Skip to main content
SpringerLink
Log in

Historical change in the outbreak dynamics of an invading forest insect

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The population dynamics and impacts of non-native species often change following their initial establishment, with impacts either increasing or decreasing over time. The reasons why the abundance of an invading species may change are varied but often reflect changes in the way in which populations interact with resident communities. Here we analyze changes in the outbreak dynamics of Lymantria dispar (formerly known to as the “gypsy moth”), a Eurasian foliage-feeding insect that has been established in N. America for ca. 150 years. We find that during the course of this species’ presence in N. America, it has continually exhibited population dynamics in which populations reach outbreak levels, resulting in defoliation of large forested areas. However, there is evidence of some changes in both the periodicity and synchrony of these outbreaks. We hypothesize that the accidental introduction of an entomopathogenic nucleopolyhedrosis virus around 1906 resulted in populations shifting from a pattern of sustained outbreaks to oscillatory dynamics with periodic outbreaks synchronized over large distances. We analyze historical L. dispar population data that provide some evidence in support of this hypothesis. There is also evidence that the more recent establishment of the fungal pathogen Entomophaga maimaiga has caused a decrease in the amplitude of L. dispar outbreaks since its emergence in 1989.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abbott KC, Dwyer G (2008) Using mechanistic models to understand synchrony in forest insect populations: the North American gypsy moth as a case study. Am Nat 172:613–624

    Article  PubMed  Google Scholar 

  • Allstadt AJ, Haynes KJ, Liebhold AM, Johnson DM (2013) Long-term shifts in the cyclicity of outbreaks of a forest-defoliating insect. Oecologia 172:141–151

    Article  PubMed  Google Scholar 

  • Allstadt AJ, Liebhold AM, Johnson DM, Davis RE, Haynes KJ (2015) Temporal variation in the synchrony of weather and its consequences for spatiotemporal population dynamics. Ecology 96:2935–2946

    Article  PubMed  Google Scholar 

  • Bjørnstad ON (2000) Cycles and synchrony: two historical ‘experiments’ and one experience. J Anim Ecol 69:869–873

    Article  PubMed  Google Scholar 

  • Bjørnstad ON, Falck W (2001) Nonparametric spatial covariance functions: estimation and testing. Environ Ecol Stat 8:53–70

    Article  Google Scholar 

  • Bjørnstad ON, Liebhold AM, Johnson DM (2008) Transient synchronization following invasion: revisiting Moran’s model and a case study. Pop Ecol 50:379–389

    Article  Google Scholar 

  • Bjørnstad ON, Robinet C, Liebhold AM (2010) Geographic variation in the North American gypsy moth cycles: sub-harmonics, generalist predators and spatial coupling. Ecology 91:106–118

    Article  PubMed  Google Scholar 

  • Blackburn TM, Essl F, Evans T, Hulme PE, Jeschke JM, Kühn I, Kumschick S, Marková Z, Mrugała A, Nentwig W, Pergl J (2014) A unified classification of alien species based on the magnitude of their environmental impacts. PLoS Biol 12:e1001850

    Article  PubMed  PubMed Central  Google Scholar 

  • Burgess AF, Baker WL (1938) The gypsy and brown-tail moths and their control. US Dept Agric Circ 464

  • Burgess AF (1944) The gypsy moth and the brown-tail moth - history of the work for prevention of spread and extermination of these insects in North America. 343 p. online at https://naldc.nal.usda.gov/catalog/6124364

  • Campbell RW (1967) The analysis of numerical change in gypsy moth populations. For Sci Monogr 33:1–34

    Google Scholar 

  • Clifton EH, Castrillo LA, Gryganskyi A, Hajek AE (2019) A pair of native fungal pathogens drives decline of a new invasive herbivore. PNAS 116:9178–9180

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733

    Article  Google Scholar 

  • Dalgleish HJ, Nelson CD, Scrivani JA, Jacobs DF (2015) Consequences of shifts in abundance and distribution of American chestnut for restoration of a foundation forest tree. Forests 7:4

    Article  Google Scholar 

  • Desurmont GA, Donoghue MJ, Clement WL, Agrawal AA (2011) Evolutionary history predicts plant defense against an invasive pest. PNAS 108:7070–7074

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dwyer G, Dushoff J, Yee SH (2004) The combined effects of pathogens and predators on insect outbreaks. Nature 430:341–345

    Article  PubMed  CAS  Google Scholar 

  • Elkinton JS, Liebhold AM (1990) Population dynamics of gypsy moth in North America. Ann Rev Entomol 35:571–596

    Article  Google Scholar 

  • Epanchin-Niell RS, Liebhold AM (2015) Benefits of invasion prevention: effect of time lags, spread rates, and damage persistence. Ecol Econ 116:146–153

    Article  Google Scholar 

  • Fei S, Morin RS, Oswalt CM, Liebhold AM (2019) Biomass losses resulting from insect and disease invasions in US forests. PNAS 116:17371–17376

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Forbush EH, Fernald CH (1896) The gypsy moth. Porthetria dispar (Linn.). The gypsy moth. Porthetria dispar (Linn.). Wright & Potter, Boston

  • Gandhi KJ, Herms DA (2010) Direct and indirect effects of alien insect herbivores on ecological processes and interactions in forests of eastern North America. Biol Invas 12:389–405

    Article  Google Scholar 

  • Glaser RW (1915) Wilt of gypsy-moth caterpillar. J Agric Res 4:101–126

    Google Scholar 

  • Hajek AE, Eilenberg J (2018) Natural enemies: an introduction to biological control. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Hajek AE, Humber RA, Elkinton JS (1995) Mysterious origin of Entomophaga maimaiga in North America. Am Entomol 41:31–43

    Article  Google Scholar 

  • Hajek AE, Tobin PC, Haynes KJ (2015) Replacement of a dominant viral pathogen by a fungal pathogen does not alter the collapse of a regional forest insect outbreak. Oecologia 177:785–797

    Article  PubMed  Google Scholar 

  • Hamed KH, Rao RA (1998) A modified Mann-Kendall trend test for autocorrelated data. J Hydrol 204:182–196

    Article  Google Scholar 

  • Haynes KJ, Walter JA, Liebhold AM (2019) Population spatial synchrony enhanced by periodicity and low detuning with environmental forcing. Proc R Soc B 286:20182828

    Article  PubMed  PubMed Central  Google Scholar 

  • Howard LO, Fiske WF (1911) The importation into the United States of the parasites of the gipsy moth and the brown-tail moth: a report of progress, with some consideration of previous and concurrent efforts of this kind. US Dept Agric Bull No. 91. US Government Printing Office, Washington

  • Jeffries MJ, Lawton JH (1984) Enemy free space and the structure of ecological communities. Biol J Linn Soc 23:269–286

    Article  Google Scholar 

  • Johnson DM, Liebhold AM, Bjørnstad ON (2006) Geographical variation in the periodicity of gypsy moth outbreaks. Ecography 29:367–374

    Article  Google Scholar 

  • Johnson DM, Liebhold AM, Bjørnstad ON, McManus ML (2005) Circumpolar variation in periodicity and synchrony among gypsy moth populations. J Anim Ecol 74:882–892

    Article  Google Scholar 

  • Jones JN (1910) Further studies on the nature of the wilt disease of the gypsy moth Larvae. In: Rane FW (ed) The State Forester of Massachusetts, Seventh Annual Report, 1910. Boston. pp 100–105

  • Liebhold AM (1992) Are North American populations of gypsy moth (Lepidoptera: Lymantriidae) bimodal? Environ Entomol 21:221–229

    Article  Google Scholar 

  • Liebhold AM, Simons EE, Sior A, Unger JD (1993) Forecasting defoliation caused by the gypsy moth from field measurements. Environ Entomol 22:26–32

    Article  Google Scholar 

  • Liebhold AM, Gottschalk KW, Mason DA, Bush RR (1997b) Evaluation of forest susceptibility to the gypsy moth across the conterminous United States. J for 95:20–24

    Google Scholar 

  • Liebhold AM, Haynes KJ, Bjørnstad ON (2012) Spatial synchrony of insect outbreaks. pages. In: Barbosa P, LeTourneau DK, Agrawal AA (eds) Insect outbreaks revisited. Wiley, New York, pp 113–125

    Chapter  Google Scholar 

  • Liebhold A, Thorpe K, Ghent J, Lyons DB (1994) Gypsy moth egg mass sampling for decision-making: a user’s guide. US Dept Agric Forest Service NA-TP-04–94

  • Liebhold AM, Gottschalk KW, Luzader ER, Bush R, Twardus DB (1997a) Gypsy moth in the United States: an atlas. US Dept Agric Forest Service Gen Tech Rep NE-233

  • Morin RS, Liebhold AM (2016) Invasive forest defoliator contributes to the impending downward trend of oak dominance in eastern North America. Forestry 89:284–289

    Article  Google Scholar 

  • Nielsen C, Milgroom MG, Hajek AE (2005) Genetic diversity in the gypsy moth fungal pathogen Entomophaga maimaiga from founder populations in North America and source populations in Asia. Mycol Res 109:941–950

    Article  PubMed  CAS  Google Scholar 

  • Patakamuri SK, O'Brien N (2019) modifiedmk: Modified Versions of Mann Kendall and Spearman's Rho Trend Tests. R package version 1.3.0. https://CRAN.R-project.org/package=modifiedmk

  • Reardon RC, Podgwaite JD (1976) Disease-parasitoid relationships in natural populations of Lymantria dispar (Lep.: Lymantriidae) in the northeastern United States. Entomophaga 21:333–341

    Article  Google Scholar 

  • Reardon RC (1981) Rearing, evaluating, and attempting to establish exotic species and redistributing established species, attempts before 1960. In: Doane CC, McManus ML (eds) The gypsy moth: research toward integrated pest management. US Dept Agric Tech Bull, Washington, pp 348–351

    Google Scholar 

  • Reiff W (1911) The “wilt disease” or" flacherie" of the gypsy moth. Wright & Potter, Boston

    Book  Google Scholar 

  • Rogers DM, Burgess AF (1910) Report on the field work against the gipsy moth and the brown-tail moth. US Dept Agrc Bur Entomol Bulletin No 87, Washington

    Book  Google Scholar 

  • Simberloff D, Gibbons L (2004) Now you see them, now you don’t!–population crashes of established introduced species. Biol Invas 6:161–172

    Article  Google Scholar 

  • Smith HR, Lautenschlager RA, Doane CC, McManus ML (1981) Gypsy moth predators. In: Doane CC, McManus ML (eds) The gypsy moth: research toward integrated pest management. US Dept Agric Tech Bull, Washington, pp 96–125

    Google Scholar 

  • Speare AT, Colley RH (1912) The artificial use of the browntail fungus in Massachusetts, with practical suggestions for private experiment, and a brief note on a fungus disease of the gypsy caterpillar. Wright & Potter, Boston

    Google Scholar 

  • U.S. Forest Service (2020) Gypsy moth digest (online database). https://www.fs.usda.gov/naspf/programs/forest-health-protection/gypsy-moth-digest

  • Vilà M, Hulme PE (eds) (2017) Impact of biological invasions on ecosystem services. Springer International Publishing, Cham

    Google Scholar 

  • Weseloh RM (1998) Possibility for recent origin of the gypsy moth (Lepidoptera: Lymantriidae) fungal pathogen Entomophaga maimaiga (Zygomycetes: Entomophthorales) in North America. Environ Entomol 27:171–177

    Article  Google Scholar 

  • Williams DW, Liebhold AM (1995) Influence of weather on the synchrony of gypsy moth (Lepidoptera: Lymantriidae) outbreaks in New England. Environ Entomol 24:987–995

    Article  Google Scholar 

  • Williams DW, Fuester RW, Metterhouse WW, Balaam RJ, Bullock RH, Chianesei RJ (1991) Oak defoliation and population density relationships for the gypsy moth (Lepidoptera: Lymantriidae). J Econ Entomol 84:1508–1514

    Article  Google Scholar 

  • Williamson M (1996) Biological Invasions. Chapman & Hall, London

    Google Scholar 

  • Woods SA, Elkinton JS, Murray KD, Liebhold AM, Gould JR, Podgwaite JD (1991) Transmission dynamics of a nuclear polyhedrosis virus and predicting mortality in gypsy moth (Lepidoptera: Lymantriidae) populations. J Econ Entomol 84:423–430

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the USDA Forest Service, The Charles Bullard Fellowship Program at Harvard Forest and Grants from the National Science Foundation Macro systems Biology Program (Grant Numbers 1241932, 1638702) and Grant EVA4.0, No. CZ.02.1.01/0.0/0.0/16_019/0000803 financed by OP RDE. JAW was supported by The Nature Conservancy and NSF grant OAC-1839024. We thank Eugene Luzader for technical assistance. The authors are grateful to reviewers and editors whose comments greatly improved the paper.

Funding

USDA Forest Service, The Charles Bullard Fellowship Program at Harvard Forest, National Science Foundation Macrosystems Biology Program, Czech Ministry of Education Operational Programme for Research, Development and Education, The Nature Conservancy

Author information

Authors and Affiliations

  1. USDA Forest Service Northern Research Station, Morgantown, WV, 26505, USA

    Andrew M. Liebhold

  2. Faculty of Forestry and Wood Sciences, Czech University of Life Sciences Prague, 165 21, Praha 6-Suchdol, Czech Republic

    Andrew M. Liebhold

  3. Department of Entomology, Cornell University, Ithaca, NY, 14853, USA

    Ann E. Hajek

  4. Department of Environmental Sciences, University of Virginia, Charlottesville, VA, 22904, USA

    Jonathan A. Walter

  5. The Blandy Experimental Farm, University of Virginia, Boyce, VA, 22620, USA

    Kyle J. Haynes

  6. Department of Environmental Conservation, University of Massachusetts, Amherst, MA, 01003, USA

    Joseph Elkinton

  7. Carnegie Museum of Natural History, Pittsburgh, PA, 15213, USA

    Rose-Marie Muzika

Authors
  1. Andrew M. Liebhold
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ann E. Hajek
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jonathan A. Walter
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kyle J. Haynes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joseph Elkinton
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rose-Marie Muzika
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrew M. Liebhold.

Ethics declarations

Conflicts of interest

The authors that they have declare no conflict of interest.

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Code availability

Code used during the current study are available from the corresponding author on reasonable request.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liebhold, A.M., Hajek, A.E., Walter, J.A. et al. Historical change in the outbreak dynamics of an invading forest insect. Biol Invasions 24, 879–889 (2022). https://doi.org/10.1007/s10530-021-02682-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-021-02682-6

Keywords

Search

Navigation