Journal of Chemical Ecology

, Volume 28, Issue 12, pp 2377–2398 | Cite as

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)

  • Martin L. Cipollini
  • Eric Paulk
  • Donald F. Cipollini
Article

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.

Carbon–nutrient balance cost of defense Epitrix induced defense insect herbivory Manduca sexta nitrogen supplementation optimal defense plant secondary metabolites Solanum carolinense 

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REFERENCES

  1. Alchemy Mindworks, Inc. 1997. Graphic Workshop for Windows. Alchemy Mindworks, Inc., Beeton, Ontario, Canada.Google Scholar
  2. Appel, H.M. 1993. The role of phenolics in ecological systems: The importance of oxidation. J. Chem. Ecol. 19:1521–1552.CrossRefGoogle Scholar
  3. 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
  4. 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
  5. 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.CrossRefGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. Birner, J. 1969. Determination of total steroid bases in Solanum species. J. Pharm. Sci. 58:258–259.CrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. Broadway, R.M. 1995. Are insects resistant to plant proteinase inhibitors? J. Insect Physiol. 41:107–116.CrossRefGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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.CrossRefGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. Budini, R., Tonelli, D., and Girotti, S. 1980. Analysis of total phenols using the Prussian Blue method. J. Agric. Food Chem. 28:1236–1238.CrossRefGoogle Scholar
  17. 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
  18. Cipollini, D. F. 1998. The induction of soluble peroxidase activity in bean leaves by wind-induced mechanical perturbation. Am. J. Bot. 85:1586–1591.CrossRefGoogle Scholar
  19. Cipollini, D. F. and Bergelson, J. 2000. Environmental and developmental regulation of trypsin inhibitor activity in Brassica napus. J. Chem. Ecol. 26:1411–1422.CrossRefGoogle Scholar
  20. 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.CrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. Cipollini, M. L. and Levey, D. J. 1997a. Antifungal activity of Solanum fruit glycoalkaloids: implications for frugivory and seed dispersal. Ecology 78:799–809.CrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. 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
  26. Coley, P. D., Bryant, J. P., and Chapin, F. S., III. 1985. Resource availability and plant antiherbivore defense. Science 230:895–899.CrossRefGoogle Scholar
  27. Dixon, R. A. and Paiva, N. L. 1995. Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097.CrossRefGoogle Scholar
  28. Feller, I. C. 1995. Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove (Rhizophora mangle). Ecol. Monogr. 65:477–505.CrossRefGoogle Scholar
  29. 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.CrossRefGoogle Scholar
  30. 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.CrossRefGoogle Scholar
  31. 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.CrossRefGoogle Scholar
  32. 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
  33. Graham, H. 1992. Stabilization of the Prussian Blue color in the determination of polyphenols. J. Agric. Food Chem. 40:801–805.CrossRefGoogle Scholar
  34. 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.CrossRefGoogle Scholar
  35. Hare, J. D. 1983. Seasonal variation in plant-insect associations: utilization of Solanum dulcamara by Leptinotarsa decemlineata. Ecology 64:345–361.CrossRefGoogle Scholar
  36. 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.CrossRefGoogle Scholar
  37. 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
  38. Haukioja, E. S. 1991. Induction of defenses in trees. Annu. Rev. Entomol. 36:25–42.CrossRefGoogle Scholar
  39. 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.CrossRefGoogle Scholar
  40. Hermes, D. A. and Mattson, W. J. 1992. The dilemma of plants: to grow or defend. Q. Rev. Biol. 67:283–335.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. 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.CrossRefGoogle Scholar
  44. 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.CrossRefGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. Jones, C. G., and Hartley, S. E. H. 1999. A protein competition model of phenolic allocation. Oikos 86:27–44.CrossRefGoogle Scholar
  47. 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.CrossRefGoogle Scholar
  48. Karban, R. and Baldwin, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago, Illinois.CrossRefGoogle Scholar
  49. 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.CrossRefGoogle Scholar
  50. 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
  51. Koiwa, H., Bressan, R. A., and Hasegawa, P.M. 1997. Regulation of proteinase inhibitors and plant defense. Trends Plant Sci. 2:379–384.CrossRefGoogle Scholar
  52. Langenheim, J. H. 1994. Higher plant terpenoids: a phytocentric overview of their ecological roles. J. Chem. Ecol. 20:1223–1280.CrossRefGoogle Scholar
  53. 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.CrossRefGoogle Scholar
  54. Linhart, Y. B. 1991. Disease, parasitism, and herbivory: multidimensional challenges in plant evolution. Trends Ecol. Evol. 6:392–396.CrossRefGoogle Scholar
  55. Mauricio, R. 1998. Costs of resistance to natural enemies in field populations of the annual plant, Arabidopsis thaliana. Am. Nat. 151:20–28.PubMedGoogle Scholar
  56. Microsoft, Inc. 1991- 1998. Windows Paint for Windows. Microsoft, Inc., Seattle, Washington.Google Scholar
  57. 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.CrossRefGoogle Scholar
  58. Muzika, R.-M. 1993. Terpenes and phenolics in response to nitrogen fertilization: a test of the carbon/nutrient balance hypothesis. Chemoecology 4:3–7.CrossRefGoogle Scholar
  59. National Institutes of Health. 2000. Image J. V. 1.19. National Institutes of Health. Washington, D.C.Google Scholar
  60. 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.CrossRefGoogle Scholar
  61. 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.CrossRefGoogle Scholar
  62. 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
  63. 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.CrossRefGoogle Scholar
  64. Simple Interactive Statistical Analysis. 2001. Bonferroni Correction On-Line. Adjustment for Multiple Comparisons. Simple Interactive Statistical Analysis, http://home.clara.net/sisa/bonhlp.htm.Google Scholar
  65. 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
  66. 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.CrossRefGoogle Scholar
  67. 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.CrossRefGoogle Scholar
  68. Tingey, W. M. 1984. Glycoalkoloids as pest resistance factors. Am. Potato J. 61:157–167.CrossRefGoogle Scholar
  69. 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.CrossRefGoogle Scholar
  70. 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.CrossRefGoogle Scholar
  71. 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
  72. 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
  73. 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.CrossRefGoogle Scholar
  74. 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

Copyright information

© Plenum Publishing Corporation 2002

Authors and Affiliations

  • Martin L. Cipollini
    • 1
  • Eric Paulk
    • 1
  • Donald F. Cipollini
    • 2
  1. 1.Department of BiologyMount BerryUSA
  2. 2.Department of Biological SciencesWright State UniversityDaytonUSA

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