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Quantifying in Situ Rates of Phlorotannin Synthesis and Polymerization in Marine Brown Algae

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Abstract

Using three species of marine brown algae, we describe a stable isotope labeling technique to quantify: (1) in situ rates of phlorotannin synthesis, (2) phlorotannin polymerization or aging, and (3) the related allocation of carbon resources to secondary metabolism. In our field and laboratory assays, Lobophora variegata (Bahamas), Sargassum pteropleuron (Bahamas), and Fucus distichus (California, USA) assimilated various quantities of 13C, but all allocated ≤ 1% of the assimilated carbon to the production of phlorotannins. We quantified rates of phlorotannin synthesis both as micrograms of compound produced per gram of tissue per unit of time and as micrograms of compound produced per gram of C assimilated per unit of time. Rates of synthesis, normalized to account for differences in potential photosynthetic rates, are comparable to previously reported rates of phlorotannin accumulation. The aging of phlorotannins from low- (<30 kDa) to high- (>30 kDa) molecular-size polymers was observed in S. pteropleuron within a 28-hr period. Our results indicate that, using this labeling technique, it is possible to make precise measurements of allelochemical metabolism and resource allocation, which are useful both in critically evaluating the assumptions made by ecological models of plant chemistry and in estimating the partial metabolic cost of specific secondary metabolites.

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REFERENCES

  • Arnold, T. M., Tanner, C. E., and Hatch, W. I. 1995. Phenotypic variation in polyphenolic content of the tropical brown alga Lobophora variegata as a function of nitrogen availability. Mar. Ecol. Prog. Ser. 123:177–183.

    Google Scholar 

  • Baldwin, I. T., and Ohnmeiss, T. E. 1994. Coordination of photosynthetic and alkaloidal responses to damage in uninducible and inducible Nicotina sylvestris. Ecology 75:1003–1014.

    Google Scholar 

  • Baldwin, I. T., Karb, M. J., and Ohnmeiss, T. E. 1994. Allocation of 15N from nitrate to nicotine: Production and turnover of a damage-induced mobile defense. Ecology 75:1703–1713.

    Google Scholar 

  • Bazzaz, F. A., Chiariello, P. D., Coley, P. D., and Pitelka, L. F. 1987. Allocating resources to reproduction and defense. BioScience 37:58–67.

    Google Scholar 

  • Bernays, E. A., Cooper-Driver, G., and Bilgener, M. 1989. Herbivores and plant tannins. Adv. Ecol. Res. 19:263–302.

    Google Scholar 

  • Boettcher, A. A., and Targett, N. M. 1993. Role of polyphenolic molecular size in reduction of assimilation efficiency in Xiphister mucosus. Ecology 74:891–903.

    Google Scholar 

  • Boutton, T. W. 1991. Stable carbon isotope ratios of natural materials: I. Sample preparation and mass spectrometric analysis, pp. 155–171, in D. C. Colman and B. Fry (eds.). Carbon Isotope Techniques. Academic Press, San Diego, California.

    Google Scholar 

  • Briggs, M. A., and Schultz, J. C. 1990. Chemical defense production in Lotus corniculatus L. II. Trade-offs among growth, reproduction, and defense. Oecologia 83:32–37.

    Google Scholar 

  • Bryant, J. P., Chapin, F. S., Reichardt, P. B., and Clausen, T. P. 1987. Response of winter chemical defense in Alaska paper birch and green alder to manipulation of plant carbon/nutrient balance. Oecologia 72:510–514.

    Google Scholar 

  • Burbott, A. J., and Loomis, W. D. 1969. Evidence for metabolic turnover of monoterpenes in peppermint. Plant Physiol. 44:173–179.

    Google Scholar 

  • Chew, F. S., and Rodman, J. E. 1979. Plant Resources for chemical defense, pp. 271–300, in G. A. Rosenthal and D. H. Janzen (eds.). Herbivores: Their interactions with secondary metabolites. Academic Press. New York.

    Google Scholar 

  • Coley, P. D. 1986. Costs and benefits of defense by tannins in a neotropical tree. Oecologia 70:238–241.

    Google Scholar 

  • Coley, P. D., Bryant, J. P., and Chapin III, F. S. 1985. Resource availability and plant anti-herbivore defense. Science 230:895–899.

    Google Scholar 

  • Croteau, R., Burbott, A. J., and Loomis, W. D. 1972. Biosynthesis of mono-and sesui-terpenes in peppermint from glucose-14C and 14CO2. Phytochemistry 11:2459–2467.

    Google Scholar 

  • Denton, A., Chapman, A. R. O., and Markham, J. 1990. Size specific concentrations of phlorotannins (anti-herbivore compounds) in three species of Fucus. Mar. Ecol. Prog. Ser. 65:103–104.

    Google Scholar 

  • Fagerstrom, T. 1989. Anti-herbivore chemical defense in plants: A note on the concept of cost. Am. Nat. 133:281–287.

    Google Scholar 

  • Feeny, P. P. 1976. Plant apparency and chemical defense. Recent Adv. Phytochem. 10:1–40.

    Google Scholar 

  • Geiselman, J. A. 1980. Ecology of chemical defenses of algae against the herbivorous snail Littorina littorea in the New England rocky intertidal community. PhD thesis. Woods Hole Oceanographic Institution, Woods Hole, Massachusetts.

    Google Scholar 

  • Gershenzon, J., Murtagh, G. J., and Croteau, R. 1993. Absence of rapid terpene turnover in several species of terpene accumulating plants. Oecologia 96:583–592.

    Google Scholar 

  • Han, K., and Lincoln, D. E. 1994. The evolution of carbon allocation to plant secondary metabolites: A genetic analysis of cost in Diplacus aurantiacus. Evolution 48(5):1550–1563.

    Google Scholar 

  • Hatch, W. I., Tanner, C. E., Butler, N. M., and O'Brien, E. P. 1993. A Micro-Folin-Denis Method for the Rapid Quantification of Phenolic Compounds in Marine Plants and Animals. International Society of Chemical Ecology. Tampa, Florida (abstract).

    Google Scholar 

  • Hay, M. E., and Fenical, W. 1988. Marine plant-herbivore interactions: The ecology of chemical defense. Annu. Rev. Syst. Ecol. 19:111–145.

    Google Scholar 

  • Herms, D. A., and Mattson, W. J. 1992. The dilemma of plants: To grow or defend. Q. Rev. Biol. 67:283–335.

    Google Scholar 

  • Ilvessalo, H., and Tuomi, J. 1989. Nutrient availability and accumulation of phenolic compounds in the brown algae Fucus vesiculosus. Mar. Biol. 101:115–119.

    Google Scholar 

  • Lerdau, M., and Gershenzon, J. 1997. Allocation theory and chemical defense, pp. 265–277, in F. A. Bazzaz and J. Grace (eds.). Plant Resource Allocation. Academic Press, San Diego, California.

    Google Scholar 

  • Lerdau, M., Litvak, M., and Monson, R. 1994. Plant chemical defense: monoterpenes and the growth-differentiation balance hypothesis. Trends Ecol. Evol. 9(2):58.

    Google Scholar 

  • Littler, M. M., and Arnold, K. E. 1984. Primary productivity of marine macroalgal functional-form groups from southwestern North America. J. Phycol. 18:307–311.

    Google Scholar 

  • Mihaliak, C. A., Gershenzon, J., and Crouteau, R. 1991. Lack of rapid monoterpene turnover in rooted plants: Implications for theories of plant chemical defense. Oecologica 87:373–376.

    Google Scholar 

  • Mole, S., Butler, L. G., Hagerman, A. E., and Waterman, P. G. 1989. Ecological tannin assays: A critique. Oecologia 78:93–96.

    Google Scholar 

  • Norris, J. N., and Fenical, W. 1982. Chemical defenses in tropical marine algae, pp. 417–431, in K. Rutzler and I. G. Macintyre (eds.). The Atlantic Barrier Reef Ecosystem at Carrie Bow Cay, Belize, Smithsonian Contribution to the Marine Sciences. Smithsonian Institute Press, Washington, DC.

    Google Scholar 

  • Peckol, P., Krane, J. M., and Yates, J. L. 1996. Interactive effects of inducible defense and resource availability on phlorotannins in the North Atlantic brown alga Fucus vesiculosus. Mar. Ecol. Prog. Ser. 138:209–217.

    Google Scholar 

  • Pederson, A. 1984. Studies on phenol content and heavy metal uptake in fucoids. Hydrobiologia 116/117:498–504.

    Google Scholar 

  • Pfister, C. A. 1992. Costs of reproduction in the intertidal kelp: Patterns of allocation and life history consequences. Ecology 73:1586–1596.

    Google Scholar 

  • Ragan, M. A., and Glombitza, K. W. 1986. Phlorotannins, brown algal polyphenolics, pp. 129–241, in F. E. Round and D. J. Chapman (eds.). Progress in Phycological Research, Volume 4. Biopress, Bristol, England.

    Google Scholar 

  • Ragan, M. A., and Jensen, A. 1978. Quantitative studies on brown algal phenols. II. Seasonal variation in polyphenolic content of Ascophyllum nodosum (L.) Le Jol. And Fucus vesiculosus (L.). J. Exp. Mar. Biol. Ecol. 34:245–258.

    Google Scholar 

  • Reichardt, P. B., Chapin, F. S., III, Bryant, J. P., Mattes, B. R., and Clausen, T. P. 1991. Carbon/nutrient balance as a predictor of plant defense in Alaskan balsam poplar: Potential importance of metabolite turnover. Oecologia 82:217–226.

    Google Scholar 

  • Rhoades, D. F., and Cates, R. G. 1976. Toward a general theory of plant antiherbivore chemistry. Recent Adv. Phytochem. 10:168–213.

    Google Scholar 

  • Rosenthal, G. A., and Janzen, D. H. 1979. Herbivores, their interaction with secondary plant metabolites. Academic Press, New York.

    Google Scholar 

  • Sharp, J. H. 1973. A quick and simple measurement for total inorganic carbon in seawater pp. 143–144, in Research on the Marine Food Chain. Progress report to the U.S. Atomic Energy Commission. University of Califgrnia, San Diego Institute of Marine Resources.

  • Steinberg, P. D. 1984. Algal chemical defense against herbivores: Allocation of phenolic compounds in the kelp Alaria marginata. Science 223:405–407.

    Google Scholar 

  • Steinberg, P. D. 1992a. Geographical variation in brown algal polyphenolics and other secondary metabolites: Comparison between temerate Australasia and North America. Oecologia 78:373–382.

    Google Scholar 

  • Steinberg, P. D. 1992b. Geographical variation in the interaction between marine herbivores and secondary metabolites, pp. 51–92, in V. J. Paul (ed.). Ecological Roles of Marine Natural Products. Cornell University Press, Ithaca, New York.

    Google Scholar 

  • Steinberg, P. D. 1995. Seasonal variation in the relationship between growth rate and phlorotannin production in the kelp Eklonia radiata. Oecologia 102:169–173.

    Google Scholar 

  • Targett, N. M., Coen, L. D., Boettcher, A. A., and Tanner, C. E. 1992. Biogeographic comparisons of marine algal polyphenolics: Evidence against a latitudinal trend. Oecologicau 89:464–470.

    Google Scholar 

  • Targett, N. M., Boettcher, A. A., Targett, T. E., and Vrolijk, N. H. 1995. Tropical marine herbivore assimilation of phenolic-rich plants. Oecologia 103:170–179.

    Google Scholar 

  • Tugwell, S., and Branch, G. M. 1989. Differential polyphenolic distribution among tissues in the kelps Ecklonia maxima, Laminaria pallida, and Macrocystis angustifolia in relation to plant-defense theory. J. Exp. Mar. Biol. Ecol. 129:219–230.

    Google Scholar 

  • Tuomi, J. 1992. Toward integration of plant defense theories. Trends Ecol. Evol. 7:365–367.

    Google Scholar 

  • Tuomi, J., Ilvessalo, H., Miemela, P., Siren, S., and Jormalainen, V. 1989. With-in plant variation in phenolic content and toughness of the brown alga Fucus vesiculosus. L. Bot. Mar. 32:505–509.

    Google Scholar 

  • Van Aalstyne, K. L. 1988. Grazing increases polyphenolic defenses in the intertidal brown alga Fucus distichus. Ecology 69:655–663.

    Google Scholar 

  • Van Alstyne, K. L. 1995. Comparison of three methods for quantifying brown algal polyphenolic compounds. J. Chem. Ecol. 21:45–58.

    Google Scholar 

  • Waterman, P. G., and Mole, S. 1994. Analysis of Phenolic Plant Metabolites. Blackwell Scientific, Oxford, p. 238.

    Google Scholar 

  • Wu, Y., and Gretz, M. R. 1993. Stable isotope labeling method for studies of saccharide metabolism in Agardhiella subulata. Hydrobiologia 260/261:595–600.

    Google Scholar 

  • Yates, J. L., and Peckol, P. 1993. Effects of nutrient availability and herbivory on polyphenolics in the seaweed Fucus vesiculosus. Ecology 74:1757–1766.

    Google Scholar 

  • Zangerl, A. R., and Bazzaz, F. A. 1992. Theory and pattern in plant defense allocation, pp. 363–391, in R. S. Fritz and E. L. Simms (eds.). Plant Resistance to Herbivores and Pathogens. Chicago, University of Chicago Press.

    Google Scholar 

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  1. Graduate College of Marine Studies, University of Delaware, Lewes, Delaware, 19958

    Thomas M. Arnold & Nancy M. Targett

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  1. Thomas M. Arnold
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Arnold, T.M., Targett, N.M. Quantifying in Situ Rates of Phlorotannin Synthesis and Polymerization in Marine Brown Algae. J Chem Ecol 24, 577–595 (1998). https://doi.org/10.1023/A:1022373121596

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