Skip to main content
Log in

The Dynamics of Carbon–Nutrient Balance: Effects of Cottonwood Acclimation to Short- and Long-Term Shade on Beetle Feeding Preferences

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

Abstract

The carbon–nutrient balance hypothesis (CNBH) predicts that shading should increase leaf palatability to herbivores by decreasing concentrations of carbon (C) -based chemical defenses and increasing nitrogen (N). We measured cottonwood (Populus deltoids) growth, leaf chemistry, and beetle (Plagiodera versicolora) feeding preferences on saplings grown in either continuous high (HH) or low (LL) light, and saplings switched from high to low (HL) or low to high (LH) light for nine days. As expected, based on the CNBH, shading increased total N and decreased total phenol glycoside (C-based secondary metabolites) concentrations in plants from all shade treatments (LL, HL, and LH), relative to HH plants, with plant growth and gross leaf chemistry being affected by initial and final light regime. In contrast, while specific phenol glycoside concentrations were affected by the initial and final light regime, they also showed an initial × final light interaction. Beetles tended to prefer LL to HH plants. Beetles unexpectedly preferred HH to either HL or LH switched plants, most likely because high concentrations of a specific phenol glycoside – salicin – occurred in both switched treatments and inhibited beetle feeding. Plant chemical allocation during light acclimation led to unpredictable changes in specific C-based compounds, even though plant growth and gross chemistry conformed to expectations for shading effects and the CNBH. The response of this herbivore to altered concentrations of a specific compound confounded predictions based on average dynamics of suites of chemicals. Our findings may help explain why relationships between light availability and herbivory in field studies, where light varies on many time scales, can differ from those predicted by the CNBH. Understanding both dynamic plant chemical responses to altered resource availability and controls over allocation to specific compounds would likely enhance future predictability of specific environment-plant-herbivore interactions.

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.

Similar content being viewed by others

REFERENCES

  • Aide, T. M., and Zimmerman, J. K. 1990. Patterns of insect herbivory, growth, and survivorship in juveniles of a neotropical liana. Ecology 41:1412-1421.

    Google Scholar 

  • Barker, H. R., and Barker, B. M. 1984. Multivariate Analysis of Variance (MANOVA). The University of Alabama Press, University, Alabama.

    Google Scholar 

  • Basset, Y. 1991. The spatial distribution of herbivory, mines and galls within an Australian rain forest tree. Biotropica 23:271-281.

    Google Scholar 

  • Bingaman, B. R., and Hart, E. R. 1993. Clonal and leaf age variation in Populus phenolic glycosides: Implications for host selection by Chrysomela scripta (Coleoptera: Chrysomelidae). Environ. Entomol. 22:397-403.

    Google Scholar 

  • Bryant, J. P. 1987. Feltleaf willow-snowshoe hare interactions: Plant carbon/nutrient balance and floodplain succession. Ecology 68:1319-1327.

    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 

  • 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 

  • Coleman, J. S., and Jones, C. G. 1988. Plant stress and insect performance: Cottonwood, ozone and a leaf beetle. Oecologia 76:57-61.

    Google Scholar 

  • Collinge, S. K., and Louda, S. M. 1988. Herbivory by leaf minors in response to experimental shading of a native crucifer. Oecologia 76:559-566.

    Google Scholar 

  • Dudt, J. F., and Shure, D. J. 1994. The influence of light and nutrients on foliar phenolics and herbivory. Ecology 75:86-89.

    Google Scholar 

  • Folgarait, P. J., Marquis, R. J., Ingvarsson, P., Braker, H. E., and Arguedas, M. 1995. Patterns of attack by insect herbivores and a fungus on saplings in a tropical tree plantation. Environ. Entomol. 24:1487-1494.

    Google Scholar 

  • Grime, J. P. 1966. Shade avoidance and shade tolerance in flowering plants, pp. 187-207, in R. Bainbridge, G. C. Evans, and O. Rackham (eds.). Light as an Ecological Factor. Blackwell Scientific, Oxford.

    Google Scholar 

  • Harrison, S. 1987. Treefall gaps versus forest understory as environments for a defoliating moth on a tropical forest shrub. Oecologia 72:65-68.

    Google Scholar 

  • Hosner, J. F., and Minckler, L. F. 1963. Bottomland and hardwood forests of southern Illinois—regeneration and succession. Ecology 44:29-41.

    Google Scholar 

  • Jones, C. G., and Coleman, J. S. 1988. Plant stress and insect behavior: Cottonwood, ozone, and the feeding and oviposition preference of a beetle. Oecologia 76:51-56.

    Google Scholar 

  • Jones, C. G., and Coleman, J. S. 1989. Biochemical indicators of air pollution in trees: Unambiguous signals based on secondary metabolites and nitrogen in fast-growing species, pp. 261-273, in National Research Council (eds.). Biologic Markers Air Pollution Stress and Damage in Forests. National Academy Press, Washington, D.C.

    Google Scholar 

  • Jones, C. G., Hare, J. D., and Compton, S. 1989. Measuring plant protein with the Bradford assay. J. Chem. Ecol. 15:979-992.

    Google Scholar 

  • Jones, C. G., Hopper, R. F., Coleman, J. S., and Krishik, V. A. 1993. Control of systemically induced herbivore resistance by plant vascular architecture. Oecologia 93:452-456.

    Google Scholar 

  • Jones, C. G., Coleman, J. S., and Findlay, S. 1994. Effects of ozone on interactions between plants, consumers and decomposers, pp. 339-363, in R. G. Alsher and A. Wellburn (eds.). Plant Responses to the Gaseous Environment. Chapman and Hall, London.

    Google Scholar 

  • Larcher, W. 1980. Plant Physiological Ecology. Springer-Verlag, New York.

    Google Scholar 

  • Larson, P. R., and Isebrands, J. G. 1971. The plastochron index as applied to developmental studies of cottonwood. Can. J. For. Res. 1:1-11.

    Google Scholar 

  • Larsson, S., Wiren, A., Lundgren, L., and Ericsson, T. 1986. Effects of light and nutrient stress on leaf phenolic chemistry in Salix dasclados and susceptibility to Galerucella lineola. Oikos 47:205-210.

    Google Scholar 

  • Lincoln, D. E., and Mooney, H. A. 1984. Herbivory on Diplacus aurantiacus shrubs in sun and shade. Oecologia 64:173-176.

    Article  Google Scholar 

  • Lindroth, R. L., and Pajutee, M. S. 1987. Chemical analysis of phenolic glycosides: Art, facts, and artifacts. Oecologia 74:144-148.

    Google Scholar 

  • Lindroth, R. L., Hsia, M. T. S., and Scriber, J. M. 1987. Seasonal patterns on the phytochemistry of three Populus species. Biochem. Syst. Ecol. 15:681-686.

    Google Scholar 

  • Lindroth, R. L., Reich, P. B., Tjoelker, M. G., Volin, J. C., and Oleksyn, J. 1993. Light environment alters response to ozone stress in seedlings of Acer saccharum Marsh. and hybrid Populus L. III. Consequences for performance of gypsy moth. New Phytol. 124:647-651.

    Google Scholar 

  • Louda, S. M., and Rodman, J. E. 1983. Concentration of glucosinolates in relation to habitat and insect herbivory for the native crucifer Cardamine cordifolia. Biochem. Syst. Ecol. 11:199-207.

    Google Scholar 

  • Louda, S. M., Dixon, P. M., and Huntly, N. J. 1987. Herbivory in sun versus shade at a natural meadow-woodland ecotone in the Rocky Mountains. Vegetatio 72:141-149.

    Google Scholar 

  • Lowman, M. D. 1992. Leaf growth dynamics and herbivory in five species of Australian rain-forest canopy tree. J. Ecol. 80:433-447.

    Google Scholar 

  • Maiorana, V. C. 1981. Herbivory in sun and shade. Biol. J. Linn. Soc. 15:151-156.

    Google Scholar 

  • Mole, S., and Waterman, P. G. 1988. Light-induced variation in phenolic levels in foliage of rainforest plants. II. Potential significance to herbivores. J. Chem. Ecol. 14:23-34.

    Google Scholar 

  • Mole, S., Ross, J. A. M., and Waterman, P. G. 1988. Light-induced variation in phenolic levels in foliage of rainforest plants. J. Chem. Ecol. 14:1-21.

    Google Scholar 

  • Nichols-Orians, C. 1991. Environmentally induced differences in plant traits: Consequences for susceptibility to a leaf-cutter ant. Ecology 72:1609-1623.

    Google Scholar 

  • Orians, C. M. 1995. Preserving leaves for tannin and phenolic glycoside analysis: A comparison of methods using three willow taxa. J. Chem. Ecol. 21:1235-1243.

    Google Scholar 

  • Peterson, N. C., and Smitley, D. R. 1991. Susceptibility of selected shade and flowering trees to gypsy moth (Lepidoptera: Lymantridae). J. Econ. Entomol. 84:587-592.

    Google Scholar 

  • Picard, S., Chenault, J., Augustin, S., and Venot, C. 1994. Isolation of a new phenolic compound from leaves of Populus deltoides. J. Nat. Prod. 57:808-810.

    Google Scholar 

  • Reichardt, P. B., Chapin, F. S., 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 88:401-406.

    Google Scholar 

  • Scheiner, S. M. 1993. MANOVA: Multiple response variables and multispecies interactions, pp. 94-112, in S. M. Scheiner and J. Gurevitch (eds.). Design and Analysis of Ecological Experiments. Chapman and Hall, New York.

    Google Scholar 

  • Sims, D. A., and Pearcy, R. W. 1991. Photosynthesis and respiration in Alocasia macrorriza following transfers to high and low light. Oecologia 86:447-453.

    Google Scholar 

  • Smith, H. 1981. Adaptation to shade, pp. 159-173, in C. B. Johnson (ed.). Physiological Processes Limiting Plant Productivity. Butterworths, London.

    Google Scholar 

  • Tahvanainen, J., Helle, E., and Kettunen, J. 1985. Phenolic levels govern the food selection pattern of willow feeding leaf beetles. Oecologia 67:52-56.

    Google Scholar 

  • Wade, M. J., and Breden, F. 1986. Life history of natural populations of the imported willow leaf beetle, Plagiodera versicolora (Coleoptera: Chrysomelidae). Ann. Entomol. Soc. Am. 55:171-180.

    Google Scholar 

  • Wait, D. A. 1992. Effect of nutrient addition rates on growth, chemistry, and physiology of Populus deltoides, and the feeding preference and consumption of Chrysomela scripta and Lymantria dispar. MS thesis. State University of New York, College of Environmental Science and Forestry, Syracuse, New York.

    Google Scholar 

  • Wait, D. A., Jones, C. G., and Coleman, J. S. 1998. Effects of nitrogen fertilization on leaf chemistry and beetle feeding are mediated by leaf development. Oikos. 82:502-504.

    Google Scholar 

  • Waring, R. H., McDonald, A. J. S., Larsson, S., Ericsson, T., Wiren, A., Arwidsso, E., Ericsson, A., and Lohammar, T. 1985. Differences in chemical composition of plants grown at constant relative growth rates with stable mineral nutrition. Oecologia 66:157-160.

    Google Scholar 

  • Waterman, P. G., Ross, J. A. M., and McKey, D. B. 1984. Factors affecting levels of some phenolic compounds, digestibility, and nitrogen content of the mature leaves of Barteria fistulosa (Passifloraceae). J. Chem. Ecol. 10:387-401.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Crone, E.E., Jones, C.G. The Dynamics of Carbon–Nutrient Balance: Effects of Cottonwood Acclimation to Short- and Long-Term Shade on Beetle Feeding Preferences. J Chem Ecol 25, 635–656 (1999). https://doi.org/10.1023/A:1020966206840

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1020966206840

Navigation