Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Induced resistance in the indeterminate growth of aspen (Populus tremuloides)


Studies of induction in trees have examined rapid induced resistance (RIR) or delayed induced resistance (DIR), but have not examined induction that occurs in leaves produced by indeterminately growing trees subsequent to, but in the same season as, damage. We refer to induction that occurs during this time period as intermediate-delayed induced resistance (IDIR). We assessed the influences of genetic and environmental factors, and their interactions, on temporal and spatial variation in induction and on tradeoffs between induced and constitutive levels of resistance in indeterminately growing saplings of aspen (Populus tremuloides). We utilized a common garden of 12 aspen genotypes experiencing two levels of defoliation and two levels of soil nutrients. We assessed concentrations of phenolic glycosides and condensed tannins in damaged leaf remnants collected 1 week after defoliation to examine rapid and local induction, and in undamaged leaves produced 8 weeks after defoliation to assess intermediate-delayed and systemic induction. In general, tannins showed RIR, while phenolic glycosides expressed IDIR. For both classes of allelochemicals, we found high estimates of broad-sense heritability and genetic variation in both induced and constitutive levels. Genetic variation may be maintained by both direct costs of allelochemicals and by costs of inducibility (phenotypic plasticity). Such costs may drive the tradeoff exhibited between induced and constitutive levels of phenolic glycosides. IDIR may be important in reducing total-season tissue loss by providing augmented resistance against late summer herbivores in trees that have experienced damage earlier in the season. Herbivore-resistant compensatory growth is especially beneficial to young trees growing in competitive environments.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3


  1. Agrawal AA, Conner JK, Johnson MTJ, Wallsgrove R (2002) Ecological genetics of an induced plant defense against herbivores: additive genetic variance and costs of phenotypic plasticity. Evolution 56:2206–2213

  2. Agrell J, McDonald EP, Lindroth RL (2000) Effects of CO2 and light on tree phytochemistry and insect performance. Oikos 88:259–272

  3. Arnold TM, Schultz JC (2002) Induced sink strength as a prerequisite for induced tannin biosynthesis in developing leaves of Populus. Oecologia 130:585–593

  4. Arnold T, Appel H, Patel V, Stocum E, Kavalier A, Schultz J (2004) Carbohydrate translocation determines the phenolic content of Populus foliage: a test of the sink-source model of plant defense. New Phytol 164:157–164

  5. Ayres MP, Clausen TP, MacLean SF Jr, Redman AM, Reichardt PB (1997) Diversity of structure and antiherbivore activity in condensed tannins. Ecology 78:1696–1712

  6. Bailey JK, Bangert RK, Schweitzer JA, Trotter RT III, Shuster SM, Whitham TG (2004) Fractal geometry is heritable in trees. Evolution 58:2100–2102

  7. Bryant JP, Clausen TP, Reichardt PB, McCarthy MC, Werner RA (1987) 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 73:513–517

  8. Cerezke HF, Volney WJA (1995) Forest insect pests in the northwest region. In: Armstrong JA, Ives WGH (eds) Forest insect pests in Canada. Canadian Forest Service, Science and Sustainable Development Directorate, Ottawa, pp 59–72

  9. Clark CW, Harvell CD (1992) Inducible defenses and the allocation of resources—a minimal model. Am Nat 139:521–539

  10. Clausen TP, Evans T, Reichardt PB, Bryant JP (1989) A simple method for the isolation of salicortin, tremulacin and tremuloiden from quaking aspen (Populus tremuloides). J Nat Prod 52:207–209

  11. 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 71–83

  12. Close DC, McArthur C (2002) Rethinking the role of many plant phenolics–protection from photodamage not herbivores? Oikos 99:166–172

  13. Coley PD, Bryant JP, Chapin FS III (1985) Resource availability and plant antiherbivore defense. Science 230:895–899

  14. van Dam NM, Vrieling K (1994) Genetic variation in constitutive and inducible pyrrolizidine alkaloid levels in Cynoglossum officinale L. Oecologia 99:374–378

  15. Falconer DS (1985) Introduction to quantitative genetics. Longman, London

  16. Feeny PP (1976) Plant apparency and chemical defense. Rec Adv Phytochem 10:1–40

  17. Gatehouse JA (2002) Plant resistance towards insect herbivores: a dynamic interaction. New Phytol 156:145–169

  18. Glynn C, Herms DA, Egawa M, Hansen R, Mattson WJ (2003) Effects of nutrient availability on biomass allocation as well as constitutive and rapid induced herbivore resistance in poplar. Oikos 101:385–397

  19. Haile FJ, Higley LG, Specht JE, Spomer SM (1998) Soybean leaf morphology and defoliation tolerance. Agronomy J 90:353–362

  20. Harvell CD (1998) Genetic variation and polymorphism in the inducible spines of a marine bryozoan. Evolution 52:80–86

  21. Haukioja E (1990) Induction of defenses in trees. Annu Rev Ent 36:25–42

  22. 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 120:295–303

  23. Hemming JDC, Lindroth RL (1995) Intraspecific variation in aspen phytochemistry: effects on performance of gypsy moths and forest tent caterpillars. Oecologia 103:79–88

  24. Hemming JDC, Lindroth RL (1999) Effects of light and nutrient availability on aspen: growth, phytochemistry, and insect performance. J Chem Ecol 25:1687–1714

  25. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

  26. Hunter MD, Schultz JC (1995) Fertilization mitigates chemical induction and herbivore responses within damaged oak trees. Ecology 76:1226–1232

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

  28. Hwang S-Y, Lindroth RL (1998) Consequences of clonal variation in aspen phytochemistry for late season folivores. Ecoscience 5:508–516

  29. Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago

  30. Karban R, Myers JH (1989) Induced plant responses to herbivory. Annu Rev Ecol Syst 20:331–348

  31. Kellam SJ, Tisch MH, Walker JRL (1992) Screening of New Zealand native plants for enzyme-inhibitor activities. N Z J Bot 30:199–203

  32. Koricheva J, Nykanen H, Gianoli E (2004) Meta-analysis of trade-offs among plant antiherbivore defenses: are plants jacks-of-all-trades, masters of all? Am Nat 163:E64–E75

  33. Lindroth RL, Koss PA (1996) Preservation of Salicaceae leaves for phytochemical analyses: further assessment. J Chem Ecol 22:765–771

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

  35. Mattson WJ, Palmer SR (1988) Changes in foliar minerals and phenolics in trembling aspen, Populus tremuloides, in response to artificial defoliation. In: Mattson WJ, Levieux J, Bernard-Dagan C (eds) Mechanisms of woody plant defenses against insects: search for pattern. Springer, Berlin Heidelberg New York, pp 157–169

  36. Mattson WJ, Herms DA, Witter JA, Allen DC (1991) Woody plant grazing systems: North American outbreak folivores and their host plants. In: Baranchikov YN, Mattson WJ, Hain FP, Payne TL (eds) Forest insect guilds: patterns of interaction with host trees. USDA Forest Service, Northeastern Forest Experiment Station, Gen Tech Rep NE-153, Radnor, pp 53–84

  37. 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 81:49–65

  38. Nef L (1988) Interactions between the leaf miner, Phyllocnistis suffusella, and poplars. In: Mattson WJ, Levieux J, Bernard-Dagan C (eds) Mechanisms of woody plant defenses against insects: search for pattern. Springer, Berlin Heidelberg New York, pp 3–38

  39. 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-Madison

  40. Osier TL, Lindroth RL (2001) Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. J Chem Ecol 27:1289–1313

  41. Osier TL, Lindroth RL (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

  42. Parry D, Herms DA, Mattson WJ (2003) Responses of an insect folivore and its parasitoids to multiyear experimental defoliation of aspen. Ecology 84:1768–1783

  43. Peters DJ, Constabel CP (2002) Molecular analysis of herbivore-induced condensed tannin synthesis: cloning and expression of dihydroflavonol reductase from trembling aspen (Populus tremuloides). Plant J 32:701–712

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

  45. Prentice RM (1955) The life history and some aspects of the ecology of the large aspen tortrix, Choristoneura conflictana (Wlkr) (N Comb) (Lepidoptera: Tortricidae). Can Entomol 87:461–473

  46. Relyea RA (2002) Costs of phenotypic plasticity. Am Nat 159:272–282

  47. Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interaction with secondary plant metabolites. Academic, New York, pp 3–54

  48. Robison DJ, Raffa KF (1997) Effects of constitutive and inducible traits of hybrid poplars on forest tent caterpillar feeding and population ecology. For Sci 43:252–267

  49. Ruuhola TM, Sipura M, Nousiainen O, Tahvanainen J (2001) Systemic induction of salicylates in Salix myrsinifolia (Salisb). Ann Bot 88:483–497

  50. SAS Institute Inc. (2001) JMP Start Statistics, 2nd edn. Duxbury Press, Pacific Grove

  51. Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185

  52. Tiffin P, Rausher MD (1999) Genetic constraints and selection acting on tolerance to herbivory in the common morning glory Ipomoea purpurea. Am Nat 154:700–716

  53. Wright JW (1976) Introduction to forest genetics. Academic, New York

  54. Zangerl AR, Berenbaum MR (1990) Furanocoumarin induction in wild parsnip: genetics and populational variation. Ecology 71:1933–1940

Download references


This research was supported by NSF grant DEB-0074427 to R.L.L. and an EPA STAR Fellowship to M.T.S. We thank Jack Donaldson for micropropagating the trees used in this study and Laura Riel, Patrick Murray, Krissy Lindroth, and Nikki Lindroth for their assistance with tree maintenance and defoliation. Lynn Hummel and Isaac Kabera provided advice and access to field equipment. We thank Heidi Barnhill and Brian Rehill for their technical expertise and assistance with chemical analyses. Helen Bothwell helped with sample preparation and tannin analysis and Ed Mondor provided statistical advice. Don Waller, Tom Whitham, and two anonymous reviewers provided valuable comments that helped to improve the manuscript.

Author information

Correspondence to Michael T. Stevens.

Additional information

Communicated by Jim Ehleringer

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Stevens, M.T., Lindroth, R.L. Induced resistance in the indeterminate growth of aspen (Populus tremuloides). Oecologia 145, 297–305 (2005).

Download citation


  • Defoliation
  • Genotype × environment interaction
  • Herbivory
  • Phenotypic plasticity
  • Plant defense