Abstract
Predictions of the carbon-nutrient balance hypothesis were tested using a study of within-species phytochemical variation in the arroyo willow,Salix lasiolepis. The prediction that a balance between nutrients (total protein) and carbon-based secondary metabolites (total phenols) should exist was supported using water treatment and fertilizer experiments and wild willow clones. Leaf nitrogen content and net photosynthetic rates of plants potted in soil in which parental plants grew was low, indicating that wild plants exist under relatively low nutrient status-high carbon balance conditions. The hypothesis also correctly predicted positive relationships between shoot length and phenols in glasshouse plants, wild plants, and plants in the water treatment experiment and negative relationships between shoot length and phenols in the fertilizer treatment experiment. Total phenolic glycosides, fragilin, picein, salicortin, tremulacin, and tremuloidin all correlated positively with shoot length in glasshouse plants on a carbon-biased balance, and male willows had generally lower levels of phenolic glycosides than females. Salicortin and tremulacin showed the strongest positive relationships with shoot length.
Similar content being viewed by others
References
Bryant, J.P. 1987. Feltleaf willow-snowshoe hare interactions: Plant carbon/nutrient balance and implications for floodplain succession.Ecology 68:1319–1327.
Bryant, J.P., Chapin, F.S., andKlein, D.R. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory.Oikos 40:357–368.
Coley, P.D. 1983. Herbivory and defensive characteristics of tree species in a lowland tropical forest.Ecol. Monogr. 53:209–233.
Craig, T.P., Price, P.W., andItami, J.K. 1986. Resource regulation by a stem-galling sawfly on the arroyo willow.Ecology 67:419–425.
Craig, T.P., Itami, J.K., andPrice, P.W. 1988. Plant wound compounds from oviposition scars used in host discrimination by a stem-galling sawfly.J. Insect Behav. 1:343–356.
Danell, K., Elmqvist, T., Ericson, L., andSalomonson, A. 1985. Sexuality in willows and preference by bark-eating voles: Defense or not?Oikos 44:82–90.
Denno, R.F., andMcClure, M.S. (eds.). 1983. Variable Plants and Herbivores in Natural and Managed Systems. Academic Press, New York.
Duffey, S.S., Bloem, K.A., andCampbell, B.C. 1986. Consequences of sequestration of plant natural products in plant-insect-parasitoid interactions, pp. 31–60,in D.J. Boethel and R.D. Eikenbary (eds.). Interactions of Plant Resistance and Parasitoids and Predators of Insects. Ellis Horwood, Chichester, U.K.
Field, C., andMooney, H.A. 1986. The photosynthesis-nitrogen relationships in wild plants, pp. 25–55,in T.J. Givnish (ed.). On the Economy of Plant Form and Function. Cambridge University Press, New York.
Gill, D.E. 1986. Individual plants as genetic mosaics: Ecological organisms versus evolutionary individuals, pp. 321–343,in M.J. Crawley (ed.). Plant Ecology. Blackwell Scientific Publications, Oxford.
Jones, F.G.W. 1976. Pests, resistance and fertilizers, pp. 233–258,in V. Taysi (ed.). Fertilizer Use and Plant Health. Proceedings 12th International Potash Institute, Der Bund A.G., Worblaufan-Bern, Switzerland.
Joseffson, E. 1970. Glucosinolate content and amino acid composition of rapeseed meal as affected by S and N nutrition.J. Sci. Food Agric. 21:98–103.
Julkunen-Tiitto, R. 1985. Phenolic constituents in the leaves of northern willows: methods for the analysis of certain phenolics.J. Agric. Food Chem. 33:213–217.
Julkunen-Tiitto, R., andTahvanainen, J. 1989. The effect of the sample preparation method on extractable phenolics of Salicaceae species.Planta Med. In press.
Kiraly, Z. 1976. Plant disease resistance as influenced by biochemical effects of nutrients in fertilizers, pp. 33–45,in V. Taysi (ed.). Fertilizer Use and Plant Health. Proceedings 12th International Potash Institute, Der Bund A.G., Worblaufen-Bern, Switzerland
Kirkham, D.S. 1954. Significance of the ratio of the water soluble aromatic and nitrogen constituents of apple and pear in the host-parasite relationship ofVenturia sp.Nature 137:690–691.
Lindroth, R.L., andPajutee, M.S. 1987. Chemical analysis of phenolic glycosides: Art, facts, and artifacts.Oecologia 74:144–148.
Lindroth, R.L., Hsia, M.T.S., andScriber, J.M. 1987. Characterization of phenolic glycosides from quaking aspen.Biochem. Syst. Ecol. 15:677–680.
Lindroth, R.L., Scriber, J.M., andHsia, M.T.S. 1988. Chemical ecology of the tiger swallowtail: Mediation of host use by phenolic glycosides.Ecology. 63:814–822.
Mattson, W.J. 1980. Herbivory in relation to plant nitrogen content.Annu. Rev. Ecol. Syst. 11:119–161.
Mattson, W.J., andScriber, J.M. 1987. Nutritional ecology of insect folivores of woody plants: Nitrogen, water, fiber, and mineral considerations, pp. 105–146,in F. Slansky and J.G. Rodriguez (eds.). Nutritional Ecology of Insects, Mites, Spiders, and Related Invertebrates. Wiley, New York.
Meier, B., Sticher, O., andBettschart, A. 1985. Weidenrinden-Qualität: Gesamtsalicinbestimmung in Weidenrinden und Weidenpräparaten mit HPLC.Dtsch. Apoth. Ztg. 125:341–347.
Mihaliak, C.A., Couvet, D., andLincoln, D.E. 1987. Inhibition of feeding by a generalist insect due to increased volatile leaf terpenes under nitrate-limiting conditions.J. Chem. Ecol. 13:2059–2067.
Palo, R.T. 1984. Distribution of birch (Betula spp.), willow (Salix spp.) and poplar (Populus spp.) secondary metabolites and their potential role as chemical defense against herbivores.J. Chem. Ecol. 10:499–520.
Phillips, R., andHenshaw, G.G. 1979. The regulation of synthesis of phenolics in stationary phase cell cultures ofAcer pseudoplatanus L.J. Exp. Biol. 28:785–794.
Pitelka, L.F., andAshmun, J.W. 1985. The physiology and ecology of connections between ramets in clonal plants, pp. 399–435,in J. Jackson, L. Buss, and R. Cook (eds.). The Population Biology and Evolution of Clonal Organisms. Yale University Press, New Haven.
Price, P.W., andClancy, K.M. 1986a. Multiple effects of precipitation onSalix lasiolepis and populations of the stem-galling sawfly,Euura lasiolepis.Ecol. Res. 1:1–14.
Price, P.W., andClancy, K.M. 1986b. Interactions among three trophic levels: Gall size and parasitoid attack.Ecology 67:1593–1600.
Price, P.W., andCraig, T.P. 1984. Life history, phenology, and survivorship of a stem-galling sawfly,Euura lasiolepis (Hymenoptera: Tenthredinidae), on the arroyo willow,Salix lasiolepis in Northern Arizona.Ann. Entomol. Soc. Am. 77:712–719.
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.
Scriber, J.M. 1984. Nitrogen nutrition of plants and insect invasion, pp. 441–460,in R.D. Hauck (ed.). Nitrogen in Crop Production. American Society of Agronomists, Madison, Wisconsin.
Scriber, J.M., andSlansky, F. 1981. The nutritional ecology of immature insects.Annu. Rev. Entomol. 26:183–211.
Slansky, F., andScriber, J.M. 1985. Food consumption and utilization, pp. 87–163,in G.A. Kerkut, and L.I. Gilbert (eds.). Comprehensive Insect Physiology, Biochemistry and Pharmacology. Pergamon, New York.
Thieme, H. 1965. Die Phenolglykosidespektren und der Glykosidgehalt der mitteldeutchenSalix arten.Pharmazie 20:570–574.
Waller, D.M. 1986. The dynamics of growth and form, pp. 291–320,in M.J. Crawley (ed.). Plant Ecology. Blackwell Scientific Publications, Oxford.
Waring, G.L. andPrice, P.W. 1988. Consequences of host plant chemical and physical variability to an associated herbivore.Ecol. Res. 3:207–216.
Watson, M.A., andCasper, B.B. 1984. Morphogenetic constraints on patterns of carbon distribution in plants.Annu. Rev. Ecol. Syst. 15:233–258.
Whitham, T.G., Williams, A.G., andRobinson, A.M. 1984. The variation principle: Individual plants as temporal and spatial mosaics of resistance to rapidly evolving pests, pp. 15–51,in P.W. Price, C.N. Slobodchikoff, and W.S. Gaud (eds.). A New Ecology: Novel Approaches to Interactive Systems. Wiley, New York.
Winner, W., andMooney, H.A. 1980. Ecology of SO2 resistance. I. Effect of fumigation on gas exchange of deciduous and evergreen shrubs.Oecologia 44:290–295.
Wolfson, J.L. 1980. Oviposition response ofPieris rapae to environmentally induced variation inBrassica nigra.Entomol. Exp. Appl. 27:223–232.
Zucker, W.V. 1982. How aphids choose leaves: The role of phenolics in host selection by a galling aphid.Ecology 63:972–981.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Price, P.W., Waring, G.L., Julkunen-Tiitto, R. et al. Carbon-nutrient balance hypothesis in within-species phytochemical variation ofSalix lasiolepis . J Chem Ecol 15, 1117–1131 (1989). https://doi.org/10.1007/BF01014816
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01014816