, Volume 136, Issue 2, pp 244–251 | Cite as

Phenological variation as protection against defoliating insects: the case of Quercus robur and Operophtera brumata

Plant Animal Interactions


Phenological synchrony between budburst and emergence of larvae is critical for the fitness of many spring-feeding insect herbivores. Therefore, large intraspecific variation in timing of budburst of the host may have a negative effect on the herbivore. We studied how asynchrony between emergence of larvae and budburst affects the fitness of Operophtera brumata (Lepidoptera: Geometridae), a major defoliator of Quercus robur, which can adapt to the phenology of a single tree. It is known that, in maturing leaves of Q. robur, accumulation of condensed tannins has a negative effect on growth of O. brumata. However, there is no information about the effect of hydrolysable tannins and other phenolics that are potential antifeedants. In this study, we also analysed changes in secondary chemistry of the foliage of Q. robur and how different compounds are correlated with growth and survival of O. brumata. The effect of asynchrony on O. brumata was studied in rearing experiments. The neonate larvae were incubated without food for different periods of time. The decline in nutritional quality of foliage was estimated by rearing cohorts of larvae with manipulated hatching times on the leaves of ten individual Q. robur trees. For the chemical analysis, the foliage of these trees was sampled at regular intervals. In the absence of foliage, mortality of neonate larvae started to increase exponentially soon after the larvae emerged. If the larvae missed budburst, the decline in nutritional quality of the foliage led to increased mortality and lower body mass (= fecundity). Hydrolysable tannins were not significantly correlated with performance of the larvae. Only condensed tannins were found to correlate negatively with the growth and survival of O. brumata. Certain individual trees were unsuitable hosts for O. brumata because the decline in quality of the foliage was very rapid. Based on regression equations for increasing rate of mortality and decreasing fecundity, we calculated that a relatively small mismatch of ±30 degree days between budburst and hatching of larvae leads to a 50% decrease in the fitness of O. brumata. Thus, large phenological variation within a Q. robur stand can limit the colonisation of neighbouring trees by dispersing larvae. Furthermore, the hybridisation of moths adapted to phenologically different trees may lead to maladapted phenology of their offspring.


Host colonisation Herbivore fitness Insect herbivory Plant phenolics Tannins 


  1. Ayres MP, MacLean SF Jr (1987) Development of birch leaves and growth energetics of Epirrita autumnata (Geometridae). Ecology 68:558–568Google Scholar
  2. Ayres MP, Clausen TP, MacLean SF Jr, Redman AM, Reichardt PB (1997) Diversity of structure and antiherbivory activity in condensed tannins. Ecology 78:1696–1712Google Scholar
  3. Chen Z, Kolb TE, Clancy KM (2001) Mechanisms of Douglas-fir resistance to western spruce budworm defoliation: bud burst phenology, photosynthetic compensation and growth rate. Tree Physiol 21:1159–1169CrossRefPubMedGoogle Scholar
  4. Connor EF, Adams-Manson RH, Carr TG, Beck MW (1994) The effects of host plant phenology on the demography and population dynamics of the leaf-mining moth, Cameria hamadryadella (Lepidoptera: Gracillariidae). Ecol Entomol 19:111–120Google Scholar
  5. Crawley MJ, Akhteruzzaman M (1988) Individual variation in the phenology of oak trees and its consequences for herbivorous insects. Funct Ecol 2:409–415Google Scholar
  6. Du Merle P (1988) Phenological resistance of oaks to the green leafroller, Tortrix viridiana (Lepidoptera: Tortricidae). In: Mattson WJ, Levieux J, Bernard-Dagan C (eds) Mechanisms of woody plant defences against insects. Springer, Berlin Heidelberg New York, pp 215–226Google Scholar
  7. Edland T (1971) Wind dispersal of the winter moth larvae Operophtera brumata L. (Lep., Geometridae) and its relevance to control measures. Nor Entomol Tidsskr 18:103–107Google Scholar
  8. Edmunds GF, Alstad DN (1978) Coevolution in insect herbivores and conifers. Science 199:941–945Google Scholar
  9. Embree DG (1965) The population dynamics of the winter moth in Nova Scotia, 1954–62. Mem Entomol Soc Can 46:1–57Google Scholar
  10. Feeny P (1968) Effect of oak leaf tannins on larval growth of the winter moth Operophtera brumata. J Insect Physiol 14:805–817Google Scholar
  11. Feeny P (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51:565–581Google Scholar
  12. Fox CW, Waddell KJ, Groeters FR, Mosseau TA (1997) Variation in budbreak phenology affects the distribution of a leafmining beetle (Brachys tessellatus) on turkey oak (Quercus laevis). Ecoscience 4:480–489Google Scholar
  13. Graf B, Borer F, Höpli HU, Höhn H, Dorn S (1995) The winter moth, Operophtera brumata L. (Lep., Geometridae) on apple and cherry: spatial and temporal aspects of recolonization in autumn. J Appl Entomol 119:295–301Google Scholar
  14. Holliday NJ (1977) Population ecology of winter moth (Operophtera brumata) on apple in relation to larval dispersal and time of bud burst. J Appl Ecol 14:803–813Google Scholar
  15. Hough JA, Pimentel D (1978) Influence of host foliage on development, survival and fecundity of gypsy moth. Environ Entomol 7:97–102Google Scholar
  16. Humphrey JW, Swaine MD (1997) Factors affecting the natural regeneration of Quercus in Scottish oakwoods. II. Insect defoliation of trees and seedlings. J Appl Ecol 34:585–593Google Scholar
  17. Hunter AF, Lechowicz MJ (1992) Foliage quality changes during canopy development of some northern hardwood trees. Oecologia 89:316–323Google Scholar
  18. Hunter MD (1990) Differential susceptibility to variable plant phenology and its role in competition between two insect herbivores on oak. Ecol Entomol 15:401–408Google Scholar
  19. Hunter MD (1992) A variable insect-plant interaction: the relationship between tree budburst phenology and population levels of insect herbivores among trees. Ecol Entomol 16:91–95Google Scholar
  20. Julkunen-Tiitto R, Sorsa S (2001) Testing the drying methods for willow flavonoids, tannins and salicylates. J Chem Ecol 27:779–789CrossRefPubMedGoogle Scholar
  21. Kause A, Ossipov V, Haukioja E, Lempa K, Hanhimäki S, Ossipova S (1999) Multiplicity of biochemical factors determining quality of growing birch leaves. Oecologia 120:102–112CrossRefGoogle Scholar
  22. Kolb TE, Teulon DAJ (1991) Relationship between sugar maple budburst phenology and pear thrips damage. Can J For Res 21:1043–1048Google Scholar
  23. Lill JT, Marquis RJ (2001) The effects of leaf quality on herbivore performance and attack from natural enemies. Oecologia 126:418–428CrossRefGoogle Scholar
  24. Marino PC, Cornell HV (1993) Adult feeding and oviposition of Phytomyza ilicicola (Diptera: Agromyzidae) in response to leaf and tree phenology. Environ Entomol 22:1294–1301Google Scholar
  25. Mopper S, Simberloff D (1995) Differential herbivory in an oak population: the role of plant phenology and insect performance. Ecology 76:1233–1241Google Scholar
  26. Porter LJ, Hrstich LN, Chan BG (1986) The conversion of proanthocyanidins and prodelphinidins to cyanidins and delphinidins. Phytochemistry 25:223–230Google Scholar
  27. Quiring DT (1992) Rapid change in suitability of white spruce for a specialist herbivore, Zeiraphera canadensis, as a function of leaf age. Can J Zool 70:2132–2138Google Scholar
  28. Quiring DT (1994) Influence of inter-tree variation in time of budburst of white spruce on herbivory and the behaviour and survivorship of Zeiraphera canadensis. Ecol Entomol 19:17–25Google Scholar
  29. Rice WR (1989) Analyzing tables of statistical tests. Evolution 42:223–225Google Scholar
  30. Roland J, Myers JH (1987) Improved insect performance from host-plant defoliation: winter moth on oak and apple. Ecol Entomol 12:409–414Google Scholar
  31. Rossiter MC, Schultz JC, Baldwin IT (1988) Relationships among defoliation, red oak phenolics, and gypsy moth growth and reproduction. Ecology 69:267–277Google Scholar
  32. Scalbert A, Haslam E (1987) Polyphenols and chemical defence of the leaves of Quercus robur. Phytochemistry 26:3191–3195CrossRefGoogle Scholar
  33. Scriber JM, Slansky F Jr (1981) Nutritional ecology of immature insects. Annu Rev Entomol 26:183–211Google Scholar
  34. SigmaPlot (1999) SigmaPlot 5.0 Users Guide. SPSS, ChicagoGoogle Scholar
  35. Speyer W (1941) Weitere Beiträge zur Biologie und Bekämpfung des Kleinen Frostspanners (Cheimatobia brumata L.). Arb Physiol Angew Entomol Berlin-Dahlem 8:245–261Google Scholar
  36. SPSS (2000) SPSS Base 10.0 Users Guide. SPSS, ChicagoGoogle Scholar
  37. Tammaru T (1998) Determination of adult size in folivorous moth: constraints at instar level? Ecol Entomol 23:80–89Google Scholar
  38. Tikkanen O-P, Lyytikäinen-Saarenmaa P (2002) Adaptation of a generalist moth, Operophtera brumata, to variable budburst phenology of host plants. Entomol Exp Appl 103:123–133CrossRefGoogle Scholar
  39. Tikkanen O-P, Niemelä P, Keränen J (2000) Growth and development of a generalist insect herbivore, Operophtera brumata, on original and alternative host plants. Oecologia 122:529–536CrossRefGoogle Scholar
  40. Van Dongen S, Matthysen E, Dhondt AA (1996) Restricted male winter moth (Operophtera brumata L.) dispersal among host trees. Acta Oecol 17:319–229Google Scholar
  41. Van Dongen S, Backeljau T, Matthysen E, Dhondt AA (1997) Synchronization of hatching date with budburst of individual host trees (Quercus robur) in the winter moth (Operophtera brumata) and its fitness consequences. J Anim Ecol 66:113–121Google Scholar
  42. Van Zandt PA, Mopper S (1998) A meta-analysis of adaptive deme formation ín phytophagous insect populations. Am Nat 152:595–604CrossRefGoogle Scholar
  43. Varley GC, Gradwell GR (1968) Population models for the winter moth. In: Southwood TRE (ed) Symposia of the royal entomological society of London No. 4. Blackwell, Oxford, pp 132–142Google Scholar
  44. Wint W (1983) The role of alternative host-plant species in the life of a polyphagous moth, Operophtera brumata (Lepidoptera: Geometridae). J Anim Ecol 52:439–450Google Scholar

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© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Department of BiologyUniversity of JoensuuJoensuuFinland

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