Will plant vigor and tolerance be genetically correlated? Effects of intrinsic growth rate and self-limitation on regrowth Authors
Cite this article as: Weis, A.E., Simms, E.L. & Hochberg, M.E. Evolutionary Ecology (2000) 14: 331. doi:10.1023/A:1010950932468 Abstract
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
This revised version was published online in July 2006 with corrections to the Cover Date.
Abrahamson, W.G. and Weis, A.E. (1997)
Evolutionary Ecology across Three Trophic Levels: Goldenrods, Gallmakers, and Natural Enemies. Princeton University Press, Princeton, NJ.
Ackerly, D. (1999) Self-shading, carbon gain and leaf dynamics: a test of alternative optimality models.
Ackerly, D.D. and Bazzaz, F.A. (1995) Leaf dynamics, self-shading and carbon gain in seedlings of a tropical pioneer tree.
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.
Augspurger, C.K. (1984) Light requirements of neotropical tree seedlings: a comparative study of growth and survival.
Belsky, A.J. (1986) Does herbivory benefit plants? A review of the evidence.
Benner, B.L. (1988) Effects of apex removal and nutrient supplementation on branching and seed production in
Am. J. Bot.
Bergelson, J. and Crawley, M.J. (1992) The effects of grazing on the performance of individuals and populations of scarlet gilia,
Bilbrough, C.J. and Richards, J.H. (1993) Growth of sagebrush and brittlebush following simulated winter browsing: mechanisms of tolerance.
Blackman, V.H. (1919) The compound interest law and plant growth.
Brokaw, N.V.L. (1987) Gap-phase regeneration of three pioneer species in a topical forest.
Coley, P., Bryant, J.P. and Chapin III, F.S. (1985) Resource availability and plant antiherbivore defense.
De Jong, G. (1990) Quantitative genetics of reaction norms.
J. Evolutionary Biol
De Jong, T. and Van der Meijden, E. (2000) On the correlation between allocation to defense and regrowth in plants.
Field, C.B. (1983) Allocating leaf nitrogen for the maximization of carbon gain: leaf age as a control on the allocation program.
Futuyma, D.J. and Philippi, T.E. (1987) Genetic variation and covariation in responses to host plants by
Geber, M.A. (1990) The cost of meristem limitation in
: negative genetic correlations between fecundity and growth.
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.
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.
Hendrix, S.D. (1979) Compensatory reproduction in a biennial herb
Pastinaca sativa following insect Depressaria pastinacella defloration. Oecologia
Hendrix, S.D. and Trapp, E.J. (1989) Floral herbivory in
: do compensatory responses offset reductions in fitness?
Hilbert, D.W., Swift, D.M., Deteling, J.K. and Dyer, M.I. (1981) Relative growth rates and the grazing optimization hypothesis.
Hirose, T. and Werger, M.J.A. (1987) Maximization of daily canopy photosynthesis with respect to the leaf nitrogen allocation pattern in the canopy.
Hochwender, C., Marquis, R. and Stowe, K. (2000) The potential for and constraints on the evolution of compensatory ability in
Honda, H. and Fisher, J.B. (1978) Tree branch angle: maximizing effective leaf area.
Horn, H.S. (1971)
The Adaptive Geometry of Trees. Princeton University Press, Princeton, NJ.
Hunt, R. (1982)
Plant Growth Curves: The Functional Approach to Plant Growth Analysis. Edward Arnold, London, UK.
Islam, Z. and Crawley, M.J. (1983) Compensation and regrowth in ragwort (
Senecio jacobeae) attacked by the cinnabar moth ( Tyria jacobeae). J. Ecol.
Iwasa, Y. and Cohen, D. (1989) Optimal growth schedule of a perennial plant.
Iwasa, Y. and Kubo, T. (1997) Optimal size of storage for recovery after unpredictable disturbances.
Juenger, T. and Bergelson, J. (2000) The evolution of compensation to herbivory in scarlet gilia,
: herbivore-imposed natural selection and the quantitative genetics of tolerance.
Kozlowski, J. (1992) Optimal allocation of resources to growth and reproduction: implications for age and size at maturity.
Trends Ecol. Evol.
Krupnick, G.A., Weis, A.E. and Campbell, D.R. (1999) The consequences of floral herbivory for pollinator services to
Lennartson, T., Toumi, J. and Nilsson, P. (1997) Evidence for an evolutionary history of over-compensation in the grassland biennial
Marby, C.M. and Wayne, P.W. (1997) Defoliation of the annual herb
: mechanisms underlying reproductive compensation.
Mauricio, R., Rausher, M.D. and Burdick, D.S. (1997) Variation in the defense strategies of plants: Are resistance and tolerance mutually exclusive?
McMahon, T. (1973) Size and shape in biology.
Meyer, G.A. (1998) Patterns of defoliation and its effects on photosynthesis and growth of goldenrod.
Niklas, K.J. (1988) The role of phyllotactic pattern as a “developmental constraint” on the interception of light by leaf surfaces.
Nowak, R.S. and Caldwell, M.M. (1984) A test of compensatory photosynthesis in the field: implications for herbivory tolerance.
Osterheld, M. (1992) Effect of defoliation intensity on aboveground and belowground relative growth rates.
Osterheld, M. and McNaughton, S.J. (1991) Effect of stress and time for recovery on the amount of compensatory growth after grazing.
Paige, K. (1992) Overcompensation in response to mammalian herbivory: from mutualistic to antagonistic interactions.
Paige, K. (1999) Regrowth following ungulate herbivory in
: geographic evidence for overcompensation.
Paige, K.N. and Whitham, T.G. (1987) Overcompensation in response to mammalian herbivory: the advantage of being eaten.
Rosenthal, J.P. and Welter, S.C. (1995) Tolerance to herbivory by a stemboring caterpillar in architecturally distinct maize and wild relatives.
Simms, E.L. and Triplett, J.K. (1994) Costs and benefits of plant responses to disease: resistance and tolerance.
Stowe, K.A. (1998) Experimental evolution of resistance in
: correlated response of tolerance in lines selected for glucosinolate content.
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.
Sun, D. (1992) Trampling resistance, recovery and growth rate of 8 plant species.
Agri. Ecosyst. Environ.
Tiffen, P. and Rausher, M.D. (1999) Genetic constraints and selection acting on tolerance to herbivory in the common morning glory,
Trumble, Y.T., Kolodny-Hirsch, D.M. and Ting, I.P. (1993) Plant compensation for arthropod herbivory.
Ann. Rev. Entomol.
Wareing, P., Khalifa, M. and Terharne, K. (1968) Rate-limiting processes in photosynthesis at saturating light intensities.
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.
Windel, P.N. and Franz, E.H. (1979) The effects of insect parasitism on plant competition: greenbugs and barley.
Woledge, J. (1986) The effect of age and shade on the photosynthesis of white clover leaves.
Yamamura, K. (1997) Optimality in the spatial leaf distribution of the weed
L. Ecological Modeling
CrossRef Copyright information
© Kluwer Academic Publishers 2000