Evolutionary Ecology

, Volume 14, Issue 4–6, pp 289–314 | Cite as

Plant tolerance and resistance in food webs: community-level predictions and evolutionary implications

  • Jonathan M. Chase
  • Mathew A. Leibold
  • Ellen Simms
Article

Abstract

While evolutionary ecologists emphasize different ways in which plants can evolutionarily respond to herbivory, such as resistance or tolerance, community ecology has lagged in its understanding of how these different plant traits can influence interactions, abundance, composition, and diversity within more complex food webs. In this paper, we present a series of models comparing community level outcomes when plants either resist or tolerate herbivory. We show that resistance and tolerance can lead to very different outcomes. A particularly important result is that resistant species should often coexist locally with other, less resistant competitors, whereas tolerant species should not be able to coexist locally with less tolerant competitors, although priority effects allow them to coexist regionally. We also use these models to suggest some insights into the evolution of these traits within more complex communities. We emphasize how understanding the differential effects of plant tolerance and resistance in food webs provides greater appreciation of a variety of empirical patterns that heretofore have appeared enigmatic.

coexistence food webs herbivory plant resistance plant tolerance priority effects trade-offs 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abrahamson, W.G. and Weis, A.E. (1997) Evolutionary Ecology Across Three Trophic Levels: Goldenrods, Gallmakers, and Natural Enemies. Princeton University Press, Princeton, NJ.Google Scholar
  2. Adler, F.R. and Karban, R. (1994) Defended fortresses or moving targets? Another model of inducible defenses inspired by military metaphors. Am. Nat. 144, 813-832.CrossRefGoogle Scholar
  3. Agrawal, A.A. (1998) Algal defense, grazers, and their interactions in aquatic trophic cascades. Acta Oecologica 19, 331-337.CrossRefGoogle Scholar
  4. Agrawal, A.A., Strauss, S. and Stout, M. (1999) Cost of induced responses and tolerance to herbivory in male and female fitness components of wild radish. Evolution 53, 1093-1104.CrossRefGoogle Scholar
  5. Augustine, D.J. and McNaughton, S.J. (1998) Ungulate effects on the functional species composition of plant communities: herbivore selectivity and plant tolerance. J. Wildlife Manag. 62, 1165-1183.Google Scholar
  6. Berenbaum, M. and Zangerl, A. (1999) Genetic variation in cytochrome P450-based resistance to plant allelochemicals and insecticides. In H. Olff, V.K. Brown and R.H. Drent (eds) Herbivores: Between Plants and Predators. Blackwell Science, Oxford, pp. 55-84.Google Scholar
  7. Chase, J.M. (1999a) Food web effects of prey size-refugia: variable interactions and alternative stable equilibria. Am. Nat. 154, 559-570.PubMedCrossRefGoogle Scholar
  8. Chase, J.M. (1999b) To grow or reproduce? The role of life-history plasticity in food web dynamics. Am. Nat. 154, 571-586.PubMedCrossRefGoogle Scholar
  9. Chase, J.M., Leibold, M.A., Downing, A.L. and Shurin, J.B. (2000) The effects of productivity, herbivory and plant species turnover in grassland food webs. Ecology 81, 2485-2497.CrossRefGoogle Scholar
  10. Chesson, P.L. (1991) A need for niches? Trends Ecol. Evol. 6, 26-28.CrossRefGoogle Scholar
  11. Cline, M. (1994) The role of hormones and apical dominance: new approaches to an old problem in plant development. Physiologia Plantarum 90, 230-237.CrossRefGoogle Scholar
  12. Coley, P.D., Bryant, J.P. and Chapin, F.S. (1985) Resource availability and plant antiherbivore defense. Science 230, 895-899.Google Scholar
  13. De Jong, T.J. and Van der Meijden, E. (2000) On the correlation between allocation to defense and regrowth in plants. Oikos 88, 503-508.CrossRefGoogle Scholar
  14. Ehrlich, P.R. and Raven, P.H. (1964) Butterflies and plants: a study in coevolution. Evolution 18, 586-608.CrossRefGoogle Scholar
  15. Ehrlich, P.R. and Birch, L.C. (1967) The ‘balance of nature’ and ‘population control'. Am. Nat. 101, 97-107.CrossRefGoogle Scholar
  16. Elser, J.J. and Urabe, J. (1999) The stoichiometry of consumer-driven nutrient recycling: theory, observations, and consequences. Ecology 80, 735-751.CrossRefGoogle Scholar
  17. Fineblum, W.L. and Rausher, M.D. (1995) Tradeoff between resistance and tolerance to herbivore damage in a morning glory. Nature 377, 517-520.CrossRefGoogle Scholar
  18. Fretwell, S.D. (1977) The regulation of plant communities by food chains exploiting them. Perspect. Biol. Med. 20, 169-185.Google Scholar
  19. Fritz, R.S. and Simms, E.L. (eds) (1992) Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics. University of Chicago Press, Chicago.Google Scholar
  20. Gause, G.F. (1936) The Struggle for Existence. Williams and Wilkins, Baltimore.Google Scholar
  21. Grammatikopoulos, G., Kyparissis, A., Drilias, P., Petropoulou, Y. and Manetas, Y. (1998) Effects of UV-B radiation on cuticle thickness and nutritional value of leaves in two Mediterranean evergreen sclerophylls. J. Plant Physiol. 153, 506-512.Google Scholar
  22. Grover, J.P. (1994) Assembly rules for communities of nutrient-limited plants and specialist herbivores. Am. Nat. 143, 258-282.CrossRefGoogle Scholar
  23. Grover, J.P. (1995) Competition, herbivory, and enrichment: nutrient-based models for edible and inedible plants. Am. Nat. 145, 746-774.CrossRefGoogle Scholar
  24. Grover, J.P. (1997) Resource Competition. Chapman and Hall, London, UK.Google Scholar
  25. Grover, J.P. and Holt, R.D. (1998) Disentangling resource and apparent competition: realistic models for plant-herbivore communities. J. Theor. Biol. 191, 353-376.CrossRefGoogle Scholar
  26. Hairston, N.G. Jr. and Hairston, N.G. Sr. (1993) Cause-effect relationships in energy flow, trophic structure, and interspecific interactions. Am. Nat. 142, 379-411.CrossRefGoogle Scholar
  27. Hairston, N.G. Jr. and Hairston, N.G. Sr. (1997) Does food web complexity eliminate trophic-level dynamics? Am. Nat. 149, 1001-1007.CrossRefGoogle Scholar
  28. Hairston, N.G., Smith, F.E. and Slobodkin, L.B. (1960) Community structure, population control, and competition. Am. Nat. 94, 421-425.CrossRefGoogle Scholar
  29. Hochwender, C., Marquis, R. and Stowe, K. (2000) The potential for and constraints on the evolution of compensatory ability in Asclepias syriaca. Oecologia 122, 361-370.CrossRefGoogle Scholar
  30. Holt, R.D., Grover, J.D. and Tilman, D. (1994) Simple rules for interspecific dominance in systems with exploitative and apparent competition. Am. Nat. 144, 741-777.CrossRefGoogle Scholar
  31. Hunter, M.D. and Price, P.W. (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73, 724-732.Google Scholar
  32. Huntly, N. (1991) Herbivores and the dynamics of communities and ecosystems. Annu. Rev. Ecol. Syst. 21, 477-504.CrossRefGoogle Scholar
  33. Jefferies, R.L. (2000) Allochthonous inputs: integrating population changes and food-web dynamics. Trends Ecol. Evol. 15, 19-22.PubMedCrossRefGoogle Scholar
  34. Krebs, C.J. et al. (1995) Impact of food and predation on the snowshoe hare cycle. Science 269, 1112-1115.Google Scholar
  35. Leibold, M.A. (1989) Resource edibility and the effects of predators and productivity on the outcomes of trophic interactions. Am. Nat. 134, 922-949.CrossRefGoogle Scholar
  36. Leibold, M.A. (1995) The niche concept revisited: mechanistic models and community context. Ecology 76, 1371-1382.CrossRefGoogle Scholar
  37. Leibold, M.A. (1996) A graphical model of keystone predators in food webs: trophic regulation of abundance, incidence and diversity patterns in communities. Am. Nat. 147, 784-812.CrossRefGoogle Scholar
  38. Leibold, M.A. (1998) Similarity and local co-existence of species in regional biotas. Evol. Ecol. 12, 95-110.CrossRefGoogle Scholar
  39. Leibold, M.A. (1999) Biodiversity and nutrient enrichment in pond plankton communities. Evol. Ecol. Res. 1, 73-95.Google Scholar
  40. Leibold, M.A., Chase, J.M. Shurin, J.B. and Downing, A. (1997) Species turnover and the regulation of trophic structure. Annu. Rev. Ecol. Sys. 28, 467-494.CrossRefGoogle Scholar
  41. Lindeman, R.L. (1942) The trophic-dynamic aspect of ecology. Ecology 23, 399-418.CrossRefGoogle Scholar
  42. MacArthur, R.H. (1972) Geographical Ecology: Patterns in the Distribution of Species. Princeton University Press, Princeton, New Jersey.Google Scholar
  43. Marquis, R.J. (1996) Plant architecture, sectoriality and plant tolerance to herbivores. Vegetatio 127, 85-97.CrossRefGoogle Scholar
  44. Mauricio, R., Rausher, M.D. and Burdick, D.S. (1997) Variation in the defense strategies of plants: are resistance and tolerance mutually exclusive? Ecology 78, 101-1311.CrossRefGoogle Scholar
  45. Van der Meijden, E., Wijn, H. and Verkaar, J. (1988) Defence and regrowth: alternative plant strategies in the struggle against herbivores. Oikos 51, 355-363.Google Scholar
  46. Moen, J., Gardfjell, H. Oksanen, L., Ericson, L. and Ekerholm, P. (1993) Grazing by food-limited microtine rodents on a productive experimental plant community: does the “green desert” exist? Oikos 68, 401-413.Google Scholar
  47. Mole, S. (1994) Trade-offs and constraints in plant-herbivore defence theory: a life-history perspective. Oikos 71, 3-12.Google Scholar
  48. Morris, W.F. and Dwyer, G. (1997) Population consequences of constitutive and inducible resistance: herbivore spatial spread. Am. Nat. 149, 1071-1090.CrossRefGoogle Scholar
  49. Murdoch, W.W. (1966) Community structure, population control, and competition: a critique. Am. Nat. 100, 219-226.CrossRefGoogle Scholar
  50. Murdoch, W.W., Nisbet, R.M., McCaughley, E., de Roos, A.M. and Gurney, W.S.C. (1998) Plankton abundance and dynamics across nutrient levels: tests of hypotheses. Ecology 79, 1339-1356.CrossRefGoogle Scholar
  51. Oksanen, L. (1991) Trophic levels and trophic dynamics: A consensus emerging? Trends Ecol. Evol. 6, 58-60.CrossRefGoogle Scholar
  52. Oksanen, L., Fretwell, S.D., Arrüda, J. and Nïemala P. (1981) Exploitation ecosystems in gradients of primary productivity. Am. Nat. 118, 240-261.CrossRefGoogle Scholar
  53. Oksanen, L. and Oksanen, T. (2000) The logic and realism of the hypothesis of exploitation ecosystems. Am. Nat. 155, 703-723.PubMedCrossRefGoogle Scholar
  54. Olff, H. and Ritchie, M.E. (1998) Effects of herbivores on grassland plant diversity. Trends Ecol. Evol. 13, 261-265.CrossRefGoogle Scholar
  55. Olson, B.E. and Richards, J.H. (1988) Tussock regrowth after grazing: intercalary meristem and axillary bud activity of tillers of Agropyron desertorum. Oikos 51, 374-382.Google Scholar
  56. Phillips, O.M. (1974) The equilibrium and stability of simple marine systems. II. Herbivores. Archiv für Hydrobiologie 73, 310-333.Google Scholar
  57. Polis, G.A. (1999) Why are parts of the world green? Multiple factors control productivity and the distribution of biomass. Oikos 86, 3-15.Google Scholar
  58. Polis, G.A. and Strong, D.R. (1996) Food web complexity and community dynamics. Am. Nat. 147, 813-846.CrossRefGoogle Scholar
  59. Ritchie, M.E. and Tilman, D. (1995) Response of legumes to herbivores and nutrients during succession on a nitrogen-poor soil. Ecology 76, 2648-2655.CrossRefGoogle Scholar
  60. Ritchie, M.E., Tilman, D. and Knops, J.M.H. (1998) Herbivore effects on plant and nitrogen dynamics in oak savanna. Ecology 79, 165-177.CrossRefGoogle Scholar
  61. Rosenthal, J.P. and Kotanen, P.M. (1994) Terrestrial plant tolerance to herbivory. Trends Ecol. Evol. 9, 145-148.CrossRefGoogle Scholar
  62. Rosenzweig, M.L. (1995) Species Diversity in Space and Time. Cambridge University Press, Cambridge, UK.Google Scholar
  63. Schmitz, O.J. (1994) Resource edibility and trophic exploitation in an old-field food web. Proceedings of the National Academy of Sciences (USA) 91, 5364-5367.CrossRefGoogle Scholar
  64. Schmitz, O.J. (1997) Press perturbations and the predictability of ecological interactions in a food web. Ecology 78, 55-69.CrossRefGoogle Scholar
  65. Simms, E.L. (1992) Costs of plant resistance to herbivory. In R.S. Fritz and E.L. Simms Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics. (eds) University of Chicago Press, Chicago, pp. 392-425.Google Scholar
  66. Slobodkin, L., Smith, F. and Hairston, N. (1967) Regulation in terrestrial ecosystems, and the implied balance of nature. Am. Nat. 101, 109-124.CrossRefGoogle Scholar
  67. Sterner, R. and Hesson, D.O. (1994) Algal nutrient limitation and the nutrition of aquatic herbivores. Annu. Rev. Ecol. Syst. 25, 1-29.CrossRefGoogle Scholar
  68. Stowe, K.A. (1998) Experimental evolution of resistance in Brassica rapae: correlated response to disease resistance and tolerance. Evolution 52, 703-712.CrossRefGoogle Scholar
  69. Stowe, K.A., Marquis, R.J., Hochwender, C.G. and Simms, E.L. (2000) The evolutionary ecology of tolerance to consumer damage. Annu. Rev. Ecol. Syst. 31, 565-595.CrossRefGoogle Scholar
  70. Strauss, S.Y. and Agrawal, A.A. (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol. Evol. 14, 179-185.PubMedCrossRefGoogle Scholar
  71. Tiffin, P. (2000) Are tolerance, avoidance, and antibiosis evolutionarily and ecologically equivalent responses of plants to herbivores? Am. Nat. 155, 128-138.PubMedCrossRefGoogle Scholar
  72. Tilman, D. (1982) Resource Competition and Community Structure. Princeton University Press, Princeton, New Jersey.Google Scholar
  73. Tilman, D. (1988) Plant Strategies and the Dynamics and Structure of Plant Communities. Princeton University Press, Princeton, New Jersey.Google Scholar
  74. Tilman, D. and Pacala, S. (1993) The maintenance of species richness in plant communities. In R.E. Ricklefs and D. Schluter (eds) Species Diversity in Ecological Communities: Historical and Geographical Perspectives. University of Chicago Press, Chicago, pp. 12-25.Google Scholar
  75. Turchin, P., Oksanen, L., Ekerholm, P. and Oksanen, T. (2000) Are lemmings prey or predators? Nature 405, 562-564.PubMedCrossRefGoogle Scholar
  76. Underwood, N.C. (1999) The influence of plant and herbivore characteristics on the interaction between induced resistance and herbivore population dynamics. Am. Nat. 153, 282-294.CrossRefGoogle Scholar
  77. Vance, R.R. (1978) Predation and resource partitioning in one-predator-two prey model communities. Am. Nat. 112, 797-813.CrossRefGoogle Scholar
  78. Vanni, M.J. and Layne C.D. (1997) Nutrient recycling and herbivory as mechanisms in the “top-down” effect of fish on algae in lakes. Ecology 78, 21-40.CrossRefGoogle Scholar
  79. Waide, R.B., Willig, M.R., Steiner, C.F., Mittelbach, G.G., Gough, L., Dodson, S.I., Juday, G.P. and Parameter, R. (1999) The relationship between primary productivity and species richness. Annu. Rev. Ecol. Syst. 30, 257-300.CrossRefGoogle Scholar
  80. White, T.C.R. (1993) The Inadequate Environment: Nitrogen and the Abundance of Animals. Springer-Verlag, Berlin, Germany.Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Jonathan M. Chase
    • 1
  • Mathew A. Leibold
    • 2
  • Ellen Simms
    • 3
  1. 1.Department of Biological SciencesUniversity of PittsburghPittsburghU.S.A.
  2. 2.Department of Ecology and EvolutionUniversity of ChicagoChicagoU.S.A.
  3. 3.Department of Integrative BiologyUniversity of CaliforniaBerkeleyU.S.A.

Personalised recommendations