Abstract
Very few studies have shown experimentally that plant chemical defenses actually reduce the performance of individual mammalian herbivores, much less the density of mammalian populations. We investigated the effects of representatives of three classes of plant phenoiics on the survival and growth of prairie voles by incorporating the compounds into artificial diets and feeding them to weanlings for three weeks. At low levels of protein, both quercetin (a flavonoid) and tannic acid (a hydrolyzable tannin) caused reduced growth rates; no effect occurred at high levels of protein. Quebracho (a condensed tannin) inhibited feeding and thus was lethal at all levels of protein. These results indicate that plant phenolics are likely to influence the performance and dynamics of natural populations of microtine rodents by reducing the quality of available forage. The hypothesis that the primary mode of action of the phenoiics is the reduction of digestibility of protein was not supported. The reduced growth caused by both quercetin and tannic acid could be attributed primarily to their toxicity. The effect of quebracho resulted from reduced intake (unpalatability).
Similar content being viewed by others
References
Association of Official Analytical Chemists. 1975. Official Methods of Analysis. Association of Official Analytical Chemists, Washington D.C. 1094 pp.
Batzli, G.O. 1983a.The role of nutrition in population cycles of microtine rodents.Acta. Zool. Fenn. In press.
Batzli, G.O. 1983b. Responses of arctic rodent populations to nutritional factors.Oikos 40: 396–406.
Berenbaum, M., andFeeny, P. 1981. Toxicity of angular furanocoumarins to swallowtail butterflies: Escalation in a coevolutionary arms race?Science 212:927–929.
Bernays, E.A., andChamberlain, D.J. 1980. A study of tolerance of ingested tannin inSchistocerca gregaria.J. Insect Physiol. 26:415–420.
Bernays, E.A., Chamberlain, D.J., andMcCarthy, P. 1980. The differential effects of ingested tannic acid on different species of Acridoidea.Entomol. Exp. Appl. 28:158–166.
Bernays, E.A., Chamberlain, D.J., andLeather, E.M. 1981. Tolerance of acridids to ingested condensed tannin.J. Chem. Ecol. 7:247–256.
Bitter, T., andMuir, H.M. 1962. A modified uronic acid carbazole reaction.Anal. Biochem. 4:330–334.
Booth, A.N., Masri, M.S., Robbins, D.J., Emerson, O.H., Jones, F.T., andDeEds, F. 1959. The metabolic fate of gallic acid and related compounds.J. Biol. Chem. 234:3014–3016.
Bryant, J.P. 1981. Phytochemical deterrence of snowshoe hare browsing by adventitious shoots of four Alaskan trees.Science 213:889–890.
Bryant, J.P., andKuropat, P.J. 1980. Selection of winter forage by subarctic browsing vertebrates: The role of plant chemistry.Annu. Rev. Ecol. Syst. 11:261–285.
Cooper-Driver, G., Finch, S., andSwain, T. 1977. Seasonal variation in secondary plant compounds in relation to the palatability ofPteridium aquilinum.Biochem. Syst. Ecol. 5:177–183.
Dauterman, W.C. 1980. Physiological factors affecting metabolism of xenobiotics, pp. 133–142,in E. Hodgson and F.E. Guthrie (eds.). Introduction to biochemical toxicology. Elsevier North Holland, New York, 437 pp.
Feeny, P.P. 1970. Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars.Ecology 51:565–581.
Feeny, P.P. 1976. Plant apparency and chemical defense.Rec. Adv. Phytochem. 10:1–40.
Fewtrell, C.M.S., andGomperts, B.D. 1977. Effect of flavone inhibitors of transport ATPases on histamine secretion from rat mast cells.Nature 265:635–636.
Gartlan, J.S., McKey, D.B., Waterman, P.G., Mbi, C.N., andStruhsaker, T.T. 1980. A comparative study of the phytochemistry of two African rain forests.Biochem. Syst. Ecol. 8:401–422.
Goldstein, J.L., andSwain, T. 1965. The inhibition of enzymes by tannins.Phytochemistry 4:185–192.
Harborne, J.B. 1979. Flavonoid pigments, pp. 619–655,in G.A. Rosenthal and D.H. Janzen (eds.). Herbivores. Their Interaction with Secondary Plant Metabolites. Academic Press, New York, 718 pp.
Harley, K.L.S., andThorsteinson, A.J. 1967. The influence of plant chemicals on the feeding behavior, development, and survival of the two-striped grasshopper,Melanoplus bivittatus (Say), Acrididae, Orthoptera.Can. J. Zool. 45:305–319.
Harris, P. 1960. Production of pine resin and its effect on survival ofRhyacionia buoliana (Schiff.) (Lepidoptera: Olethreutidae).Can. J. Zool. 38:121–130.
Haukioja, E. 1980. On the role of plant defenses in the fluctuation of herbivore populations.Oikos 35:202–213.
Joslyn, M.A., andGlick, Z. 1969. Comparative effects of gallotannic acid and related phenolics on the growth of rats.J. Nutr. 98:119–126.
Jung, H.G., andBatzli, G.O., 1981. Nutritional ecology of microtine rodents: Effects of plant extracts on the growth of arctic microtines.J. Mammal. 62:286–292.
Kendall, W.A., andSherwood, R.T. 1975. Palatability of leaves of tall fescue and reed canarygrass and of some of their alkaloids to meadow voles.Agron. J. 67:667–671.
Kendall, W.A., andLeath, K.T. 1976. Effect of saponins on palatability of alfalfa to meadow voles.Agron. J. 68:473–476.
Lake, B.G., Longland, R.C., Gangolli, S.D., andLloyd, A.G. 1976. The influence of some foreign compounds on hepatic xenobiotic metabolism and the urinary excretion of D-glucuronic acid metabolites in the rat.Toxicol. Appl. Pharmacol. 35:113–122.
Lawton, J.H., andMcNeill, S. 1979. Between the devil and the deep blue sea: on the problem of being a herbivore, pp. 223–244,in R.M. Anderson, D.B. Turner, and L.R. Taylor (eds.). Population Dynamics. Blackwell Scientific Publications, London, 434 pp.
Lichtenstein, E.P., Morgan, D.G., andMueller, C.H. 1964. Naturally occurring insecticides in cruciferous crops.J. Agric. Food Chem. 12:158–161.
Lincoln, D.E., Newton, T.S., Ehrlich, P.R., andWilliam, K.S. 1982. Coevolution of the checkerspot butterflyEuphydryas chalcedona and its larval food plantDiplacus aurantiacus: Larval response to protein and leaf resin.Oecologia 52:216–223.
Lindroth, R.L., andBatzli, G.O. 1983. Detoxication of some naturally occurring phenolics by prairie voles: A rapid assay of glucuronidation metabolism.Biochem. Syst. Ecol. 11: 405–409.
Lindroth, R.L., Batzli, G.O., andGuntenspergen, G.R. 1983. Artificial diets for use in nutritional studies with microtine rodents.J. Mammal. 65:139–143.
Nagy, J.G., andTengerdy, R.P. 1967. Antibacterial action of essential oils ofArtemisia as an ecological factor. I. Antibacterial action of the volatile oils ofArtemisia tridentata andArtemisia nova on aerobic bacteria.Appl. Microbiol. 15:819–821.
Nagy, J.G., andTengerdy, R.P. 1968. Antibacterial action of essential oils ofArtemisia as an ecological factor. II. Antibacterial action of the volatile oils ofArtemisia tridentata (big sagebrush) on bacteria from the rumen of mule deer.Appl. Microbiol. 16:441–444.
Oates, J.F., Swain, T., andZantovska, J. 1977. Secondary compounds and food selection byColobus monkeys.Biochem. Syst. Ecol. 5:317–321.
Oh, H.K., Sakai, T., Jones, M.B., andLonghurst, W.M. 1967. Effects of various essential oils isolated from Douglas-fir needles upon sheep and deer rumen microbial activity.Appl. Microbial. 15:777–784.
Oh, H.K., Jones, M.B., andLonghurst, W.M. 1968. Comparison of rumen microbial inhibition resulting from various essential oils isolated from relatively unpalatable plant species.Appl. Microbiol. 16:39–44.
Oh, H.K., Jones, M.B., Longhurst, W.M., andConnolly, G.E. 1970. Deer browsing and rumen microbial fermentation of Douglas-fir as affected by fertilization and growth stage.For. Sci. 16:21–27.
Price, P.W., Bouton, C.E., Gross, P., McPheron, B.A., Thompson, J.N., andWeis, A.E. 1980. Interactions among three trophic levels: Influence of plants on interactions between insect herbivores and natural enemies.Annu. Rev. Ecol. Syst. 11:41–65.
Rhoades, D.F. 1979. Evolution of plant chemical defense against herbivores, pp. 3–54,in G.A. Rosenthal and D.H. Janzen (eds.). Herbivores. Their interaction with Secondary Plant Metabolites. Academic Press, New York, 718 pp.
Rhoades, D.F., andCates, R.G. 1976. Toward a general theory of plant antiherbivore chemistry.Rec. Adv. Phytochem. 10:168–213.
Roux, D.G., Ferreira, D., andBotha, J.J. 1980. Structural considerations in predicting the utilization of tannins.J. Agric. Food Chem. 28:216–222.
Schultz, J.C., andBaldwin, I.T. 1982. Oak leaf quality declines in response to defoliation by gypsy moth larvae.Science 217:149–151.
Schuster, L. 1964. Metabolism of drugs and toxic substances.Annu. Rev. Biochem. 33:571–596.
Schwartz, C.C., Regelin, W.L., andNagy, J.G. 1980. Deer preference for juniper forage and volatile oil treated foods.J. Wildl. Manage. 44:114–120.
Scriber, J.M. 1981. Sequential diets, metabolic costs, and growth ofSpodoptera eridania (Lepidoptera: Noctuidae) feeding upon dill, lima bean, and cabbage.Oecologia 51:175–180.
Shaver, T.N., andLukefahr, M.J. 1969. Effect of flavonoid pigments and gossypol on growth and development of the bollworm, tobacco budworm, and pink bollworm.J. Econ. Entomol. 62:643–646.
Soo Hoo, D.F., andFraenkel, G. 1964. The resistance of ferns to the feeding ofProdenia eridania larvae.Ann. Entom. Soc. Am. 57:788–790.
Swain, T. 1979. Tannins and lignins, pp. 657–692,in G.A. Rosenthal and D.H. Janzen (eds.). Herbivores. Their Interaction with Secondary Plant Metabolites. Academic Press, New York, 718 pp.
Wagner, H. 1977. Phenolic compounds in plants of pharmaceutical interest.Rec. Adv. Phytochem. 12:589–616.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lindroth, R.L., Batzli, G.O. Plant phenolics as chemical defenses: Effects of natural phenolics on survival and growth of prairie voles (Microtus ochrogaster). J Chem Ecol 10, 229–244 (1984). https://doi.org/10.1007/BF00987851
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00987851