Skip to main content
Log in

Rising CO2, secondary plant metabolism, plant-herbivore interactions and litter decomposition

Theoretical considerations

  • Indirect Responses to CO2 Enrichment: Interactions With Soil Organisms and Soil Processes
  • Published:
Vegetatio Aims and scope Submit manuscript

Abstract

A brief account is given of the ecological significance of quantitatively important secondary plant compounds, mainly those of a phenolic nature, in herbivory and decomposition. Phenolic compounds accumulate to a greater extent in slow-growing species than in fast-growing ones, particularly when soil conditions (nutrients, water) restrict growth. Two hypotheses to explain the increased concentration of phenolics when soil conditions are unfavorable are presented. The first hypothesis (the ‘carbon supply model of secondary plant metabolism’) considers the increased levels of non-structural carbohydrates as the major trigger. The second hypothesis (the ‘amino acid diversion model of secondary plant metabolism’) states that increased accumulation of phenolics stems from a decreased use of a common precursor (phenylalanine or tyrosine) for protein synthesis. Current experimental evidence, though still fairly limited, supports the second hypothesis, but further testing is required before the first model can be rejected. So far, there is very little evidence for a direct effect of atmospheric CO2 on the concentration of secondary compounds in higher plants. However, there are likely to be indirect effects, due to a stronger limitation by the nitrogen supply in plants whose growth has been promoted by atmospheric CO2. It is concluded that it is very likely that phenolic compounds accumulate to a greater extent in plants exposed to elevated CO2, due to a greater limitation of nutrients, rather than as a direct effect of elevated CO2.

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

  • Aber, J. D. & Melillo, J. M. 1982. Nitrogen immobilization in decaying hardwood leaf litter as a function of initial nitrogen and lignin content. Can. J. Bot. 60: 2263–2269.

    Google Scholar 

  • Akey, D. H. & Kimball, B. A. 1989. Growth and development of the beet armyworm on cotton grown in enriched carbon dioxide atmosphere. Southwestern Entomol. 14: 255–260.

    Google Scholar 

  • 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 atmosphere. Envir. Entomol. 17: 452–455.

    Google Scholar 

  • Baas, W. J. 1989. Secondary plant compounds, their ecological significance and consequences for the carbon budget. Introduction of the carbon/nutrient cycle theory. In: Lambers, H., Cambridge, M. L., Konings, H. & Pons, T. L. (eds), Causes and consequences of variation in growth rate and productivity of higher plants, pp. 313–340. SPB Academic Publishing, The Hague.

    Google Scholar 

  • Baldwin, I. T., Olson, R. K. & Reiners, W. A. 1983. Protein-binding phenolics and the inhibition of nitrification in subalpine balsam fir soils. Soil Biol. Biochem. 15: 419–423.

    Google Scholar 

  • Berendse, F., Berg, B. & Bosatta, E. 1987. The effect of lignin and nitrogen on the decomposition of litter in nutrient-poor ecosystems: a theoretical approach. Can. J. Bot. 65: 1116–1120.

    Google Scholar 

  • Berg, B. & Staaf, H. 1981. Leaching, accumulation and release of nitrogen in decomposing forest litter. Ecol. Bull. 33: 163–178.

    Google Scholar 

  • Brown, S. A. 1981. Coumarins. In: Conn, E. E. (ed), The Biochemistry of Plants, Vol. 7, pp. 269–300. Academic Press, New York.

    Google Scholar 

  • 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 

  • 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 

  • Chou, C.-H & Kuo, Y.-L. 1986. Allelopathic research of subtropical vegetation in Taiwan. Alleopathic exclusion of understorey byLeucaena leucophylla (Lam.) de Wit. J. Chem. Ecol. 12: 1431–1448.

    Google Scholar 

  • Coley, P. D. 1983. Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecological Monographs 53: 209–233.

    Google Scholar 

  • Coley, P. D. 1986. Costs and benefits of defense by tannins in a neotropical tree. Oecologia 70: 238–241.

    Google Scholar 

  • Couteaux, M.-M., Mousseau, M., Célérier, M.-L. & Bottner, P. 1991. Increased atmospheric CO2 and litter quality: decomposition of sweet chestnut leaf litter with animal food webs of different complexities. Oikos 61: 54–64.

    Google Scholar 

  • Curtis, P. S., Drake, B. G., Leadley, P. W., Arp, W. J. & Whigham, D. F. 1989a. Growth and senescence in plant communities exposed to elevated CO2 on an estuarine marsh. Oecologia 78: 20–26.

    Google Scholar 

  • Curtis, P. S., Drake, B. G. & Whigham, D. F. 1989b. Nitrogen and carbon dynamics in C3 and C4 estuarine marsh plants grown under elevated CO2 in situ. Oecologia 78: 297–301.

    Google Scholar 

  • Dicke, M. & Sabelis, M. W. 1989. Does it pay to advertize for body guards? In: Lambers, H., Cambridge, M. L., Konings, H. & Pons, T. L. (eds), Causes and consequences of variation in growth rate and productivity of higher plants, pp. 341–358. SPB Academic Publishing, The Hague.

    Google Scholar 

  • Fajer, E. D. 1989. The effect 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 

  • Fajer, E. D., Bowers, M. D. & Bazzaz, F. A. 1989. The effect of enriched carbon dioxide atmospheres on plant/insect herbivore interactions. Science 243: 1198–1200.

    Google Scholar 

  • Fajer, E. D., Bowers, M. D. and Bazzaz, F. A. 1989. The effects of enriched CO2 atmospheres on the buckeye butterfly,Junonia coenia. Ecology 72: 751–754.

    Google Scholar 

  • Fox, R. H., Myers, R. J. K. & Vallis, I. 1990. The nitrogen mineralization rate of legume residues in soil as influenced by their polyphenol, lignin, and nitrogen contents. Plant Soil 129: 251–259.

    Google Scholar 

  • Gershenzon, J. 1984. Changes in the levels of plant secondary metabolites under water and nutrient stress. In: Timmermann, B. N., Steelink, C. & Loewus, F. A. (eds), Phytochemical Adaptations to Stress, Rec. Adv. Phytochem., Vol. 18, pp. 273–320. Plenum, New York.

    Google Scholar 

  • Glyphis, J. P. & Puttick,m G. M. 1989. Phenolics, nutrition and insect herbivory in some garrigue and maquis plant species. Oecologia 78: 259–263.

    Google Scholar 

  • Grisebach, H. 1981. Lignins. In: Conn, E. E. (ed). The Biochemistry of Plants, Vol. 7, pp. 457–478. Academic Press, New York.

    Google Scholar 

  • Gross, G. G. 1981. Penolic acids. In: Conn, E. E. (ed). The Biochemistry of Plants, Vol. 7, pp. 301–316. Academic Press, New York.

    Google Scholar 

  • Harborne, J. B. 1988. Introduction to Ecological Biochemistry. Academic Press, London

    Google Scholar 

  • Haslam, E. 1981. Vegetable tannins. In: Conn, E. E. (ed). The Biochemistry of Plants, Vol. 7, pp. 527–556. Academic Press, New York.

    Google Scholar 

  • Haslam, E. 1988. Plant polyphenols (syn. vegetable tannins) and chemical defense — a reappraisal. J. Chem. Ecol. 14: 1789–1805.

    Google Scholar 

  • Howe, H. F. & Westley, L. C. 1988. Ecological relationships of Plants and Animals. Oxford University Press, New York

    Google Scholar 

  • Johnson, N. D., Brain, S. A. & Ehrlich, P. R. 1985. The role of leaf resin in the interaction betweenEriodictyon californicum (Hydrophyllaceae) and its herbivore,Trirhabda diducta (Crysomelida) Oecologia 66: 106–110.

    Google Scholar 

  • Johnson, R. H. & Lincoln, D. E. 1990. Sagebrush and grassshopper responses to atmospheric carbon dioxide concentration. Oecologia 84: 103–110.

    Google Scholar 

  • Kimmerer, T. W. & Potter, D. A. 1987. Nutritional quality of specific leaf tissues and selective feeding by a specialist leafminer. Oecologia 71: 548–551.

    Google Scholar 

  • Krause, J. & Reznik, H. 1972. Die Einfluss der Phosphat-und Nitratversorgung auf den Phenylpropanoidstofwechsel in Buchweizenblättern (Fagopyrum esculentum Moench). Z. Pflanzenphysiol. 68: 134–143.

    Google Scholar 

  • Kuiters, A. T. 1990. Role of phenolic substances from decomposing forest litter in plant-soil interactions. Acta Bot. Neerl. 39: 329–348.

    Google Scholar 

  • Laine, K. M. & Henttonen, H. 1987. Phenolics/nitrogen rations in the blueberryVaccinium myrtillus in relation to temperature and microtine density in Finnish Lapland. Oikos 50: 389–395.

    Google Scholar 

  • Lamb, D. 1975. Patterns of nitrogen mineralization in the forest floor of stands ofPinus radiata on different soils. J. Ecol. 63: 615–625.

    Google Scholar 

  • Lambers, H. & Poorter, H. 1992. Inherent variation in growth rate between higher plants: A search for physiological causes and ecological consequences. Adv. Ecol. Res. 22, in press

  • Lambers, H. & Rychter, A. 1989. The biochemical background of variation in respiration rate: respiratory pathways and chemical composition. In: Lambers, H., Cambridge, M. L., Konings, H. & Pons, T. L. (eds), Causes and Consequences of Variation in Growth Rate and Productivity of Higher Plants, pp. 199–225. SPB Academic Publishing, The Hague.

    Google Scholar 

  • Larsson, S., Wirén, A., Lundgren, L. & Ericsson, T. 1986. Effects of light and nutrient stress on leaf phenolic chemistry inSalix dasyclados and susceptibility toGalerucella lineola. Oikos 47: 205–210.

    Google Scholar 

  • Lewis, N. G. & Yamomoto, E. 1990. Lignin: occurrence, biogenesis and biodegradation. Annu. Rev. Plant Physiol. Mol. Biol. 41: 455–496.

    Google Scholar 

  • Lincoln, D. E. 1980. Leaf resin flavonoids ofDiplacus aurantiacus. Biochem. Syst. Ecol., 8, 397–400

    Google Scholar 

  • Lincoln, D. E. & Couvet, D. 1989. The effect of carbon supply on allelochemicals and caterpillar consumption of peppermint. Oecologia 78: 112–114.

    Google Scholar 

  • Lincoln, D. E., Newton, F. S., Ehrlich, P. R., & Williams, K. S. 1982. Coevolution of the checkerspot butterflyEuphydras chalcedona and its larval food plantDiplacus auranticus: Larval response to protein and leaf resin. Oecologia 52: 216–223.

    Google Scholar 

  • Lincoln, D. E., Sionit, N. & Strain, B. R. 1984. Growth and feeding response ofPseudoplusia includens to host plants grown in controlled carbon dioxide atmospheres. Environ. Entomol. 13: 1527–1530.

    Google Scholar 

  • Lincoln, D. E., Couvet, D. & Sionit, N. 1986. Responses of an insect herbivore to host plants grown in carbon dioxide enriched atmospheres. Oecologia 69: 556–560.

    Google Scholar 

  • Lindroth, R. L. 1989. Biochemical detoxication: mechanism of different tiger swallowtail tolerance to phenolic glycosides. Oecologia 81: 219–224.

    Google Scholar 

  • Lindroth, R. L. & Batzli, G. O. 1984. Plant phenolics as chemical defenses: effects of natural phenolics on survival and growth of prairie voles (Microtus ochrogaster). J. Chem. Ecol. 10: 229–244.

    Google Scholar 

  • Lindroth, R. L. & Peterson, S. S. 1988. Effects of plant phenols on performance of southern aemyworm larvae. Oecologia 75: 185–189.

    Google Scholar 

  • Maby, T. J. & Ulubelen, A. 1980. Chemistry and utilization of phenylpropanoids including flavonoids, coumarins and lignans. Agric. Food Chemistry 28: 188–196.

    Google Scholar 

  • Manuwoto, S. & Scriber, J. M. 1986. Effects of hydrolyzable tannin on growth and development of two species of polyphagous lepidoptera:Spodoptera eridiana andCallosamia prometha. Oecologia 69: 225–230.

    Google Scholar 

  • Margna, U. 1977. Control at the level of substrate supply-An alternative in the regulation of phenylpropanoid accumulation in plant cells. Phytochemistry 16: 419–426.

    Google Scholar 

  • Margna, U., Margna, E. & Vainjärv, T. 1989. Influence of nitrogen nutrition on the utilization of L-phenylalanine for building flavonoids in buckwheat seedlings. J. Plant Physiol. 134: 697–702.

    Google Scholar 

  • Markham, K. R. 1971. A chemotaxonomic approach to he selection of opossum resistant willows and poplars for use in soil conservation. New Zealand J. Science 14: 179–186.

    Google Scholar 

  • McKey, D. 1979. The distribution of secondary compounds within plants. In: Rosenthal, G. A. & Janzen, D. H. (eds), Herbivores, their Interaction with SAecondary Plant Metabolites, pp. 56–134. Academic Press, New York

    Google Scholar 

  • Mihaliak, C. A. & Lincoln, D. E. 1989. Changes in leaf mono-and sesquiterpene metabolism with nitrate-availability and leaf age inHeterotheca subaxillaris. J. Chem. Ecol. 15: 1579–1588.

    Google Scholar 

  • Nicolai, V. 1988. Phenolic and mineral content of leaves influences decomposition in European forest ecosystems. Oecologia 75: 575–579.

    Google Scholar 

  • Phillips, R. & Henshaw, G. G. 1977. The regulation of synthesis of phenolics in stationary cell cultures odAcer pseudoplatanus L. J. Exp. Bot. 28: 785–794.

    Google Scholar 

  • Pirie, A. & Mullins, M. G. 1976. Changes in anthocyanin and phenolics content of grapevine leaf and fruit tissue treated with sucrose, nitrate, and abscisic acid. Plant Physiol. 58: 468–472.

    Google Scholar 

  • Poorter, H. 1991. Interspecific Variation in the Relative Growth Rate of Plants: The Underlying Mechanisms. PhD Thesis, Univ. Utrecht

  • Rees, S. B. & Harborne, J. B. 1985. The role of sesquiterpene lactones and phenolics in the chemical defence of the chicory plant. Phytochemistry 10: 2225–2231.

    Google Scholar 

  • Rhoades, D. F. 1977. Integrated antiherbivore, antidesiccant and ultraviolet screening properties of creosotebush resin. Bioch. Syst. Ecol. 5: 281–290.

    Google Scholar 

  • Stuhlfauth, T. & Fock, H. P. 1990. Effects of whole season CO2 enrichment on the cultivation of a medicinal plant,Digitalis lanata. J. Agron. Crop. Sci. 164: 168–173.

    Google Scholar 

  • Taper, M. L. & Case, T. J. 1987. Interactions between oak tannins and parasite community structure: Unexpected benefits of tannins to cynipid gall-wasps. Oecologia 71, 254–261.

    Google Scholar 

  • Waring, R. H., McDonald, A. J. S., Larsson, S., Ericsson, T., Wiren, A., Arwidsson, E., Ericsson, A. & 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. & McKey, D. 1989. Herbivory and secondary compounds in rain-forest plants. In: Lieth, H. & Werger, M. J. A. (eds), Tropical Rain Forest Ecosystems, pp. 513–536. Elsevier, Amsterdam.

    Google Scholar 

  • Williams, W. E., Garbutt, K., Bazzaz, F. A. & Vitousek, P. M. 1986. The response of plants to elevated CO2. IV. Two deciduous-forest communities. Oecologia 69: 454–459.

    Google Scholar 

  • Wong, S.-C. 1979. Elevated atmospheric partial pressure of CO2 and plant growth. I. Interactions of nitrogen nutrition and photosynthetic capacity in C3 and C4 plants. Oecologia 44: 68–74.

    Google Scholar 

  • Wong, S.-C. 1990. Elevated atmospheric partial pressure of CO2 and plant growth. II. Non-structural carbohydrate content in cotton plants and its effect on growth parameters. Photosynthesis Research 23: 171–180.

    Google Scholar 

  • Yelle, S., Beeson, R. C.Jr., Trudel, M. J. & Gosselin, A. 1989. Acclimation of two tomato species to high atmospheric CO2. I. Sugar and starch concentrations. Plant Physiol. 90: 1465–1472.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lambers, H. Rising CO2, secondary plant metabolism, plant-herbivore interactions and litter decomposition. Vegetatio 104, 263–271 (1993). https://doi.org/10.1007/BF00048157

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00048157

Keywords

Navigation