, Volume 172, Issue 1, pp 141–151 | Cite as

Long-term shifts in the cyclicity of outbreaks of a forest-defoliating insect

  • Andrew J. AllstadtEmail author
  • Kyle J. Haynes
  • Andrew M. Liebhold
  • Derek M. Johnson
Population ecology - Original research


Recent collapses of population cycles in several species highlight the mutable nature of population behavior as well as the potential role of human-induced environmental change in causing population dynamics to shift. We investigate changes in the cyclicity of gypsy moth (Lymantria dispar) outbreaks by applying wavelet analysis to an 86-year time series of forest defoliation in the northeastern United States. Gypsy moth population dynamics shifted on at least four occasions during the study period (1924–2009); strongly cyclical outbreaks were observed between ca. 1943–1965 and ca. 1978–1996, with noncyclical dynamics in the intervening years. During intervals of cyclical dynamics, harmonic oscillations at cycle lengths of 4–5 and 8–10 years co-occurred. Cross-correlation analyses indicated that the intensity of suppression efforts (area treated by insecticide application) did not significantly reduce the total area of defoliation across the region in subsequent years, and no relationship was found between insecticide use and the cyclicity of outbreaks. A gypsy moth population model incorporating empirically based trophic interactions produced shifting population dynamics similar to that observed in the defoliation data. Gypsy moth cycles were the result of a high-density limit cycle driven by a specialist pathogen. Though a generalist predator did not produce an alternative stable equilibrium, cyclical fluctuations in predator density did generate extended intervals of noncyclical behavior in the gypsy moth population. These results suggest that changes in gypsy moth population behavior are driven by trophic interactions, rather than by changes in climatic conditions frequently implicated in other systems.


Gypsy moth Lymantria dispar Generalist predator Insecticide Nonlinear dynamics 



Valuable advice on the use of wavelet analysis was provided by Y. Liu, B. Cazelles, and G.P. Compo. We thank the Morgantown Field Office of the USDA Forest Service Forest Health Protection for providing historical aerial spraying data, and Jonathan Walter, the editor, and an anonymous reviewer for their helpful comments. This research was funded by the University of Virginia’s Blandy Experimental Farm, a USDA-NRI grant (2006-35306-17264) to D.M.J., and an NSF grant (1020614) to K.J.H.

Supplementary material

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Supplementary material 1 (DOCX 23 kb)


  1. Bauch CT, Earn DJ (2003) Transients and attractors in epidemics. P R Soc B 270:1573CrossRefGoogle Scholar
  2. Berryman AA (1991) The gypsy moth in North America: a case of successful biological control? Trends Ecol Evol 6:110–111CrossRefGoogle Scholar
  3. Berryman AA (2002) Population cycles: the case for trophic interactions. Oxford University Press, New YorkGoogle Scholar
  4. Bjørnstad ON, Liebhold AM, Johnson DM (2008) Transient synchronization following invasion: revisiting Moran’s model and a case study. Popul Ecol 50:379–389CrossRefGoogle Scholar
  5. Bjørnstad ON, Robinet C, Liebhold AM (2010) Geographic variation in North American gypsy moth cycles: subharmonics, generalist predators, and spatial coupling. Ecology 91:106–118PubMedCrossRefGoogle Scholar
  6. Boulanger Y, Arseneault D (2004) Spruce budworm outbreaks in eastern Quebec over the last 450 years. Can J For Res 34:1035–1043CrossRefGoogle Scholar
  7. Box GE, Cox DR (1964) An analysis of transformations. J Roy Stat Soc B Met 26:211–252Google Scholar
  8. Campbell RW, Sloan RJ (1977) Natural regulation of innocuous gypsy moth populations. Environ Entomol 6:315–322Google Scholar
  9. Cazelles B, Chavez M, Magny GC, Guégan JF, Hales S (2007) Time-dependent spectral analysis of epidemiological time-series with wavelets. J R Soc Interface 4:625PubMedCrossRefGoogle Scholar
  10. Chatfield C (2004) The analysis of time series: an introduction. CRC, Boca RatonGoogle Scholar
  11. Costantino RF, Cushing JM, Dennis B, Desharnais RA (1995) Experimentally induced transitions in the dynamic behaviour of insect populations. Nature 375:227–230CrossRefGoogle Scholar
  12. Dennis B, Desharnais RA, Cushing JM, Costantino RF (1997) Transitions in population dynamics: equilibria to periodic cycles to aperiodic cycles. J Anim Ecol 66:704–729CrossRefGoogle Scholar
  13. Doane CC (1975) Infectious sources of nuclear polyhedrosis virus persisting in natural habitats of the gypsy moth. Environ Entomol 4:392–394Google Scholar
  14. Dwyer G, Dushoff J, Elkinton JS, Levin SA (2000) Pathogen-driven outbreaks in forest defoliators revisited: building models from experimental data. Am Nat 156:105–120PubMedCrossRefGoogle Scholar
  15. Dwyer G, Dushoff J, Yee SH (2004) The combined effects of pathogens and predators on insect outbreaks. Nature 430:341–345PubMedCrossRefGoogle Scholar
  16. Elias SP, Witham JW, Hunter ML Jr (2004) Peromyscus leucopus abundance and acorn mast: population fluctuation patterns over 20 years. J Mammal 85:743–747CrossRefGoogle Scholar
  17. Elkinton JS, Liebhold AM (1990) Population dynamics of gypsy moth in North America. Annu Rev Entomol 35:571–596CrossRefGoogle Scholar
  18. Elkinton JS, Healy WM, Buonaccorsi JP, Boettner GH, Hazzard AM, Smith HR (1996) Interactions among gypsy moths, white-footed mice, and acorns. Ecology 77:2332–2342CrossRefGoogle Scholar
  19. Elkinton JS, Liebhold AM, Muzika RM (2004) Effects of alternative prey on predation by small mammals on gypsy moth pupae. Popul Ecol 46:171–178CrossRefGoogle Scholar
  20. Esper J, Büntgen U, Frank DC, Nievergelt D, Liebhold A (2007) 1200 years of regular outbreaks in alpine insects. P R Soc B 274:671CrossRefGoogle Scholar
  21. Farge M (1992) Wavelet transforms and their applications to turbulence. Annu Rev Fluid Mech 24:395–458CrossRefGoogle Scholar
  22. Fox J (2002) An R and S-Plus companion to applied regression. Sage Publications, Inc., Thousand Oaks, CA, USAGoogle Scholar
  23. Grushecky ST, Liebhold AM, Greer R, Smith RL (1998) Does forest thinning affect predation on gypsy moth (Lepidoptera: Lymantriidae) larvae and pupae. Environ Entomol 27:268–276Google Scholar
  24. Hassell MP, Lawton JH, May RM (1976) Patterns of dynamical behaviour in single-species populations. J Anim Ecol 45:471–486CrossRefGoogle Scholar
  25. Hastings A (2004) Transients: the key to ecological understanding? Trends Ecol Evol 19:39–45PubMedCrossRefGoogle Scholar
  26. Haynes KJ, Liebhold AM, Fearer TM, Wang G, Norman GW, Johnson DM (2009a) Spatial synchrony propagates through a forest food web via consumer–resource interactions. Ecology 90:2974–2983Google Scholar
  27. Haynes KJ, Liebhold AM, Johnson DM (2009b) Spatial analysis of harmonic oscillation of gypsy moth outbreak intensity. Oecologia 159:249–256PubMedCrossRefGoogle Scholar
  28. Haynes KJ, Liebhold AM, Johnson DM (2012) Elevational gradient in the cyclicity of a forest-defoliating insect. Popul Ecol 54:239–250Google Scholar
  29. Henson SM, Cushing JM, Costantino RF, Dennis B, Desharnais RA (1998) Phase switching in population cycles. P R Soc B 265:2229CrossRefGoogle Scholar
  30. Ims RA, Henden JA, Killengreen ST (2008) Collapsing population cycles. Trends Ecol Evol 23:79–86PubMedCrossRefGoogle Scholar
  31. Johnson DM, Bjørnstad ON, Liebhold AM (2006a) Landscape mosaic induces traveling waves of insect outbreaks. Oecologia 148:51–60PubMedCrossRefGoogle Scholar
  32. Johnson DM, Liebhold A, Bjørnstad ON (2006b) Geographical variation in the periodicity of gypsy moth outbreaks. Ecography 29:367–374CrossRefGoogle Scholar
  33. Leonard DE (1981) Bioecology of the gypsy moth. In: Doane CC, McManus ML (eds) The gypsy moth: research toward integrated pest management (technical bulletin). US Department of Agriculture, Washington, DC, pp 9–29Google Scholar
  34. Liebhold A, McManus M (1999) The evolving use of insecticides in gypsy moth management. J For 97:20–23Google Scholar
  35. Liebhold AM, Simons EE, Sior A, Unger JD (1993) Forecasting defoliation caused by the gypsy moth from field measurements. Environ Entomol 22:26–32Google Scholar
  36. Liebhold A, Luzader E, Reardon R, Bullard A, Roberts A, Ravlin W, Delost S, Spears B (1996) Use of a geographic information system to evaluate regional treatment effects in a gypsy moth (Lepidoptera: Lymantriidae) management program. J Econ Entomol 89:1192–1203Google Scholar
  37. Liebhold A, Elkinton J, Williams D, Muzika RM (2000) What causes outbreaks of the gypsy moth in North America? Popul Ecol 42:257–266CrossRefGoogle Scholar
  38. Liu Y, San Liang X, Weisberg RH (2007) Rectification of the bias in the wavelet power spectrum. J Atm Oce Tech 24:2093–2102CrossRefGoogle Scholar
  39. May R (1974) Biological populations with non-overlapping generations: stable points, stable cycles and chaos. Science 186:645–647PubMedCrossRefGoogle Scholar
  40. Rohani P, Miramontes O, Hassell MP (1994) Quasiperiodicity and chaos in population models. P R Soc B 258:17–22CrossRefGoogle Scholar
  41. Royama T (1992) Analytical population dynamics. Kluwer, DordrechtGoogle Scholar
  42. Sardeshmukh PD, Compo GP, Penland C (2000) Changes of probability associated with El Niño. J Clim 13:4268–4286CrossRefGoogle Scholar
  43. Schauber EM, Ostfeld RS, Jones CG (2004) Type III functional response of mice to gypsy moth pupae: is it stabilizing? Oikos 107:592–602CrossRefGoogle Scholar
  44. Speer JH, Swetnam TW, Wickman BE, Youngblood A (2001) Changes in Pandora moth outbreak dynamics during the past 622 years. Ecology 82:679–697CrossRefGoogle Scholar
  45. Swetnam TW, Lynch AM (1993) Multicentury, regional-scale patterns of western spruce budworm outbreaks. Ecol Monogr 63:399–424CrossRefGoogle Scholar
  46. Torrence C, Compo GP (1998) A practical guide to wavelet analysis. B Am Meteorol Soc 79:61–78CrossRefGoogle Scholar
  47. Wang G, Wolff JO, Vessey SH, Slade NA, Witham JW, Merritt JF, Hunter ML, Elias SP (2009) Comparative population dynamics of Peromyscus leucopus in North America: influences of climate, food, and density dependence. Popul Ecol 51:133–142CrossRefGoogle Scholar
  48. Williams DW, Liebhold AM (1995) Influence of weather on the synchrony of gypsy moth (Lepidoptera: Lymantriidae) outbreaks in New England. Environ Entomol 24:987–995Google Scholar
  49. Williams DW, Fuester RW, Metterhouse WW, Balaam RJ, Bullock RH, Chianesei R (1991) Oak defoliation and population density relationships for the gypsy moth. J Econ Entomol 84:1508–1514Google Scholar
  50. Williamson M, Gaston KJ (1999) A simple transformation for sets of range sizes. Ecography 22:674–680CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Andrew J. Allstadt
    • 1
    Email author
  • Kyle J. Haynes
    • 1
  • Andrew M. Liebhold
    • 2
  • Derek M. Johnson
    • 3
  1. 1.The Blandy Experimental FarmUniversity of VirginiaBoyceUSA
  2. 2.USDA Forest Service, Northern Research StationMorgantownUSA
  3. 3.Department of BiologyVirginia Commonwealth UniversityRichmondUSA

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