, Volume 139, Issue 1, pp 55–65 | Cite as

Long-term effects of defoliation on quaking aspen in relation to genotype and nutrient availability: plant growth, phytochemistry and insect performance

  • Tod L. OsierEmail author
  • Richard L. Lindroth
Plant Animal Interactions


This research tested the long-term effects of defoliation on aspen chemistry and growth in relation to genotype and nutrient availability. We grew saplings of four aspen genotypes in a common garden under two conditions of nutrient availability, and subsequently subjected them to two levels of artificial defoliation. Artificial defoliation suppressed plant growth, and saplings of the four genotypes did not show evidence of genetic variation in tolerance to defoliation. Phenolic glycoside concentrations did not respond to defoliation, but were influenced by genotype and nutrient availability. Condensed tannins responded to defoliation and varied among genotypes. Although defoliation affected condensed tannins, plant quality was not altered in a manner important for gypsy moth performance. Regression analyses suggested that phenolic glycoside concentrations accounted for most of the variation in insect performance. The lack of a strong response important for herbivores was surprising given the severity of the defoliation treatment (nearly 100% of leaf area was removed). In this study, plant genotype was of primary importance, nutrient availability was of secondary importance and long-term induced responses were unimportant as determinants of insect performance.


Plant-insect interactions Tolerance Genotype × environment Defoliation Nutrient availability 



This research was supported by USDA NRI Competitive Grant no. 95–37302–1810, NSF grant DEB 0074427 and UW Hatch Project no. 3931 to R.L.L. We thank Sarah Glodoski, Sarah Wood, Heidi Barnhill and Brian Kopper for technical assistance. Lynn Hummel and Laura Van Slyke provided invaluable assistance at the Walnut Street greenhouses. Thanks to Jen Klug, Eric Kruger and Ken Raffa for comments on the manuscript, Rick Nordheim for statistical advice and Gary Bernon (USDA APHIS) for providing gypsy moth eggs.


  1. Agrawal AA, Strauss SY, Stout MJ (1999) Costs of induced responses and tolerance to herbivory in male and female fitness components of wild radish. Evolution 53:1093–1104Google Scholar
  2. Ayres MP, Clausen TP, MacLean SF, Redman AM, Reichardt PB (1997) Diversity of structure and antiherbivore activity in condensed tannins. Ecology 78:1696–1712Google Scholar
  3. Baldwin IT (1990) Herbivory simulations in ecological research. Trends Ecol Evol 5:91–93CrossRefGoogle Scholar
  4. Barnes BV (1969) Natural variation and delineation of clones of Populus tremuloides and P. grandidentata in Northern Lower Michigan. Silvae Genet 18:130–142Google Scholar
  5. Bassman J, Myers W, Dickmann DI, Wilson L (1982) Effects of simulated insect damage on early growth of nursery-grown hybrid poplars in northern Wisconsin, USA. Can J For Res 12:1–9Google Scholar
  6. Bryant JP, Julkunen-Tiitto R (1995) Ontogenic development of chemical defense by seedling resin birch: energy cost of defense production. J Chem Ecol 21:883–896Google Scholar
  7. Bryant JP, Chapin FSI, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368Google Scholar
  8. Bryant JP, Chapin FSI, Reichardt PB, Clausen TP (1987a) Response of winter chemical defense in Alaska paper birch and green alder to manipulation of plant carbon/nutrient balance. Oecologia 72:510–514Google Scholar
  9. Bryant JP, Clausen TP, Reichardt PB, McCarthy MC, Werner RA (1987b) Effect of nitrogen-fertilization upon the secondary chemistry and nutritional-value of quaking aspen (Populus tremuloides Michx) leaves for the large aspen tortrix (Choristoneura conflictana Walker). Oecologia 73:513–517Google Scholar
  10. Bryant JP, Reichardt PB, Clausen TP, Werner RA (1993) Effects of mineral-nutrition on delayed inducible resistance in Alaska paper birch. Ecology 74:2072–2084Google Scholar
  11. Clausen TP, Reichardt PB, Bryant JP, Werner RA, Post K, Frisby K (1989) Chemical model for short-term induction in quaking aspen (Populus tremuloides) foliage against herbivores. J Chem Ecol 15:2335–2346Google Scholar
  12. Clausen TP, Reichardt PB, Bryant JP, Werner RA (1991) Long-term and short-term induction in quaking aspen: related phenomena? In: Tallamy DW, Raupp MJ (eds) Phytochemical induction by herbivores. Wiley, New York, pp 71–83Google Scholar
  13. Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335Google Scholar
  14. Dickmann DI, Stuart KW (1983) The culture of poplars in eastern North America. Michigan State University, East Lansing, MichiganGoogle Scholar
  15. Farrar RR, Barbour JD, Kennedy GG (1989) Quantifying food consumption and growth in insects. Ann Entomol Soc Am 82:593–598Google Scholar
  16. Fineblum WL, Rausher MD (1995) Tradeoff between resistance and tolerance to herbivore damage in a morning glory. Nature 377:517–520Google Scholar
  17. Gertz AK, Bach CE (1995) Effects of light and nutrients on tomato plant compensation for herbivory by Manduca sexta (Lepidoptera: Sphingidae). Great Lakes Entomol 27:217–222Google Scholar
  18. Hagerman AE, Butler LG (1980) Condensed tannin purification and characterization of tannin-associated proteins. J Agric Food Chem 28:947–952Google Scholar
  19. Hamilton JG, Zangerl AR, DeLucia EH, Berenbaum MR (2001) The carbon-nutrient balance hypothesis: its rise and fall. Ecol Lett 4:86–95CrossRefGoogle Scholar
  20. Hanhimaki S (1989) Induced resistance in mountain birch: defense against leaf-chewing insect guild and herbivore competition. Oecologia 81:242–248Google Scholar
  21. Hartley SE, Lawton JH (1991) Biochemical aspects and significance of the rapidly induced accumulation of phenolics in birch foliage. In: Tallamy DW, Raupp MJ (eds) Phytochemical induction by herbivores. Wiley, New York, pp 105–132Google Scholar
  22. Haukioja E, Koricheva J (2000) Tolerance to herbivory in woody vs herbaceous plants. Evol Ecol 14:551–562Google Scholar
  23. Haukioja E, Neuvonen S (1985) Induced long-term resistance of birch (Betula pubescens) foliage against defoliators: defensive or incidental? Ecology 66:1303–1308Google Scholar
  24. Havill NP, Raffa KF (1999) Effects of elicitation treatment and genotypic variation on induced resistance in Populus: impacts on gypsy moth (Lepidoptera: Lymantriidae) development and feeding behavior. Oecologia 120:295–303CrossRefGoogle Scholar
  25. Hemming JDC, Lindroth RL (1995) Intraspecific variation in aspen phytochemistry: effects on performance of gypsy moths and forest tent caterpillars. Oecologia 103:79–88Google Scholar
  26. Hemming JDC, Lindroth RL (1999) Effects of light and nutrient availability on aspen: growth, phytochemistry, and insect performance. J Chem Ecol 25:1687–1714Google Scholar
  27. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335Google Scholar
  28. Hodson AC (1981) The response of aspen (Populus tremuloides) to artificial defoliation. Great Lakes Entomol 14:167–169Google Scholar
  29. Houle G (1999) Nutrient availability and plant gender influences on the short-term compensatory response of Salix planifolia ssp planifolia to simulated leaf herbivory. Can J For Res 29:1841–1846CrossRefGoogle Scholar
  30. Hwang S-Y, Lindroth RL (1997) Clonal variation in foliar chemistry of aspen: effects on gypsy moths and forest tent caterpillars. Oecologia 111:99–108CrossRefGoogle Scholar
  31. Hwang S-Y, Lindroth RL (1998) Consequences of clonal variation in aspen phytochemistry for late season herbivores. Ecoscience 5:508–516Google Scholar
  32. Jones CG, Hartley SE (1999) A protein competition model of phenolic allocation. Oikos 86:27–44Google Scholar
  33. Kaitaniemi P, Ruohomäki K, Ossipov V, Haukioja E, Pihlaja K (1998) Delayed induced changes in the biochemical composition of host plant leaves during an insect outbreak. Oecologia 116:182–190CrossRefGoogle Scholar
  34. Kaitaniemi P, Neuvonen S, Nyyssonen T (1999) Effects of cumulative defoliations on growth, reproduction, and insect resistance in mountain birch. Ecology 80:524–532Google Scholar
  35. Kinney KK, Lindroth RL, Jung SM, Nordheim EV (1997) Effects of CO2 and NO3 availability on deciduous trees: phytochemistry and insect performance. Ecology 78:215–230Google Scholar
  36. Koricheva J (2002) The Carbon-Nutrient Balance Hypothesis is dead: long live the Carbon-Nutrient Balance Hypothesis? Oikos 98:536CrossRefGoogle Scholar
  37. Lang CA (1958) Simple microdetermination of Kjeldahl nitrogen in biological materials. Anal Chem 30:1692–1694Google Scholar
  38. Lerdau M, Coley PD (2002) Benefits of the Carbon-Nutrient Balance Hypothesis. Oikos 98:533CrossRefGoogle Scholar
  39. Liebhold A, Elkinton J, Williams D, Muzika RM (2000) What causes outbreaks of the gypsy moth in North America? Popul Ecol 42:257–266Google Scholar
  40. Lindroth RL, Hwang S-Y (1996) Diversity, redundancy, and multiplicity in chemical defense systems of aspen. In: Romeo JT, Saunders JA, Barbosa P (eds) Phytochemical diversity and redundancy in ecological interactions. Plenum, New York, pp 25–56Google Scholar
  41. Lindroth RL, Kinney KK (1998) Consequences of enriched atmospheric CO2 and defoliation: chemistry and gypsy moth performance. J Chem Ecol 24:1677–1695CrossRefGoogle Scholar
  42. Lindroth RL, Koss PA (1996) Preservation of Salicaceae leaves for phytochemical analyses: further assessment. J Chem Ecol 22:765–771Google Scholar
  43. Lindroth RL, Kinney KK, Platz CL (1993) Responses of deciduous trees to elevated atmospheric CO2: productivity, phytochemistry, and insect performance. Ecology 74:763–777Google Scholar
  44. Lindroth RL, Roth S, Nordheim EV (2001) Genotypic variation in response of quaking aspen (Populus tremuloides) to atmospheric CO2 enrichment. Oecologia 126:371–379CrossRefGoogle Scholar
  45. Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS system for mixed models. SAS Institute, Cary, N.C., USAGoogle Scholar
  46. Mattson WJ, Palmer SR (1988) Changes in levels of foliar minerals and phenolics in trembling aspen, Populus tremuloides , in response to artificial defoliation. In: Mattson WJ, Levieux JC, Dagan B (eds) Mechanisms of woody plant defences against insects: search for pattern. Springer, Berlin Heidelberg New York, pp 157–169Google Scholar
  47. Mauricio R, Rausher MD, Burdick DS (1997) Variation in the defense strategies of plants: are resistance and tolerance mutually exclusive? Ecology 78:1301–1311Google Scholar
  48. Mitton JB, Grant MC (1996) Genetic variation and the natural history of quaking aspen. Bioscience 46:25–31Google Scholar
  49. Mutikainen P, Walls M (1995) Growth, reproduction and defense in nettles: responses to herbivory modified by competition and fertilization. Oecologia 104:487–495Google Scholar
  50. Mutikainen P, Walls M, Ovaska J, Keinänen M, Julkunen-Tiitto R, Vapaavuori E (2000) Herbivore resistance in Betula pendula: effect of fertilization, defoliation, and plant genotype. Ecology 81:49–65Google Scholar
  51. Neuvonen S, Haukioja E, Molarius A (1987) Delayed inducible resistance against a leaf-chewing insect in four deciduous tree species. Oecologia 74:363–369Google Scholar
  52. Nitao JK, Zangerl AR, Berenbaum MR, Hamilton JG, Delucia EH (2002) CNB: requiescat in pace? Oikos 98:539Google Scholar
  53. Osier TL (2001) Genotype and environment as determinants of intraspecific variation in quaking aspen phytochemistry and consequences for an insect herbivore. PhD thesis, University of Wisconsin–MadisonGoogle Scholar
  54. Osier TL, Lindroth RL (2001) Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. J Chem Ecol 27:1289–313PubMedGoogle Scholar
  55. Osier TL, Hwang SY, Lindroth RL (2000) Effects of phytochemical variation in quaking aspen Populus tremuloides clones on gypsy moth Lymantria dispar performance in the field and laboratory. Ecol Entomol 25:197–207CrossRefGoogle Scholar
  56. Parkinson JA, Allen SE (1975) A wet oxidation procedure suitable for the determination of nitrogen and mineral nutrients in biological material. Commun Soil Sci Plant Anal 6:1–11Google Scholar
  57. Perala DA (1990) Populus tremuloides Michx. Quaking Aspen. In: Burns RM, Honkala BH (eds) Silvics of North America. United States Department of Agriculture; Forest Service, Washington, D.C.Google Scholar
  58. Porter LJ, Hrstich LN, Chan BG (1986) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230Google Scholar
  59. Raubenheimer D, Simpson SJ (1992) Analysis of covariance: an alternative to nutritional indices. Entomol Exp Appl 62:221–231Google Scholar
  60. Reichenbacker RR, Schultz RC, Hart ER (1996) Artificial defoliation effect on Populus growth, biomass production, and total nonstructural carbohydrate concentration. Environ Entomol 25:632–642Google Scholar
  61. Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DH (eds) Herbivores, their interaction with secondary plant metabolites. Academic Press, New York, pp 3–54Google Scholar
  62. Robison DJ, Raffa KF (1994) Characterization of hybrid poplar clones for resistance to the forest tent caterpillar. For Sci 40:686–714Google Scholar
  63. Roth SK, Lindroth RL, Volin JC, Kruger EL (1998) Enriched atmospheric CO2 and defoliation: effects on tree chemistry and insect performance. Global Change Biol 4:419–430CrossRefGoogle Scholar
  64. Roy BA, Kirchner JW (2000) Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54:51–63PubMedGoogle Scholar
  65. Ruohomäki K, Hanhimaki S, Haukioja E, Iso-Iivari L, Neuvonen S, Niemelä P, Suomela J (1992) Variability in the efficacy of delayed inducible resistance in mountain birch. Entomol Exp Appl 62:107–115Google Scholar
  66. Ruohomäki K, Chapin FSI, Haukioja E, Neuvonen S, Suomela J (1996) Delayed inducible resistance in mountain birch in response to fertilization and shade. Ecology 77:2302–2311Google Scholar
  67. SAS (1999) SAS User’s Guide: Statistics. SAS Institute, Cary, N.C.Google Scholar
  68. Shen CS, Bach CE (1997) Genetic variation in resistance and tolerance to insect herbivory in Salix cordata . Ecol Entomol 22:335–342CrossRefGoogle Scholar
  69. Sokal RR, Rohlf FJ (1995) Biometry. Freeman, New YorkGoogle Scholar
  70. Stowe KA (1998) Experimental evolution of resistance in Brassica rapa: correlated response of tolerance in lines selected for glucosinolate content. Evolution 52:703–712Google Scholar
  71. Stowe KA, Marquis RJ, Hochwender CG, Simms E.L. (2000) The evolutionary ecology of tolerance to consumer damage. Annu Rev Ecol Syst 31:565–595Google Scholar
  72. Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185PubMedGoogle Scholar
  73. Tuomi J, Niemelä P, Chapin FSI, Bryant JP, Siren S (1988) Defensive responses of trees in relation to their carbon/nutrient balance. In: Mattson WJ, Levieux JC, Dagan B (eds) Mechanisms of woody plant defences against insects: search for pattern. Springer, Berlin Heidelberg New York, pp 57–72Google Scholar
  74. Tuomi J, Torbjörn F, Niemelä P (1991) Carbon allocation, phenotypic plasticity, and induced defenses. In: Tallamy DW, Raupp MJ (eds) Phytochemical induction by herbivores. Wiley, New York, pp 85–104Google Scholar
  75. Waldbauer GP (1968) The consumption and utilization of food by insects. Adv Insect Physiol 5:229–288Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Department of EntomologyUniversity of Wisconsin-MadisonMadisonUSA
  2. 2.Biology DepartmentFairfield UniversityFairfieldUSA

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