Marine Biology

, Volume 109, Issue 2, pp 335–343

Lack of avoidance of phenolic-rich brown algae by tropical herbivorous fishes

  • P. D. Steinberg
  • K. Edyvane
  • R. de Nys
  • R. Birdsey
  • I. A. van Altena
Article

Abstract

High levels of polyphloroglucinol phenolics in marine brown algae are usually interpreted as a defensive response to herbivory. However, tropical brown algae generally contain very low levels of phenolics, even though herbivory in many tropical systems (e.g. coral reefs) is intense. This apparent paradox would be explained if polyphenolics did not deter tropical herbivores, in which case selection by herbivores for high levels of phenolics in tropical algae would be weak. To examine this hypothesis, in February 1989 we presented mixed assemblages of herbivorous fishes on the Great Barrier Reef with tropical, phenolic-poor brown algae (primarilySargassum spp.) and closely related (conspecifics in one instance) phenolic-rich temperate species. Different species of brown algae were eaten at very different rates, but these differences were not correlated with variation in the phenolic levels among the plants. TLC and NMR analyses showed no evidence of other, non-polar, metabolites in these algae, with the exception of the temperate speciesHomoeostrichus sinclairii. Thus, variation in non-polar metabolites also did not explain the differences in susceptibility to herbivores among these algae. We conclude that the herbivorous fishes studied here were not deterred by phenolic-rich algae, which suggests that levels of phenolics in many tropical algae may generally be low due to their ineffectiveness as defences. However, alternative explanations for the pattern are possible, and these are discussed.

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Literature cited

  1. Bakus, G. J., Green, G. (1974). Toxicity in sponges and holothurians: a geographic pattern. Science, N.Y. 185: 951–952Google Scholar
  2. Bakus, G. J., Targett, N. M., Schulte, B. (1986). Chemical ecology of marine organisms: an overview. J. chem. Ecol. 12: 951–985Google Scholar
  3. Bernays, E. A., Cooper-Driver G., Bilgener, M. (1989). Herbivores and plant tannins. Adv. ecol. Res. 19: 263–302Google Scholar
  4. Brock, R. E. (1982). A critique of the visual census method for assessing coral reef populations. Bull. mar. Sci. 32: 269–276Google Scholar
  5. Bryant, J., Chapin, III, F. S., Klein, D. R. (1983). Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40: 357–368Google Scholar
  6. Carpenter, R. (1986). Partitioning herbivory and its effects on coral reef algal communities. Ecol. Monogr. 56: 345–363Google Scholar
  7. Coley, P. D., Bryant, J. P., Chapin, F. S. (1985). Resource availability and plant antiherbivore defense. Science, N. Y. 230: 895–899Google Scholar
  8. Coll, J. C., Bowden, B. F. (1986). The application of vacuum liquid chromatography to the separation of terpene mixtures. J. nat. Products (Lloydia) 49: 934–936Google Scholar
  9. Day, R. W., Quinn, G. P. (1989). Comparisons of treatments after an analysis of variance in ecology. Ecol. Monogr. 59: 433–463Google Scholar
  10. Denton, G. R. W., Burdon-Jones, C. (1986). Trace metals in waters of the Great Barrier Reef. Mar. Pollut. Bull. 17: 95–98Google Scholar
  11. Estes, J. A., Steinberg, P. D. (1988). Predation, herbivory and kelp evolution. Paleobiology 14: 19–36Google Scholar
  12. Faulkner, D. J. (1984). Marine natural products: metabolites of marine algae and herbivorous marine mollusks. Nat. Product. Rep. 1: 251–280Google Scholar
  13. Faulkner, D. J. (1986). Marine natural products. Nat. Product. Rep. 3: 1–33Google Scholar
  14. Fenical, W. (1980). Distributional and taxonomic features of toxinproducing marine algae. In: Abbott, I. A., Foster, M. S., Eklund, L. F. (eds.) Pacific seaweed aquaculture. California Sea Grant College Program, Institute of Marine Resources, University of California, La Jolla, California, USA, p. 144–151Google Scholar
  15. Fowler, A. J. (1987). The development of sampling strategies for population studies of coral reef fishes. A case study. Coral Reefs 6: 49–58Google Scholar
  16. Gaines, S. D., Lubchenco, J. (1982). A unified approach to marine plant-herbivore interactions. II. Biogeography. A. Rev. Ecol. Syst. 13: 111–138Google Scholar
  17. Geiselman, J. A., McConnell, O. J. (1981). Polyphenols in the brown algaeFucus vesiculosus andAscophyllum nodosum: chemical defenses against the herbivorous snailLittorina littorea. J. chem. Ecol. 7: 1115–1133Google Scholar
  18. Green, G. (1977). Ecology of toxicity in marine sponges. Mar. Biol. 40: 207–215Google Scholar
  19. Hatcher, B. G., Larkum, A. W. D. (1983). An experimental analysis of factors controlling the standing crop of the epilithic algal community on a coral reef. J. exp. mar. Biol. Ecol. 69: 61–84Google Scholar
  20. Hay, M. E. (1981). The functional morphology of turf-forming seaweeds: persistence in stressful marine habitats. Ecology 62: 739–750Google Scholar
  21. Hay, M. E. (1984). Predictable spatial escapes from herbivory: how do these affect the evolution of herbivore resistance in tropical marine communities? Oecologia 64: 396–407Google Scholar
  22. Hay, M. E. (1985). Spatial patterns of herbivore impact and their importance in maintaining algal species richness. Proc. 5th int. coral Reef Congr. 4: 29–34. [Gabrié, C. et al. (eds.) Antenne Museum-EPHE, Moorea, French Polynesia]Google Scholar
  23. Hay, M. E., Duffy, J. E., Fenical, W., Gustafason, K. (1988). Chemical defense in the seaweedDictyopteris delicatula: differential effects against reef fishes and amphipods. Mar. Ecol. Prog. Ser. 48: 185–192Google Scholar
  24. Hay, M. E., Fenical, W. (1988). Marine plant-herbivore interactions: the ecology of chemical defense. A. Rev. Syst. Ecol. 19: 111–145Google Scholar
  25. Hay, M. E., Fenical, W., Gustafason, K. (1987). Chemical defense against diverse coral-reef herbivores. Ecology 68: 1581–1592Google Scholar
  26. Horn, M. H. (1989). Biology of marine herbivorous fishes. Oceanogr. mar. Biol. A. Rev. 27: 167–272Google Scholar
  27. Ilvessalo, H., Tuomi, J. (1989). Nutrient availability and accumulation of phenolic compounds in the brown algaFucus vesiculosus. Mar. Biol. 101: 115–119Google Scholar
  28. Johnson, C. R., Mann, K. H. (1986). The importance of plant defense abilities to the structure of seaweed comunities: the kelpLaminaria longicruris de la Pylaie survives grazing by the snailLacuna vincta (Montagu) at high population densities. J. exp. mar. Biol. Ecol. 97: 231–267Google Scholar
  29. Kato, T., Kumanireng, A. S., Ichinose, I., Kitihara, Y., Kakinada, Y., Kato, Y. (1975). Structure and synthesis of active component from a marine alga,Sargassum tortile, which inhibits the settling of swimming larvae ofCoryne uchidai. Chemy Lett. (Chem. Soc. Japan, Tokyo) 1975: 335–338Google Scholar
  30. Lewis, S. M., Norris, J. N., Searles, R. B. (1987). The regulation of morphological plasticity by herbivory. Ecology 68: 636–641Google Scholar
  31. Littler, M. M., Taylor, P. R., Littler, D. S. (1983). Algal resistance to herbivory on a Caribbean barrier reef. Coral Reefs 5: 63–71Google Scholar
  32. Mayer, A. M., Harel, E. (1979). Polyphenol oxidases in plants. Phytochem. 18: 193–215Google Scholar
  33. McClure, J. W. (1978). The physiology of phenolic compounds in plants. Recent Adv. Phytochem. 12: 525–556Google Scholar
  34. Padilla, D. K. (1985). Structural resistance of algae to herbivores. A biomechanical approach. Mar. Biol. 90: 103–109Google Scholar
  35. Paul, V. J., Fenical, W. (1987). Natural products chemistry and chemical defense in tropical marine algae of the phylum Chlorophyta. In: Scheuer, P. S. (ed.) Bioorganic marine chemistry. Springer-Verlag, Heidelberg, p. 1–29Google Scholar
  36. Paul, V. J., Hay, M. E. (1986). Seaweed susceptibility to herbivory: chemical and morphological correlates. Mar. Ecol. Prog. Ser. 33: 255–264Google Scholar
  37. Ragan, M. A., Glombitza, K.-W. (1986). Phlorotannins, brown algal polyphenols. Prog. phycol. Res. 4: 129–241Google Scholar
  38. Ragan, M. A., Jensen, A. (1977). Quantitative studies on brown algal polyphenols. I. Estimation of absolute polyphenol-content ofAscophyllum nodosum (L.) andFucus vesiculosus (L.) J. exp. mar. Biol. Ecol. 34: 245–258Google Scholar
  39. Renaud, P. E., Hay, M. E., Schmitt, T. (1990). Interactions of plant stress and herbivory: interspecific variation in the susceptibility of a palatable vs an unpalatable seaweed to sea urchin grazing. Oecologia 82: 217–226Google Scholar
  40. Rhoades, D. (1979). Evolution of plant defenses against herbivory. In: Rosenthal, G. A., Janzen, D. H. (eds.) Herbivores. Academic Press, New YorkGoogle Scholar
  41. Russ, G. (1984). Distribution and abundance of herbivorous grazing fishes in the central Great Barrier Reef. I. Levels of variability across the entire continental shelf. Mar. Ecol. Prog. Ser. 20: 23–34Google Scholar
  42. Scott, F., Russ, G. (1987). Effects of grazing on species composition of the epilithic algal community on coral reefs of the Central Great Barrier Reef. Mar. Ecol. Prog. Ser. 39: 293–304Google Scholar
  43. Shizuru, Y., Matsukawa, S., Ojika, M., Yamada, K. (1982). Two new farnesylacetone derivatives from the brown algaSargassum micracanthum. Phytochem. 21: 1808–1809Google Scholar
  44. Steinberg, P. D. (1985). Feeding preferences ofTegula funebralis and chemical defenses in marine brown algae. Ecol. Monogr. 55: 333–349Google Scholar
  45. Steinberg, P. D. (1986). Chemical defenses and the susceptibility of tropical marine algae to herbivores. Oecologia 69: 628–630Google Scholar
  46. Steinberg, P. D. (1988). The effects of quantitative and qualitative variation in phenolic compounds on feeding in three species of marine invertebrate herbivores. J. exp. mar. Biol. Ecol. 120: 221–237Google Scholar
  47. Steinberg, P. D. (1989). Biogeographical variation in brown algal polyphenolics and other secondary metabolites: comparison between temperate Australasia and North America. Oecologia 78: 373–382Google Scholar
  48. Steinberg, P. D., Paul, V. J. (1990). Fish feeding and chemical defenses of tropical brown algae in Western Australia. Mar. Ecol. Prog. Ser. 58: 253–259Google Scholar
  49. Steinberg, P. D., van Altena, I. A. (1991). Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecol. Monogr. (in press)Google Scholar
  50. Steneck, R. S. (1983). Escalating herbivory and resulting adaptive trends in calcareous algal crusts. Paleobiology 9: 44–61Google Scholar
  51. Steneck, R. S. (1986). The ecology of coralline algal crusts: convergent patterns and adaptive strategies. A. Rev. Ecol. Syst. 17: 273–303Google Scholar
  52. Swain, T., Hillis, W. E. (1959). The phenolic constituents ofPrunus domesticus. I. The quantitative analysis of phenolic constituents. J. Sci. Fd Agric. 10: 63–68Google Scholar
  53. Targett, N. M., Targett, T. E., Vrolijk, N. H., Ogden, J. C. (1986). Effect of macrophyte secondary metabolites on feeding preferences of the herbivorous parrotfishSparisoma radians. Mar. Biol. 92: 141–148Google Scholar
  54. Van Alstyne, K. L. (1988). Herbivore grazing increases polyphenolic defenses in the intertidal brown algaFucus distichus. Ecology 69: 655–663Google Scholar
  55. Van Alstyne, K. L., Paul, V. J. The biogeography of polyphenolic compounds in marine macroalgae: temperate brown algal defenses deter feeding by tropical herbivorous fishes. Oecologia (in press)Google Scholar
  56. Vermeij, G. J. (1978). Biogeography and adaptation. Harvard Press, Cambridge, Massachusetts, USAGoogle Scholar
  57. Womersley, H. B. S. (1987). The marine benthic flora of South Australia. Part II. South Australian Government Printing Division, Adelaide, Southern Australia, AustraliaGoogle Scholar
  58. Wylie, C. R., Paul, V. J. (1988). Feeding preferences of the surgeonfishZebrasoma flavascens in relation to chemical defenses of tropical algae. Mar. Ecol. Prog. Ser. 45: 23–32Google Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • P. D. Steinberg
    • 1
  • K. Edyvane
    • 2
  • R. de Nys
    • 3
  • R. Birdsey
    • 2
  • I. A. van Altena
    • 4
  1. 1.School of Biological SciencesUniversity of SydneySydneyAustralia
  2. 2.School of Biological SciencesJames Cook UniversityTownsvilleAustralia
  3. 3.Department of Chemistry and BiochemistryJames Cook UniversityTownsvilleAustralia
  4. 4.Department of Organic ChemistryUniversity of AdelaideAdelaideAustralia
  5. 5.School of Biological SciencesUniversity of New South WalesKensingtonAustralia

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