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Effect of Nitrogen and Water Treatment on Leaf Chemistry in Horsenettle (Solanum carolinense), and Relationship to Herbivory by Flea Beetles (Epitrix spp.) and Tobacco Hornworm (Manduca sexta)

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Abstract

We studied the interaction between plants (horsenettle; Solanum carolinense) and herbivorous insects (flea beetles; Epitrix spp., and tobacco hornworm; Manduca sexta) by focusing on three questions: (1) Does variation in nitrogen availability affect leaf chemistry as predicted by the carbon-nutrient balance (CNB) hypothesis? (2) Does variation in plant treatment and leaf chemistry affect insect feeding? (3) Is there an interaction between the insect herbivores that is mediated by variation in leaf chemistry? For three successive years (1998–2001), we grew a set of clones of 10 maternal plants under two nitrogen treatments and two water treatments. For each plant in the summer of 2000, we assayed herbivory by hornworms in both indoor (detached leaf) and outdoor (attached leaf) assays, as well as ambient flea beetle damage. Estimates of leaf material consumed were made via analysis of digitized leaf images. We also assayed leaves for total protein, phenolic, and glycoalkaloid content, and for trypsin inhibitor, polyphenol oxidase, and peroxidase activity. Despite strong effects of nitrogen treatment on growth and reproduction, only total protein responded as predicted by CNB. Leaf phenolic levels were increased by nitrogen treatment, polyphenol oxidase activity was decreased, and other leaf parameters were unaffected. Neither hornworm nor flea beetle herbivory could be related to plant treatment or genotype or to variation in any of the six leaf chemical parameters. A negative relationship between flea beetle and hornworm herbivory was found, but was not apparently mediated by any of the measured leaf chemicals. Because leaf resistance was maintained in low nitrogen plants at the apparent expense of growth and reproduction, our results support the concept of a fitness cost of defense, as predicted by the optimal defense hypothesis.

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REFERENCES

  • Alchemy Mindworks, Inc. 1997. Graphic Workshop for Windows. Alchemy Mindworks, Inc., Beeton, Ontario, Canada.

    Google Scholar 

  • Appel, H.M. 1993. The role of phenolics in ecological systems: The importance of oxidation. J. Chem. Ecol. 19:1521–1552.

    Article  CAS  Google Scholar 

  • Baldwin, I. T. 1994. Chemical changes rapidly induced by folivory, pp. 1–23, in E. A. Bernays (ed.). Insect-Plant Interactions, Volume V. CRC Press, London.

    Google Scholar 

  • Baldwin, I. T. 1999. The jasmonate cascade and the complexity of induced defence against herbivore attack, pp. 155–186, in M. Wink (ed.). Functions of Plant Secondary Metabolites and their Exploitation in Biotechnology. Sheffield Academic Press, London.

    Google Scholar 

  • Baldwin I. T., OESCH, R. C., MERHIGE, P. M., and HAYES, K. 1993. Damage-induced root nitrogen metabolism in Nicotiana sylvestris: testing C/N predictions for alkaloid production. J. Chem. Ecol. 19:3029–3043.

    Article  CAS  Google Scholar 

  • Bate, N. J., Orr, J., Weiting, N., Meromi, A., Nadler-Hassar, T., Doerner, P.W., Dixon, R. A., Lamb, C. J., and Elkind, Y. 1994. Quantitative relationship between phenylalanine ammonialyase levels and phenylpropanoid accumulation in transgenic tobacco identifies a rate-determining step in natural product synthesis. Proc. Natl. Acad. Sci. USA 91:7608–7612.

    Article  CAS  Google Scholar 

  • Berenbaum, M. R. and Zangerl, A. R. 1988. Stalemates in the coevolutionary arms race: syntheses, synergisms, and sundry other sins, pp. 113–132, in K. Spencer (ed.). Chemical Mediation of Coevolution. American Institute of Biological Sciences and Academic Press, San Diego, California.

    Chapter  Google Scholar 

  • Berryman, A. A. 1988. Toward a unified theory of plant defense, pp. 39–55, in W. J. Mattson, J. Levieux, and C. Bernard-Dagan (eds.). Mechanisms of Woody Plant Defenses Against Insects: Search for Pattern. Springer-Verlag, New York.

    Chapter  Google Scholar 

  • Birner, J. 1969. Determination of total steroid bases in Solanum species. J. Pharm. Sci. 58:258–259.

    Article  CAS  Google Scholar 

  • Bolter, C. J., Latoszek-Green, M., and Tenuta, M. 1998. Dependence of methyl jasmonate-and wound-induced cysteine proteinase inhibitor activity on nitrogen concentration. J. Plant Physical 152:427–432.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Broadway, R.M. 1995. Are insects resistant to plant proteinase inhibitors? J. Insect Physiol. 41:107–116.

    Article  CAS  Google Scholar 

  • Bryant, J. P., Chapin, F. S., III, and Klein, D. R. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368.

    Article  CAS  Google Scholar 

  • Bryant, J. P., Chapin, F. S., III, Reichardt, P. B., and Clausen, T. 1985. Adaptation to resource availability as a determinant of chemical defense strategies in woody plants, pp. 219–237, in G. A. Cooper-Driver, T. Swain, and E. E. Conn (eds.). Chemically Mediated Interactions between Plants and Other Organisms (Recent Advances in Phytochemistry, Volume 19). Plenum Press, New York.

    Chapter  Google Scholar 

  • Bryant, J. P., Reichardt, P. B., Clausen, T. P., and Werner, R. A. 1993. Effects of mineral nutrition on delayed inducible resistance in Alaska paper birch. Ecology 74:2072–2084.

    Article  Google Scholar 

  • Budini, R., Tonelli, D., and Girotti, S. 1980. Analysis of total phenols using the Prussian Blue method. J. Agric. Food Chem. 28:1236–1238.

    Article  CAS  Google Scholar 

  • Campa, A. 1991. Biological roles of plant peroxidases: known and potential function, pp. 25–50, in J. Everse, K. E. Everse, and M. B. Grisham (eds.). Peroxidases in Chemistry and Biology, Vol II. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Cipollini, D. F. 1998. The induction of soluble peroxidase activity in bean leaves by wind-induced mechanical perturbation. Am. J. Bot. 85:1586–1591.

    Article  CAS  Google Scholar 

  • Cipollini, D. F. and Bergelson, J. 2000. Environmental and developmental regulation of trypsin inhibitor activity in Brassica napus. J. Chem. Ecol. 26:1411–1422.

    Article  CAS  Google Scholar 

  • Cipollini, D. F. and Bergelson, J. 2001. Plant density and nutrient availability constrain constitutive and wound-induced expression of trypsin inhibitors in Brassica napus. J. Chem. Ecol. 27:593–610.

    Article  CAS  Google Scholar 

  • Cipollini, D. F. and Redman, A.M. 1999. Age-dependent effects of jasmonic acid treatment and wind exposure on foliar oxidase activity and insect resistance in tomato. J. Chem. Ecol. 25:271–281.

    Article  CAS  Google Scholar 

  • Cipollini, M. L. and Levey, D. J. 1997a. Antifungal activity of Solanum fruit glycoalkaloids: implications for frugivory and seed dispersal. Ecology 78:799–809.

    Article  Google Scholar 

  • Cipollini, M. L. and Levey, D. J. 1997b. Why are some fruits toxic? Glycoalkaloids in Solanum and fruit choice by vertebrates. Ecology 78:782–798.

    Article  Google Scholar 

  • Cipollini, M. L., Drake, B. G., and Whigham, D. 1993. Effects of elevated CO2 on growth and carbon/nutrient balance in deciduous woody shrub Lindera benzoin (L.) Blume (Lauraceae). Oecologia 96:339–346.

    Article  Google Scholar 

  • Cipollini, M. L., Bohs, L., Mink, K., Paulk, E., and Boehning-Gaese, K. 2001. Patterns of secondary compounds within fleshy fruits: ecology and phylogeny, pp. 111–128, in D. J. Levey, W. R. Silva, and M. Galetti (eds.). Seed Dispersal and Frugivory: Ecology, Evolution and Conservation. CABI Publishing, Wallingford, Oxfordshire, United Kingdom.

    Google Scholar 

  • Coley, P. D., Bryant, J. P., and Chapin, F. S., III. 1985. Resource availability and plant antiherbivore defense. Science 230:895–899.

    Article  CAS  Google Scholar 

  • Dixon, R. A. and Paiva, N. L. 1995. Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097.

    Article  CAS  Google Scholar 

  • Feller, I. C. 1995. Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove (Rhizophora mangle). Ecol. Monogr. 65:477–505.

    Article  Google Scholar 

  • Flanders, K. L., Hawkes, J. G., Radcliffe, E. B., and Lauer, F. I. 1992. Insect resistance in potatoes: sources, evolutionary relationships, morphological and chemical defenses, and ecogeographical associations. Euphytica 61:83–111.

    Article  CAS  Google Scholar 

  • Fragoyiannis, D. A., Mckinlay, R. G., and D'MELLO, J. P. F. 1998. Studies of the growth, development and reproductive performance of the aphid Myzus persicae on artificial diets containing potato glycoalkaloids. Entomol. Exp. Applic. 88:59–66.

    Article  CAS  Google Scholar 

  • Gebauer, R., Strain, B. R., and Reynolds, J. F. 1998. The effect of elevated CO2 and N availability on tissue concentrations and whole plant pools of carbon-based secondary compounds in loblolly pine (Pinus taeda). Oecologia 113:29–36.

    Article  Google Scholar 

  • Gershenzon, J. 1994. The cost of plant chemical defense against herbivory: a biochemical perspective, pp. 105–173, in E. A. Bernays (ed.). Insect-Plant Interactions, Volume V. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Graham, H. 1992. Stabilization of the Prussian Blue color in the determination of polyphenols. J. Agric. Food Chem. 40:801–805.

    Article  CAS  Google Scholar 

  • Hamilton, J. G., Zangerl, A. R., Delucia, E. H., and Berenbaum, M. R. 2001. The carbon-nutrient balance hypothesis: its rise and fall. Ecol. Lett. 4:86–95.

    Article  Google Scholar 

  • Hare, J. D. 1983. Seasonal variation in plant-insect associations: utilization of Solanum dulcamara by Leptinotarsa decemlineata. Ecology 64:345–361.

    Article  Google Scholar 

  • Hare, J. D. 1987. Growth of Leptinotarsa decemlineata larvae in response to simultaneous variation in protein and glycoalkoloid concentration. J. Chem. Ecol. 13:39–46.

    Article  CAS  Google Scholar 

  • Hartley, S. E. and Jones, C. G. 1997. Plant chemistry and herbivory, or why the world is green, pp. 284–324, in M. J. Crawley (ed.). Plant Ecology. Blackwell Science, Oxford.

    Google Scholar 

  • Haukioja, E. S. 1991. Induction of defenses in trees. Annu. Rev. Entomol. 36:25–42.

    Article  CAS  Google Scholar 

  • Haukioja, E., Hanhimaki, S., and Walter, G. H. 1994. Can we learn about herbivory on eucalypts from research on birches, or how general are general plant- herbivore theories? Aust. J. Ecol. 19:1–9.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hoffland, E., Dicke, M., Van Tintelen, W., Dijkman, H., and Van Beusichem, M. L. 2000. Nitrogen availability and defense of tomato against two-spotted spider mite. J. Chem. Ecol. 26:2697–2711.

    Article  CAS  Google Scholar 

  • Hoffland, E., Van Beusichem, M. L., and Jeger, M. J. 1999. Nitrogen availability and susceptibility of tomato leaves to Botrytis cinerea. Plant Soil 210:263–272.

    Article  CAS  Google Scholar 

  • Howles, P. A., Sewalt, V. J. H., Priva, N. L., Elkind, Y., Bate, N. J., Lamb, C., and Dixon, R. A. 1996. Overexpression of L-phenylalamine ammonia lyase in transgenic tobacco plants reveals control points for flux into phenylpropanoid biosynthesis. Plant Physiol. 112:1617–1624.

    Article  CAS  Google Scholar 

  • Iason, G.R. and Hester, A. J. 1993. The response of heather (Calluna vulgaris) to shade and nutrients - predictions of the carbon-nutrient balance hypothesis. J. Ecol. 81:75–80.

    Article  Google Scholar 

  • Jones, C. G., Hare, J. D., and Compton, S. J. 1989. Measuring plant protein with the Bradford assay. 1. Evaluation and standard methodology. J. Chem. Ecol. 15:979–992.

    Article  CAS  Google Scholar 

  • Jones, C. G., and Hartley, S. E. H. 1999. A protein competition model of phenolic allocation. Oikos 86:27–44.

    Article  CAS  Google Scholar 

  • Kainulainen, P., Holopainen, J., Palomaki, V., and Holopainen, T. 1996. Effects of nitrogen fertilization on secondary chemistry and ectomycorrhizal state of Scots pine seedlings and on growth of grey pine aphid. J. Chem. Ecol. 22:617–636.

    Article  CAS  Google Scholar 

  • Karban, R. and Baldwin, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago, Illinois.

    Book  Google Scholar 

  • Keinanen, M., Julkunen-Tiitto, R., Mutikainen, P., Walls, M., Ovaska, J., and Vapaauori, E. 1999. Trade-offs in phenolic metabolism of silver birch: effects of fertilization, defoliation, and genotype. Ecology 80:1970–1986.

    Article  Google Scholar 

  • Kinney, K. K., Lindroth, R. L., Jung, S. M., and Nordheim, E. V. 1997. Effects of CO2 and NO- 3 availability on deciduous trees: phytochemistry and insect performance. Ecology 78:215–230.

    Google Scholar 

  • Koiwa, H., Bressan, R. A., and Hasegawa, P.M. 1997. Regulation of proteinase inhibitors and plant defense. Trends Plant Sci. 2:379–384.

    Article  Google Scholar 

  • Langenheim, J. H. 1994. Higher plant terpenoids: a phytocentric overview of their ecological roles. J. Chem. Ecol. 20:1223–1280.

    Article  CAS  Google Scholar 

  • Lavola, A. and Julkunen-Tiitto, R. 1994. The effect of elevated carbon dioxide and fertilization on primary and secondary metabolites in birch, Betula pendula (Roth). Oecologia 99:315–321.

    Article  CAS  Google Scholar 

  • Linhart, Y. B. 1991. Disease, parasitism, and herbivory: multidimensional challenges in plant evolution. Trends Ecol. Evol. 6:392–396.

    Article  CAS  Google Scholar 

  • Mauricio, R. 1998. Costs of resistance to natural enemies in field populations of the annual plant, Arabidopsis thaliana. Am. Nat. 151:20–28.

    CAS  PubMed  Google Scholar 

  • Microsoft, Inc. 1991- 1998. Windows Paint for Windows. Microsoft, Inc., Seattle, Washington.

    Google Scholar 

  • Mutikainen, P., Walls, M., Ovaska, J., Keinanen, M., Julkunen-Tiitto, R., and Vapaavuori, E. 2000. Herbivore resistance in Betula pendula: effect of fertilization, defoliation, and plant genotype. Ecology 81:49–65.

    Article  Google Scholar 

  • Muzika, R.-M. 1993. Terpenes and phenolics in response to nitrogen fertilization: a test of the carbon/nutrient balance hypothesis. Chemoecology 4:3–7.

    Article  CAS  Google Scholar 

  • National Institutes of Health. 2000. Image J. V. 1.19. National Institutes of Health. Washington, D.C.

    Google Scholar 

  • Nowacki,E., Jurzysta, M., Gorski, P., Nowacka, D., and Waller, G. R. 1976. Effect of nitrogen nutrition on alkaloid metabolism in plants. Biochem. Physiol. Pflanzen 169:231–240.

    Article  CAS  Google Scholar 

  • 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 88:401–406.

    Article  CAS  Google Scholar 

  • 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 Plant Secondary Metabolites. Academic Press, New York.

    Google Scholar 

  • Ruohomaki, K., Chapin, F. S., III, Haukioja, E., Neuvonen, S., and Suomela, J. 1996. Delayed inducible resistance in Mountain Birch in response to fertilization and shade. Ecology 77:2302–2311.

    Article  Google Scholar 

  • Simple Interactive Statistical Analysis. 2001. Bonferroni Correction On-Line. Adjustment for Multiple Comparisons. Simple Interactive Statistical Analysis, http://home.clara.net/sisa/bonhlp.htm.

  • Stamp, N. E. 1992. Theory of plant-insect herbivore interactions on the inevitable brink of resynthesis. Bull. Ecolog. Soc. Am. 73:29–34.

    Google Scholar 

  • Stout, M. J., Brovont, R. A., and Duffey, S. S. 1998. Effect of nitrogen availability on expression of constitutive and inducible chemical defenses in tomato, Lycopersicon esculentum. J. Chem. Ecol. 24: 945–963.

    Article  CAS  Google Scholar 

  • Thaler, J. S., Stout, M. J., Karban, R., and Duffey, S. S. 1996. Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field. J. Chem. Ecol. 22:1767–1781.

    Article  CAS  Google Scholar 

  • Tingey, W. M. 1984. Glycoalkoloids as pest resistance factors. Am. Potato J. 61:157–167.

    Article  CAS  Google Scholar 

  • Tuomi, J., Niemela, P., Haukioja, E., Siren, S., and Neuvonen, S. 1984. Nutrient stress: an explanation for plant anti-herbivore responses to defoliation. Oecologia 61:208–210.

    Article  Google Scholar 

  • Van Gelder, W. M. J. 1984. A new hydrolysis technique for steroid glycoalkaloids with unstable aglycones from Solanum spp. J. Sci. Food Agric. 35:487–494.

    Article  CAS  Google Scholar 

  • Van Gelder, W. M. J. 1990. Chemistry, toxicology, and occurrence of steroidal glycoalkaloids:potential contaminants of the potato (Solanum tuberosum L.), pp. 117–156, in A.-F.M. Rizk (ed.) Poisonous Plant Contamination of Edible Plants. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Waterman, P. and Mole, S. 1989. Extrinsic factors influencing production of secondary metabolites in plants, pp. 107–134, in E. A. Bernays (ed.) Insect- Plant Interactions, Volume I. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Wink, M. 1998. Chemical ecology of alkaloids, pp. 265–300 in M. F. Roberts, and M. Wink (eds.) Alkaloids: Biochemistry, Ecology, and Medicinal Applications. Plenum Press, New York.

    Chapter  Google Scholar 

  • Wink, M. 1999. Introduction, pp. 1–16, in M. Wink (ed.) Functions of Plant Secondary Metabolites and their Exploitation in Biotechnology. CRC Press, Boca Raton, Florida.

    Google Scholar 

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  1. Department of Biology, 430 Berry College, Mount Berry, Georgia, 30149, USA

    Martin L. Cipollini & Eric Paulk

  2. Department of Biological Sciences, Wright State University, 3640 Colonel Glenn Highway, Dayton, Ohio, 45435-0001, USA

    Donald F. Cipollini

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  1. Martin L. Cipollini
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Cipollini, M.L., Paulk, E. & Cipollini, D.F. Effect of Nitrogen and Water Treatment on Leaf Chemistry in Horsenettle (Solanum carolinense), and Relationship to Herbivory by Flea Beetles (Epitrix spp.) and Tobacco Hornworm (Manduca sexta). J Chem Ecol 28, 2377–2398 (2002). https://doi.org/10.1023/A:1021494315786

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