Effects of secondary metabolites on digestion in marine herbivores

Marine Chemical Ecology

Volumn , Issue , 2001, Pages 391-412

  Targett, Nancy M ^a   Arnold, Thomas M ^b  

^a UNIVERSITY OF DELAWARE   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85055364288     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1201/9781420036602     Document Type: Chapter

References (206)

1. Faulkner, D.J., Marine natural products, Nat. Prod. Rep., 16, 155, 1999.
2. Pawlik, J.R., Chemical ecology of the settlement of benthic marine invertebrates, in Oceanogr. Mar. Biol. Ann. Rev., 30, 273, 1992.
3. Maier, I., Gamete orientation and induction of gametogenesis by pheromones in algae and plants, Plant Cell Environ., 16, 891, 1993.
4. Maier, I., Brown algal pheromones, Prog. Phycol. Res., 11, 51, 1995.
5. Forward, R.B., Jr., Frankel, D.A.Z., and Rittschof, D., Molting of megalopae from the blue crab Callinectes sapidus: effects of offshore and estuarine cues, Mar. Ecol. Prog. Ser., 113, 55, 1994.
6. Boland, W., The chemistry of gamete attraction: chemical structures, biosynthesis, and (a)biotic degradation of algal pheromones, Proc. Natl. Acad. Sci. U.S.A., 92, 37, 1995.
7. Coll, J.C., Bowden, B.F., Meehan, G.V., Konig, G.M., Carroll, A.R., Tapiolas, D.M., Alino, P.M., Heaton, A., and de Nys, R., Chemical aspects of mass spawning in corals. 1. Sperm-attractant molecules in the eggs of the scleractinian coral Montipora digitata, Mar. Biol., 118, 177, 1994.
8. Coll, J.C., Leone, P.A., Bowden, B.F., Carroll, A.R., Koenig, G.M., Heaton, A., de Nys, R., Maida, M., Alino, P.M., Willis, R.H., Babcock, R.C., Florian, Z., Clayton, M.N., Miller, R.L., and Alderslade, P.N., Chemical aspects of mass spawning in corals. 2. (-)-Epi-thunbergol, the sperm attractant in the eggs of the soft coral Lobophytum crassum (Cnidaria: Octocorallia), Mar. Biol., 123, 137, 1995.
9. Morse, A.N.C. and Morse, D.E., Flypapers for coral and other planktonic larvae, Bioscience, 46, 254, 1996.
10. Clare, A.S., Eicosanoids and egg-hatching synchrony in barnacles: evidence against a dietary precursor to egg-hatching pheromone, J. Chem. Ecol., 23, 2299, 1997.
11. Welch, J.M., Rittschof, D., Bullock, T.M., and Forward, R.B., Jr., Effects of chemical cues on settlement behavior of blue crab Calllinectes sapidus postlarvae, Mar. Ecol. Prog. Ser., 154, 143, 1997.
12. Hay, M.E. and Fenical, W., Marine plant-herbivore interactions: the ecology of chemical defense, Annu. Rev. Ecol. Syst., 19, 111, 1988.
13. Hay, M.E. and Fenical, W., Chemical mediation of seaweed-herbivore interactions, in Plant-Animal Interactions in the Marine Benthos, John, D.M., Hawkins, S.J., and Price, J.H., Eds., Clarendon Press, Oxford, UK, 1992, 319.
14. Duffy, J.E. and Hay, M.E., Seaweed adaptations to herbivory, Bioscience, 40, 368, 1990.
15. Hay, M.E., Fish seaweed interactions of coral reefs: effects of herbivorous fishes and adaptations of their prey, in The Ecology of Fishes on Coral Reefs, Sale, P.F., Ed., Academic Press, San Diego, CA, 1991, 96.
16. Hay, M.E., Marine chemical ecology: what’s known and what’s next?, J. Exp. Mar. Biol. Ecol., 200, 103, 1996.
17. Coll, J.C., The chemistry and chemical ecology of octocorals (Coelenterata, Anthozoa, Octocorallia), Chem. Rev., 92, 613, 1992.
18. Hay, M.E. and Steinberg, P.D., The chemical ecology of plant-herbivore interactions, in Herbivores their Interaction with Secondary Plant Metabolites: Evolutionary and Ecological Processes, Vol. 2, 2nd ed., Rosenthal, G.A. and Berenbaum, M., Eds., Academic Press, New York, 1992, 371.
19. Paul, V.J., Ecological Roles of Marine Natural Products, Comstock Publishing Associates, Cornell University Press, Ithaca, NY, 1992.
20. Lindquist, N., Hay, M.E., and Fenical, W., Defense of ascidians and their conspicuous larvae: adult vs. larval chemical defenses, Ecol. Monogr., 62, 547, 1992.
21. Proksch, P., Defensive roles for secondary metabolites from marine sponges and sponge-feeding nudibranchs, Toxicon, 32, 639, 1994.
22. Pawlik, J.R., Charnas, B., Toonen, R.J., and Fenical, W., Defenses of Caribbean sponges against predatory reef fish. 1. Chemical deterrency, Mar. Ecol. Prog. Ser., 127, 183, 1995.
23. McClintock, J.B. and Baker, B.J., A review of the chemical ecology of Antarctic marine invertebrates, Am. Zool., 37, 329, 1997.
24. Hay, M.E., Piel, J., Boland, W., and Schnitzler, I., Seaweed sex pheromones and their degradation products frequently suppress amphipod feeding but rarely suppress sea urchin feeding, Chemoecology, 8, 91, 1998.
25. Targett, N.M. and Arnold, T.M., Predicting the effects of brown algal phlorotannins on marine herbivores in tropical and temperate oceans, J. Phycol., 34, 195, 1998.
26. Nolen, T.G., Johnson, P.M., Kicklighter, C.K., and Capo, T., Ink secretion by the marine snail Aplysia californica enhances its ability to escape from a natural predator, J. Comp. Physiol., A176, 239, 1995.
27. Pavia, H., Cervin, G., Lindgren, A., and Åberg, P., Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum, Mar. Ecol. Prog. Ser., 157, 139, 1997.
28. Adler, F.R. and Morris, W.F., A general test for interaction modification, Ecology, 75, 1552, 1994.
29. Billick, I. and Case, T.J., Higher order interactions in ecological communities: what are they and how can they be detected?, Ecology, 75, 1529, 1994.
30. Kareiva, P., Higher order interactions as a foil to reductionist ecology, Ecology, 75, 1527, 1994.
31. Wootton, J.T., Putting the pieces together: testing the independence of interactions among organisms, Ecology, 75, 1544, 1994.
32. Cronin, G. and Hay, M.E., Susceptibility to herbivores depends on recent history of both the plant and animal, Ecology, 77, 1531, 1996.
33. Choat, J.H. and Clements, K.D., Vertebrate herbivores in marine and terrestrial environments: a nutritional ecology perspective, Annu. Rev. Ecol. Syst., 29, 375, 1998.
34. Boettcher, A.A. and Targett, N.M., Role of polyphenolic molecular size in reduction of assimilation efficiency in Xiphister mucosus, Ecology, 74, 891, 1993.
35. Targett, N.M., Boettcher, A.A., Targett, T.E., and Vrolijk, N.H., Tropical marine herbivore assimilation of phenolic-rich plants, Oecologia, 103, 170, 1995.
36. Duffy, J.E. and Paul, V.J., Prey nutritional quality and the effectiveness of chemical defenses against tropical reef fishes, Oecologia, 90, 333, 1992.
37. Hay, M.E., Kappel, Q.E., and Fenical, W., Synergisms in plant defenses against herbivores: interactions of chemistry, calcification, and plant quality, Ecology, 75, 1714, 1994.
38. Choat, J.H., The biology of herbivorous fishes on coral reefs, in The Ecology of Fishes on Coral Reefs, Sale, P.F., Ed., Academic Press, San Diego, CA, 1991, 120.
39. Horn, M.H. and Ojeda, F.P., Herbivory, in Intertidal Fishes, Horn, M.H., Martin, K.L.M., and Chotkowski, M.A., Eds., Academic Press, San Diego, CA, 1999, 399.
40. Jobling, M., Environmental Biology of Fishes, Chapman and Hall, London, 1995.
41. Bromley, P.J., The role of gastric evacuation experiments in quantifying the feeding rates of predatory fish, Rev. Fish Biol. Fisher., 4, 36, 1994.
42. Gerking, S.D., Feeding Ecology of Fish, Academic Press, San Diego, CA, 1994.
43. Lobel, P.S., Trophic biology of herbivorous reef fish: alimentary pH and digestive capabilities, J. Fish. Biol., 19, 365, 1981.
44. Horn, M.H., Biology of marine herbivorous fishes, Oceanogr. Mar. Biol. Annu. Rev., 27, 167, 1989.
45. Horn, M.H. and Messer, K.S., Fish guts as chemical reactors: a model of the alimentary canals of marine herbivorous fishes, Mar. Biol., 113, 527, 1992.
46. Kloareg, B. and Quatrano, R.S., Structure of the cell walls of marine algae and ecophysiological functions of the matrix polysaccharides, Oceanogr. Mar. Biol. Ann. Rev., 26, 259, 1988.
47. Pollak, P.E. and Montgomery, W.L., Giant bacterium (Epulopiscium fishelsoni) influences digestive enzyme activity of an herbivorous surgeonfish (Acanthurus nigrofuscus), Comp. Biochem. Physiol., 108A, 657, 1994.
48. Ojeda, F.P. and Cáceres, C.W., Digestive mechanisms in Aplodactylus punctatus (Valenciennes): a temperate marine herbivorous fish, Mar. Ecol. Prog. Ser., 118, 37, 1995.
49. Clements, K.D. and Choat, J.H., Comparison of herbivory in the closely-related marine fish genera Girella and Kyphosus, Mar. Biol., 127, 579, 1997.
50. Rimmer, D.W. and Wiebe, W.J., Fermentative microbial digestion in herbivorous fishes, J. Fish Biol., 31, 229, 1987.
51. Clements, K.D., Fermentation and gastrointestinal microorganisms in fishes, in Gastrointestinal Microbiology, Vol. 1, Mackie, R.I. and White, B.A., Ed., Chapman and Hall, New York, 1997, 156.
52. Targett, T.E. and Targett, N.M., Energetics of food selection by the herbivorous parrotfish Sparisoma radians: roles of assimilation efficiency, gut evacuation rate, and algal secondary metabolites, Mar. Ecol. Prog. Ser., 66, 13, 1990.
53. Horn, M.H., Mailhiot, K.F., Fris, M.B., and McClanahan, L.L., Growth, consumption, assimilation and excretion in the marine herbivorous fish Cebidichthys violaceus (Girard) fed natural and high protein diets, J. Exp. Mar. Biol. Ecol., 190, 97, 1995.
54. Gerking, S.D., Assimilation and maintenance ration of an herbivorous fish, Sarpa salpa, feeding on a green alga, Trans. Am. Fish. Soc., 113, 378, 1984.
55. Anderson, T.A., Mechanisms of digestion in the marine herbivore, the luderick, Girella tricuspidata (Quoy and Gaimard), J. Fish Biol., 39, 535, 1991.
56. Sturm, E.A. and Horn, M.H., Food habits, gut morphology and pH, and assimilation efficiency of the zebraperch Hermosilla azurea, an herbivorous kyphosid fish of temperate marine waters, Mar. Biol., 132, 515, 1998.
57. Zemke-White, W.L., Clements, K.D., and Harris, P.J., Acid lysis of macroalgae by marine herbivorous fishes: myth or digestive mechanism?, J. Exp. Mar. Biol. Ecol., 233, 95, 1999.
58. Targett, N.M., unpublished data.
59. Fishelson, L., Montgomery, W.L., and Myrberg, A.A., Jr., A unique symbiosis in the gut of tropical herbivorous surgeonfish (Acanthuridae: Teleostei) from the Red Sea, Science, 229, 49, 1985.
60. Clements, K.D., Gleeson, V.P., and Slaytor, M., Short-chain fatty acid metabolism in temperate marine herbivorous fish, J. Comp. Physiol. B, 164, 372, 1994.
61. Rimmer, D.W., Changes in the diet and the development of microbial digestion in juvenile buffalo bream, Kyphosus cornelii, Mar. Biol., 92, 443, 1986.
62. Clements, K.D. and Choat, J.H., Fermentation in tropical marine herbivorous fishes, Physiol. Zool., 68, 355, 1995.
63. Barwell, C.J., Blunde, G., and Manandhar, P.D., Isolation and characterization of brown algal polyphenols as inhibitors of α-amylase, lipase and trypsin, J. Appl. Phycol., 1, 319, 1989.
64. Kandel, J.S., Horn, M.H., and Van Antwerp, W., Volatile fatty acids in the hindguts of herbivorous fishes from temperate and tropical marine waters, J. Fish Biol., 45, 527, 1994.
65. Stellwag, E.J., Smith, T.D., and Luczkovich, J.J., Characterization and ecology of carboxymethylcellulase- producing anaerobic bacterial communities associated with the intestinal tract of the pinfish, Lagodon rhomboides, Appl. Environ. Micro., 61, 813, 1995.
66. Stevens, C.E., Comparative Physiology of the Vertebrate Digestive System, Cambridge University Press, Cambridge, UK, 1988.
67. Seeto, G.S., Veivers, P.C., Clements, K.D., and Slaytor, M., Carbohydrate utilisation by microbial symbionts in the marine herbivorous fishes Odax cyanomelas and Crinodous lophodon, J. Comp. Physiol. B, 165, 571, 1996.
68. Purchon R.D., The Biology of the Mollusca, Pergamon Press, Oxford, UK, 1977.
69. Dall, W. and Moriarty, D.J.W., Functional aspects of nutrition and digestion, in The Biology of Crustacea, Vol. 5, Mantel, L.H., Ed., Academic Press, New York, 1983, 215.
70. Tugwell, S. and Branch, G.M., Effects of herbivore gut surfactants on kelp polyphenol defenses, Ecology, 73, 205, 1992.
71. Hammen, C.S., Marine Invertebrates: Comparative Physiology, Hammen, C.S., Ed., University Press of New England, Hanover, N.H., 1980.
72. Lawrence, J.M., Digestion, in Echinoderm Nutrition, Lawrence, J.M. and Jangoux, M., Eds., A.A. Balkema, Rotterdam, 1982.
73. Klinger, T.S., McClintock, J.B., and Watts, S.A., Activities of digestive enzymes of polar and subtropical echinoderms, Polar Biol., 18, 154, 1997.
74. Anderson, J.M., Aspects of nutritional physiology, in Physiology of Echinodermata, Boolootian, R.A., Ed., John Wiley & Sons, New York, 1966, 329.
75. de Ridder, C. and Jangoux, M., Digestive systems: Echinoidea, in Echinoderm Nutrition, Jangoux, M. and Lawrence, J.M., Eds., A.A. Balkema, Rotterdam, 1982, 213.
76. de Ridder, C. and Lawrence, J.M., Food and feeding mechanisms: Echinoidea, in Echinoderm Nutrition, Jangoux, M. and Lawrence, J.M., Eds., A.A. Balkema, Rotterdam, 1982, 57.
77. Lawrence, J.M., A Functional Biology of Echinoderms, Johns Hopkins University Press, Baltimore, MD, 1987.
78. Lawrence, J.M., On the relationships between marine plants and sea urchins, Oceanogr. Mar. Biol. Annu. Rev., 13, 213, 1975.
79. Klinger, T.S., Activities and kinetics of digestive- and β-glucosidase and β-galactosidase of five species of echinoids (Echinodermata), Comp. Biochem. Physiol., 78A, 597, 1984.
80. Binyon, J., Salinity tolerance and ionic regulation, in Physiology of Echinodermata, Boolootian, R.A., Ed., John Wiley & Sons, New York, 1966, 359.
81. Binyon, J., Physiology of Echinoderms, Pergamon Press, Oxford, New York, 1972.
82. Ruppert, E.E. and Barnes, R.D., Invertebrate Zoology, Saunders College Publishing Co., Philadelphia, 1994.
83. Unkles, S.E., Bacterial flora of the sea urchin Echinus esculentus, Appl. Env. Microb., 34, 347, 1977.
84. Guerinot, M. and Patriquin, D., N2-fixing vibrios isolated from the gastrointestinal tract of sea urchins, Can. J. Microbiol., 27, 311, 1981.
85. Guerinot, M. and Patriquin, D., The association of N2-fixing bacteria with sea urchins, Mar. Biol., 62, 197, 1981.
86. Kohn, A.J., Feeding biology of gastropods, in The Mollusca, Vol. 5 (Part 2), Wilbur, K.M., Ed., Academic Press, New York, 1983, 1.
87. Fretter, V. and Graham, A., British Prosobranch Molluscs, Royal Society of London, London, UK, 1962.
88. Galli, D. and Giese, A., Carbohydrate digestion in a herbivorous snail, Tegula funebralis, J. Exp. Zool., 140, 415, 1959.
89. Gacesa, P., Minireview: enzymic degradation of alginates, Int. J. Biochem., 24, 545, 1992.
90. Owen, G., Digestion, in Physiology of Mollusca, Wilbur, K. and Yonge, C., Eds., Academic Press, London, UK, 1966, 53.
91. Eales, N.B., Aplysia, Liverpool Marine Biological Committee, Proc. Trans. Liverpool Biol. Soc. L.M.B.C. Mem., 35, 183, 1921.
92. Fretter, V., The structure and function of the alimentary canal of some species of Polyplacophora (Mollusca), Trans. R. Soc. Edinb., 59 (Part I), 119, 1937.
93. Fretter, V., The structure and function of the alimentary canal of some tectibranch molluscs, Trans. R. Soc. Edinb., 59 (Part III), 599, 1939.
94. Graham, A., The structure and function of the alimentary canal of aeolid molluscs, with a discussion on their nematocysts, Trans. R. Soc. Edinb., 59 (Part II), 267, 1938.
95. Howells, H.H., The structure and function of the alimentary canal of Aplysia punctata, Q. J. Microsc. Sci., 83, 357, 1942.
96. Stallard, M.O. and Faulkner, D.J., Chemical constituents of the digestive gland of the sea hare Aplysia californica. I. Importance of the diet, Comp. Biochem. Physiol. B, 49, 25, 1974.
97. Stallard, M.O. and Faulkner, D.J., Chemical constituents of the digestive gland of Aplysia californica. II. Chemical transformation, Comp. Biochem. Physiol. B, 49, 37, 1974.
98. Kandel, E.R., Behavioral Biology of Aplysia, W.H. Freeman and Co., San Francisco, CA, 1979.
99. Coelho, L., Prince, J., and Nolen, T.G., Processing of defensive pigment in Aplysia californica:acquisition, modification and mobilization of the red algal pigment r-phycoerythrin by the digestive gland, J. Exp. Biol., 201, 425, 1998.
100. Shram, F.R., Crustacea, Oxford University Press, New York, 1986, 8.
101. Monk, D.C., The digestion of cellulose and other dietary components, and pH of the gut in the amphipod Gammarus pulex (L.), Freshwater Biol., 7, 431, 1977.
102. Borowsky, R. and Guarna, M.M., Excess amylase in Gammarus palustris (Crustacea: Amphipoda); its release into and possible roles in the environment, Mar. Biol., 101, 529, 1989.
103. Bärlocher, F. and Howatt, S.L., Digestion of carbohydrates and protein by Gammarus mucronatus Say (Amphipoda), J. Exp. Mar. Biol. Ecol., 104, 229, 1986.
104. Stuart, V., Head, E.J.H., and Mann, K.H., Seasonal changes in the digestive enzyme levels of the amphipod Corophium volutator (Pallas) in relation to diet, J. Exp. Mar. Biol. Ecol., 88, 243, 1985.
105. Rhoades, D.F. and Cates, R.G., Toward a general theory of plant antiherbivore chemistry, in Recent Advances in Phytochemistry, Volume 10, Biochemical Interaction Between Plants and Insects, Wallace, J.W. and Mansell, R.L., Eds., Plenum Press, New York, 1976, 168.
106. Swain, T., Tannins and lignins, in Herbivores: Their Interaction with Secondary Plant Metabolites, Rosenthal, G.A. and Janzen, D.H., Eds., Academic Press, New York, 1979, 657.
107. Ragan, M.A. and Glombitza, K.W., Phlorotannins, brown algal polyphenols, Prog. Phycol. Res., 4, 130, 1986.
108. Hagerman, A.E. and Butler, L.G., Tannins and lignins, in Herbivores: Their Interaction with Secondary Plant Metabolites: The Chemical Participants, Vol. 1, 2nd edition, Rosenthal, G.A. and Berenbaum, M.R., Eds., Academic Press, New York, 1991, 355.
109. Ragan, M.A., Physodes and the phenolic compounds of brown algae. Composition and significance of physodes in vivo, Bot. Mar., 19, 145, 1976.
110. Kaur, I. and Vijayaraghavan, M.R., Physode distribution and genesis in Sargassum vulgare (C. Agardh and Sargassum johnstonii Setchell and Gardner), Aquat. Bot., 45, 375, 1992.
111. Schmitt, T.M., Hay, M.E., and Lindquist, N., Constraints on chemically-mediated coevolution: multiple functions for seaweed secondary metabolites, Ecology, 76, 107, 1995.
112. Vreeland, V. and Laetsch, W.M., A gelling carbohydrate in algal cell wall formation, in Organisation and Assembly of Plant and Animal Extracellular Matrix, Adair, W.S. and Mecham, R.P., Eds., Academic Press, San Diego, CA, 1990, 137.
113. Schoenwaelder, M.E.A. and Clayton, M.N., The secretion of phenolic compounds following fertilization in Acrocarpia paniculata (Fucales, Phaeophyta), Phycologia, 37, 40, 1998.
114. Schoenwaelder, M.E.A. and Clayton, M.N., Secretion of phenolic substances into the zygote wall and cell plate in embryos of Hormosira and Acrocarpia (Fucales, Phaeophyceae), J. Phycol., 34, 969, 1998.
115. Geiselman, J.A. and McConnell, O.J., Polyphenols in brown algae Fucus vesiculosus and Ascophyllum nodosum: chemical defenses against the marine herbivorous snail, Littorina littorea, J. Chem. Ecol., 7, 1115, 1981.
116. Steinberg, P.D., Algal chemical defense against herbivores: allocation of phenolic compounds in the kelp Alaria marginata, Science, 223, 405, 1984.
117. Steinberg, P.D., Phenolic compounds in brown algae: chemical defenses against marine herbivores, Ph.D. thesis, University of California, Santa Cruz, Santa Cruz, California, 1984.
118. Steinberg, P.D., Feeding preferences of Tegula funebralis and chemical defenses of marine brown algae, Ecol. Monogr., 5, 333, 1985.
119. Steinberg, P.D., 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, 1988.
120. Steinberg, P.D. and van Altena, I.A., Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia, Ecol. Monogr., 62, 189, 1992.
121. Irelan, C.D. and Horn, M.H., Effects of macrophyte secondary chemicals on food choice and digestive efficiency of Cebidichthys violaceus (Girard), an herbivorous fish of temperate marine waters, J. Exp. Mar. Biol. Ecol., 153, 179, 1991.
122. Steinberg, P.D., Geographical variation in the interaction between marine herbivores and brown algal secondary metabolites, in Marine Chemical Ecology, Paul, V.J., Ed., Cornell Press, New York, 1992, 51.
123. Scalbert, A., Antimicrobial properties of tannins, Phytochemistry, 30, 3875, 1991.
124. Stern, J.L., Brown algal phlorotannins and marine invertebrate herbivore digestion, Ph.D. thesis, University of New South Wales, Sydney, Australia, 1998.
125. Arnold, T.M. and Targett, N.M., Quantifying in situ rates of phlorotannin synthesis and polymerization in marine brown algae, J. Chem. Ecol., 24, 577, 1998.
126. Arnold, T.M., In situ rates of phlorotannin synthesis, polymerization, and turnover in marine brown algae: an evaluation of terrestrial-derived ecological theories in the marine environment, Ph.D. thesis, University of Delaware, Newark, Delaware, 1998.
127. Van Alstyne, K.L., Ehlig, J.M., and Whitman, S.L., Feeding preferences for juvenile and adult algae depend on algal stage and herbivore species, Mar. Ecol. Prog. Ser., 180, 179, 1999.
128. Targett, N.M., Coen, L.D., Boettcher, A.A., and Tanner, C.E., Biogeographic comparisons of marine algal polyphenolics: evidence against a latitudinal trend, Oecologia, 89, 464, 1992.
129. Pavia, H. and Åberg, P., Spatial variation in polyphenolic content of Ascophyllum nodosum (Fucales, Phaeophyta), Hydrobiologia, 326/327, 199, 1996.
130. Van Alstyne, K.L., McCarthy, J.J., III, Hustead, C.L., and Duggins, D.O., Geographic variation in polyphenolic levels of Northeastern Pacific kelps and rockweeds, Mar. Biol., 133, 371, 1999.
131. Denton, A., Chapman, A.R.O., and Markham, J., Size-specific concentration of phlorotannins (antiherbivore compounds) in three species of Fucus, Mar. Ecol. Prog. Ser., 65, 103, 1990.
132. Pederson, A., Studies on phenol content and heavy metal uptake in fucoids, Hydrobiologia, 116/117, 498, 1984.
133. Tugwell, S. and Branch, G.M., Differential polyphenolic distribution among tissues in the kelps Ecklonia maxima, Laminaria pallida and Macrocystis angustifolia in relation to plant-defence theory, J. Exp. Mar. Biol. Ecol., 129, 219, 1989.
134. Tuomi, J., Ilvessalo, H., Miemela, P., Siren, S., and Jormalainen, V., Within-plant variation in phenolic content and toughness of the brown alga Fucus vesiculosus L., Bot. Mar., 32, 505, 1989.
135. Pfister, C.A., Costs of reproduction in the intertidal kelp: patterns of allocation and life history consequences, Ecology, 73, 1586, 1992.
136. Poore, A.G.B., Selective herbivory by amphipods inhabiting the brown alga Zonaria angustata, Mar. Ecol. Prog. Ser., 107, 113, 1994.
137. Ragan, M.A. and Jensen, A., Quantitative studies on brown algal phenols. I. Estimation of absolute polyphenol content of Ascophyllum nodosum (L.) Le Jol. and Fucus vesiculosus (L.), J. Exp. Mar. Biol. Ecol., 30, 209, 1977.
138. Geiselman, J.A., Ecology of chemical defenses of algae against the herbivorous snail littorina littorea in the New England rocky intertidal community, Ph.D. thesis, WHOI, Woods Hole, MA, 1980.
139. Steinberg, P.D., Seasonal variation in the relationship between growth rate and phlorotannin production in the kelp Ecklonia radiata, Oecologia, 102, 169, 1995.
140. Ilvessalo, H. and Tuomi, J., Nutrient availability and accumulation of phenolic compounds in the brown alga Fucus vesiculosus, Mar. Biol., 101, 115, 1989.
141. Yates, J.L. and Peckol, P., Effects of nutrient availability and herbivory on polyphenolics in the seaweed Fucus vesiculosus, Ecology, 74, 1757, 1993.
142. Arnold, T.M., Tanner, C.E., and Hatch, W.I., Phenotypic variation in polyphenolic content of the tropical brown alga Lobophora variegata as a function of nitrogen availability, Mar. Ecol. Prog. Ser., 123, 177, 1995.
143. Peckol, P., Krane, J.M., and Yates, J.L., Interactive effects of inducible defense and resource availability on phlorotannins in the North Atlantic brown alga Fucus vesiculosus, Mar. Ecol. Prog. Ser., 138, 209, 1996.
144. Arnold, T.M. and Targett, N.M., unpublished data.
145. Cronin, G. and Hay, M.E., Effects of light and nutrient availability on the growth, secondary chemistry, and resistance to herbivory of two brown seaweeds, Oikos, 77, 93, 1996.
146. Van Alstyne, K.L., Grazing increases polyphenolic defenses in the intertidal brown alga Fucus distichus, Ecology, 69, 655, 1988.
147. Hammerstrom, K., Dethier, M.N., and Duggins, D.O., Rapid phlorotannin induction and relaxation in five Washington kelps, Mar. Ecol. Prog. Ser., 165, 203, 1998.
148. Hay, M.E., The role of seaweed chemical defenses in the evolution of feeding specialization and in the mediation of complex interactions, in Ecological Roles of Marine Natural Products, Paul, V.J., Ed., Comstock Publishing Associates, Ithaca, NY, 1992, 93.
149. Steinberg, P.D., Estes, J.A., and Winter, F.C., Evolutionary consequences of food chain length in kelp forest communities, Proc. Natl. Acad. Sci. USA, 92, 8145, 1995.
150. Cooper-Driver, G.A. and Bhattacharya, M., Role of phenolics in plant evolution, Phytochemistry, 49, 1165, 1998.
151. Steinberg, P.D., Biogeographical variation in brown algal polyphenolics and other secondary metabolites:comparison between temperate Australasia and North America, Oecologia, 78, 373, 1989.
152. Boettcher, A.A., The role of polyphenolic molecular size in the reduction of assimilation efficiency in some marine herbivores, Master’s thesis, University of Delaware, Newark, Delaware, 1992.
153. Steinberg, P.D., Edyvane, K., de Nys, R., Birdsey, R., and Van Altena, I.A., Lack of avoidance of phenolic-rich algae by tropical herbivorous fishes, Mar. Biol., 109, 335, 1991.
154. Steinberg, P.D. and Paul, V.J., Fish feeding and chemical defenses of tropical brown algae in Western Australia, Mar. Ecol. Prog. Ser., 58, 253, 1990.
155. Van Alstyne, K.L. and Paul, V.J., The biogeography of polyphenolic compounds in marine macroalgae:temperate brown algal defenses deter feeding by tropical herbivorous fishes, Oecologia, 84, 158, 1990.
156. Taniguchi, K., Kurata, K., and Suzuki, M., Feeding-deterrent effect of phlorotannins from the brown alga Ecklonia stolonifera against the abalone Haliotis discus hannai, Nippon Suisan Gakkaishi, 57, 2065, 1991.
157. Van Altena, I.A. and Steinberg, P.D., Are differences in the responses between North American and Australasian marine herbivores to phlorotannins due to differences in phlorotannin structure?, Biochem. Syst. Ecol., 20, 493, 1992.
158. Bernays, E.A., Cooper-Driver, G., and Bilgener, M., Herbivores and plant tannins, Adv. Ecol. Res., 19, 263, 1989.
159. Bernays, E.A., Plant tannins and insect herbivores: an appraisal, Ecol. Entomol., 6, 353, 1981.
160. Martin, J.S., Martin, M.M., and Bernays, E.A., Failure of tannic acid to inhibit digestion or reduce digestibility of plant protein in gut fluids of insect herbivores: implications for theories of plant defense, J. Chem. Ecol., 13, 605, 1987.
161. Karowe, D.N., Differential effect of tannic acid on two tree-feeding lepidoptera: implications for theories of plant anti-herbivore chemistry, Oecologia, 80, 507, 1989.
162. Clausen, T.P., Provenza, F.D., Burritt, E.A., Reichardt, P.B., and Bryant, J.P., Ecological implications of condensed tannin structure: a case study, J. Chem. Ecol., 16, 2381, 1990.
163. Appel, J., Phenolics in ecological interactions: the importance of oxidation, J. Chem. Ecol., 19, 1521, 1993.
164. Stern, J.L., Hagerman, A.E., Steinberg, P.D., and Mason, P.K., Phlorotannin-protein interactions, J. Chem. Ecol., 22, 1877, 1996.
165. Ayres, M.P., Clausen, T.P., Maclean, S.F., Jr., Redman, A.A.M., and Reichardt, P.B., Diversity of structure and antiherbivore activity in condensed tannins, Ecology, 78, 1696, 1997.
166. Appel, H.M. and Martin, M.M., Gut redox conditions in herbivorous lepidopteran larvae, J. Chem. Ecol., 16, 3277, 1990.
167. Martin M.M. and Martin, J.S., Surfactants: their role in preventing the precipitation of proteins by tannins in insect guts, Oecologia, 61, 342, 1984.
168. Martin, M.M., Rockholm, D.C., and Martin, J.S., Effects of surfactants, pH, and certain cations on precipitation of proteins by tannins, J. Chem. Ecol., 11, 485, 1985.
169. Austin, P.J., Suchar, L.A., Robbins, C.T., and Hagerman, A.E., Tannin-binding proteins in saliva of deer and their absence in saliva of sheep and cattle, J. Chem. Ecol., 15, 1335, 1989.
170. Mole, S., Butler, L.G., and Iason, G., Defense against dietary tannin in herbivores: a survey for proline rich salivary proteins in mammals, Biochem. Syst. and Ecol., 18, 287, 1990.
171. Hanley, T.A., Robbins, C.T., Hagerman, A.E., and McArthur, C., Predicting digestible protein and digestible dry-matter in tannin-containing forages consumed by ruminants, Ecology, 73, 537, 1992.
172. McArthur, C., Sanson, G.D., and Beal, A.M., Salivary proline-rich proteins in mammals: Roles in oral homeostasis and counteracting dietary tannin, J. Chem. Ecol., 21, 663, 1995.
173. Juntheikki, M.R., JulkunenTiitto, R., and Hagerman, A.E., Salivary tannin-binding proteins in root vole (Microtus oeconomus Pallas), Biochem. Syst. Ecol., 24, 25, 1996.
174. Konno, K., Hirayama, C., and Shinbo, H., Glycine in digestive juice: a strategy of herbivorous insects against chemical defense of host plants, J. Insect Physiol., 43, 217, 1997.
175. Konno, K., Hirayama, C., and Shinbo, H., Unusually high concentration of free glycine in the midgut content of the silkworm, Bombyx mori, and other lepidopteran larvae, Comp. Biochem. Physiol., 115A, 229, 1996.
176. Feeny, P.P., Inhibitory effect of oak leaf tannins on the hydrolysis of proteins by trypsin, Phytochemistry, 8, 2119, 1969.
177. Zucker, W.V., Tannins: does structure determine function? An ecological perspective, Am. Nat., 121, 335, 1983.
178. Harborne, J.B., Introduction to Ecological Biochemistry, 3rd ed., Academic Press, London, UK, 1988.
179. Hagerman, A.E. and Klucher, K.M., Tannin-protein interactions, in Plant Flavonoids in Biology and Medicine: Biochemical, Pharmacological, and Structure Activity Relationships, Middleton, E. and Harborne, J., Eds., Alan R. Liss, Inc., New York, 1996.
180. Haslam, E., Plant polyphenols (syn. vegetable tannins) and chemical defenses -- a reappraisal, J. Chem. Ecol., 14, 1789, 1988.
181. Felton, G.W., Donato, K., Del Vecchio, R.J., and Duffey, S.S., Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores, J. Chem. Ecol., 15, 2667, 1989.
182. Felton, G.W., Workman, J., and Duffey, S.S., Avoidance of antinutritive plant defense: role of midgut pH in Colorado potato beetle, J. Chem. Ecol., 18, 571, 1992.
183. Felton, G.W., Donato, K.K., Broadway, R.M., and Duffey, S.S., Impact of oxidized plant phenolics on the nutritional quality of dietary protein to anoctuid herbivore, Spodoptera exigua, J. Insect Physiol., 38, 277, 1992.
184. Oh, H.I., Hoff, J.E., Armstrong, G.S., and Haff, L.A., Hydrophobic interaction in tannin-protein complexes, J. Agr. Food Chem., 28, 394, 1980.
185. Mole, S. and Waterman, P.G., Tannic acid and proteolytic enzymes: enzyme inhibition or substrate deprivation? Phytochem., 26, 99, 1987.
186. Mole, S., Butler, L.G., Hagerman, A.E., and Waterman, P.G., Ecological tannin assays: a critique, Oecologia, 78, 93, 1989.
187. Targett, T., unpublished data.
188. Winter, F.C. and Estes, J.A., Experimental evidence for the effects of polyphenolic compounds from Dictyoneurum californicum Ruprecht (Phaeophyta: Laminariales) on feeding rate and growth in the red abalone Haliotus rufescens Swainson, J. Exp. Mar. Biol. Ecol., 155, 263, 1992.
189. Hoover, K., Kishida, K.T., DiGiorgio, L.A., Workman, J., Alaniz, S.A., Hammock, B.D., and Duffey, S.S., Inhibition of baculoviral disease by plant-mediated perocidase activity and free radical generation, J. Chem. Ecol., 24, 1949, 1998.
190. Hay, M.E., Duffy, J.E., and Pfister, C.A., Chemical defense against different marine herbivores: are amphipods insect equivalents? Ecology, 68, 1567, 1987.
191. Pennings, S.C. and Carefoot, T.H., Post-ingestive consequences of consuming secondary metabolites in sea hares (Gastropoda: Opisthobranchia), Comp. Biochem. Physiol., 111C, 249, 1995.
192. Pennings, S.C. and Paul, V.J., Effect of plant toughness, calcification, and chemistry on herbivory by Dolabella auricularia, Ecology, 73, 1606, 1992.
193. Schupp, P.J. and Paul, V.J., Calcification and secondary metabolites in tropical seaweeds: variable effects on herbivorous fishes, Ecology, 75, 1172, 1994.
194. Meyer, K.D. and Paul, V.J., Variation in secondary metabolite and aragonite concentrations in the tropical green seaweed Neomeris annulata: effects on herbivory by fishes, Mar. Biol., 122, 537, 1995.
195. Pennings, S.C., Puglisi, M.P., Pitlik, T.J., Himaya, A.C., and Paul, V.J., Effects of secondary metabolites and CaCO3 on feeding by surgeonfishes and parrotfishes: within-plant comparisons, Mar. Ecol. Prog. Ser., 134, 49, 1996.
196. Pennings, S.C. and Paul, V.J., Sequestration of dietary secondary metabolites by three species of sea hares: location, specificity and dynamics, Mar. Biol., 117, 535, 1993.
197. Paul, V.J. and Pennings, S.C., Diet-derived chemical defenses in the sea hare Stylocheilus longicauda (Quoy et Gaimard 1824), J. Exp. Mar. Biol. Ecol., 151, 227, 1991.
198. Pennings, S.C., Paul, V.J., Dunbar, D.C., Hamann, M.T., Lumbang, W.A., Novack, B., and Jacobs, R.S., Unpalatable compounds in the marine gastropod Dolabella auricularia: distribution and effect of diet, J. Chem. Ecol., 25, 735, 1999.
199. de Nys, R., Steinberg, P.D., Rogers, C.N., Charlton, T.S., and Duncan, M.W., Quantitative variation of secondary metabolites in the sea hare Aplysia parvula and its host plant, Delisea pulchra, Mar. Ecol. Prog. Ser., 130, 135, 1996.
200. Doty, M.S. and Aguilar-Santos, G., Transfer of toxic algal substances in marine food chains, Pac. Sci., 24, 351, 1970.
201. Jensen, K.R., Defensive behavior and toxicity of ascoglossan opisthobranch Mourgan agermaineae Marcus, J. Chem. Ecol., 10, 475, 1984.
202. Paul, V.J. and Van Alstyne, K.L., Use of ingested algal diterpenoids by Elysia halimedae Macnae (Opisthobranchia:Ascoglossa) as antipredator defenses, J. Exp. Mar. Biol. Ecol., 119, 15, 1988.
203. Jensen, K.R., Behavioural adaptations and diet specificity of sacoglossan opisthobranchs, Ethol. Ecol. Evol., 6, 87, 1994.
204. Gavagnin, M., Marin, A., Castelluccio, F., Villani, G., and Cimino, G., Defensive relationships between Caulerpa prolifera and its shelled sacoglossan predators, J. Exp. Mar. Biol. Ecol., 175, 197, 1994.
205. Cimino, G., Crispino, A., Di Marzo, V., Gavagnin, M., and Ros, J.D., Oxytoxins, bioactive molecules produced by the marine opisthobranch mollusc Oxynoe olivacea from a diet-derived precursor, Experientia, 46, 767, 1990.
206. Hay, M.E., The ecology and evolution of seaweed-herbivore interactions on coral reefs, Coral Reefs, 16, S67, 1997.