Skip to main content

Advertisement

Log in

Rapid shifts in the chemical composition of aspen forests: an introduced herbivore as an agent of natural selection

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The global ecological impacts of introduced and exotic species can be dramatic, leading to losses in biodiversity and ecosystem “meltdown”, however, the evolutionary impacts of introduced species are much less understood. Further, very few studies have examined whether mammalian herbivores can act as agents of natural selection for plant traits. We examined the hypothesis that variation in aspen phytochemistry resulted in selective herbivory by Cervus elaphus (elk), an introduced mammalian herbivore. With the experimental removal of a large elk exclosure, elk selectively eliminated 60% of an aspen population previously protected from herbivory resulting in a dramatic shift in the phytochemical composition of the aspen forest. Selection gradients (β) varied from 0.52 to 0.66, well above average relative to other studies of selection. These results indicate that introduced herbivores can have rapid evolutionary consequences even on long lived native species. Because there are fundamental links between phytochemistry, biodiversity and ecosystem processes, the effects of an introduced herbivore are likely to have cascading impacts on the services ecosystems provide.

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.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Arnold SJ (1983) Morphology, performance and fitness. Am Zool 23:347–361

    Google Scholar 

  • Bailey JK, Whitham TG (2002) Interactions among fire, aspen and elk affect insect diversity: reversal of a community response. Ecology 83:1701–1712

    Google Scholar 

  • Bailey JK, Whitham TG (2003) Interactions among elk, aspen, galling sawflies and insectivorous birds. Oikos 101:127–134

    Article  Google Scholar 

  • Bailey JK, Schweitzer JA, Rehill BJ et al. (2004) Beavers as molecular geneticists: a genetic basis to the foraging of an ecosystem engineer. Ecology 85:603–608

    Article  Google Scholar 

  • Baker WL, Munroe JA, Hessl AE (1997) The effects of elk on aspen in the winter range in Rocky Mountain National Park. Ecography 20:155–165

    Article  Google Scholar 

  • Basey JM, Jenkins SH, Busher PE (1988) Optimal central-place foraging by beavers: tree-size selection in relation to defensive chemicals of quaking aspen. Oecologia 76:278–282

    Article  Google Scholar 

  • Basey JM, Jenkins SH, Miller GC (1990) Food selection by beavers in relation to inducible defenses of Populus tremuloides. Oikos 59:57–62

    Article  Google Scholar 

  • Brodie ED III, Moore AJ, Janzen FJ (1995) Visualizing and quantifying natural selection. Tr Ecol Evol 10:313–318

    Article  Google Scholar 

  • Brown TM (1996) Molecular genetics and the evolution of pesticide resistance. Washington, DC: American Chemical Society

    Google Scholar 

  • Bryant JP (1981) Phytochemical deterrence of snowshoe hare browsing by adventitious shoots of four Alaskan trees. Science 313:889–890

    Article  Google Scholar 

  • Conner JK, Hartl DL (2004) A primer of ecological genetics. Sinauer, Sunderland Massachusettes

    Google Scholar 

  • Cyr H, Pace ML (1993) Magnitudes and patterns of herbivory in aquatic and terrestrial ecosystems. Nature 361:148–150

    Article  Google Scholar 

  • Donaldson JR, Stevens MT, Barnhill HR et al. (2006) Variation in aspen (Populus tremuloides Michx.) leaf chemistry: developmental shifts in allocation result in diverse chemical landscapes. J. Chem. Ecol. (in press)

  • Ellison AM, Bank MS, Clinton BD et al. (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3:479–486

    Article  Google Scholar 

  • Endler J (1986) Natural selection in the wild. Princeton University Press, New Jersey

    Google Scholar 

  • Groombridge B (ed) (1992) Global biodiversity: status of earth’s living resources. Chapman and Hall, London

    Google Scholar 

  • Hagerman AE, Butler LG (1980) Condensed tannin purification and characterization of tannin-associated protein. J Agric Food Chem 28:947–952

    Article  PubMed  CAS  Google Scholar 

  • Hairston NG Jr, Lampert W, Caceres CE et al. (1999) Rapid evolution revealed by dormant eggs. Nature 401:446

    Article  Google Scholar 

  • Hereford J, Hansen TF, Houle D (2004) Comparing strengths of directional selection: how strong is strong? Evolution 58:2133–2143

    PubMed  Google Scholar 

  • Hessl A (2002) Aspen, elk and fire: the effects of human institution on ecosystem processes. Bioscience 52:1011–1022

    Article  Google Scholar 

  • Hoffmeister DF (1986) Mammals of Arizona. University of Arizona Press Tucson, AZ

    Google Scholar 

  • Janzen FJ, Stern HS (1998) Logistic regression for empirical studies of multivariate selection. Evolution 52:1564–1571

    Article  Google Scholar 

  • Kingsolver JG, Hoekstra HE, Hoekstra JM et al. (2001) The strength of phenotypic selection in natural populations. Am Nat 157:245–261

    Article  Google Scholar 

  • Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226

    Article  Google Scholar 

  • Lindroth RL, Hwang S-Y (1996) Diversity, redundancy and multiplicity in chemical defense systems of aspen. In: Romeo J (ed) Recent advances in phytochemistry, vol 33. Plenum Press, New York, pp 25–56

    Google Scholar 

  • Lindroth RL, Kinney KK, Platz CL (1993) Responses of deciduous trees to elevated atmospheric CO2: productivity, phytochemistry and insect performance. Ecology 74:763–777

    Article  CAS  Google Scholar 

  • Mauricio R, Rausher MD (1997) Experimental manipulation of putative selection agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 51:1435–1444

    Article  Google Scholar 

  • Minchin PR (1987) An evaluation of the relative robustness of techniques for ecological ordination. Vegetatio 69:89–107

    Article  Google Scholar 

  • O’Reilly-Wapstra JM, McArthur C, Potts BM (2002) Genetic variation in Eucalyptus globulus to marsupial browsers. Oecologia 130:289–296

    Google Scholar 

  • O’Reilly-Wapstra JM, McArthur C, Potts BM (2004) Linking plant genotype, plant defensive chemistry and mammal browsing in a Eucalyptus species. Func Ecol 18:677–684

    Article  Google Scholar 

  • Palo RT (1984) Distribution of birch (Betula spp.), willow (Salix spp.), and poplar (Populus spp.) secondary metabolites and their potential role as chemical defense against herbivores. J Chem Ecol 10:499–520

    Article  CAS  Google Scholar 

  • Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461

    Article  PubMed  CAS  Google Scholar 

  • Porter LJ, Hrstich LN, Chan BG (1986) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230

    Article  CAS  Google Scholar 

  • Pusenius J, Prittinen K, Heimonen J et al. (2002) Choice of voles among genotypes of birch seedlings: its relationship with seedling quality and preference of insects. Oecologia 130:426–432

    Article  Google Scholar 

  • Richter TE, Ronald PC (2000) The evolution of disease resistance genes. Plant Mol Bio 42:195–204

    Article  CAS  Google Scholar 

  • Roff DA (1997) Evolutionary quantitative genetics. Chapman and Hall, New York

    Google Scholar 

  • Rolf JM (2001) Aspen fencing in northern Arizona: a 15 year perspective. USDA Forest Service Proceedings RMRS-P-18. pp 193–196

  • Romme WH, Turner MG, Wallace LL et al. (1995) Aspen, elk, and fire in northern Yellowstone National Park. Ecology 76:2097–2106

    Article  Google Scholar 

  • Romme WH, Turner MG, Tuskan GA et al. (2005) Establishment, persistence, and growth of aspen (Populus tremuloides) seedlings in Yellowstone National Park. Ecology 86:404–418

    Article  Google Scholar 

  • Simberloff D (2001) Biological invasions—how are they affecting us and what can we do about them? West North Am Nat 61:308–315

    Google Scholar 

  • Simberloff D, Parker IM, Windle PN (2005) Introduced species policy, management and future research needs. Fron Ecol Environ 3:12–20

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry. W. H. Freeman and Company, New York

    Google Scholar 

  • Still WC, Kahn M, Mitra A (1978) Rapid chromatographic technique for preparative separations with moderate resolution. J Org Chem 43:2923–2925

    Article  CAS  Google Scholar 

  • Stinchcombe JR, Rausher MD (2001) Diffuse selection on resistance to deer herbivory in the ivyleaf morning glory, Ipomea hederacea. Am Nat 158:376–388

    Article  Google Scholar 

  • Stinchcombe JR, Rausher MD (2002) The evolution of tolerance to deer herbivory: modifications caused by the abundance of insect herbivores. Proc R Soc Lond 269:1241–1246

    Article  Google Scholar 

  • Stinchcombe JR (2005) Measuring natural selection on proportional traits: comparisons of three types of selection estimates for resistance and susceptibility to herbivore damage. Evol Ecol 19:363–373

    Article  Google Scholar 

  • Thompson JN (1998) Rapid evolution as an ecological process. Tr Ecol Evol 13:329–332

    Article  Google Scholar 

  • Thompson JN, Reichman OJ, Morin PJ et al. (2001) Frontiers in ecology. Bioscience 51:15–24

    Article  Google Scholar 

  • Verheyden-Tixier H, Duncan P (2000) Selection for small amounts of hydrolysable tannins by a concentrate-selecting mammalian herbivore. J Chem Ecol 26:351–358

    Article  CAS  Google Scholar 

  • Whitham TG, Bailey JK, Schweitzer JA et al. (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7:510–523

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Special thanks to Christy Grow and James Andrade for help in the field. Thanks to John Stinchcombe for helpful comments on the manuscript. This research was supported by National Science Foundation Integrative Research Challenges in Environmental Biology and Frontiers in Integrative Biological Research grants. A grant from the National Science Foundation (IOB 0421917) supported D. Irschick.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joseph K. Bailey.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bailey, J.K., Schweitzer, J.A., Rehill, B.J. et al. Rapid shifts in the chemical composition of aspen forests: an introduced herbivore as an agent of natural selection. Biol Invasions 9, 715–722 (2007). https://doi.org/10.1007/s10530-006-9071-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-006-9071-z

Keywords

Navigation