Vegetatio

, Volume 104, Issue 1, pp 273–280 | Cite as

The influence of plant carbon dioxide and nutrient supply on susceptibility to insect herbivores

  • D. E. Lincoln
Indirect Responses to CO2 Enrichment: Interactions With Soil Organisms and Soil Processes

Abstract

The carbon/nutrient ratio of plants has been hypothesized to be a significant regulator of plant susceptibility of leaf-eating insects. As rising atmospheric carbon dioxide stimulates photosynthesis, host plant carbon supply is increased and the accompanying higher levels of carbohydrates, especially starch, apparently ‘dilute’ the protein content of the leaf. When host plant nitrogen supply is limited, plant responses include increased carbohydrate accumulation, reduced leaf protein content, but also increased carbon-based defensive chemicals. No change, however, has been observed in the concentration of leaf defensive allelochemicals with elevated carbon dioxide during host plant growth. Insect responses to carbon-fertilized leaves include increased consumption with little change in growth, or alternatively, little change in consumption with decreased growth, as well as enhanced leaf digestibility, reduced nitrogen use efficiency, and reduced fecundity. The effects of plant carbon and nutrient supply on herbivores appear to result, at least in part, from independent processes affecting secondary metabolism.

Keywords

Herbivory Carbon/Nitrogen ratio Allelochemicals Chemical defense Carbon dioxide 

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References

  1. Akey, D. H. & Kimball, B. A. 1989. Growth and development of the beet armyworm on cotton grown in an enriched carbon dioxide atmosphere. Southwestern Entomol. 14: 255–260.Google Scholar
  2. Akey, D. H., Kimball, B. A. & Mauney, J. R. 1988. Growth and development of the Pink Bollworm,Pectinophora gossypiella (Lepidoptera: Gelechiidae), on bolls of cotton grown in enriched carbon dioxide atmospheres. Envir. Entomol. 17: 452–455.Google Scholar
  3. Bazzaz, F. A. 1990. The response of natural ecosystems to the rising global CO2 levels. Ann. Rev. Ecol. Syst. 21: 167–196.Google Scholar
  4. Bazzaz, F. A., Garbutt, K. & Williams, W. E. 1985. Effects of increased atmospheric carbon dioxide concentration on plant communities. In: Strain, B. R. & Cure, J. D. (eds), Direct Effects of Increased Carbon Dioxide on Vegetation, pp. 155–170, DOE/ER-0238, U. S. Dept. of Energy, Washington.Google Scholar
  5. Bloom, A. J., Chapin, F. S. & Mooney, H. A. 1985. Resource limitation in plants- an economic analogy. Ann. Rev. Ecol. Syst. 16: 363–392.Google Scholar
  6. Bryant, J. P., Chapin, F. S. & Klein, D. R. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40: 357–368.Google Scholar
  7. Bryant, J. P., Chapin, F. S., Reichardt, P. B. & 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
  8. Burkett, B. N. & Schneiderman, H. A. 1974. Roles of oxygen and carbon dioxide in the control of spiracular function inCecropia pupae. Biol. Bull. 147: 274–293.Google Scholar
  9. Butler, G. D., Kimball, B. A. & Mauney, J. R. 1986. Populations ofBemisia tabaci (Homoptea: Aleyrodidae) on cotton grown in open-top field chambers enriched with CO2. Environ. Entomol. 15: 61–63.Google Scholar
  10. Caldwell, M. M. 1971. Solar UV irradiation and the growth and development of higher plants. In: Giese, A. C. (ed), Photophysiology VI, pp. 131–268. Academic Press, New York.Google Scholar
  11. Cave, G. L., Tolley, C. & Strain, B. R. 1981. Effect of carbon dioxide enrichment on chlorophyll content, starch content and starch grain structure inTrifolium subterraneum leaves. Physiol. Plant. 51: 171–174.Google Scholar
  12. Chapin, F. S. 1980. The mineral nutrition of wild plants. Ann. Rev. Ecol. Syst. 11: 261–285.Google Scholar
  13. Coley, P. D. 1987. Interspecific variation in plant antiherbivore properties: The role of habitat quality and rate of disturbance. New Phytol. 106: 251–263.Google Scholar
  14. Coley, P. D., Byrant, J. P. & Chapin, F. S. 1985. Resource availability and plant antiherbivore defense. Science 230: 895–7899.Google Scholar
  15. Cook, A. G. 1977. Nutrient chemicals as phagostimulants forLocusta migratoria (L.). Ecol. Entomol. 2: 113–121.Google Scholar
  16. Ehrlich, P. R. & Raven, P. H. 1964. Butterflies and plants, a study in coevolution. Evolution 18: 586–608.Google Scholar
  17. Fajer, E. D. 1989. The effects of enriched CO2 atmospheres on plant-insect herbivore interactions: growth responses of larvae of the specialist butterfly,Junonia coenia (Lepidoptera: Nymphalidae). Oecologia 81: 514–520.Google Scholar
  18. Fajer, E. D., Bowers, M. D. & Bazzaz, F. A. 1989. The effects of enriched carbon dioxide atmospheres on plant/insect herbivore interactions. Science 243: 1198–1200.Google Scholar
  19. Fajer, E. D., Bowers, M. D. & Bazzaz, F. A. 1991. The effects of enriched CO2 atmospheres on the buckeye butterflyJunonia coenia. Ecology 72: 751–754.Google Scholar
  20. Fajer, E. D., Bowers, M. D. & Bazzaz, F. A. 1992. The effects of enriched CO2 environments on the production of carbon-based allelochemicals inPlantago: a test of the carbon nutrient balance hypothesis. Amer. Naturalist: in press.Google Scholar
  21. Feeny, P. P. 1976. Plant apparency and chemical defense. Rec. Adv. Phytochem. 10: 1–40.Google Scholar
  22. Fox, L. R. & Morrow, P. A. 1983. Estimates of damage by herbivorous insects onEucalyptus trees. Austr. J. Ecol. 8: 139–147.Google Scholar
  23. Gbolade, A. A. & Lockwood, G. B. 1990. Metabolic studies of volatile constituents in tissue cultures ofPetroselinum crispum (Mill) Nyman. J. Plant Physiol. 136: 198–202.Google Scholar
  24. Gershenzon, J. 1984. Changes in the level of plant secondary metabolites under water and nutrient stress. Rec. Adv. Phytochem. 18: 273–320.Google Scholar
  25. Hahlbrock, K. & Scheel, D. 1989. Physiology and molecular biology of phenylpropanoid metabolism. Ann. Rev. Plant. Physiol. 40: 347–369.Google Scholar
  26. Haslam, E. 1986. Secondary metabolism — fact and fiction. Nat. Prod. Rep. 1986: 217–249.Google Scholar
  27. Hoyle, G. 1960. The action of carbon dioxide gas on an insect spiracular muscle. J. Insect Physiol. 4: 63–79.Google Scholar
  28. Janzen, D. H. 1974. Tropical blackwater rivers, animals, and mast fruiting by the Dipterocarpaceae. Biotropica 6: 69–103.Google Scholar
  29. Johnson, R. H. & Lincoln, D. E. 1990. Sagebrush and grass-hopper responses to atmospheric carbon dioxide concentration. Oecologia 84: 103–110.Google Scholar
  30. Johnson, R. H. & Lincoln, D. E. 1991. Sagebrush carbon allocation patterns and grasshopper nutrition: the influence of carbon dioxide enrichment and soil mineral limitation. Oecologia 87: 127–134.Google Scholar
  31. Jonasson, S., Bryant, J. P., Chapin, F. S. & Andersson, M. 1986. Plant phenols and nutrients in relation to variations in climate and rodent grazing. Amer. Naturalist 128: 394–408.Google Scholar
  32. Lambers, H. 1993. Rising CO2, secondary plant metabolism, plant-herbivore interactions and litter decomposition. Theoretical considerations. Vegetatio 104/105: 263–271.Google Scholar
  33. Lincoln, D. E. & Couvet, D. 1989. The effect of carbon supply on allocation to allelochemicals and caterpiller consumption of peppermint. Oecologia 78: 112–114.Google Scholar
  34. Lincoln, D. E., Sionit, N. & Strain, B. R. 1984. Growth and feeding responses ofPseudopleusia includens (Lepidoptera: Noctuidae) to host plants grown in controlled carbon dioxide atmospheres. Env. Entomol. 13: 1527–1530.Google Scholar
  35. Lincoln, D. E., Couvet, D. & Sionit, N. 1986. Response of an insect herbivore to host plants grown in enriched carbon dioxide atmospheres. Oecologia 69: 556–560.Google Scholar
  36. MacCracken, M. C. & Luther, F. M. 1985. Detecting the Climatic Effects of Increasing Carbon Dioxide. US Dept of Energy DOE/ER-0235, Washington.Google Scholar
  37. Margna, U., Margna, E. & Vainjarv, T. 1989. Influence of nitrogen nutrition on the utilization of l-phenylalanine for building flavonoids in buckwheat seedling tissues. J. Plant Physiol. 134: 697–702.Google Scholar
  38. Mattson, W. 1980. Nitrogen and herbivory. Ann. Rev. Ecol. Syst. 11: 119–162.Google Scholar
  39. Mihaliak, C. A. & Lincoln, D. E. 1985. Growth pattern and carbon allocation to volatile leaf terpenes under nitrogenlimiting conditions inHeterotheca subaxillaris (Asteraceae). Oecologia 66: 423–426.Google Scholar
  40. Mihaliak, C. A. & Lincoln, D. E. 1989. Plant biomass partitioning and chemical defense: response to defoliation and nitrate limitation. Oecologia 80: 122–126.Google Scholar
  41. Montjoy, C. S. 1992. The effects of elevated carbon dioxide on the growth, reproduction and food consumption byMelanoplus differentialis andMelanoplus sanguinipes feeding onAndropogon gerardii. M. Sc. Thesis. University of South Carolina, Columbia.Google Scholar
  42. Nafziger, E. D. & Koller, H. R. 1976. Influence of leaf starch concentration on carbon dioxide assimilation in soybean. Plant Physiol. 57: 560–563.Google Scholar
  43. Nicholas, J. & Sillans, D. 1989. Direct effects of atmospheric carbon dioxide on insects. Ann. Rev. Entomol. 20: 111–130.Google Scholar
  44. Oechel, W. & Strain, B. R. 1985. Native species responses to increased carbon dioxide concentration. In: Strain, B. R. & Cure, J. D. (eds) Direct Effects of Increasing Carbon Dioxide on Vegetation. DOE/ER-0238, Department of Energy, Washington.Google Scholar
  45. Osbrink, W. L. A., J. T., Trumble & Wagner, R. E. 1987. Host suitability ofPhaseolus lunata forTrichoplusia ni (Lepidoptera: Noctuidae) in controlled carbon dioxide atmospheres. Environ. Entomol. 16: 639–644.Google Scholar
  46. Phillips, R. & Henshaw, G. G. 1977. The regulation of synthesis of phenolics in stationary phase cell cultures ofAcer pseudoplatanus L. J. Exp. Bot. 28: 785–794.Google Scholar
  47. Price, P. W., Bouton, C. E., Gross, P., McPheron, B. A., Thompson, J. N. & Weis, A. E. 1980. Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Ann. Rev. Ecol. Syst. 11: 41–65.Google Scholar
  48. Price, P. W., Waring, G. L., Julkunen-Tiitto, R., Tahvanainen, J., Mooney, H. A. & Craig, T. P. 1989. Carbon-nutrient balance hypothesis in within-species phytochemical variation ofSalix lasiolepis. J. Chem. Ecol. 15: 1117–1131.Google Scholar
  49. Reichle, D. E., Goldstein, R. A., Van, Hook, R. Ia. and Dodson, G. J. (1973). Analysis of insect consumption in a forest canopy. Ecology 54: 1076–1084.Google Scholar
  50. Schneider, S. H. 1987. The greenhouse effect: science and policy. Science 243: 771–781.Google Scholar
  51. Scriber, J. M. 1977. Limiting effects of low leaf-water content on the nitrogen utilization, energy budget, and larval growth ofHyalophora cecropia (Lepidoptera: Saturniidae). Oecologia 28: 269–287.Google Scholar
  52. Scriber, J. M. & Slansky, F. 1981. The nutritional ecology of immature insects. Ann. Rev. Entomol. 26: 183–211.Google Scholar
  53. Slansky, F. & Rodriguez, J. G. (eds) 1987. Nutritional Ecology of Insects, Mites, Spiders and Related Invertebrates. Wiley Interscience, New York.Google Scholar
  54. Strain, B. R. & Bazzaz, F. 1983. Terrestrial plant communities. In CO2 and Plants: The Response of Plants to Rising Levels of Atmospheric Carbon Dioxide AAAS Selected Symposium 84. Westview Press, Boulder.Google Scholar
  55. Strain, B. R. & Cure, J. D. (eds) 1985. Direct Effects of Increasing Carbon Dioxide on Vegetation. DOE/ER-0238. pp. 286. U.S. Department of Energy, Washington.Google Scholar
  56. Takeda, J. 1988. Light-induced synthesis of anthocyanin in carrot cells in suspension. J. Exp. Bot. 39: 1065–1077.Google Scholar
  57. Tans, P. P., Fung, I. Y. & Takahashi, T. 1990. Observational constraints on the global atmospheric CO2 budget. Science 247: 1431–1438.Google Scholar
  58. Tevini, M., Braun, J. & Fieser, G. 1991. The protective function of the epidermal layer of rye seedlings against ultraviolet-B radiation. Photochem. Photobiol. 53: 329–333.Google Scholar
  59. Tsukaya, H., Ohshima, T., Naito, S., Chino, M. & Komeda, Y. 1991. Sugar-dependent expression of the CHS-A gene for chalcone synthase from petunia in transgenicArabadopsis. Plant. Physiol. 97: 1414–1421.Google Scholar
  60. Vu, J. C. V., Allen, L. H. & Bowes, G. 1989. Leaf ultrastructure, carbohydrates and protein of soybeans grown under CO2 enrichment. Environ. Exp. Bot. 29: 141–147.Google Scholar
  61. Waterman, P. G., Ross, J. A. M. & McKey, D. B. 1984. Factors affecting levels of some phenolic compounds, digestibility, and nitrogen content of the mature leaves ofBarteria fistulosa (Passifloraceae). J. Chem. Ecol. 10: 387–401.Google Scholar
  62. Williams, W. E., Garbutt, K., Bazzaz, F. A. & Vitousek, P. M. 1986. The response of plants to elevated CO2 IV. Two deciduous-forest tree communities. Oecologia 69: 454–459.Google Scholar
  63. Zangerl, A. R. & Bazzaz, F. A. 1984. The response of plants to elevated CO2. II. Competitive interactions among annual plants under varying light and nutrients. Oecologia 62: 412–417.Google Scholar

Copyright information

© Kluwer Academic Publishers 1993

Authors and Affiliations

  • D. E. Lincoln
    • 1
  1. 1.Department of Biological SciencesUniversity of South CarolinaColumbiaUSA

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