Tropical marine herbivore assimilation of phenolic-rich plants
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Abstract
Phenolics in marine brown algae have been thought to follow a latitudinal gradient with high phenolic species in high latitudes and low phenolic species in low latitudes. However, tropical brown algae from the western Caribbean have been shown to be high in phlorotannin concentration, indicating that latitude alone is not a reasonable predictor of marine plant phenolic concentrations. This study shows that the range of high phenolic phaeophytes is not limited to the western Caribbean but encompasses the western tropical Atlantic, including Bermuda and the Caribbean, where algal phlorotannin concentrations can be as high as 25% dry weight (DW). Assimilation efficiencies (AEs) of phenolic-rich and phenolic-poor plants were examined in three tropical marine herbivores (the parrotfish, Sparisoma radians, and the brachyuran crab, Mithrax sculptus, from Belize and the parrotfish, Sparisoma chrysopterum, from Bermuda). AEs of phenolic-rich food by each of the three herbivore species were uniformly high, suggesting that high plant phenolic concentrations did not affect AEs in these species. This is in contrast to some temperate marine herbivores where phenolic concentrations of 10% DW have been shown to drastically reduce AE. The apparent contradiction is discussed in light of the effects of specific herbivore gut characteristics on successful herbivory of high phenolic brown algae.
Key words
Phlorotannin Polyphenolics Herbivore Assimilation efficiency Brown algaePreview
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References
- Andersen RA, Todd JR (1968) Estimation of total tobacco plant phenols by their binding to polyvinylpyrrolidone. Tobac Sci 12: 107–111Google Scholar
- Anderson TA (1988) The effect of feeding frequency on utilization of algal nutrients by the marine herbivore, the luderick, Girella tricuspidata (Quoy and Gaimard). J Fish Biol 32: 911–921Google Scholar
- Andrew NL, Jones GP (1990) Patch formation by herbivorous fish in a temperate Australian kelp forest. Oecologia 85: 57–68Google Scholar
- Appel HM (1993) Phenolics in ecological interactions: the importance of oxidation. J Chem Ecol 19: 1521–1552Google Scholar
- Appel HM, Martin MM (1990) Gut redox conditions in herbivorous lepidopteran larvae. J Chem Ecol 16: 3277–3290Google Scholar
- Appel HM, Schultz JC (1992) Activity of phenolics in insects may require oxidation. In: Hemingway RW (ed) Plant polyphenols: biogenesis, chemical properties, and significance. Plenum Press, New YorkGoogle Scholar
- Barbehenn R, Martin MM (1992) The protective role of the peritrophic membrane in the tannin-tolerant larvae of Orgyia leucostigma (Lepidoptera). J Insect Physiol 38: 973–980Google Scholar
- Berenbaum M (1980) Adaptive significance of midgut pH in larval Lepidoptera. Am Nat 115: 138–146Google Scholar
- Bernays EA (1981) Plant tannins and insect herbivores: an appraisal. Ecol Entomol 6: 353–360Google Scholar
- Bernays EA, Cooper Driver G, Bilgener M (1989) Herbivores and plant tannins. Adv Ecol Res 19: 263–302Google Scholar
- Boettcher AA (1992) The role of polyphenolic molecular size in the reduction of assimilation efficiency in some marine herbivores. Masters thesis, University of Delaware, Newark, DelGoogle Scholar
- Boettcher AA, Targett NM (1993) Role of polyphenolic molecular size in reduction of assimilation efficiency in Xiphister mucosus. Ecology 74: 891–903Google Scholar
- Brafield AE (1985) Laboratory studies of energy budgets. In: Tytler P, Calow P (eds) Fish energetics, new perspectives. Johns Hopkins University Press, Baltimore, pp 257–281Google Scholar
- Coen LD (1988) Herbivory by Caribbean majid crabs: feeding ecology and plant susceptibility. J Exp Mar Biol Ecol 122: 257–276Google Scholar
- Coen LD, Tanner CE (1989) Morphological variation and differential susceptibility to herbivory in the tropical brown alga Lobophora variegata. Mar Ecol Prog Ser 54: 287–298Google Scholar
- Dall W, Moriarty DJW (1983) Functional aspects of nutrition and digestion. In: Mantel LH (ed) The biology of crustacea, vol 5, Academic Press, New York, pp 215–261Google Scholar
- Edwards TW, Horn MH (1982) Assimilation efficiency of a temperate-zone intertidal fish (Cebidichthys violaceus) fed diets of macroalgae. Mar Biol 67: 247–253Google Scholar
- Elliot JM (1976) Energy losses in the waste products of brown trout (Salmo: Trutta L.). J Anim Ecol 45: 561–580Google Scholar
- Feeny PP (1969) Inhibitory effect of oak leaf tannins on the hydrolysis of proteins by trypsin. Phytochem 8: 2119–2126Google Scholar
- Geesey GG, Alexander GV, Bray RN, Miller AC (1984) Fish fecal pellets are a source of minerals for inshore reef communities. Mar Ecol Prog Ser 15: 19–25Google Scholar
- Geiselman JA, McConnell OJ (1981) Polyphenols in brown algae Fucus vesiculosus and Ascophyllum nodosum: chemical defenses against the marine herbivorous snail, Littorina littorea. J Chem Ecol 7: 1115–1133Google Scholar
- Gerking SD (1984) Assimilation and maintenance ration of an herbivorous fish, Sarpa salpa, feeding on a green alga. Trans Am Fish Soc 113: 378–387Google Scholar
- Hagerman AE, Butler LG (1991) Tannins and Lignins. In: Rosenthal GA, Berenbaum M (eds) Herbivores, their interaction with secondary plant metabolites: the chemical participants, vol 1. Academic Press, New York, pp 355–388Google Scholar
- Hay ME, Fenical W (1988) Marine plant-herbivore interactions: the ecology of chemical defense. Annu Rev of Syst Ecol 19: 111–145Google Scholar
- Horn MH (1989) Biology of marine herbivorous fishes. Oceanogr Mar Biol Annu Rev 27: 167–272Google Scholar
- Horn MH, Neighbors MA (1984) Protein and nitrogen assimilation as a factor predicting the seasonal macroalgal diet of the monkeyface prickleback. Trans Am Fish Soc 113: 388–396Google Scholar
- Horn MH, Neighbors MA, Rosenberg MJ, Murray SN (1985) Assimilation of carbon from dietary and nondietary macroalgae by a temperate-zone intertidal fish, Cebidichthys violaceus (Girard) (Teleostei: Stichaeidae). J Exp Mar Biol Ecol 86: 241–253Google Scholar
- Horn MH, Neighbors MA, Murray SN (1986) Herbivore responses to a seasonally fluctuating food supply: growth potential of two temperate intertidal fishes based on the protein and energy assimilated from their macroalgal diets. J Exp Mar Biol Ecol 103: 217–234Google Scholar
- Irelan CD, Horn MH (1991) 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: 179–194Google Scholar
- Lassuy DR (1984) Diet, intestinal morphology, and nitrogen assimilation efficiency in the damselfish, Stegastes lividus, in Guam. Environ Biol Fish 10: 183–193Google Scholar
- Lobel PS, Ogden JC (1981) Foraging by the herbivorous parrotfish Sparisoma radians. Mar Biol 64: 173–183Google Scholar
- Martin MM, Martin JS (1984) Surfactants: their role in preventing the precipitation of proteins by tannins in insect guts. Oecologia 61: 342–345Google Scholar
- Martin MM, Rockholm DC, Martin JS (1985) Effects of surfactants, pH, and certain cations on precipitation of proteins by tannins. J Chem Ecol 11: 485–494Google Scholar
- Montgomery WL, Gerking SD (1980) Marine macroalgae as foods for fishes: an evaluation of potential food quality. Environ Biol Fish 5: 143–153Google Scholar
- Purchon RD (1977) The biology of the mollusca. Pergamon Press, OxfordGoogle Scholar
- Ragan MA, Glombitza KW (1986) Phlorotannins, brown algal polyphenols. In: Round FE, Chapman DJ (eds) Progress in phycological research, vol 4. Biopress, Bristol, UK, pp 129–241Google Scholar
- Ragan MA, Jensen A (1977) 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: 209–221Google Scholar
- Rosenthal GA, Berenbaum M (eds) (1991a) Herbivores, their interaction with secondary plant metabolites: the chemical participants, vol 1. Academic Press, New YorkGoogle Scholar
- Rosenthal GA, Berenbaum M (eds) (1991b) Herbivores, their interaction with secondary plant metabolites: the chemical participants, vol 2. Academic Press, New YorkGoogle Scholar
- Rosenthal GA, Janzen DH (1979) Herbivores, their interaction with secondary plant metabolites. Academic Press, New YorkGoogle Scholar
- Steinberg PD (1984) Algal chemical defense against herbivores: allocation of phenolic compounds in the kelp Alaria marginata. Science 223: 405–407Google Scholar
- Steinberg PD (1985) Feeding preferences of Tegula funebralis and chemical defenses of marine brown algae. Ecol Monogr 5: 333–349Google Scholar
- Steinberg PD (1988) 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
- Steinberg PD (1992) Geographical variation in the interaction between marine herbivores and brown algal secondary metabolites. In: Paul VJ (ed) Marine chemical ecology. Cornell Press, New York, pp 51–91Google Scholar
- Steinberg PD, van Altena FA (1992) Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecol Monogr 62: 189–222Google Scholar
- Steinberg PD, Paul VJ (1990) Fish feeding and chemical defenses of tropical brown algae in Western Australia. Mar Ecol Prog Ser 58: 253–259Google Scholar
- Steinberg PD, Edyvane K, de Nys R, Birdsey R, van Altena FA (1991) Lack of avoidance of phenolic rich brown algae by tropical herbivorous fishes. Mar Biol 109: 335–343Google Scholar
- Swain T (1979) Tannins and lignins. In: Rosenthal GA, Janzen DH (eds) Herbivores, their interactions with secondary plant metabolites. Academic Press, New York, pp 657–682Google Scholar
- Swain T, Hillis WE (1959) The phenolic constituents of Prunus domestica. I. The quantitative analysis of phenolic constituents. J Sci Food Agric 10: 63–68Google Scholar
- Targett NM, Targett TE, Vrolijk NH, Ogden JC (1986) Effect of macrophyte secondary metabolites on feeding preferences of the herbivorous parrotfish Sparisoma radians. Mar Biol 92: 141–148Google Scholar
- Targett NM, Coen LD, Boettcher AA, Tanner CE (1992) Biogeographic comparisons of marine algal polyphenolics: evidence against a latitudinal trend. Oecologia 89: 464–470Google Scholar
- Targett TE, Targett NM (1990) 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: 13–21Google Scholar
- Tugwell S, Branch GM (1992). Effects of herbivore gut surfactants on kelp polyphenol defenses. Ecology 73: 205–215Google Scholar
- Van Alstyne KL (1988) Grazing increases polyphenolic defenses in the intertidal brown alga Fucus distichus. Ecology 69: 655–663Google Scholar
- Van Alstyne KL, Paul VJ (1990) The biogeography of polyphenolic compounds in marine macroalgae: temperate brown algal defenses deter feeding by tropical herbivorous fishes. Oecologia 84: 158–163Google Scholar
- Waterman PG, Mole S (1994) Analysis of phenolic plant metabolites. Blackwell Scientific, LondonGoogle Scholar
- Yates JL, Peckol P (1993) Effects of nutrient availability and herbivory on polyphenolics in the seaweed Fucus vesiculosus. Ecology 74: 1757–1766Google Scholar
- Zapata O, McMillan C (1979) Phenolic acids in seagrasses. Aquat Bot 7: 307–317Google Scholar
- Zucker WV (1983) Tannins: does structure determine function? An ecological perspective. Am Nat 121: 335–365Google Scholar