Skip to main content
Log in

Age-Related Shifts in Leaf Chemistry of Clonal Aspen (Populus tremuloides)

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Developmental changes in plant structure and function can influence both mammalian and arthropod feeding preferences for many woody plant species. This study documents age-related changes that occur in the leaf chemistry of trembling aspen (Populus tremuloides Michx., Salicaceae) and discusses implications for the herbivore community and ecosystem processes. We collected leaves from replicate ramets from six age classes (1–25+ yr) in each of seven aspen clones growing in south central Wisconsin, USA. Chemical analyses were conducted to determine concentrations of condensed tannins, phenolic glycosides (salicortin and tremulacin), nitrogen, starch, and soluble sugars. Each variable differed significantly among clones and among age classes. On average, condensed tannin concentrations doubled in the first five years and then remained fairly constant among older age classes. Combined phenolic glycoside (salicortin + tremulacin) concentrations were high in the youngest ramets (ca. 19%) and decreased sharply with age. Developmental changes in tannin, salicortin, and tremulacin concentrations exceeded those of nitrogen and carbohydrates. Developmental shifts of this magnitude, and the age-related tradeoff that occurs between condensed tannins and phenolic glycosides, are likely to have significant influence on the herbivore community of aspen and may influence leaf litter decomposition and nutrient cycling.

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agrawal, A. A., Gorski, P. M., and Tallamy, D.W. 1999. Polymorphism in plant defense against herbivory: Constitutive and induced resistance in Cucumis sativus. J. Chem. Ecol. 25:2285–2304.

    Article  CAS  Google Scholar 

  • Awmack, C. S. and Leather, S. R. 2002. Host plant quality and fecundity in herbivorous insects. Annu. Rev. Ent. 47:817–844.

    Article  CAS  Google Scholar 

  • Ayres, M. P., Clausen, T. P., MacLean S. F. Jr., Redman, A. M., and Reichardt, P. B. 1997. Diversity of structure and antiherbivore activity in condensed tannins. Ecology 78:1696–1712.

    Article  Google Scholar 

  • Basey, J. M., Jenkins, S. H., and Busher P. E. 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 

  • Boege, K. and Marquis, R. J. 2005. Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol. Evol. 20:441–448.

    Article  PubMed  Google Scholar 

  • Brink, R. A. 1962. Phase change in higher plants and somatic cell heredity. Q. Rev. Biol. 37:1–22.

    Article  Google Scholar 

  • Bryant, J. P. 1981. Phytochemical deterrence of snowshoe hare browsing by adventitious shoots of four Alaskan trees. Science 213:889–890.

    Article  PubMed  CAS  Google Scholar 

  • Bryant, J. P. and Julkunen-Tiitto, R. 1995. Ontogenic development of chemical defense by seedling resin birch: energy cost of defense production. J. Chem. Ecol. 21:883–896.

    Article  CAS  Google Scholar 

  • Close, D. C. and McArthur, C. 2002. Rethinking the role of many plant phenolics—protection from photodamage not herbivores? Oikos 99:166–172.

    Article  CAS  Google Scholar 

  • Cole, C. 2005. Allelic and population variation of microsatellite loci in aspen (Populus tremuloides). New Phytol. 167:155–164.

    Article  PubMed  CAS  Google Scholar 

  • Crawley, M. J. 1983. Herbivory, the Dynamics of Animal–Plant Interactions. Blackwell Scientific Publications, Oxford, England.

    Google Scholar 

  • Dickson, L. L. and Whitham, T. G. 1996. Genetically-based plant resistance traits affect arthropods, fungi, and birds. Oecologia 106:400–406.

    Article  Google Scholar 

  • Donaldson, J. R. 2005. Benefits and Costs of Phytochemical Defense in Aspen–Insect Interactions: Causes and Consequences of Phytochemical Variation. Ph.D. dissertation. University of Wisconsin, Madison.

  • Donaldson, J. R., Kruger, E. L., and Lindroth R. L. 2006. Competition- and resource-mediated tradeoffs between growth and defensive chemistry in trembling aspen (Populus tremuloides). New Phytol. 169:561–570.

    Article  PubMed  CAS  Google Scholar 

  • Edwards, W. R. N. 1978. Effect of salicin content on palatability of Populus foliage to opossum (Trichosurus vulpecula). N. Z. J. Sci. 21:103–106.

    CAS  Google Scholar 

  • Erwin, E. A., Turner, M. G., Lindroth, R. L., and Romme, W. H. 2001. Secondary plant compounds in seedling and mature aspen (Populus tremuloides) in Yellowstone National Park, Wyoming. Am. Midl. Nat. 145:299–308.

    Article  Google Scholar 

  • Gill, D. E., Chao, L., Perkins, S. L., and Wolf, J. B. 1995. Genetic mosaicism in plants and clonal animals. Annu. Rev. Ecol. Syst. 26:423–444.

    Article  Google Scholar 

  • Hättenschwiler, S. and Vitousek, P. M. 2000. The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol. Evol. 15:238–243.

    Article  PubMed  Google Scholar 

  • Hwang, S.-Y. and Lindroth, R. L. 1997. Clonal variation in foliar chemistry of aspen: effects on gypsy moths and forest tent caterpillars. Oecologia 111:99–108.

    Article  Google Scholar 

  • Jones, C. S. 1999. An essay on juvenility, phase change, and heteroblasty in seed plants. Int. J. Plant Sci. 160:S105–S111.

    Article  PubMed  Google Scholar 

  • Karban, R. and Baldwin, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago.

    Google Scholar 

  • Karban, R. and Thaler, J. S. 1999. Plant phase change and resistance to herbivory. Ecology 80:510–517.

    Article  Google Scholar 

  • Kay, C. E. and Bartos, D. L. 2000. Ungulate herbivory on Utah aspen: assessment of long-term exclosures. J. Range Manag. 53:145–153.

    Article  Google Scholar 

  • Kearsley, M. J. C. and Whitham, T. G. 1989. Developmental-changes in resistance to herbivory—implications for individuals and populations. Ecology 70:422–434.

    Article  Google Scholar 

  • Kearsley, M. J. C. and Whitham, T. G. 1998. The developmental stream of cottonwoods affects ramet growth and resistance to galling aphids. Ecology 79:178–191.

    Article  Google Scholar 

  • Kellam, S. J., Tisch, M. H., and Walker, J. R. L. 1992. Screening of New-Zealand native plants for enzyme-inhibitor activities. N. Z. J. Bot. 30:199–203.

    Google Scholar 

  • Kozlowski, T. T. 1971. Growth and Development of Trees, Vol. 1. Academic Press, New York.

    Google Scholar 

  • Kraus, T. E. C., Dahlgren, A., and Zasoski, R. J. 2003. Tannins in nutrient dynamics of forest ecosystems—a review. Plant Soil 256:41–66.

    Article  CAS  Google Scholar 

  • Laitinen, M. L., Julkunen-Tiitto, R., and Rousi, M. 2000. Variation in phenolic compounds within a birch (Betula pendula) population. J. Chem. Ecol. 26:1609–1622.

    Article  CAS  Google Scholar 

  • Laitinen, M. L., Julkunen-Tiitto, R., Tahvanainen, J., and Rousi, M. 2005. Variation in birch (Betula pendula) shoot secondary chemistry due to genotype, environment, and ontogeny. J. Chem. Ecol. 31:697–717.

    Article  PubMed  CAS  Google Scholar 

  • Lawrence, R., Potts, B. M., and Whitham, T. G. 2003. Relative importance of plant ontogeny, host genetic variation, and leaf age for a common herbivore. Ecology 84:1171–1178.

    Article  Google Scholar 

  • Lindroth, R. L. and Hwang, S.-Y. 1996a. Diversity, redundancy and multiplicity in chemical defense systems of aspen. Recent Adv. Phytochem. 30:25–56.

    CAS  Google Scholar 

  • Lindroth, R. L. and Hwang, S.-Y. 1996b. Clonal variation in foliar chemistry of quaking aspen (Populus tremuloides Michx.). Biochem. Syst. Ecol. 24:357–364.

    Article  CAS  Google Scholar 

  • Lindroth, R. L., Hsia, M. T. S., and Scriber, J. M. 1987. Seasonal patterns in the phytochemistry of three Populus species. Biochem. Syst. Ecol. 15:681–686.

    Article  CAS  Google Scholar 

  • Lindroth, R. L., Kinney, K. K., and Platz, C. L. 1993. Responses of deciduous trees to elevated atmospheric CO2: productivity, phytochemistry and insect performance. Ecology 74:763–777.

    Article  CAS  Google Scholar 

  • Lindroth, R. L., Osier, T. L., Barnhill, H. R. H., and Wood, S. A. 2002. Effects of genotype and nutrient availability on phytochemistry of trembling aspen (Populus tremuloides Michx.) during leaf senescence. Biochem. Syst. Ecol. 30:297–307.

    Article  CAS  Google Scholar 

  • Madritch, M. D., Donaldson, J. R., and Lindroth, R. L. 2006. Genetic identity of Populus tremuloides litter influences decomposition and nutrient release in a mixed forest stand. Ecosystems (in press).

  • Magyar, G., Kertesz, M., and Oborny, B. 2004. Resource transport between ramets alters soil resource pattern: a simulation study on clonal growth. Evol. Ecol. 18:469–492.

    Article  Google Scholar 

  • Martinsen, G. D., Driebe, E. M., and Whitham, T. G. 1998. Indirect interactions mediated by changing plant chemistry: beaver browsing benefits beetles. Ecology 79:192–200.

    Article  Google Scholar 

  • Mattson, W. J., Herms, D. A., Witter, J. A., and Allen, D. C. 1991. Woody plant grazing systems: North American outbreak folivores and their host plants, pp. 53–84, in Y. N. Baranchikov, W. J. Mattson, F. P. Hain, and T. L. Payne (eds.). Forest Insect Guilds: Patterns of Interaction with Host Trees. USDA Forest Service, Northeastern Forest Experiment Station, Radnor, PA, Gen. Tech. Rep. NE-153.

  • Mitton, J. B. and Grant, M. C. 1996. Genetic variation and the natural history of quaking aspen. Bioscience 46:25–31.

    Article  Google Scholar 

  • Northup, R. R., Dahlgren, R. A., and McColl, J. G. 1998. Polyphenols as regulators of plant–litter–soil interactions in northern California's pygmy forest: a positive feedback? Biogeochemistry 42:189–220.

    Article  CAS  Google Scholar 

  • Orians, C. M. and Jones, C. G. 2001. Plants as resource mosaics: a functional model for predicting patterns of within-plant resource heterogeneity to consumers based on vascular architecture and local environmental variability. Oikos 94:493–504.

    Article  Google Scholar 

  • Osier, T. L. and Lindroth, R. L. 2001. Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. J. Chem. Ecol. 27:1289–1313.

    Article  PubMed  CAS  Google Scholar 

  • Osier, T. L. and Lindroth, R. L. 2004. Long-term effects of defoliation on quaking aspen in relation to genotype and nutrient availability: plant growth, phytochemistry and insect performance. Oecologia 139:55–65.

    Article  PubMed  Google Scholar 

  • Osier, T. L. and Lindroth, R. L. 2006. Genotype and environment determine allocation to and consts of resistance in quaking aspen. Oecologia (in press).

  • Pavia, H., Toth, G. B., and Åberg, P. 2002. Optimal defense theory: elasticity analysis as a tool to predict intraplant variation in defenses. Ecology 83:891–897.

    Article  Google Scholar 

  • Porter, L. J., Hrstich, L. N., and Chan, B. G. 1986. The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230.

    Article  CAS  Google Scholar 

  • Reichardt, P. B., Bryant, J. P., Mattes, B. R., Clausen, T. P., Chapin, F. S. III, and Meyer, M. 1990. Winter chemical defense of Alaskan balsam poplar against snowshoe hares. J. Chem. Ecol. 16:1941–1959.

    Article  CAS  Google Scholar 

  • Rhoades, D. F. 1979. Evolution of plant chemical defense against herbivores, pp. 3–54, in G. A. Rosenthal and D. H. Janzen (eds.). Herbivores: Their Interaction with Secondary Plant Metabolites. Academic Press, Inc., New York.

    Google Scholar 

  • Riipi, M., Ossipov, V., Lempa, K., Haukioja, E., Koricheva, J., Ossipova, S., and Pihlaja, K. 2002. Seasonal changes in birch leaf chemistry: are there trade-offs between leaf growth, and accumulation of phenolics? Oecologia 130:380–390.

    Article  Google Scholar 

  • SAS Institute Inc. 1999. SAS/Stat User's Guide, Version 8.02 for Windows. Cary, NC, USA.

  • SAS Institute Inc. 2001. JMP version 4.0.4. Duxbury Press, Pacific Grove, CA.

  • Schimel, J. P., Van Cleve, K., Cates, R. G., Clausen, T. P., and Reichardt, P. B. 1996. Effects of balsam poplar (Populus balsamifera) tannins and low molecular weight phenolics on microbial activity in taiga floodplain soil: implications for changes in N cycling during succession. Can. J. Bot. 74:84–90.

    Article  CAS  Google Scholar 

  • Schultz, J. C. 1988. Many factors influence the evolution of herbivore diets, but plant chemistry is central. Ecology 69:896–897.

    Article  Google Scholar 

  • Schweitzer, J. A., Bailey, J. K., Rehill, B. J., Martinsen, G. D., Hart, S. C., Lindroth, R. L., Keim, P., and Whitham, T. G. 2004. Genetically based trait in a dominant tree affects ecosystem processes. Ecol. Lett. 7:127–134.

    Article  Google Scholar 

  • Shelton, A. L. 2000. Variable chemical defences in plants and their effects on herbivore behaviour. Evol. Ecol. Res. 2:231–249.

    Google Scholar 

  • Stevens, M. T. and Lindroth, R. L. 2005. Induced resistance in the indeterminate growth of aspen (Populus tremuloides). Oecologia 145:298–306.

    Article  PubMed  Google Scholar 

  • Suomela, J. and Ayres, M. P. 1994. Within-tree and among-tree variation in leaf characteristics of mountain birch and its implications for herbivory. Oikos 70:212–222.

    Article  Google Scholar 

  • Swihart, R. K. and Bryant, J. P. 2001. Importance of biogeography and ontogeny of woody plants in winter herbivory by mammals. J. Mammal. 82:1–21.

    Article  Google Scholar 

  • Swihart, R. K., Bryant, J. P., and Newton, L. 1994. Latitudinal patterns in consumption of woody plants by snowshoe hares in the eastern United States. Oikos 70:427–434.

    Article  Google Scholar 

  • Tahvanainen, J., Julkunen-Tiitto, R., and Kettunen, J. 1985. Phenolic glycosides govern the food selection pattern of willow feeding leaf beetles. Oecologia 67:52–56.

    Article  Google Scholar 

  • Tuskan, G. A., Francis, K. E., Russ, S. L., Romme, W. H., and Turner, M. G. 1996. RAPD markers reveal diversity within and among clonal and seedling stands of aspen in Yellowstone National Park, U.S.A. Can. J. For. Res. 26:2088–2098.

    Article  Google Scholar 

  • Waltz, A. M. and Whitham, T. G. 1997. Plant development affects arthropod communities: opposing impacts of species removal. Ecology 78:2133–2144.

    Article  Google Scholar 

  • Watkinson, A. R. 1986. Plant population dynamics, pp. 137–184, in M. J. Crawley (ed.). Plant Ecology. Blackwell Scientific, Oxford, England.

    Google Scholar 

  • Zar, J. H. 1999. Biostatistical Analysis, 4th edn. Prentice Hall, Englewood Cliffs.

    Google Scholar 

Download references

Acknowledgments

We thank Brian Rehill for thoughtful discussion, comments on the manuscript, and insights about the effects of plant development on phytochemistry and ecological processes. We also thank anonymous reviewers whose comments improved the manuscript. Support for this work was provided from NSF grant DEB-0074427.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jack R. Donaldson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Donaldson, J.R., Stevens, M.T., Barnhill, H.R. et al. Age-Related Shifts in Leaf Chemistry of Clonal Aspen (Populus tremuloides). J Chem Ecol 32, 1415–1429 (2006). https://doi.org/10.1007/s10886-006-9059-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-006-9059-2

Keywords

Navigation