Evolutionary Ecology

, Volume 14, Issue 4–6, pp 331–352

Will plant vigor and tolerance be genetically correlated? Effects of intrinsic growth rate and self-limitation on regrowth

  • Arthur E. Weis
  • Ellen L. Simms
  • Michael E. Hochberg


Plants are known to maintain fitness despite herbivore attack by a variety of damage-induced mechanisms. These mechanisms are said to confer tolerance, which can be measured as the slope of fitness over the proportion of plant biomass removed by herbivore damage. It was recently supposed by Stowe et al. (2000) that another plant property, general vigor, has little effect on tolerance. We developed simple models of annual monocarpic plants to determine if a genetic change in components of growth vigor will also change the fitness reaction to damage. We examined the impact of intrinsic growth rate on the tolerance reaction norm slope assuming plants grow geometrically, i.e., without self-limitation. In this case an increase in intrinsic growth rate decreases tolerance (the reaction norm slope becomes more negative). A logistic growth model was used to examine the impact of self-limiting growth on the relationship between intrinsic growth rate and the tolerance reaction norm slope. With self-limitation, the relationship is sensitive to the timing of attack. When attack is early and there is time for regrowth, increasing growth rate increases tolerance (slope becomes less negative). The time limitations imposed by late attack prevent appreciable regrowth and induce a negative relationship between growth rate and tolerance. In neither of these simple cases will the correlation between vigor and tolerance constrain selection on either trait. However, a positive correlation between growth rate and self-limitation will favor fast growth/strong self-limitation in a high-damage environment, but slow growth/weak self-limitation in a low-damage environment. Thus, fundamental growth rules that determine vigor have constitutive effects on tolerance. The net costs and benefits of damage-induced tolerance mechanisms will thus be influenced by the background imposed by fundamental growth rules.

growth rate herbivory plant defense tolerance 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  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. Ackerly, D. (1999) Self-shading, carbon gain and leaf dynamics: a test of alternative optimality models. Oecologia 119, 300-310.CrossRefGoogle Scholar
  3. Ackerly, D.D. and Bazzaz, F.A. (1995) Leaf dynamics, self-shading and carbon gain in seedlings of a tropical pioneer tree. Oecologia 101, 289-298.CrossRefGoogle Scholar
  4. Amir, S. and Cohen, D. (1990) Optimal reproductive effort and the timing of reproduction of annual plants in a randomly varying environment. J. Theor. Biol. 147, 17-42.Google Scholar
  5. Augspurger, C.K. (1984) Light requirements of neotropical tree seedlings: a comparative study of growth and survival. J. Ecol 72, 777-795.CrossRefGoogle Scholar
  6. Belsky, A.J. (1986) Does herbivory benefit plants? A review of the evidence. Am. Nat. 127, 870-892.CrossRefGoogle Scholar
  7. Benner, B.L. (1988) Effects of apex removal and nutrient supplementation on branching and seed production in Thlaspi arvense (Brassicaceae). Am. J. Bot. 75, 645-651.CrossRefGoogle Scholar
  8. Bergelson, J. and Crawley, M.J. (1992) The effects of grazing on the performance of individuals and populations of scarlet gilia, Ipomopsis aggregata. Oecologia 90, 435-441.CrossRefGoogle Scholar
  9. Bilbrough, C.J. and Richards, J.H. (1993) Growth of sagebrush and brittlebush following simulated winter browsing: mechanisms of tolerance. Ecology 74, 481-492.CrossRefGoogle Scholar
  10. Blackman, V.H. (1919) The compound interest law and plant growth. Ann. Bot. 33, 353-360.Google Scholar
  11. Brokaw, N.V.L. (1987) Gap-phase regeneration of three pioneer species in a topical forest. J. Ecol. 75, 9-19.CrossRefGoogle Scholar
  12. Coley, P., Bryant, J.P. and Chapin III, F.S. (1985) Resource availability and plant antiherbivore defense. Science 230, 895-899.Google Scholar
  13. De Jong, G. (1990) Quantitative genetics of reaction norms. J. Evolutionary Biol 3, 447-468.CrossRefGoogle Scholar
  14. De Jong, T. and Van der Meijden, E. (2000) On the correlation between allocation to defense and regrowth in plants. Oikos 88, 503-508.CrossRefGoogle Scholar
  15. Field, C.B. (1983) Allocating leaf nitrogen for the maximization of carbon gain: leaf age as a control on the allocation program. Oecologia 56, 341-347.CrossRefGoogle Scholar
  16. Futuyma, D.J. and Philippi, T.E. (1987) Genetic variation and covariation in responses to host plants by Alsophila pometaria (Lepidoptera: Geometridae). Evolution 41, 269-279.CrossRefGoogle Scholar
  17. Geber, M.A. (1990) The cost of meristem limitation in Polygonum arenastrum: negative genetic correlations between fecundity and growth. Evolution 44, 799-819.CrossRefGoogle Scholar
  18. Givnish, T.J. (1995) Plant stems: biomechanical adaptation for energy capture and influence on species distributions. In B.L. Gartner (ed.) Plant Stems: Physiology and Functional Morphology. Academic Press, New York, NY, pp. 3-49.Google Scholar
  19. Gold, W.G. and Caldwell, M.M. (1990) The effect of the spatial pattern of defoliation on regrowth of a tussock grass, III. Photosynthesis, canopy structure and light interception. Oecologia 82, 12-17.CrossRefGoogle Scholar
  20. Hendrix, S.D. (1979) Compensatory reproduction in a biennial herb Pastinaca sativa following insect Depressaria pastinacella defloration. Oecologia 42, 107-118.Google Scholar
  21. Hendrix, S.D. and Trapp, E.J. (1989) Floral herbivory in Pastinaca sativa: do compensatory responses offset reductions in fitness? Evolution 43, 891-895.CrossRefGoogle Scholar
  22. Hilbert, D.W., Swift, D.M., Deteling, J.K. and Dyer, M.I. (1981) Relative growth rates and the grazing optimization hypothesis. Oecologia 51, 14-18.CrossRefGoogle Scholar
  23. Hirose, T. and Werger, M.J.A. (1987) Maximization of daily canopy photosynthesis with respect to the leaf nitrogen allocation pattern in the canopy. Oecologia 72, 520-526.CrossRefGoogle Scholar
  24. 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
  25. Honda, H. and Fisher, J.B. (1978) Tree branch angle: maximizing effective leaf area. Science 199, 888-889.Google Scholar
  26. Horn, H.S. (1971) The Adaptive Geometry of Trees. Princeton University Press, Princeton, NJ.Google Scholar
  27. Hunt, R. (1982) Plant Growth Curves: The Functional Approach to Plant Growth Analysis. Edward Arnold, London, UK.Google Scholar
  28. Islam, Z. and Crawley, M.J. (1983) Compensation and regrowth in ragwort (Senecio jacobeae) attacked by the cinnabar moth (Tyria jacobeae). J. Ecol. 2, 828-843.Google Scholar
  29. Iwasa, Y. and Cohen, D. (1989) Optimal growth schedule of a perennial plant. Am. Nat. 133, 480-505.CrossRefGoogle Scholar
  30. Iwasa, Y. and Kubo, T. (1997) Optimal size of storage for recovery after unpredictable disturbances. Evolutionary Ecol. 11, 41-65.CrossRefGoogle Scholar
  31. Juenger, T. and Bergelson, J. (2000) The evolution of compensation to herbivory in scarlet gilia, Ipomopsis aggregata: herbivore-imposed natural selection and the quantitative genetics of tolerance. Evolution 54, 764-777.PubMedCrossRefGoogle Scholar
  32. Kozlowski, J. (1992) Optimal allocation of resources to growth and reproduction: implications for age and size at maturity. Trends Ecol. Evol. 7, 15-19.CrossRefGoogle Scholar
  33. Krupnick, G.A., Weis, A.E. and Campbell, D.R. (1999) The consequences of floral herbivory for pollinator services to Isomeris arborea. Ecology 80, 125-134.CrossRefGoogle Scholar
  34. Lennartson, T., Toumi, J. and Nilsson, P. (1997) Evidence for an evolutionary history of over-compensation in the grassland biennial Gentianella campestris (Gentianaceae). Am. Nat. 149, 1147-1155.CrossRefGoogle Scholar
  35. Marby, C.M. and Wayne, P.W. (1997) Defoliation of the annual herb Abutilon theophrasti: mechanisms underlying reproductive compensation. Oecologia 111, 225-232.CrossRefGoogle Scholar
  36. 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, 1301-1311.CrossRefGoogle Scholar
  37. McMahon, T. (1973) Size and shape in biology. Science 179, 1201-1204.PubMedGoogle Scholar
  38. Meyer, G.A. (1998) Patterns of defoliation and its effects on photosynthesis and growth of goldenrod. Functional Ecol. 12, 270-279.CrossRefGoogle Scholar
  39. Niklas, K.J. (1988) The role of phyllotactic pattern as a “developmental constraint” on the interception of light by leaf surfaces. Evolution 42, 1-16.CrossRefGoogle Scholar
  40. Nowak, R.S. and Caldwell, M.M. (1984) A test of compensatory photosynthesis in the field: implications for herbivory tolerance. Oecologia 61, 311-318.CrossRefGoogle Scholar
  41. Osterheld, M. (1992) Effect of defoliation intensity on aboveground and belowground relative growth rates. Oecologia 92, 313-316.CrossRefGoogle Scholar
  42. Osterheld, M. and McNaughton, S.J. (1991) Effect of stress and time for recovery on the amount of compensatory growth after grazing. Oecologia 85, 305-313.CrossRefGoogle Scholar
  43. Paige, K. (1992) Overcompensation in response to mammalian herbivory: from mutualistic to antagonistic interactions. Ecology 73, 2076-2085.CrossRefGoogle Scholar
  44. Paige, K. (1999) Regrowth following ungulate herbivory in Ipomopsis aggregata: geographic evidence for overcompensation. Oecologia 118, 316-323.CrossRefGoogle Scholar
  45. Paige, K.N. and Whitham, T.G. (1987) Overcompensation in response to mammalian herbivory: the advantage of being eaten. Am. Nat. 129, 407-416.CrossRefGoogle Scholar
  46. Rosenthal, J.P. and Welter, S.C. (1995) Tolerance to herbivory by a stemboring caterpillar in architecturally distinct maize and wild relatives. Oecologia 102, 146-155.CrossRefGoogle Scholar
  47. Simms, E.L. and Triplett, J.K. (1994) Costs and benefits of plant responses to disease: resistance and tolerance. Evolution 48, 1973-1985.CrossRefGoogle Scholar
  48. Stowe, K.A. (1998) Experimental evolution of resistance in Brassica rapa: correlated response of tolerance in lines selected for glucosinolate content. Evolution 52, 703-712.CrossRefGoogle Scholar
  49. Stowe, K.A., Marquis, R.J., Hochwender, C.G. and Simms, E.L. (2000) The evolutionary ecology of tolerance to consumer damage. Ann. Rev. Ecol Systemat. 31, 565-595.CrossRefGoogle Scholar
  50. Sun, D. (1992) Trampling resistance, recovery and growth rate of 8 plant species. Agri. Ecosyst. Environ. 15, 265-273.CrossRefGoogle Scholar
  51. Tiffen, P. and Rausher, M.D. (1999) Genetic constraints and selection acting on tolerance to herbivory in the common morning glory, Ipomoea purpurea. Am. Nat. 154, 700-716.CrossRefGoogle Scholar
  52. Trumble, Y.T., Kolodny-Hirsch, D.M. and Ting, I.P. (1993) Plant compensation for arthropod herbivory. Ann. Rev. Entomol. 38, 93-119.CrossRefGoogle Scholar
  53. Wareing, P., Khalifa, M. and Terharne, K. (1968) Rate-limiting processes in photosynthesis at saturating light intensities. Nature 220, 453-457.PubMedGoogle Scholar
  54. Weis, A.E. and Hochberg, M.E. (2000) The diverse effects of intraspecific competition on the selective advantage to resistance: a model and its predictions. Am. Nat. 156, 276-292.CrossRefGoogle Scholar
  55. Windel, P.N. and Franz, E.H. (1979) The effects of insect parasitism on plant competition: greenbugs and barley. Ecology 60, 521-529.CrossRefGoogle Scholar
  56. Woledge, J. (1986) The effect of age and shade on the photosynthesis of white clover leaves. Ann. Bot. 57, 257-262.Google Scholar
  57. Yamamura, K. (1997) Optimality in the spatial leaf distribution of the weed Portulaca oleracea L. Ecological Modeling 104, 133-143.CrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Arthur E. Weis
    • 1
  • Ellen L. Simms
    • 2
  • Michael E. Hochberg
    • 3
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of California-IrvineIrvineUSA
  2. 2.Department of Integrative BiologyUniversity of California-BerkeleyBerkeleyUSA
  3. 3.Génétique et Environment, ISEMUniversity of Montpellier IIMontpellierFrance

Personalised recommendations