Hydrobiologia

, 553:319 | Cite as

Chemical Deterrence of a Marine Cyanobacterium against Sympatric and Non-sympatric Consumers

  • Angela Capper
  • Edwin Cruz-Rivera
  • Valerie J. Paul
  • Ian R. Tibbetts
Primary Research Paper

Abstract

This study investigates the influence of mesograzer prior exposure to toxic metabolites on palatability of the marine cyanobacterium, Lyngbya majuscula. We examined the palatability of L. majuscula crude extract obtained from a bloom in Moreton Bay, South East Queensland, Australia, containing lyngbyatoxin-a (LTA) and debromoaplysiatoxin (DAT), to two groups: (1) mesograzers of L. majuscula from Guam where LTA and DAT production is rare; and (2) macro- and mesograzers found feeding on L. majuscula blooms in Moreton Bay where LTA and DAT are often prevalent secondary metabolites. Pair-wise feeding assays using artificial diets consisting of Ulvaclathrata suspended in agar (control) or coated with Moreton Bay L. majuscula crude extracts (treatment) were used to determine palatability to a variety of consumers. In Guam, the amphipods, Parhyale hawaiensis and Cymadusa imbroglio; the majid crab Menaethius monoceros; and the urchin Echinometra mathaei were significantly deterred by the Moreton Bay crude extract. The sea hares, Stylocheilus striatus, from Guam were stimulated to feed by treatment food whereas S. striatus collected from Moreton Bay showed no discrimination between food types. In Moreton Bay, the cephalaspidean Diniatys dentifer and wild caught rabbitfish Siganus fuscescens were significantly deterred by the crude extract. However, captive-bred S. fuscescens with no known experience with L.majuscula did not clearly discriminate between food choices. Lyngbyamajuscula crude extract deters feeding by most mesograzers regardless of prior contact or association with blooms.

Keywords

Lyngbya majuscula feeding deterrence lyngbyatoxin-a debromoaplysiatoxin rabbitfish (Siganus fuscescenssea hare (Stylocheilus striatus

References

  1. Avila, C. 1995Natural products of opisthobranch molluscs: A biological reviewOceanography and Marine Biology: Annual Review33487559Google Scholar
  2. Bryan, P. G. 1975Food habits, functional digestive morphology, and assimilation efficiency of the rabbitfish Signaus spinus (Pisces, Siganidae) on GuamPacific Science29269277Google Scholar
  3. Burja, A. M., Banaigs, B., Abou-Mansour, E., Burgess, J. G., Wright, P. C. 2001Marine cyanobacteria- a prolific source of natural productsTetrahedron5793479377CrossRefGoogle Scholar
  4. Capper, A., Tibbetts, I. R., O’Neil, J. M., Shaw, G. R. 2005 The fate of Lyngbya majuscula toxins in three potential consumersJournal of Chemical Ecology3115951606CrossRefPubMedGoogle Scholar
  5. Cruz-Rivera E. & V. J. Paul, 2002. Coral reef benthic cyanobacteria as food and refuge: Diversity, chemistry and complex interactions. Proceedings of 9th International Coral Reef Symposium, Bali, Indonesia, pp. 515–520.Google Scholar
  6. Dennison, W. C., O’Neil, J. M., Duffy, E. J., Oliver, P. E., Shaw, G. R. 1999Blooms of the cyanobacterium Lyngbya majuscula in coastal waters of Queensland, AustraliaBulletin de l’Institut Oceanographique Monaco, Special19501506Google Scholar
  7. Freeland, W. J., Janzen, D. H. 1974Strategies in herbivory by mammals: the role of plant secondary compoundsAmerican Naturalist108269289Google Scholar
  8. Gallimore, W. A., Galario, D. L., Lacy, C., Zhu, Y., Scheuer, P. J. 2000Two complex proline esters from the sea hare Stylocheilus longicaudaJournal of Natural Products6310221026PubMedGoogle Scholar
  9. Gerwick, W. H., Tan, T., Sitachitta, N. 2001

    Nitrogen-containing metabolites from marine cyanobacteria

    Cordell, G. A. eds. The Alkaloids: Chemistry and BiologyAcademic PressNY75184
    Google Scholar
  10. Hashimoto, Y., Konosu, S., Yasumoto, T., Kamiya, H. 1969Ciguatera in the Ryukyu and Amami IslandsBulletin of Japanese Society of Fisheries Science35316326Google Scholar
  11. Hay, M. E., Stachowicz, J. J., Cruz-Rivera, E., Bullard, S., Deal, M. S., Lindquist, N. 1998

    Bioassays with marine and freshwater organisms

    Haynes, K. F.Millar, J. R. eds. Methods in Chemical Ecology, BioassaysChapman and HallNew York39141
    Google Scholar
  12. Hayden, H. S., Blomster, J. A., Maggs, C. A., Silva, P. C., Stanthorpe, M. J., Waland, J. R. 2003Linnaeus was right all along: Ulva and Enteromorpha are not distinct generaEuropean Journal of Phycology38277294CrossRefGoogle Scholar
  13. Ito, E., Satake, M., Yasumoto, T. 2002Pathological effects of lyngbyatoxin A upon miceToxicon40551556PubMedGoogle Scholar
  14. Kato, Y., Scheuer, P. J. 1975The aplysiatoxinsPure and Applied Chemistry41114Google Scholar
  15. Lindquist, N., Hay, M. E. 1995Can small rare prey be chemically defended? The case for marine larvaeEcology7613471358Google Scholar
  16. Lockwood, J. R. 1998On the statistical analysis of multiple-choice feeding preference experimentsOecologia116475481Google Scholar
  17. Lundberg, B., Lipkin, Y. 1979Natural food of the herbivorous rabbitfish (Siganus spp) in Northern Red SeaBotanica Marina22173181CrossRefGoogle Scholar
  18. Nagle, D. G., Paul, V. J. 1998Chemical defense of a marine cyanobacterial bloomJournal of Experimental Marine Biology and Ecology2252938CrossRefGoogle Scholar
  19. Nagle, D. G., Paul, V. J. 1999Production of secondary metabolites by filamentous tropical marine cyanobacteria: Ecological functions of the compoundsJournal of Phycology3514121421Google Scholar
  20. Nagle, D. G., Paul, V. J., Roberts, M. A. 1996Ypaoamide, a new broadly acting feeding deterrent from the marine cyanobacteria Lyngbya majusculaTetrahedron Letters3762636266CrossRefGoogle Scholar
  21. Nagle, D. G., Camacho, F. T., Paul, V. J. 1998Dietary preferences of the opisthobranch mollusc Stylocheilus longicauda for secondary metabolites produced by the tropical cyanobacterium Lyngbya majusculaMarine Biology132267273CrossRefGoogle Scholar
  22. Osborne, N. J. W., Webb, P. M., Shaw, G. R. 2001The toxins of Lyngbya majuscula and their human and ecological health effectsEnvironment International27381392CrossRefPubMedGoogle Scholar
  23. Paul, V. J., Pennings, S. C. 1991Diet-derived chemical defenses in the sea hare Stylocheilus longicauda (Quoy et Gaimard 1824)Journal of Experimental Marine Biology and Ecology151227243CrossRefGoogle Scholar
  24. Paul, V. J., Nelson, S. G., Sanger, H. R. 1990Feeding preference of adult and juvenile rabbitfish Siganus argenteus in relation to chemical defenses of tropical seaweedsMarine Ecology Progress Series602334Google Scholar
  25. Pennings, S. C., Paul, V. J. 1993aSecondary chemistry does not limit dietary range of the specialist sea hare Stylocheilus longicauda (Quoy et Gaimard 1824)Journal of Experimental Marine Biology and Ecology17497113CrossRefGoogle Scholar
  26. Pennings, S. C., Paul, V. J. 1993bSequestration of dietary secondary metabolites by three species of sea hares: Location, specificity and dynamicsMarine Biology117535546CrossRefGoogle Scholar
  27. Pennings, S. C., Carefoot, T. H. 1995Post-ingestive consequences of consuming secondary metabolites in sea hares (Gastropoda: Opisthobranchia)Comparative Biochemistry and Physiology111249256Google Scholar
  28. Pennings, S. C., Weiss, A. M., Paul, V. J. 1996Secondary metabolites of the cyanobacterium Microcoleus lyngbyaceus and the sea hare Stylocheilus longicauda: Palatability and toxicityMarine Biology126735743CrossRefGoogle Scholar
  29. Rudman, W. B., 1999. Stylocheilus longicauda and Stylocheilus citrina Nomenclature discussion. [In] Sea Slug Forum http://www.seaslugforum.net/factsheet.cfm?base=stylnome date accessed 23 May 2005.Google Scholar
  30. Sims, J. K., Zandee Rilland, R. D. 1981Escharotic stomatitis caused by the ‘stinging seaweed’ Microcoleus lyngbyaceus (formerly Lyngbya majuscula)Hawaii Medical Journal40243248PubMedGoogle Scholar
  31. Thacker, R. W., Paul, V. J. 2001Are benthic cyanobacteria indicators of nutrient enrichment? Relationships between cyanobacterial abundance and environmental factors on the reef flats of GuamBulletin of Marine Science69497508Google Scholar
  32. Thacker, R. W., Nagle, D. G., Paul, V. J. 1997Effects of repeated exposures to marine cyanobacterial secondary metabolites on feeding by juvenile rabbitfish and parrotfishMarine Ecology Progress Series1472129Google Scholar
  33. Thacker, R. W., Ginsburg, D. W., Paul, V. J. 2001Effects of herbivore exclusion and nutrient enrichment on coral reef macroalgae and cyanobacteriaCoral Reefs193183331Google Scholar
  34. Westerhagen, H. 1973The natural food of rabbitfish Siganus oramin and S striolataMarine Biology22367370Google Scholar
  35. Yasumoto, T. 1998Fish poisoning due to toxins of microalgal origins in the PacificToxicon3615151518CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Angela Capper
    • 1
    • 2
  • Edwin Cruz-Rivera
    • 3
  • Valerie J. Paul
    • 2
  • Ian R. Tibbetts
    • 1
  1. 1.Centre for Marine Studies, School of Life SciencesThe University of QueenslandSt. LuciaAustralia
  2. 2.Smithsonian Marine Station at Fort PierceFort PierceUSA
  3. 3.Marine Sciences InstituteUniversity of Texas at AustinPort AransasUSA

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