, B., and Mari, X. 1993. Spread of the introduced tropical green alga Caulerpa taxifolia in northern Mediterranean waters. J. Appl. Phycol. 5:141–147.

    Article  Google Scholar 

  • Meinesz, A., Belsher, T., Thibaut, T., Antolic, B., Ben Mustapha, K., Boudouresque, C. F., Chiaverini, D., Cinelli, F., Cottalorda, J. M., Djellouli, A., El Abed, A., Orestano, C., Grau, A. M., Ivesa, L., Jaklin, A., Langar, H., Massuti-Pascual, E., Peirano, A., Tunesi, L., De Vaugelas, J., Zavodnik, N., and Zuljevic, A. 2001. The introduced alga Caulerpa taxifolia continues to spread in the Mediterranean. Biol. Invasions 3:201–210.

    Article  Google Scholar 

  • Meyer, K. D., Paul, V. J., Sanger, H. R., and Nelson, S. G. 1994. Effects of seaweed extracts and secondary metabolites on feeding by the herbivorous surgeonfish Naso lituratus. Coral Reefs 13:105–112.

    Article  Google Scholar 

  • Nelson, T. A., Lee, D. J., and Smith, B. C. 2003. Are “green tides” harmful algal blooms? Toxic properties of water-soluble extracts from two bloom-forming macroalgae, Ulva fenestrata and Ulvaria obscura (Ulvophyceae). J. Phycol. 39:874–879.

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Paul, V. J. and Hay, M. E. 1986. Seaweed susceptibility to herbivory: Chemical and morphological correlates. Mar. Ecol. Prog. Ser. 33:255–264.

    Article  CAS  Google Scholar 

  • Paul, V. J. and Van Alstyne, K. L. 1992. Activation of chemical defenses in the tropical green algae Halimeda spp. J. Exp. Mar. Biol. Ecol. 160:191–203.

    Article  CAS  Google Scholar 

  • Paul, V. J., Littler, M. M., Littler, D. S., and Fenical, W. 1987. Evidence for chemical defense in tropical green alga Caulerpa ashmeadii (Caulerpaceae: Chlorophyta): Isolation of new bioactive sesquiterpenoids. J. Chem. Ecol. 13:1171–1185.

    Article  CAS  Google Scholar 

  • Paul, V. J., Nelson, S. G., and Sanger, H. R. 1990. Feeding preferences of adult and juvenile rabbitfish Siganus argenteus in relation to chemical defenses of tropical seaweeds. Mar. Ecol. Prog. Ser. 60:23–34.

    Article  CAS  Google Scholar 

  • Paul, V. J., Meyer, K. D., Nelson, S. G., and Sanger, H. R. 1992. Deterrent effects of seaweed extracts and secondary metabolites on feeding by the rabbitfish Siganus spinus. Proc. 7th Int. Coral Reef Symp., Guam 2:867–874.

    Google Scholar 

  • Paul, V. J., Cruz-Rivera, E., and Thacker, R. W. 2001. Chemical mediation of macroalgal-herbivore interactions: Ecological and evolutionary perspectives, pp. 227–266, in J. B. McClintock and B. J. Baker (eds.). Marine Chemical Ecology. CRC Press, Boca Raton, FL.

    Google Scholar 

  • Pawlik, J. R., McFall, G., and Zea, S. 2002. Does the odor from sponges of the genus Ircinia protect them from fish predators? J. Chem. Ecol. 28:1103–1115.

    Article  PubMed  CAS  Google Scholar 

  • Pedrotti, M. L., Marchi, B., and Lemee, R. 1996. Effects of Caulerpa taxifolia secondary metabolites on the embryogenesis, larval development and metamorphosis of the sea urchin Paracentrotus lividus. Oceanol. Acta 19:255–262.

    CAS  Google Scholar 

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

    Article  Google Scholar 

  • Sousa, W. P. 1979. Experimental investigations of disturbance and ecological succession in a rocky intertidal algal community. Ecol. Monogr. 49:227–254.

    Article  Google Scholar 

  • Targett, N. M., Targett, T. E., Vrolijk, N. H., and Ogden, J. C. 1986. The effects of macrophyte secondary metabolites on feeding preferences of the herbivorous parrotfish Sparisoma radians. Mar. Biol. 92:141–148.

    Article  CAS  Google Scholar 

  • Vadas, R. L., Fenchel, T., and Ogden, J. C. 1982. Ecological studies on the sea urchin, Lytechinus variegatus, and the algal-seagrass communities of the Miskito Cays, Nicaragua. Aquat. Bot. 14:109–125.

    Article  Google Scholar 

  • Valiela, I., McClennand, J., Hauxwell, J., Behr, P. J., Hersh, D., and Foreman, K. 1997. Macroalgal blooms in shallow estuaries: Controls and ecophysiological and ecosystem consequences. Limnol. Oceanogr. 42:1105–1118.

    Article  Google Scholar 

  • Van Alstyne, K. L. and Houser, L. T. 2003. Dimethylsulfide release during macroinvertebrate grazing and its role as an activated chemical defense. Mar. Ecol. Prog. Ser. 250:175–181.

    Article  Google Scholar 

  • Van Alstyne, K. L., Wolfe, G. V., Freidenburg, T. L., Neill, A., and Hicken, C. 2001. Activated defense systems in marine macroalgae: Evidence for an ecological role for DMSP cleavage. Mar. Ecol. Prog. Ser. 213:53–65.

    Article  Google Scholar 

  • Wright, J. T., Dworjanyn, S. A., Rogers, C. N., Steinberg, P. D., Williamson, J. E., and Poore, A. G. B. 2005. Density-dependent sea urchin grazing: Differential removal of species, changes in community composition and alternative community states. Mar. Ecol. Prog. Ser. 298:143–156.

    Article  Google Scholar 

  • Wylie, C. R. and Paul, V. J. 1988. Feeding preferences of the surgeonfish Zebrasoma flavescens in relation to chemical defenses of tropical algae. Mar. Ecol. Prog. Ser. 45:23–32.

    Article  CAS  Google Scholar 

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Acknowledgments

We thank S. Reed and P. Monahan for their assistance with collection of sea urchins and algae. We are also grateful to D. Hanisak for providing G. tikvahiae for artificial feeding assays. In addition, W. Lee, J. Piraino, M. Puglisi, and R. Ritson-Williams provided significant assistance in the laboratory. Finally, commentary from anonymous reviewers and G. Cronin was appreciated. Grants funding this project were awarded to V.J.P. from the Smithsonian Marine Science Network (SMS contribution no. 645) and the Florida Center of Excellence for Biomedical and Marine Biotechnology (COE contribution no. P200608), and to K.L.V. from the National Science Foundation (IBN-0090825).

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Authors and Affiliations

  1. Smithsonian Marine Station, 701 Seaway Drive, Fort Pierce, FL, 34949, USA

    Amy A. Erickson, Valerie J. Paul & Lisa M. Kwiatkowski

  2. Shannon Point Marine Center, 1900 Shannon Point Road, Anacortes, WA, 98221, USA

    Kathryn L. Van Alstyne

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  1. Amy A. Erickson
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  2. Valerie J. Paul
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Correspondence to Amy A. Erickson.

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Erickson, A.A., Paul, V.J., Van Alstyne, K.L. et al. Palatability of Macroalgae that Use Different Types of Chemical Defenses. J Chem Ecol 32, 1883–1895 (2006). https://doi.org/10.1007/s10886-006-9116-x

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  • DOI: https://doi.org/10.1007/s10886-006-9116-x

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