Journal of Chemical Ecology

, Volume 26, Issue 6, pp 1393–1410 | Cite as

Evidence for Metabolic Turnover of Polyphenolics in Tropical Brown Algae

  • Thomas M. Arnold
  • Nancy M. Targett

Abstract

Polyphenolic chemical defenses of plants have traditionally been classified as immobile or quantitative and as such are believed to have low to negligible rates of turnover. This assumption is an important element in many ecological theories of chemical defense that invoke cost versus benefit relationships, because (1) turnover increases the metabolic cost of maintaining an effective level of defense, and (2) changes in the rate of turnover could affect the conclusions of studies that rely upon static concentration (standing crop) measurements, since changes in compound synthesis may not emerge as corresponding changes in compound concentration. By using a stable-isotope labeling technique, we measured rates of synthesis and turnover for the polyphenolic compounds of marine brown algae in laboratory and field experiments. During the laboratory experiment, we observed the relatively rapid turnover of phlorotannins in a population of the tropical brown alga Lobophora variegata. In order to determine if such metabolic turnover in brown algae occurred under natural conditions, we then measured in situ rates of synthesis, polymerization, and turnover for extractable phlorotannins in two species of tropical marine brown algae, Sargassum hystrix var. buxifolium (Fucales) and Dictyopteris justii (Dictyotales), over a 17-day period in the field. We found that phlorotannins in L. variegata and S. hystrix var. buxifolium demonstrated rapid rates of turnover in laboratory culture and in situ field experiments, respectively. The trends for D. justii also support the presence of turnover. Results indicate that (1) the assumption that algal polyphenolics can be grouped with the tannins of vascular plants as "immobile" defenses needs to be reevaluated, (2) estimates of the metabolic cost of algal polyphenolics that presume negligible rates of turnover may significantly underestimate the total cost of defense, and (3) studies designed to test the predictions of ecological theories for the phlorotannin concentrations of tropical brown algae may be affected by changes in the rates of metabolic turnover.

Brown algae chemical defense Dictyoperis justii Lobophora variegata metabolic turnover phlorotannins polyphenols Sargassum hystrix 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

REFERENCES

  1. Arnold, T. M., and Targett, N. M. 1998. Quantifying in situ rates of phlorotannin synthesis and polymerization in marine brown algae. J. Chem. Ecol. 24:577–595.Google Scholar
  2. 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
  3. Boettcher, A. A., and Targett, N. M. 1993. Role of polyphenolic molecular size in the reduction of assimilation efficiency in Xiphister mucosus. Ecology 74:891–903.Google Scholar
  4. 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
  5. Carlson, D. J., and Carlson, M. L. 1984. Reassessment of exudation by fucoid macroalgae. Limnol. Oceanogr. 29:1077–1087.Google Scholar
  6. Clayton, M. N., and Ashburner, C. M. 1994. Secretion of phenolic bodies following fertilization in Durvillaea potatorum (Durvillaeales, Phaeophyta) Eup. J. Phycol. 29:1–9.Google Scholar
  7. Coen L. C., and Tanner, C. E. 1989. Morphological variation and differential susceptibility to herbivory in the tropical brown algae Lobophora variegata. Mar. Ecol. Prog. Ser., 54:287–298.Google Scholar
  8. Coley, P. D., Bryant, J. P., and Chapin, F. S., III. 1985. Resource availability and plant antiherbivory defense. Science 230:895–899.Google Scholar
  9. Craigie, J. S., and Mclachlan, J. 1964. Excretion of colored ultraviolet-absorbing substances by marine algae. Can. J. Bot. 42:23–33.Google Scholar
  10. Cronin, G., and Hay, M. E. 1996. Effects of light and nutrient availability on the growth, secondary chemistry, and resistance to herbivory of two brown seaweeds. Oikos 7:93–106.Google Scholar
  11. Denton, A., Chapman, A. R. O., and Markham, J. 1990. Size specific concentration of phlorotannins (anti-herbivore compounds) in three species of Fucus. Mar. Ecol. Prog. Ser. 65:103–104.Google Scholar
  12. Fagerstrom, T. 1989. Anti-herbivore chemical defense in plants: A note of the concept of cost. Am. Nat. 133:281–287.Google Scholar
  13. Geiselman, J. A., and Mcconnell, O. J. 1981. Polyphenols in the brown algae Fucus vesiculosus and Ascophyllum nodosum: Chemical defenses against the marine herbivorous snail, Littorina littorea. J. Chem. Ecol. 7:1115–1133.Google Scholar
  14. 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
  15. Hammerstrom, K., Dethier, M. N., and Duggins, D. O. 1998. Rapid phlorotannin induction and relaxation in five Washington kelps. Mar. Ecol. Prog. Ser. 165:293–305Google Scholar
  16. 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
  17. 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
  18. Jennings, J. G., and Steinberg, P. D. 1994. In situ exudation of phlorotannins by the sublittoral kelp Ecklonia radiata. Mar. Biol. 121:349–354.Google Scholar
  19. Jensen, A. 1959. Understokelser I forbindelse med produksjon av tangmel. Morsk Inst. For Tnag-og Tareforsk. Forelob. Rapp. 83:1–11.Google Scholar
  20. Langlois, G. A. 1975. Effect of algal exudates on substratum selection by motile telotrochs of the marine peritrich ciliate Vortivella marina. J. Protozool. 22:115–123.Google Scholar
  21. Lapointe, B. E. 1989. Macroalgal production and nutrient relations in oligotrophic areas of Florida Bay. Bull. Mar. Sci. 44:312–323.Google Scholar
  22. Mihiliak, C. A., Gershenzon, J., and Croteau, R. 1991. Lack of rapid monoterpene turnover in rooted plants: Implications for theories of plant chemical defense. Oecologia 87:373–376.Google Scholar
  23. 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 Marine Sciences. Smithsonian Institute Press, Washington, D.C.Google Scholar
  24. 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
  25. Peckol, P., Krane, J. M., and Yates, J. L. 1996. Interactive effects of inducible defense and resource availability on the phlorotannins in the North Atlantic brown alga Fucus vesiculosus. Mar. Ecol. Prog. Ser. 138:209–217.Google Scholar
  26. Pederson, A. 1984. Studies on phenol content and heavy metal uptake in fucoids. Hydrobiologia 116 /117:498–504.Google Scholar
  27. Pfister, C. A. 1992. Costs of reproduction in the kelp: Patterns of allocation and life history consequences. Ecology 73:1586–1596.Google Scholar
  28. Prince, J. S., and O'neal, S. W. 1979. The ecology of Sargassum pteropleuron Grunow (Phaeophyceae, Fucales) in the waters off South Florida I. Growth, reproduction, and population structure. Phycologia 18:109–114.Google Scholar
  29. 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.Google Scholar
  30. Ragan, M. A. and 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. 30:209–221.Google Scholar
  31. Ragan, M., and Jensen, A. 1979. Quantitative studies on brown algal phenols: Light-mediated exudation of polyphenols from Ascophyllum nodosum ( L.) Le Jol. J. Exp. Mar. Biol. Ecol. 36:91–101.Google Scholar
  32. 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
  33. Sattler, E. 1974. Ein neuer Typ gerbstoffhaltiger Polyphenole aus der Braunalge Halidrys siliquosa. Dissertation, Bonn, 108 pp.Google Scholar
  34. Schoenwaelder, M. E. A., and Clayton, M. N. 1998. The secretion of phenolic compounds following fertilization in Acrocarpia paniculata ( Fucales, Phaeophyta) Phycologia 37:40–46.Google Scholar
  35. Schoenwaelder, M. E. A., and Clayton, M. N. 1999. The presence of phenolics compounds in isolated cell walls of brown algae. Phycologia 38:161–166.Google Scholar
  36. Sharp, J. H. 1973. A quick and simple measurement for total inorganic carbon in seawater. In: Research on the Marine Food Chain. Progress report to the U.S. Atomic Energy Commission. University of California, Institute of Marine Resources, pp. 143–144.Google Scholar
  37. Sieburth, J. MCN. 1969. Studies on algal substances in the sea. III. The production of extracellular organic matter by littoral marine algae. J. Exp. Mar. Biol. Ecol. 3:290–309.Google Scholar
  38. Sieburth, J. MCN., and Jensen, A. 1969. Studies on algal substances in the sea. II. The formation of gelbstoff (humic material) by exudates of Phaeophyta. J. Exp. Mar. Biol. Ecol. 3:275–289.Google Scholar
  39. Steinberg, P. D. 1984. Algal chemical defense against herbivores: Allocation of phenolic compounds in the kelp Alaria marginata. Science 223:405–407.Google Scholar
  40. Steinberg, P. D. 1992. 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.Google Scholar
  41. Steinberg, P. D. 1995. Seasonal variation in the relationship between growth rate and phlorotannin production in the kelp Ecklonia radiata. Oecologia 102:169–181.Google Scholar
  42. Stern, J. L., Hagerman, A. E., Steinberg, P. D., and Mason, P. K. 1996. Phlorotannin-protein interactions. J. Chem. Ecol. 22:1877–1899.Google Scholar
  43. Targett, N. M., and Arnold, T. M. 1998. Predicting the effects of brown algal phlorotannin on marine herbivores in tropical and temperate oceans. J. Phycol. 34:195–205.Google Scholar
  44. Targett, N. M., Coen, L. C., Boettcher, A. A., and Tanner, C. E. 1992. Biogeographic comparisons of marine algal polyphenolic: Evidence against a latitudinal trend. Oecologia. 89:464–470.Google Scholar
  45. Targett, N. M., Boettcher, A. A., Targett, T. E., and Vrolick, N. H. 1995. Tropical marine herbivore assimilation of phenolic-rich plants. Oecologia 103:170–179.Google Scholar
  46. 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 plantdefense theory. J. Exp. Mar. Biol. Ecol. 129:219–230.Google Scholar
  47. Tuomi, J., Ilvessalo, H., Miemela, P., Siren, S., and Jormalainen, V. 1989. Within-plant variation in phenolic content and toughness of the brown alga Fucus vesiculosus L. Bot. Mar. 32:505–509.Google Scholar
  48. Van alstyne, K. L. 1988. Grazing increases polyphenolic defenses in the intertidal brown alga Fucus distichus. Ecology 69:655–663.Google Scholar
  49. Wille, N. 1897. Beitrage zur physiologischen Anatomie der Laminariaceen. Festskr. H.m. Oscar II Reg.-Jub., K. norsk. Fredericks Univ. Christiana 2, Sec. E, No. 4, pp. 1–70.Google Scholar
  50. 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
  51. Zavodnik, N. 1981. Studies on phenolic content of some brown algae from Adriatic Sea. Proc. Int. Seaweed Symp. 10:543–548.Google Scholar
  52. Zavodnik, N., and Jensen, A. 1981. Studies on phenolic compounds of some brown algae. Proc. Int. Seaweed Symp. 8:655–660.Google Scholar

Copyright information

© Plenum Publishing Corporation 2000

Authors and Affiliations

  • Thomas M. Arnold
    • 1
  • Nancy M. Targett
    • 1
  1. 1.Graduate College of Marine StudiesUniversity of DelawareLewes
  2. 2.Pesticide Research LabPenn State University, State College

Personalised recommendations