Journal of Chemical Ecology

, Volume 38, Issue 3, pp 306–314 | Cite as

Genotypic Differences and Prior Defoliation Affect Re-Growth and Phytochemistry after Coppicing in Populus tremuloides

  • Michael T. Stevens
  • Adam C. Gusse
  • Richard L. Lindroth
Article

Abstract

Although considerable research has explored how tree growth and defense can be influenced by genotype, the biotic environment, and their interaction, little is known about how genotypic differences, prior defoliation, and their interactive effects persist in trees that re-grow after damage that severs their primary stem. To address these issues, we established a common garden consisting of twelve genotypes of potted aspen (Populus tremuloides) trees, and subjected half of the trees to defoliation in two successive years. At the beginning of the third year, all trees were severed at the soil surface (coppiced) and allowed to regenerate for five months. Afterwards, we counted the number of root and stump sprouts produced and measured the basal diameter (d) and height (h) of the tallest ramet in each pot. We collected leaves one and two years after the second defoliation and assessed levels of phenolic glycosides, condensed tannins, and nitrogen. In terms of re-growth, we found that the total number of sprouts produced varied by 3.6-fold among genotypes, and that prior defoliation decreased total sprout production by 24%. The size (d2h) of ramets, however, did not differ significantly among genotypes or defoliation classes. In terms of phytochemistry, we observed genotypic differences in concentrations of all phytochemicals assessed both one and two years after the second defoliation. Two years after defoliation, we observed effects of prior defoliation in a genotype-by-defoliation interaction for condensed tannins. Results from this study demonstrate that genotypic differences and impacts of prior defoliation persist to influence growth and defense traits in trees even after complete removal of above-ground stems, and thus likely influence productivity and plant-herbivore interactions in forests affected by natural disturbances or actively managed through coppicing.

Keywords

Aspen Condensed tannins Defense Phenolic glycosides Root sprout Stump sprout Sucker 

References

  1. Abrahamson, L. P., White, E. H., Nowak, C. A., Briggs, R. D., and Robison, D. J. 1990. Evaluating hybrid poplar clonal growth potential in a three-year old genetic selection field trial. Biomass 21:101–114.CrossRefGoogle Scholar
  2. Agrawal, A. A., Kosola, K. R., and Parry, D. 2002. Gypsy moth defoliation and N fertilization affect hybrid poplar regeneration following coppicing. Can. J. For. Res. 32:1491–1495.CrossRefGoogle Scholar
  3. Ayres, M. P., Clausen, T. P., Maclean Jr., S. F., Redman, A. M., and Reichardt, P. B. 1997. Diversity of structure and antiherbivore activity in condensed tannins. Ecology 78:1696–1712.CrossRefGoogle Scholar
  4. Bailey, J. K., Schweitzer, J. A., Rehill, B. J., Lindroth, R. L., Martinsen, G. D., and Whitham, T. G. 2004. Beavers as molecular geneticists: a genetic basis to the foraging of an ecosystem engineer. Ecology 85:603–608.CrossRefGoogle Scholar
  5. Baker, F. S. 1918. Aspen reproduction in relation to management. J. Forestry 16:389–398.Google Scholar
  6. Barnes, B. V. 1969. Natural variation and delineation of clones of Populus tremuloides and P. grandidentata in northern lower Michigan. Silvae Genetica 18:130–142.Google Scholar
  7. Barry, W. J., and Sachs, R. M. 1968. Vegetative propagation of quaking aspen. Calif. Agric. 22:14–16.Google Scholar
  8. Barton, K. E., and Koricheva, J. 2010. The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. Am. Nat. 175:481–493.PubMedCrossRefGoogle Scholar
  9. Basey, J. M., Jenkins, S. H., and Miller, G. C. 1990. Food selection by beavers in relation to inducible defenses of Populus tremuloides. Oikos 59:57–62.CrossRefGoogle Scholar
  10. Boeckler, G. A., Gershenzon, J., and Unsicker, S. B. 2011. Phenolic glycosides of the Salicaceae and their role as anti-herbivore defenses. Phytochemistry 72:1497–1509.PubMedCrossRefGoogle Scholar
  11. 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.PubMedCrossRefGoogle Scholar
  12. Bryant, J. P., Chapin III, F. S., and Klein, D. R. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368.CrossRefGoogle Scholar
  13. Dickmann, D. I., Isebrands, J. G., Blake, T. J., Kosola K., and Kort, K. 2001. Physiological ecology of poplars, pp. 77–118, in D. I. Dickmann, J. G. Isebrands, J. E. Eckenwalder, and J. Richardson (eds.), Poplar Culture in North America. NRC Research Press, Ottawa, Canada.Google Scholar
  14. Diner, B., Berteaux, D., Fyles, J. and Lindroth, R. L. 2009. Behavioral archives link the chemistry and clonal structure of trembling aspen to the food choice of North American porcupine. Oecologia 160:687–695.PubMedCrossRefGoogle Scholar
  15. 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.Google Scholar
  16. Donaldson, J. R., and Lindroth, R. L. 2004. Cottonwood leaf beetle (Coleoptera: Chrysomelidae) performance in relation to variable phytochemistry in juvenile aspen (Populus tremuloides Michx.). Environ. Entomol. 33:1505–1511.CrossRefGoogle Scholar
  17. Donaldson, J. R., and Lindroth, R. L. 2007. Genetics, environment, and their interaction determine efficacy of chemical defense in trembling aspen. Ecology 88:729–739.PubMedCrossRefGoogle Scholar
  18. Donaldson, J. R., Stevens, M. T., Barnhill, H. R., and Lindroth, R. L. 2006. Age-related shifts in leaf chemistry of clonal aspen (Populus tremuloides). J. Chem. Ecol. 32:1415–1429.PubMedCrossRefGoogle Scholar
  19. Frey, B. R., Lieffers, V. J., Landhäusser, S. M., Comeau, P. G., and Greenway, K. J. 2003. An analysis of sucker regeneration of trembling aspen. Can. J. For. Res. 33:1169–1179.CrossRefGoogle Scholar
  20. Fritz, R. S., and Simms, E. L. 1992. Plant Resistance to Herbivores and Pathogens. Ecology, Evolution, and Genetics. University of Chicago Press, Chicago.Google Scholar
  21. Hamilton, J. G., Zangerl, A. R., Delucia, E. H., and Berenbaum, M. R. 2001. The carbon-nutrient balance hypothesis: its rise and fall. Ecol. Lett. 4:86–95CrossRefGoogle Scholar
  22. Harvell, C. D. 1998. Genetic variation and polymorphism in the inducible spines of a marine bryozoan. Evolution 52:80–86.CrossRefGoogle Scholar
  23. Havill, N. P., and Raffa, K. F. 1999. Effects of elicitation treatment and genotypic variation on induced resistance in Populus: impacts on gypsy moth (Lepidoptera : Lymantriidae) development and feeding behavior. Oecologia 120:295–303.CrossRefGoogle Scholar
  24. Horton, K. W., and Maini, J. S. 1964. Aspen reproduction: its characteristics and control. Can. Dep. Forest., Forest Res. Br. Rep. 64-0-12.Google Scholar
  25. 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.CrossRefGoogle Scholar
  26. Hwang, S.-Y., and Lindroth, R. L. 1998. Consequences of clonal variation in aspen phytochemistry for late season folivores. Ecoscience 5:508–516.Google Scholar
  27. Jachmann, H. 1989. Food selection by elephants in the ‘miombo’ biome, in relation to leaf chemistry. Biochem. Syst. Ecol. 17:15–24.CrossRefGoogle Scholar
  28. Karban, R., and Baldwin, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago.Google Scholar
  29. Kim, J., Quaghebeur, H., Felton, G. W. 2011. Reiterative and interruptive signaling in induced plant resistance to chewing insects. Phytochemistry 72:1624–1634.PubMedCrossRefGoogle Scholar
  30. Laitinen, R. L., Julkunen-Tiitto, R., Rousi, M., Heinonen, J., and Tahvanainen, J. 2005. Ontogeny and environment as determinants of the secondary chemistry of three species of white birch. J. Chem. Ecol. 31:2243–2262.PubMedCrossRefGoogle Scholar
  31. Lindroth, R. L., Donaldson, J. R., Stevens, M. T., and Gusse, A. C. 2007. Browsing quality in quaking aspen (Populus tremuloides): effects of genotype, nutrients, defoliation, and coppicing. J. Chem. Ecol. 33:1049–1064.PubMedCrossRefGoogle Scholar
  32. 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.CrossRefGoogle Scholar
  33. Lindroth, R. L., and Koss, P. A. 1996. Preservation of Salicaceae leaves for phytochemical analyses: further assessment. J. Chem. Ecol. 22:765–771.CrossRefGoogle Scholar
  34. Lindroth, R. L., Scriber, J. M., and Hsia, M. T. S. 1988. Chemical ecology of the tiger swallowtail: mediation of host use by phenolic glycosides. Ecology 69:814–822.CrossRefGoogle Scholar
  35. Maini, J. S. 1968. Silvics and ecology of Populus in Canada, pp. 20–69, in J. S. Maini and J. H. Cayford (eds.), Growth and Utilization of Poplars in Canada. Minister of Forestry and Rural Development, Ottawa, Canada.Google Scholar
  36. Marquis, R. 1992. Selective impact of herbivores, pp. 301–325, in R. S. Fritz and E. L. Simms (eds.), Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics. University of Chicago Press, Chicago.Google Scholar
  37. 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. Gen. Tech. Rep. NE-153. USDA Forest Service, Northeastern Forest Experiment Station, Radnor, PA.Google Scholar
  38. Mckey, D. 1979. The distribution of secondary compounds within plants, pp. 55–133, in G. A. Rosenthal and D. H. Janzen (eds.), Herbivores: their interactions with secondary plant metabolites. Academic Press, Inc., New York.Google Scholar
  39. Mutikainen, P., Walls, M., Ovaska, J., Keinänen, M., Julkunen-Tiitto, R., and Vapaavuori, E. 2000. Herbivore resistance in Betula pendula: effect of fertilization, defoliation, and plant genotype. Ecology 81:49–65.Google Scholar
  40. Nyman, T., Paajanen, R., Heiska, S., and Julkunen-Tiitto, R. 2011. Preference-performance relationship in the gall midge Rabdophaga rosaria: insights from a common-garden experiment with nine willow clones. Ecol. Entomol. 36:200–211.CrossRefGoogle Scholar
  41. 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.PubMedCrossRefGoogle Scholar
  42. 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.PubMedCrossRefGoogle Scholar
  43. Osier, T. L., and Lindroth, R. L. 2006. Genotype and environment determine allocation to and costs of resistance in quaking aspen. Oecologia 148:293–303.PubMedCrossRefGoogle Scholar
  44. Parry, D., Herms, D. A., and Mattson, W. J. 2003. Responses of an insect folivore and its parasitoids to multiyear experimental defoliation of aspen. Ecology 84:1768–1783.CrossRefGoogle Scholar
  45. Parsons, W. F. J., Bockheim, J. G., and Lindroth, R. L. 2008. Independent, interactive, and species-specific responses to leaf litter decomposition to elevated CO2 and O3 in a northern hardwood forest. Ecosystems 11:505–519.CrossRefGoogle Scholar
  46. Perala, D. A. 1990. Populus tremuloides Michx. quaking aspen, pp. 555–569, in R. M. Burns and B. H. Honkala (eds.), Silvics of North America, vol. 2. Hardwoods. USDA Forest Service, Washington, DC.Google Scholar
  47. 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.CrossRefGoogle Scholar
  48. Rasmann, S., De Vos, M., Casteel, C. L., Tian, D., Halitschke, R., Sun, J. Y., Agrawal, A. A., Felton, G. W., Jander, G. 2012. Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiol. doi:10.1104/pp.111.187831
  49. 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 Interactions with Secondary Plant Metabolites. Academic Press, Inc., New York.Google Scholar
  50. SAS Institute INC. 2008. JMP Version 8.0.2. SAS Institute Inc., Cary, NC.Google Scholar
  51. Schier, G. A., Jones, J. R., and Winokur, R. P. 1985. Vegetative regeneration, pp. 29–33, in N. V. DeByle and R. P. Winokur (eds.), Aspen: Ecology and Management in the Western United States. General Technical Report RM-119. USDA Forest Service.Google Scholar
  52. Siemens, D. H., Lischke, H., Maggiulli, N., Schurch, S., and Roy, B. A. 2003. Cost of resistance and tolerance under competition: the defense-stress benefit hypothesis. Evol. Ecol. 17:247–263.CrossRefGoogle Scholar
  53. Smith, E. A., Collette, S. B., Boynton, T. A., Lillrose, T., Stevens, M. R., Bekker, M. F., Eggett, D., and St. Clair, S. B. 2011. Developmental contributions to phenotypic variation in functional leaf traits within quaking aspen clones. Tree Phys. 31:68–77.CrossRefGoogle Scholar
  54. St. Clair, S. B., Monson, S. D., Smith, E. A., Cahill, D. G., Calder, W. J. 2009. Altered leaf morphology, leaf resource dilution and defense chemistry induction in frost-defoliated aspen (Populus tremuloides). Tree Phys. 29:1259–1268.CrossRefGoogle Scholar
  55. Stamp, N. 2003. Out of the quagmire of plant defense hypotheses. Q. Rev. Biol. 78:23–55.PubMedCrossRefGoogle Scholar
  56. Stevens, M. T., and Esser, S. M. 2009. Growth-defense tradeoffs differ by gender in dioecious trembling aspen (Populus tremuloides). Biochem. Syst. Ecol. 37:567–573.CrossRefGoogle Scholar
  57. Stevens, M. T., and Lindroth, R. L. 2005. Induced resistance in the indeterminate growth of aspen (Populus tremuloides). Oecologia 145:298–306.PubMedCrossRefGoogle Scholar
  58. Stevens, M. T., Waller, D. M., and Lindroth, R. L. 2007. Resistance and tolerance in Populus tremuloides: genetic variation, costs, and environmental dependency. Evol. Ecol. 21:829–847.CrossRefGoogle Scholar
  59. Stevens, M. T., Kruger, E. L., and Lindroth, R. L. 2008.Variation in tolerance to herbivory is mediated by differences in biomass allocation in aspen. Funct. Ecol. 22:40–47.Google Scholar
  60. 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
  61. Tew, R. K. 1970. Root carbohydrate reserves in vegetative reproduction of aspen. Forest Science 16:318–320.Google Scholar
  62. Wooley, S. C., Walker, S., Vernon, J., and Lindroth, R. L. 2008. Aspen decline, aspen chemistry, and elk herbivory: are they linked? Rangelands 30:17–21.CrossRefGoogle Scholar
  63. Wright, J. W. 1976. Introduction to Forest Genetics. Academic Press, New York.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Michael T. Stevens
    • 1
    • 3
  • Adam C. Gusse
    • 2
    • 4
  • Richard L. Lindroth
    • 2
  1. 1.Department of BotanyUniversity of Wisconsin-MadisonMadisonUSA
  2. 2.Department of EntomologyUniversity of Wisconsin-MadisonMadisonUSA
  3. 3.Department of BiologyUtah Valley UniversityOremUSA
  4. 4.H&H SolarMadisonUSA

Personalised recommendations