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Marine Tannins: The Importance of a Mechanistic Framework for Predicting Ecological Roles

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Abstract

Since chemical ecology emerged as a field of marine science, it has been strongly influenced by studies of chemically mediated interactions in land-based systems. Marine chemical ecologists, like their terrestrial counterparts, initially focused on identifying natural products and evaluating the potential ecological roles of these products as defenses, attractants, or other cues. Now, like our land-based colleagues, we must increase our focus on the physiological and biochemical mechanisms that underlie the chemical interactions, paying particular attention to regulation of biosynthetic pathways, within-plant and between-plant signaling cues, and comparative and functional genomics. Here, we review the current state of knowledge regarding a heterogenous group of macrophyte natural products, the marine tannins and simple phenolics, to illustrate how such information is critical to future attempts to predict their ecological roles.

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REFERENCES

  • Alongi, D. M. 1987. The influence of mangrove-derived tannins on intertidal meiobenthos in tropical estuaries. Oecologia 71:537–540.

    Google Scholar 

  • Appel, H. 1993. Phenolics in ecological interactions: the importance of oxidation. J. Chem. Ecol. 19:1521–1552.

    Google Scholar 

  • Arnold, T.M. and Targett, N.M. 2000. Evidence for metabolic turnover of polyphenolics in tropical brown algae. J. Chem. Ecol. 26:1393–1410.

    Google Scholar 

  • Arnold, T. M. and Targett, N. M. 2002. To grow and defend: lack of tradeoffs for brown algal phlorotannins. Oikos. In press.

  • Arnold, T. M., Targett, N. M., Tanner, C. E., Hatch, W. I., and Ferrari, K. E. 2001. Evidence for methyl jasmonate-induced phlorotannin production in Fucus vesiculosus (Phaeophyceae). J. Phycol. 37:1026–1029.

    Google Scholar 

  • Baerlocher, F. and Newell, S. Y. 1994. Phenolics and proteins affecting palatability of Spartina leaves to the gastropod Littoraria irrorata. Mar. Ecol. 15:65–75.

    Google Scholar 

  • Basak, U. C., Das, A. B., and Das, P. 1996. Chlorophylls, carotenoids, proteins and secondary metabolites in leaves of 14 species of mangrove. Bull. Mar. Sci. 58: 654–659.

    Google Scholar 

  • Basak, U. C., Das, A. B., and Das, P. 1998. Seasonal changes in organic constituents in leaves of nine mangrove species. Mar. Freshwater Res. 49:369–372.

    Google Scholar 

  • Boettcher, A. A. and Targett, N.M. 1993. The role of polyphenolic molecular size in the reduction of assimilation efficiency in the herbivorous marine fish Xiphister mucosus. Ecology 74:891–903.

    Google Scholar 

  • Bryant, J. P., Chapin, F. S., and Klein, D. R. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368.

    Google Scholar 

  • Buchsbaum, R., Valiela, I., and Swain, T. 1984. The role of phenolic compounds and other plant constituents in feeding by Canada geese in a coastal marsh. Oecologia 63:343–349.

    Google Scholar 

  • Buchsbaum, R. N., Short, F. T., and Cheney, D. P. 1990. Phenolic-nitrogen interactions in eelgrass, Zostera marina L.: possible implications for disease resistance. Aquat. Bot. 37:291–297.

    Google Scholar 

  • Camilleri, J. 1989. Leaf choice by crustaceans in a mangrove forest in Queensland. Mar. Biol. 102:453–459. MARINE TANNINS 1931

    Google Scholar 

  • Cebrian, J., Duarte, C. M., Marba, N., Enriquez, S., Gallegos, M., and Olesen, B. 1996. Herbivory on Posidonia oceanica: magnitude and variability in the Spanish Mediterranean. Mar. Ecol. Prog. Ser. 130:147–155.

    Google Scholar 

  • Cebrian, J., Duarte, C. M., Agawin, N. S. R., and Merino, M. 1998. Leaf growth response to simulated herbivory: a comparison among seagrass species. J. Exp. Mar. Biol. Ecol. 220:67–81.

    Google Scholar 

  • Collen, J. and Davison, I. R. 1999. Reactive oxygen production and damage in intertidal Fucus spp. (Phaeophyceae). J. Phycol. 35:54–61.

    Google Scholar 

  • Cronin, G. 2001. Resource allocation in seaweeds and marine invertebrates: chemical defense patterns in relation to defense theory, p. 325–354, in J. B. McClintock and B. J. Baker (eds.). Marine Chemical Ecology CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Dawes, C. J. 1998. Marine Botany. John Wiley & Sons, New York.

    Google Scholar 

  • Den Hartog, C. 1996. Sudden declines of seagrass beds; “wasting disease” and other disasters, pp. 307–315, in J. Kuo, R. C. Phillips, K. I. Walkers, and H. Kirkman (eds.). Seagrass Biology: Proceedings of an InternationalWorkshop, 25–29 January 1996, Rottnest Island,Western Austalia.

  • Duranko, M. J. and Kuss, K. M. 1994. Effects of Labyrinthula infection on the photosynthentic capacity of Thalassia testudinum. Bull. Mar. Sci. 54:727–732.

    Google Scholar 

  • Feller, I. R. 1996. Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove (Rhizophora mangle). Ecol. Monogr. 65:477–505.

    Google Scholar 

  • Filip, Z. and Alberts, J. J. 1989. Humic substances isolated from Spartina alterniflora (Loisel.) following long-term decomposition in sea water. Sci. Total Environ. 83:273–285.

    Google Scholar 

  • Greenway, M. 1995. Trophic relationships of macrofauna within a Jamaican seagrass meadow and the role of the echinoid Lytechinus variegatus (Lamarck). Bull. Mar. Sci. 56:719–736.

    Google Scholar 

  • Hamilton, J. G., Zangerl, A. R., Delucia E. H., and Berenbaum, M. R. 2002. The carbon-nutrient balance hypothesis: its rise and fall. Ecol. Lett. 4:86–95.

    Google Scholar 

  • Hammerschmidt, R. and Smith-baker, J. A. 1999. Roles of salicylic acid in disease resistance, pp. 37–54, in A. A. Agrawal, S. Tuzun, and E. Bent (eds.). Induced Plant Defenses Against Pathogens and Herbivores: Biochemistry, Ecology, and Agriculture. APS Press, St. Paul, Minnesota.

    Google Scholar 

  • Hammerstrom, K., Dethier, M. N., and Duggins, D.O. 1998. Rapid phlorotannin induction and relaxation in five Washington kelps. Mar. Ecol. Prog. Ser. 165:293–305.

    Google Scholar 

  • Harrison, P. G. 1982. Control of microbial growth and of amphipod grazing by water-soluble compounds from the leaves of Zostera marina. Mar. Biol. 67:225–230.

    Google Scholar 

  • Harrison, P. G. and Chan, A. T. 1980. Inhibition of the growth of micro-algae and bacteria by extracts of eelgrass (Zostera marina) leaves. Mar. Biol. 61:21–26.

    Google Scholar 

  • Harrison, P. G. and Durance, C. 1989. Reductions in photosynthetic carbon uptake in epiphytic diatoms by water-soluble extracts of leaves of Zostera marina. Mar. Biol. 90:117–119.

    Google Scholar 

  • Hay, M. E. and Steinberg, P. D. 1992. The chemical ecology of plant-herbivore interactions in marine vs. terrestrial communities, p. 271–413, in (eds. G. A. Rosenthal and M. Berenbaum) Herbivores: Their Interactions with Secondary Plant Metabolites, Volume II Evolutionary and Ecological Processes & Academic Press, New York.

    Google Scholar 

  • Heck, K. L. and Valentine, J. F. 1995. Sea urchin herbivory: evidence for long-lasting effects in subtropical seagrass meadows. J. Exp. Mar. Biol. Ecol. 189:205–217.

    Google Scholar 

  • Herrmann, K. 1995. The shikimate pathway as an entry into aromatic secondary metabolism. Plant Physiol. 107:7–12.

    Google Scholar 

  • Jones, C. G. and Hartley, S. E. 1999. A protein competition model of phenolic allocation. Oikos 86:27–44.

    Google Scholar 

  • Kathiresan, K. 1992. Foliovory in Pichavaram mangroves. Environ. Ecol. 10:988–989.

    Google Scholar 

  • Kimura, M. and Wada, H. 1989. Tannins in mangrove tree roots and their role in the root environment. Soil Sci. Plant Nutr. 35:101–108. 1932 ARNOLD AND TARGETT

    Google Scholar 

  • Kubek, D. J. and Shuler, M. L. 1980. The effect of variations in carbon and nitrogen concentrations on phenolics formation in plant cell suspension cultures. J. Nat. Prod. 43:87–96.

    Google Scholar 

  • Kupper, F. C., Kloareg, B., Guern, J., and Potin, P. 2001. Oligoguluronates elicit an oxidative burst in the brown algal kelp Laminaria digitata. Plant Physiol. 125:278–291.

    Google Scholar 

  • Lavola, A., Julhunen–tiito, R., De La Rosa, T. M., Lehto, T., and Aphalo, P. J. 2000. Allocation of carbon to growth and secondary metabolites in brich seedlings under UV-B radiation and CO2 exposure. Physiol. Plant. 109:260–267.

    Google Scholar 

  • Legaz, M. E., Vicente, C., and Filho, X. L. 1985. The occurrence of lichen phenolics and their catabolites in a free-living alga, Lobophora variegata (Phaeophyta). Cryptogamie: Algol. 6:265–272.

    Google Scholar 

  • Liu, L. and McClure, J.W. 1995. Effects of UV-B on activities of enzymes of secondary metabolism in barley primary leaves. Physiol. Plant. 93:734–739.

    Google Scholar 

  • Macia, S. 2000. The effects of sea urchin grazing and drift algal blooms on a subtropical seagrass bed community. J. Exp. Mar. Biol. Ecol. 246:53–67.

    Google Scholar 

  • McMillian, C. Zapata, O., and Escobar, L. 1980. Sulphated phenolic compounds in seagrasses. Aquat. Bot. 8:267–278.

    Google Scholar 

  • Micheli, F. 1993. Feeding ecology of mangrove crabs in northeastern Australia: Mangrove litter consumption by Sesarma messa and Sesarma smithii. J. Exp. Mar. Biol. Ecol. 171:165–186.

    Google Scholar 

  • Muday, G. K. and Herrmann, K.M. 1992. Wounding induces one of two isoenzymes of 3-deoxy-Darabino-heptulosonate 7-phosphate synthase in Solanum tuberosum L. Plant Physiol. 98:496–500.

    Google Scholar 

  • Muelstein, L.K. 1988. Labyrinthula sp., a marine slime mold producing symptoms of wasting disease in eelgrass, Zostera marina. Mar. Biol. 99:465–472.

    Google Scholar 

  • Muehlstein, L. L. 1992. The host-pathogen interaction in the wasting disease of eelgrass, Zostera marina. Can. J. Bot. 70:2081–2088.

    Google Scholar 

  • Nicholson, R. L. and Hammerschmidt, R. 1992. Phenolic compounds and their role in disease resistance. Annu. Rev. Phytopathol. 30:369–389.

    Google Scholar 

  • Packter, N. M. 1980. Characterization of subspecies from a fungal fatty acid synthetase. Biochim. Biophys. Acta 615:497–508.

    Google Scholar 

  • Pavia, H. and Brock, E. 2000. Extrinsic factors influencing phlorotannin production in the brown alga Ascophyllum nodosum. Mar. Ecol. Prog. Ser. 193:285–294.

    Google Scholar 

  • Pavia, H. and Toth, G. 2000. Inducible chemical resistance to herbivory in the brown seaweed Ascophyllum nodosum. Ecology 81:3212–3225.

    Google Scholar 

  • Pavia, H. Cervin, G., Lindgren, A., and Aberg, P. 1997. Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum. Mar. Ecol. Prog. Ser. 157:139–146.

    Google Scholar 

  • Pennings, S. C., Siska, E. L., and Bertness, M. D. 2001. Latitudinal differences in plant palatability in Atlantic coast salt marshes. Ecology 82:1344–1359.

    Google Scholar 

  • Quackenbush, R. C., Bunn, D., and Lingren, W. 1986. HPLC determination of phenolic acids in the water-soluble extract of Zostera marina L. (eelgrass). Aquat. Bot. 24: 83–89.

    Google Scholar 

  • Ragan, M. A. and Craigie, J. S. 1976. Physodes and the phenolic compounds of brown algae. Isolation and characterization of phloroglucinol polymers from Fucus vesiculosus (L.). Can. J. Biochem. 54:66–73.

    Google Scholar 

  • Ragan, M. A. and Glombitza, K.-W. 1986. Phlorotannins, brown algal polyphenols. Prog. Phycol. Res. 4:130–241.

    Google Scholar 

  • Ravn, H. C., Andary, C., Kovacs, G., and Molgaard, P. 1989. Caffeic acid esters as in vitro inhibitors of plant pathogenic bacteria and fungi. Biochem. Syst. Ecol. 17:175–184.

    Google Scholar 

  • Ravn, H., Pedersen, M. F., Borum, J, Andary, C., Anthoni, U., Christpherson, C., and Nielsen, P. H. 1994. Seasonal variation and distribution of two phenolics compounds, rosmarinic acid and caffeic acid, in leaves and roots-rhizomes of eelgrass (Zostera marina L.). Ophelia 40:51–61.

    Google Scholar 

  • Reynolds, K. A. 1998. Combinational biosynthesis: Lesson learned from nature. Proc. Natl. Acad. Sci.USA 95:12744–12746.

    Google Scholar 

  • Richardson, C. J., Ferrell, G. M., and Vaithiyanathan, P. 1999. Nutrient effects on stand structure, resorption efficiency, and secondary compounds in Everglades sawgrass. Ecology 80:2182–2192.

    Google Scholar 

  • Schoenwaelder, M. E. A. and Clayton, M. N. 1999. The presence of phenolic compounds in isolated cell walls of brown algae. Phycologia 38:161–166.

    Google Scholar 

  • Seigler, D. S. 1998. Plant Secondary Metabolism. Kluwer Academic Publishing, Norwell Massachusetts.

    Google Scholar 

  • Short, F. T., Mathieson, A. C., and Nelson, J. I. 1986. Reoccurrence of the eelgrass wasting disease at the border of New Hampshire and Maine, USA. Mar. Ecol. Prog. Ser. 29:89–92.

    Google Scholar 

  • Singh, B. K., Siehl, D., and Connelly, J. A. 1991. Shikimate pathway: why does it mean so much to so many? Oxford Surveys Plant Mol. Cell. Biol. 7:143–185.

    Google Scholar 

  • Steinberg, P. D. and Van Altena, I. 1992. Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecol. Monogr. 62:189–222.

    Google Scholar 

  • Steinke, T. D., Rajh, A., and Holland, A. J. 1993. The feeding behavior of the red mangrove crab Sesarma meinerti De Man and its effect on the degradation of mangrove leaf litter. S. Afr. J. Mar. Sci. 13:151–160.

    Google Scholar 

  • Stern, J. L., Hagerman, A. E., Steinber, P. D., and Mason, P. K. 1996. Phlorotannin–protein interactions. J. Chem. Ecol. 22:1877–1899.

    Google Scholar 

  • Targett, N. M. and Arnold, T. M. 1998. Predicting the effects of brown algal phlorotannins on marine herbivores in tropical and temperate oceans. J. Phycol. 34:195–205.

    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 lattitudinal trend. Oecologia 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 

  • Thayer, G. W., Bjorndal, K. A., Ogden, J. C., Williams, S. L., and Zieman, J. C. 1984. Role of larger herbivores in seagrass communities. Estuaries 7:351–376.

    Google Scholar 

  • Toth, G. B. and Pavia, H. 2000. Water-borne cues induce chemical defense in marine algal (Ascophyllum nodosum). Proc. Natl. Acad. Sci.USA 97:14418–14420.

    Google Scholar 

  • Valentine, J. F. and Heck, K. L. 1991. The role of sea urchin grazing in regulating subtropical seagrass meadows: Evidence from field manipulations in the northern Gulf of Mexico. J. Exp. Mar. Biol. Ecol. 154:215–230.

    Google Scholar 

  • Valentine, J. F. and Heck, K. L. 2001. The role of leaf nitrogen content in determining turtlegrass (Thalassia testudinum) grazing by a generalized herbivore in the northeastern Gulf of Mexico. J. Exp. Mar. Biol. Ecol. 258:65–86.

    Google Scholar 

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

    Google Scholar 

  • Van Alstyne, K. L. 1989. Adventitious branching as a herbivore-induced defense in the intertidal brown alga Fucus distichus. Mar. Ecol. Prog. Ser. 56:169–176.

    Google Scholar 

  • Van Alstyne, K. L. 1990. Effects of wounding by the herbivorous snails Littorina sitkana and L. scutlata (Mollusca) on the growth and reproduction of the intertidal alga Fucus distichus (Phaeophyta). J. Phycol. 26:412–416.

    Google Scholar 

  • Van Alstyne, K. L., Dethier, M. N., and Duggins, D. O. 2001. Spatial patterns in macroalgal chemical defenses, pp. 301–324 in J. B. McClintock and B. J. Baker (eds). Marine Chemical Ecology. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Vergeer, L. H. T. and Denhartog, C. 1994. Omnipresence of Labyrinthulaceae in seagrasses. Aquat. Bot. 45:1–20.

    Google Scholar 

  • Vergeer, L. H. T. and Develi, A. 1997. Phenolic acids in healthy and infected leaves Zostera marina and their growth-limiting properties towards Labyrinthula zosterae. Aquat. Bot. 58:65–72. 1934 ARNOLD AND TARGETT

    Google Scholar 

  • Vergeer, L. H. T., Aarts, T. L., and De Groot. J. D. 1995. The wasting disease and the effects of abiotic factors (light intensity, temperature, salinity) and infection with Labyrinthula zosterae on the phenolic content of Zostera marina shoots. Aquat. Bot. 52:35–44.

    Google Scholar 

  • Wecker, M., Strong, D., and Grevstad, F. 2000. Integrating biological control in the integrated pest management program for Spartina alterniflora in Willapa Bay J. Shellfish Res. 19:634.

    Google Scholar 

  • Wilson, J. O., Buchsbaum, R., Valiela, I., and Swain, T. 1986. Decomposition in salt marsh ecosystems: phenolic dynamics during decay of litter of Spartina alterniflora. Mar. Ecol. Prog. Ser. 29:177–187.

    Google Scholar 

  • Zieman, J. C. and Zieman, R. T. 1989. Ecology of the seagrass meadows of the west coast of Florida: A community profile. Biological Report US Fish and Wildlife Service, 168 pp.

  • Zieman, J. C., Fourqurean, J. W., and Frankovich, T. A. 1999. Seagrass Die-off in Florida Bay: Long-term Trends in Abundance and Growth of Turtle Grass, Thalassia testudinum. Estuaries 22:460–470.

    Google Scholar 

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Arnold, T.M., Targett, N.M. Marine Tannins: The Importance of a Mechanistic Framework for Predicting Ecological Roles. J Chem Ecol 28, 1919–1934 (2002). https://doi.org/10.1023/A:1020737609151

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