Biological Invasions

, Volume 18, Issue 12, pp 3561–3573 | Cite as

All quiet on the western front? Using phenological inference to detect the presence of a latent gypsy moth invasion in Northern Minnesota

  • Patrick C. Tobin
  • Kimberly Thielen Cremers
  • Lucia Hunt
  • Dylan Parry
Original Paper


Following establishment in a new environment, invasive species expand their range through stratified diffusion, the coupling of local growth and spatial spread with long-distance movement of propagules that found new colonies. Consequently, the stages of arrival and establishment serially repeat until the entire habitat susceptible to invasion is occupied. An empirical example of such a phenomenon is the gypsy moth, Lymantria dispar (L.), invasion of northeastern Minnesota. Under a regional management program, a trapping grid is deployed along the L. dispar leading edge to detect male moth presence and inform management decisions. However, the presence of moths does not always indicate reproducing populations, and moths dispersing from populations behind the front can obscure the presence of latent invasions. We analyzed trapping data during the arrival and establishment of L. dispar in this region (2000–2012), supplemented with sentinel trap data to ascertain the timing of male moth flight (2005–2009), and derived yearly phenological predictions for male moth flight. We also used a male wing morphology metric (2007–2009) to further quantify spatial and temporal patterns associated with the L. dispar invasion. We provide evidence of an established L. dispar population when analyses suggest spatial randomness in trap catch data, and how the presence of phenologically distinct, immigrating adult moths from source populations outside of Minnesota recorded from sentinel traps could lead to the overestimation of the abundance of an established population. This work highlights the complexity of the initial invasion process even in a well-studied system for which a sensitive monitoring program exists.


Establishment Lymantria dispar Spread Stratified dispersal 



We thank Donna Leonard, John Kyhl, Ken Klein, Laura Blackburn, and Regis Young (USDA Forest Service); Natasha Northrop, Alison Rossow, Erich Borchardt, Cree Bradley, and Bob Kangas (Minnesota Department of Agriculture); and David Nesbitt (College of Environmental Science and Forestry, State University of New York) for valuable laboratory and field support. We are very grateful to Rémi St-Amant (Canadian Forest Service) for providing phenological predictions of L. dispar. We thank Joe Elkington (University of Massachusetts) for helpful comments and suggestions. We acknowledge funds from the Gypsy Moth Slow-the-Spread Foundation, Inc. (Grant Number A106307 to PCT) and the USDA Forest Service, Northern Research Station (Grant Number 11-JV-11242303-053 to DP) in support of this study.


  1. Aukema JE, McCullough DG, Von Holle B et al (2010) Historical accumulation of nonindigenous forest pests in the continental US. Bioscience 60:886–897CrossRefGoogle Scholar
  2. Beirne BP (1975) Biological control attempts by introductions against pest insects in the field in Canada. Can Entomol 107:225–236CrossRefGoogle Scholar
  3. Bigsby KM, Tobin PC, Sills EO (2011) Anthropogenic drivers of gypsy moth spread. Biol Invasions 13:2077–2090CrossRefGoogle Scholar
  4. Bjørnstad ON (2012) Package ‘ncf.’ spatial nonparametric covariance functions.
  5. Bjørnstad O, Falck W (2001) Nonparametric spatial covariance functions: estimating and testing. Environ Ecol Stat 8:53–70CrossRefGoogle Scholar
  6. Brockerhoff EG, Bain J, Kimberley M et al (2006) Interception frequency of exotic bark and ambrosia beetles (Coleoptera: Scolytinae) and relationship with establishment in New Zealand and worldwide. Can J For Res 36:289–298CrossRefGoogle Scholar
  7. Brockerhoff EG, Kimberley M, Liebhold AM et al (2014) Predicting how altering propagule pressure changes establishment rates of biological invaders across species pools. Ecology 95:594–601CrossRefPubMedGoogle Scholar
  8. Capinera JL, Barbosa P (1976) Dispersal of first-instar gypsy moth larvae in relation to population quality. Oecologia 26:53–64CrossRefGoogle Scholar
  9. Carter MR, Ravlin FW, McManus ML (1991) Changes in gypsy moth (Lepidoptera: Lymantriidae) fecundity and male wing length resulting from defoliation. Environ Entomol 20:1042–1047CrossRefGoogle Scholar
  10. Colautti R, Grigorovich I, MacIsaac H (2006) Propagule pressure: a null model for biological invasions. Biol Invasions 8:1023–1037CrossRefGoogle Scholar
  11. Doane CC, McManus ML (1981) The gypsy moth: research toward integrated pest management. Technical Bulletin 1584, United States Department of Agriculture, Washington, DCGoogle Scholar
  12. Dvorak RG, Watson AE, Christensen N et al (2012) The boundary waters canoe area wilderness: examining changes in use, users, and management challenges. United States Department of Agriculture, Rocky Mountain Research Station, Research Paper RMRS-RP-91Google Scholar
  13. Efron B, Tibshirani RJ (1993) An introduction to the bootstrap. Chapman & Hall, LondonCrossRefGoogle Scholar
  14. Elkinton JS, Liebhold AM (1990) Population dynamics of gypsy moth in North America. Annu Rev Entomol 35:571–596CrossRefGoogle Scholar
  15. Frank KL, Tobin PC, Thistle HW Jr et al (2013) Interpretation of gypsy moth frontal advance using meteorology in a conditional algorithm. Int J Biometeorol 57:459–473CrossRefPubMedGoogle Scholar
  16. Gray DR (2004) The gypsy moth life stage model: landscape-wide estimates of gypsy moth establishment using a multi-generational phenology model. Ecol Model 176:155–171CrossRefGoogle Scholar
  17. Gray DR (2009) Age-dependent postdiapause development in the gypsy moth (Lepidoptera: Lymantriidae) life stage model. Environ Entomol 38:18–25CrossRefPubMedGoogle Scholar
  18. Gray DR, Ravlin FW, Braine JA (2001) Diapause in the gypsy moth: a model of inhibition and development. J Insect Physiol 47:173–184CrossRefPubMedGoogle Scholar
  19. Hajek AE, Tobin PC (2009) North American eradications of Asian and European gypsy moth. In: Hajek AE, Glare TR, O’Callaghan M (eds) Use of microbes for control and eradication of invasive arthropods. Springer, New York, pp 71–89CrossRefGoogle Scholar
  20. Hanna M (1982) Gypsy moth (Lepidoptera: Lymantriidae) history of eradication efforts in Michigan, 1954–1981. Great Lakes Entomol 15:191–198Google Scholar
  21. Haukioja E, Ossipov V, Lempa K (2002) Interactive effects of leaf maturation and phenolics on consumption and growth of a geometrid moth. Entomol Exp Appl 104:125–136CrossRefGoogle Scholar
  22. Hunter AF (1993) Gypsy moth population sizes and the window of opportunity in the spring. Oikos 68:531–538CrossRefGoogle Scholar
  23. Hunter AF, Elkinton JS (1999) Interaction between phenology and density effects on mortality from natural enemies. J Anim Ecol 68:1093–1100CrossRefGoogle Scholar
  24. Hunter AF, Elkinton JS (2000) Effects of synchrony with host plant on populations of a spring-feeding Lepidopteran. Ecology 81:1248–1261CrossRefGoogle Scholar
  25. Johnson DM, Liebhold AM, Tobin PC et al (2006) Allee effects and pulsed invasion of the gypsy moth. Nature 444:361–363CrossRefPubMedGoogle Scholar
  26. Krause SC, Walker MA, Klonowski J et al (1994) Gypsy moth in Wisconsin—1994. In: Proceedings of the annual gypsy moth review, Portland, OR, pp 351–356Google Scholar
  27. Lance DR, Elkinton JS, Schwalbe CP (1987) Microhabitat and temperature effects explain accelerated development during outbreaks of the gypsy moth (Lepidoptera: Lymantriidae). Environ Entomol 16:202–205CrossRefGoogle Scholar
  28. Lewis MA, Kareiva P (1993) Allee dynamics and the spread of invading organisms. Theor Popul Biol 43:141–158CrossRefGoogle Scholar
  29. Liebhold AM, Tobin PC (2006) Growth of newly established alien populations: comparison of North American gypsy moth colonies with invasion theory. Popul Ecol 48:253–262CrossRefGoogle Scholar
  30. Liebhold AM, Tobin PC (2008) Population ecology of insect invasions and their management. Annu Rev Entomol 53:387–408CrossRefPubMedGoogle Scholar
  31. Liebhold A, Mastro V, Schaefer PW (1989) Learning from the legacy of Leopold Trouvelot. Bull Entomol Soc Am 35:20–22Google Scholar
  32. Liebhold AM, Halverson JA, Elmes GA (1992) Gypsy moth invasion in North America: a quantitative analysis. J Biogeogr 19:513–520CrossRefGoogle Scholar
  33. Liebhold AM, Gottschalk KW, Muzika RM et al (1995) Suitability of North American tree species to the gypsy moth: a summary of field and laboratory tests. USDA Forest Service General Technical Report NE-211, Radnor, PAGoogle Scholar
  34. Liebhold AM, Brockerhoff EG, Garrett LJ et al (2012) Live plant imports: the major pathway for forest insect and pathogen invasions of the United States. Front Ecol Environ 10:135–143CrossRefGoogle Scholar
  35. Liebhold AM, Berec L, Brockeroff EG et al (2016) Eradication of invading insect populations: from concepts to applications. Annu Rev Entomol 61:335–352CrossRefPubMedGoogle Scholar
  36. Lockwood JL, Hoopes M, Marchetti M (2007) Invasion ecology. Blackwell, MaldenGoogle Scholar
  37. Lockwood JL, Cassey P, Blackburn TM (2009) The more you introduce the more you get: the role of colonization pressure and propagule pressure in invasion ecology. Divers Distrib 15:904–910CrossRefGoogle Scholar
  38. Ludsin SA, Wolfe AD (2001) Biological invasion theory: Darwin’s contributions from the origin of species. Bioscience 51:780–789CrossRefGoogle Scholar
  39. Mason CJ, McManus ML (1981) Larval dispersal of the gypsy moth. In: Doane CC, McManus ML (eds) The gypsy moth: research toward integrated pest management. USDA Forest Service, Technical Bulletin 1584, Washington, DC, pp 161–202Google Scholar
  40. McCullough DG, Work TT, Cavey JF et al (2006) Interceptions of nonindigenous plant pests at US ports of entry and border crossings over a 17-year period. Biol Invasions 8:611–630CrossRefGoogle Scholar
  41. Minnesota Department of Natural Resources (2015) Laurentian mixed forest province.
  42. National Climatic Data Center (2015)
  43. National Oceanic and Atmospheric Administration (2015) National weather service.
  44. Odell TM, Mastro VC (1980) Crepuscular activity of gypsy moth adults (Lymantria dispar). Environ Entomol 9:613–617CrossRefGoogle Scholar
  45. Parry D, Spence JR, Volney WJA (1998) Bud break phenology and natural enemies mediate survival of early instar forest tent caterpillar (Lepidoptera: Lasiocampidae). Environ Entomol 27:1368–1374CrossRefGoogle Scholar
  46. R Development Core Team (2015) The R project for statistical computing, Vienna, Austria.
  47. Raupp MJ, Werren JH, Sadof CS (1988) Effects of short-term phenological changes in leaf suitability on the survivorship, growth, and development of gypsy moth (Lepidoptera: Lymantriidae) larvae. Environ Entomol 17:316–319CrossRefGoogle Scholar
  48. Régnière J, Sharov AA (1998) Phenology of Lymantria dispar (Lepidoptera: Lymantriidae), male flight and the effect of moth dispersal in heterogeneous landscapes. Int J Biometeorol 41:161–168CrossRefGoogle Scholar
  49. Régnière J, Sharov AA (1999) Simulating temperature-dependent ecological processes at the sub-continental scale: male gypsy moth flight phenology as an example. J Biometeorol 42:146–152CrossRefGoogle Scholar
  50. Riley CV, Vasey G (1870) Importd insects and native American insects. Am Entomol 2:110–112Google Scholar
  51. Robinet C, Lance DR, Thorpe KW et al (2008) Dispersion in time and space affect mating success and Allee effects in invading gypsy moth populations. J Anim Ecol 77:966–973CrossRefPubMedGoogle Scholar
  52. Sharov AA, Liebhold AM (1998) Model of slowing the spread of gypsy moth (Lepidoptera: Lymantriidae) with a barrier zone. Ecol Appl 8:1170–1179CrossRefGoogle Scholar
  53. Sharov AA, Roberts EA, Liebhold AM et al (1995) Gypsy moth (Lepidoptera: Lymantriidae) spread in the central Appalachians: three methods for species boundary estimation. Environ Entomol 24:1529–1538CrossRefGoogle Scholar
  54. Shigesada N, Kawasaki K, Takeda Y (1995) Modeling stratified diffusion in biological invasions. Am Nat 146:229–251CrossRefGoogle Scholar
  55. Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Evol Syst 40:81–102CrossRefGoogle Scholar
  56. Slow-the-Spread Foundation, Inc (2013)
  57. Stockhoff BA (1991) Starvation resistance of gypsy moth, Lymantria dispar (L.) (Lepidoptera: Lymantriidae): tradeoffs among growth, body size, and survival. Oecologia 88:422–429CrossRefGoogle Scholar
  58. Tobin PC (2007) Space-time patterns during the establishment of a nonindigenous species. Popul Ecol 49:257–263CrossRefGoogle Scholar
  59. Tobin PC, Blackburn LM (2007) Slow the spread: a national program to manage the gypsy moth. USDA Forest Service General Technical Report NRS-6, Newtown Square, PAGoogle Scholar
  60. Tobin PC, Blackburn LM (2008) Long-distance dispersal of the gypsy moth (Lepidoptera: Lymantriidae) facilitated its initial invasion of Wisconsin. Environ Entomol 37:87–93CrossRefPubMedGoogle Scholar
  61. Tobin PC, Liebhold AM, Roberts EA (2007) Comparison of methods for estimating the spread of a non-indigenous species. J Biogeogr 34:305–312CrossRefGoogle Scholar
  62. Tobin PC, Klein KT, Leonard DS (2009) Gypsy moth (Lepidoptera: Lymantriidae) flight behavior and phenology based upon field-deployed automated pheromone-baited traps. Environ Entomol 38:1555–1562CrossRefPubMedGoogle Scholar
  63. Tobin PC, Bai BB, Eggen DA et al (2012) The ecology, geopolitics, and economics of managing Lymantria dispar in the United States. Int J Pest Manag 53:195–210CrossRefGoogle Scholar
  64. Tobin PC, Liebhold AM, Roberts EA et al (2015) Estimating spread rates of non-native species: the gypsy moth as a case study. In: Venette RC (ed) Pest risk modelling and mapping for invasive alien species. CABI, Boston, pp 131–144Google Scholar
  65. Uelmen JA, Lindroth RL, Tobin PC et al (2016) Effects of winter temperatures, spring degree-day accumulation, and insect population source on phenological synchrony between forest tent caterpillar and host trees. For Ecol Manag 362:241–250CrossRefGoogle Scholar
  66. U.S. Forest Service (2016) Forest inventory and analysis national program.
  67. van Asch M, Visser ME (2007) Phenology of forest caterpillars and their host trees: the importance of synchrony. Annu Rev Entomol 52:37–55CrossRefPubMedGoogle Scholar
  68. Weseloh RM (1985) Dispersal, survival, and population abundance of gypsy moth, Lymantria dispar (Lepidoptera: Lymantriidae), larvae determined by releases and mark-recapture studies. Ann Entomol Soc Am 78:728–735CrossRefGoogle Scholar
  69. Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666CrossRefGoogle Scholar
  70. Work TT, McCullough DG, Cavey JF et al (2005) Arrival rate of nonindigenous insect species into the United States through foreign trade. Biol Invasions 7:323–332CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Patrick C. Tobin
    • 1
  • Kimberly Thielen Cremers
    • 2
  • Lucia Hunt
    • 2
  • Dylan Parry
    • 3
  1. 1.School of Environmental and Forest SciencesUniversity of WashingtonSeattleUSA
  2. 2.Plant Protection DivisionMinnesota Department of AgricultureSt. PaulUSA
  3. 3.College of Environmental Science and ForestryState University of New YorkSyracuseUSA

Personalised recommendations