Skip to main content
Log in

Chemical Defenses Promote Persistence of the Aquatic Plant Micranthemum umbrosum

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Five of the most common macrophytes from an aquaculture facility with high densities of the herbivorous Asian grass carp (Ctenopharyngodon idella) were commonly unpalatable to three generalist consumers—grass carp and the native North American crayfishes Procambarus spiculifer and P. acutus. The rooted vascular plant Micranthemum umbrosum comprised 89% of the total aboveground plant biomass and was unpalatable to all three consumers as fresh tissues, as homogenized pellets, and as crude extracts. Bioassay-guided fractionation of the crude extract from M. umbrosum led to four previously known compounds that each deterred feeding by at least one consumer: 3,4,5-trimethoxyallylbenzene (1) and three lignoids: β-apopicropodophyllin (2); (−)-(3S,4R,6S)-3-(3′,4′-methylenedioxy-α-hydroxybenzyl)-4-(3″,4″-dimethoxybenzyl)butyrolactone (3); and (−)-hibalactone (4). None of the remaining four macrophytes produced a chemically deterrent extract. A 16-mo manipulative experiment showed that the aboveground biomass of M. umbrosum was unchanged when consumers were absent, but the biomass of Ludwigia repens, a plant that grass carp preferentially consumed over M. umbrosum, increased over 300-fold. Thus, selective feeding by grass carp effectively eliminates most palatable plants from this community and promotes the persistence of the chemically defended M. umbrosum, suggesting that plant defenses play critical yet understudied roles in the structure of freshwater plant communities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ban, H. S., Lee, S., Kim, Y. P., Yamaki, K., Shin, K. H., and Ohuchi, K. 2002. Inhibition of prostaglandin E-2 production by taiwanin C isolated from the root of Acanthopanax chiisanensis and the mechanism of action. Biochem. Pharmacol. 64:1345–1354.

    Article  PubMed  CAS  Google Scholar 

  • Bolser, R. C., Hay, M. E., Lindquist, N., Fenical, W., and Wilson, D. 1998. Chemical defenses of freshwater macrophytes against crayfish herbivory. J. Chem. Ecol. 24:1639–1658.

    Article  CAS  Google Scholar 

  • Bradford, M. M. 1976. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 72:248–254.

    Article  PubMed  CAS  Google Scholar 

  • Cho, J. Y., Park, J., Kim, P. S., Yoo, E. S., Baik, K. U., and Park, M. H. 2001. Savinin, a lignan from Pterocarpus santalinus inhibits tumor necrosis factor-alpha production and T cell proliferation. Biol. Pharm. Bull. 24:167–171.

    Article  PubMed  CAS  Google Scholar 

  • Creed, R. P. 1994. Direct and indirect effects of crayfish grazing in a stream community. Ecology 75:2091–2103.

    Article  Google Scholar 

  • Cronin, G. 1998. Influence of macrophyte structure, nutritive value, and chemistry on the feeding choices of a generalist crayfish, pp 169–174, in E. Jeppesen, M. Sondergaard, M. Sondergaard, and K. Christoffersen (eds.). The Structuring Role of Submerged Macrophytes in Lakes. Springer, New York.

    Google Scholar 

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

  • Cronin, G., Lindquist, N., Hay, M. E., and Fenical, W. 1995. Effects of storage and extraction procedures on yields of lipophilic metabolites from the brown seaweeds Dictyota ciliolata and D. menstrualis. Mar. Ecol. Prog. Ser. 119:265–273.

    Article  Google Scholar 

  • Cronin, G., Lodge, D. M., Hay, M. E., Miller, M., Hill, A. M., Horvath, T., Bolser, R. C., Lindquist, N., and Wahl, M. 2002. Crayfish feeding preferences for fresh water macrophytes: The influence of plant structure and chemistry. J. Crust. Biol. 22:708–718.

    Article  Google Scholar 

  • Cruz-Rivera, E. and Hay, M. E. 2003. Prey nutritional quality interacts with chemical defenses to affect consumer feeding and fitness. Ecol. Monogr. 73:483–506.

    Article  Google Scholar 

  • Cyr, H. and Pace, M. L. 1993. Magnitude and patterns of herbivory in aquatic and terrestrial ecosystems. Nature 361:148–150.

    Article  Google Scholar 

  • De Vincenzi, M., De Vincenzi, A., and Silano, M. 2004. Constituents of aromatic plants: elemicin. Fitoterapia 75:615–618.

    Article  PubMed  CAS  Google Scholar 

  • Della-Greca, M., Monaco, P., Pollio, A., and Previtera, L. 1992. Structure activity relationships of phenylpropanoids as growth inhibitors of the green alga Selenastrum capricornutum. Phytochemistry 31:4119–4123.

    Article  CAS  Google Scholar 

  • Dorn, N. J. and Wojdak, J. M. 2004. The role of omnivorous crayfish in littoral communities. Oecologia 140:150–159.

    Article  PubMed  Google Scholar 

  • Duffy, J. and Hay, M. 1991. Food and shelter as determinants of food choice by an herbivorous marine amphipod. Ecology 72:1286–1298.

    Article  Google Scholar 

  • Duffy, J. and Paul, V. 1992. Prey nutritional quality and the effectiveness of chemical defenses against tropical reef fishes. Oecologia 90:333–339.

    Article  Google Scholar 

  • Faulkner, D. J. 2002. Marine natural products. Nat. Prod. Rep. 19:1–48.

    PubMed  CAS  Google Scholar 

  • Hartwell, J. L., Johnson, J. M., Fitzgerald, D. B., and Belkin, M. 1953. Podophyllotoxin from Juniperus species—savinin. J. Am. Chem. Soc. 75:235–236.

    Article  CAS  Google Scholar 

  • Hay, M. E. 1996. Marine chemical ecology: What's known and what's next? J. Exp. Mar. Biol. Ecol. 200:103–134.

    Article  CAS  Google Scholar 

  • Hay, M. E. 1997. The ecology and evolution of seaweed–herbivore interactions on coral reefs. Coral Reefs 16:S67–S76.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hay, M. and Fenical, W. 1996. Chemical ecology and marine biodiversity: insights and products from the sea. Oceanography 9:10–20.

    Google Scholar 

  • Hay, M., Fenical, W., and Gustafson, K. 1987. Chemical defense against diverse coral reef herbivores. Ecology 68:1581–1591.

    Article  CAS  Google Scholar 

  • Hay, M., Stachowicz, J., Cruz-Rivera, E., Bullard, S., Deal, M., and Lindquist, N. 1998. Bioassays with marine and freshwater macroorganisms, pp. 39–141, in K. Haynes and J. Millar (eds.). Methods in Chemical Ecology. Chapman and Hall, New York.

    Google Scholar 

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

    Article  Google Scholar 

  • Hickling, C. F. 1966. On the feeding process in the white amur, Ctenopharyngodon idella. J. Zool. 148:408–419.

    Article  Google Scholar 

  • Hobbs, H. H. 1981. The Crayfishes of Georgia. Smithsonian Institution, Washington, DC.

    Google Scholar 

  • Hutchinson, G. E. 1975. A Treatise on Limnology: Limnological Botany. Wiley, New York.

    Google Scholar 

  • Koricheva, J. 2002. Meta-analysis of sources of variation in fitness costs of plant antiherbivore defenses. Ecology 83:176–190.

    Article  Google Scholar 

  • Kubanek, J., Fenical, W., Hay, M. E., Brown, P. J., and Lindquist, N. 2000. Two antifeedant lignans from the freshwater macrophyte Saururus cernuus. Phytochemistry 54:281–287.

    Article  PubMed  CAS  Google Scholar 

  • Kubanek, J., Hay, M. E., Brown, P. J., Lindquist, N., and Fenical, W. 2001. Lignoid chemical defenses in the freshwater macrophyte Saururus cernuus. Chemoecology 11:1–8.

    Article  CAS  Google Scholar 

  • Lodge, D. M. 1991. Herbivory on freshwater macrophytes. Aquat. Bot. 41:195–224.

    Article  Google Scholar 

  • Lodge, D. and Lorman J. 1987. Reductions in submersed macrophyte biomass and species richness by the crayfish Orconectes rusticus. Can. J. Fish. Aquat. Sci. 44:591–597.

    Article  Google Scholar 

  • Lodge, D., Kershner, M., Aloi, J., and Covich, A. 1994. Effects of an omnivorous crayfish (Orconectes rusticus) on a fresh-water littoral food-web. Ecology 75:1265–1281.

    Article  Google Scholar 

  • Lodge, D., Cronin, G., Donk, E. V., and Froelich, A. 1998. Impact of herbivory on plant standing crop: Comparisons among biomes, between vascular and nonvascular plants, and among freshwater herbivore taxa, pp. 149–174, in E. Jeppesen, M. Sondergaard, M. Sondergaard, and K. Christofferson (eds.). The Structuring Role of Submerged Macrophytes in Lakes. Springer, New York.

    Google Scholar 

  • Lodge, D. M., Taylor, C. A., Holdich, D. M., and Skurdal, J. 2000. Nonindigenous crayfishes threaten North American freshwater biodiversity: lessons from Europe. Fisheries 25:7–20.

    Article  Google Scholar 

  • Marston, A., Hostettmann, K., and Msonthi, J. D. 1995. Isolation of antifungal and larvicidal constituents of Diplolophium buchanani by centrifugal partition chromatography. J. Nat. Prod. 58:128–130.

    Article  PubMed  CAS  Google Scholar 

  • Matsubara, H. 1972. Studies on synergists for insecticides. XXVII. On synergistic effect of several lignans on pyrethrins and allethrin. Bull. Inst. Chem. Res. 50:197–250.

    CAS  Google Scholar 

  • McKnight, S. K. and Hepp, G. R. 1995. Potential effect of grass carp herbivory on waterfowl foods. J. Wildl. Manage. 59:720–727.

    Article  Google Scholar 

  • Miyazawa, M., Ishikawa, Y., Toshikura, M., and Kameoka, H. 1992. Insecticidal allylbenzenes from Asiasarum heterotropoides Meak. var mandshuricum Meak. Chem. Express 7:69–72.

    CAS  Google Scholar 

  • Newman, R. M. 1991. Herbivory and detritivory on freshwater macrophytes by invertebrates—a review. J. N. Am. Benthol. Soc. 10:89–114.

    Article  Google Scholar 

  • Newman, R., Kerfoot, W., and Hanscom, Z. 1990. Watercress and amphipods—potential chemical defense in a spring stream macrophyte. J. Chem. Ecol. 16:245–259.

    Article  CAS  Google Scholar 

  • Newman, R. M., Kerfoot, W. C., and Hanscom, Z. 1996. Watercress allelochemical defends high-nitrogen foliage against consumption: effects on freshwater invertebrate herbivores. Ecology 77:2312–2323.

    Article  Google Scholar 

  • Novelo, M., Cruz, J. G., Hernandez, L., Peredmiranda, R., Chai, H. Y., Mar, W., and Pezzuto, J. M. 1993. Cytotoxic constituents from Hyptis verticillata. 6. Chemical studies on Mexican Hyptis species and biologically active natural products from Mexican medicinal plants. J. Nat. Prod. 56:1728–1736.

    Article  PubMed  CAS  Google Scholar 

  • Ostrofsky, M. and Zettler, E. 1986. Chemical defenses in aquatic plants. J. Ecol. 74:279–287.

    Article  CAS  Google Scholar 

  • Parker, J. D. and Hay, M. E. 2005. Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol. Lett. 8:959–967.

    Article  Google Scholar 

  • Pelter, A., Ward, R. S., Pritchard, M. C., and Kay, I. T. 1988. Synthesis of lignans related to the podophyllotoxin series. J. Chem. Soc.-Perkin Trans. 1:1603–1613.

    Article  Google Scholar 

  • Prusak, A. C., O'Neal, J., and Kubanek, J. 2005. Prevalence of chemical defenses among freshwater macrophytes. J. Chem. Ecol. 31:1145–1160.

    Article  PubMed  CAS  Google Scholar 

  • Rosenthal, G. A. and Berenbaum, M. R. (eds.). 1992. Herbivores: Their Interactions with Secondary Metabolites: Evolutionary and Ecological Processes. Academic Press, San Diego.

  • Seigler, D. S. 1998. Plant Secondary Metabolism. Kluwer Academic Publishers, Norwell, MA.

    Google Scholar 

  • Shelford, V. W. 1918. Conditions of existence, pp. 21–60, in H. B. Ward and G. C. Whipple (eds.). Freshwater Biology. Wiley, New York.

    Google Scholar 

  • Taylor, R. B., Lindquist, N., Kubanek, J., and Hay, M. E. 2003. Intraspecific variation in palatability and defensive chemistry of brown seaweeds: effects on herbivore fitness. Oecologia 136:412–423.

    Article  PubMed  Google Scholar 

  • USGS. 2005. Nonindigenous Aquatic Species Database [WWW Document]. URLhttp://nas.er.usgs.gov.

  • Van Dyke, J. M., Leslie, A. J., and Nall, L. E. 1984. The effects of the grass carp on the aquatic macrophytes of four Florida Lakes. J. Aquat. Plant Manage. 22:87–95.

    Google Scholar 

  • Ward, R. S. 1999. Lignans, neolignans and related compounds. Nat. Prod. Rep. 16:75–96.

    Article  CAS  Google Scholar 

  • Warner, G. F. and Green, E. I. 1995. Choice and consumption of aquatic weeds by signal crayfish (Pacifastacus leniusculus). Freshw. Crayfish 8:360–363.

    Google Scholar 

  • Wilson, D. M., Fenical, W., Hay, M., Lindquist, N., and Bolser, R. 1999. Habenariol, a freshwater feeding deterrent from the aquatic orchid Habenaria repens (Orchidaceae). Phytochemistry 50:1333–1336.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Paul Williams of the Owen and Williams Fish Hatchery for supplying grass carp, macrophytes, and the observations about fish feeding. L. Stefaniak trained the grass carp for feeding assays; D. Burkepile and W. Morrison assisted with the caging experiment. This work was supported by the National Science Foundation (Integrative Graduate Education and Research Traineeship Program), the Harry and Linda Teasley endowment to Georgia Tech, the National Park Service, and the Mid-South Aquatic Plant Management Society. D.O.C. was supported by the Henry and Camille Dreyfus Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mark E. Hay.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Parker, J.D., Collins, D.O., Kubanek, J. et al. Chemical Defenses Promote Persistence of the Aquatic Plant Micranthemum umbrosum . J Chem Ecol 32, 815–833 (2006). https://doi.org/10.1007/s10886-006-9038-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-006-9038-7

Keywords

Navigation