Biological Invasions

, Volume 15, Issue 9, pp 1925–1932 | Cite as

When one is not necessarily a lonely number: initial colonization dynamics of Adelges tsugae on eastern hemlock, Tsuga canadensis

  • Patrick C. Tobin
  • Richard M. Turcotte
  • Daniel A. Snider
Original Paper


The ability to establish successfully in a new area can vary considerably among species. In addition to the well-recognized importance of propagule pressure in driving the rates of establishment of biological invaders, the life history strategy of a species can also affect establishment success, such as in the extent to which Allee effects (positive density-dependence), and environmental and demographic stochasticity manifest themselves. We quantified the establishment success of Adelges tsugae, a non-native insect currently invading North American hemlock. We inoculated eastern hemlock host trees with varying densities of this parthenogenetic insect, from 1 to >500 progrediens ovisacs. The number of settled sistens (the subsequent generation) was positively related to the initial density. More interesting, however, was that we recorded successful establishment from released progrediens ovisacs, and the subsequent initiation of the next generation (sistens), in ≈39 % of host trees inoculated with 1 ovisac. The observation that successful establishment can be accomplished by a single ovisac produced by a single individual has important implications in the invasion dynamics and management of A. tsugae.


Biological invasions Establishment Hemlock woolly adelgid Invasion dynamics 



We would like to thank Laura Blackburn, Terry Burhans, Will Harris, John Juracko, Gino Luzader, Dani Martin, Adam Miller, George Racin, Brian Simpson, Elliott Tobin, and Lindsay Wolf for valuable field and laboratory assistance. We thank John and Judy Stewart for the use of their farm. We are also very grateful to Joe Elkinton (University of Massachusetts) and Mike Montgomery (USDA Forest Service, Northern Research Station, retired) who provided helpful advice during the initial planning stages of this study. Nathan Havill and Sandy Liebhold (USDA Forest Service, Northern Research Station) provided helpful comments on an earlier draft.


  1. Allee WC (1938) The social life of animals. W.W. Norton and Company, Inc., New York, NYCrossRefGoogle 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. Butin E, Preisser E, Elkinton J (2007) Factors affecting settlement rate of the hemlock woolly adelgid, Adelges tsugae, on eastern hemlock, Tsuga canadensis. Agric For Entomol 9:215–219CrossRefGoogle Scholar
  4. Courchamp F, Clutton-Brock T, Grenfell B (1999) Inverse density dependence and the Allee effect. Trends Ecol Evol 14:405–410PubMedCrossRefGoogle Scholar
  5. Courchamp F, Berec L, Gascoigne J (2008) Allee effects in ecology and conservation. Oxford University Press, OxfordCrossRefGoogle Scholar
  6. Drake JA, Lodge DM (2006) Allee effects, propagule pressure and the probability of establishment: risk analysis for biological invasions. Biol Invasions 8:365–375CrossRefGoogle Scholar
  7. Evans AM, Gregoire TG (2007) A geographically variable model of hemlock woolly adelgid spread. Biol Invasions 9:369–382CrossRefGoogle Scholar
  8. Gascoigne JC, Lipcius RN (2004) Allee effects driven by predation. J Appl Ecol 41:801–810CrossRefGoogle Scholar
  9. Gascoigne J, Berec L, Gregory S, Courchamp F (2009) Dangerously few liaisons: a review of mate-finding Allee effects. Popul Ecol 51:355–372CrossRefGoogle Scholar
  10. Gómez S, Orians CM, Preisser EL (2012) Exotic herbivores on a shared native host: tissue quality after individual, simultaneous, and sequential attack. Oecologia 169:1015–1024PubMedCrossRefGoogle Scholar
  11. Gouger RJ (1971) Control of Adelges tsugae on hemlock in Pennsylvania. Scientific Tree Topics 3:1–9Google Scholar
  12. Hastings A, Cuddington K, Davies KF, Dugaw CJ, Elmendorf S, Freestone A, Harrison S, Holland M, Lambrinos J, Malvadkar U, Melbourne B, Moore K, Taylor C, Thompson D (2005) The spatial spread of invasions: new developments in theory and evidence. Ecol Lett 8:91–101CrossRefGoogle Scholar
  13. Havill NP, Foottit RG (2007) Biology and evolution of Adelgidae. Annu Rev Entomol 52:325–349PubMedCrossRefGoogle Scholar
  14. Havill N, Montgomery M, Yu G, Shiyake S, Caccone A (2006) Mitochondrial DNA from hemlock woolly adelgid (Hemiptera: Adelgidae) suggests cryptic speciation and pinpoints the source of the introduction to eastern North America. Ann Entomol Soc Am 99:195–203CrossRefGoogle Scholar
  15. Havill N, Montgomery M, Keena M (2011) Hemlock woolly adelgid and its hemlock hosts: a global perspective. In: Onken B and Reardon R (eds) Implementation and status of biological control of the hemlock woolly adelgid. U.S. Forest Service, Publication FHTET-2011-04, Morgantown, WV, pp. 3–14Google Scholar
  16. Hengeveld R (1989) Dynamics of biological invasions. Chapman and Hall, LondonGoogle Scholar
  17. Hopper KR, Roush RT (1993) Mate finding, dispersal, number released, and the success of biological control introductions. Ecol Entomol 18:321–331CrossRefGoogle Scholar
  18. Johnson DM, Liebhold AM, Tobin PC, Bjørnstad ON (2006) Allee effects and pulsed invasion of the gypsy moth. Nature 444:361–363PubMedCrossRefGoogle Scholar
  19. Lagalante A, Lewis N, Montgomery M, Shields K (2006) Temporal and spatial variation of terpenoids in eastern hemlock (Tsuga canadensis) in relation to feeding by Adelges tsugae. J Chem Ecol 32:2389–2403PubMedCrossRefGoogle Scholar
  20. Lande R (1993) Risks of population extinction from demographic and environmental stochasticity and random catastrophes. Am Nat 142:911–927CrossRefGoogle Scholar
  21. Lande R (1998) Demographic stochasticity and Allee effect on a scale with isotropic noise. Oikos 83:353–358CrossRefGoogle Scholar
  22. Leung B, Drake JM, Lodge DM (2004) Predicting invasions: propagule pressure and the gravity of Allee effects. Ecology 85:1651–1660CrossRefGoogle Scholar
  23. Liebhold AM, Bascompte J (2003) The Allee effect, stochastic dynamics and the eradication of alien species. Ecol Lett 6:133–140CrossRefGoogle Scholar
  24. Liebhold AM, Tobin PC (2008) Population ecology of insect invasions and their management. Annu Rev Entomol 53:387–408PubMedCrossRefGoogle Scholar
  25. Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228PubMedCrossRefGoogle Scholar
  26. Lockwood JL, Hoopes M, Marchetti M (2007) Invasion ecology. Blackwell Publishing Ltd., Malden, MAGoogle Scholar
  27. Ludsin SA, Wolfe AD (2001) Biological invasion theory: Darwin’s contributions from The Origin of Species. Bioscience 51:780–789CrossRefGoogle Scholar
  28. McClure MS (1989) Evidence of a polymorphic life cycle in the hemlock woolly adelgid, Adelges tsugae (Homoptera: Adelgidae). Ann Entomol Soc Am 82:50–54Google Scholar
  29. McClure MS (1990) Role of wind, birds, deer, and humans in the dispersal of hemlock woolly adelgid (Homoptera: Adelgidae). Environ Entomol 19:36–43Google Scholar
  30. McClure MS (1991) Density dependent feedback and population cycles in Adelges tsugae (Homoptera: Adelgidae) on Tsuga canadensis. Environ Entomol 20:258–264Google Scholar
  31. McClure MS (1992) Hemlock woolly adelgid. Am Nurseryman 175:82–89Google Scholar
  32. McClure MS, Cheah AS-J (1999) Reshaping the ecology of invading populations of the hemlock woolly adelgid, Adelges tsugae (Homoptera: Adelgidae), in eastern North America. Biol Invasions 1:247–254CrossRefGoogle Scholar
  33. Miles PW (1990) Aphid salivary secretions and their involvement in plant toxicases. In: Cambell RK, Eikenbary RD (eds) Aphid–plant–genotype interactions. Elsevier, New York, pp 131–147Google Scholar
  34. Morin RS, Liebhold AM, Luzader ER, Lister AJ, Gottschalk KW, Twardus DB (2005) Mapping host-species abundance of three major exotic forest pests. Research Paper NE-726, USDA Forest Service, Newtown Square, PAGoogle Scholar
  35. Neter J, Wasserman W, Kutner MH (1990) Applied linear statistical models, 3rd edn. Irwin, Inc., Burr Ridge, ILGoogle Scholar
  36. Onken B, Reardon R (2011) Implementation and status of biological control of the hemlock woolly adelgid. U.S. Forest Service, Publication FHTET-2011-04, Morgantown, WVGoogle Scholar
  37. Orwig DA, Foster DR, Mausel DL (2002) Landscape patterns of hemlock decline in New England due to the introduced hemlock woolly adelgid. J Biogeogr 29:1475–1487CrossRefGoogle Scholar
  38. Paradis A (2011) Population dynamics of hemlock woolly adelgid (Adelges tsugae) in New England. University of Massachusetts, Amherst, MA, p 114Google Scholar
  39. Paradis A, Elkinton J, Hayhoe K, Buonaccorsi J (2008) Role of winter temperature and climate change on the survival and future range expansion of the hemlock woolly adelgid (Adelges tsugae) in eastern North America. Mitig Adapt Strat Glob Change 13:541–554CrossRefGoogle Scholar
  40. Raffa KF, Berryman AA (1983) The role of host plant resistance in the colonization behaviour and ecology of bark beetles. Ecol Monogr 53:27–49CrossRefGoogle Scholar
  41. R Development Core Team (2012) The R project for statistical computing
  42. Shigesada N, Kawasaki K (1997) Biological invasions: theory and practice. Oxford University Press, New York, NYGoogle Scholar
  43. Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Evol Syst 40:81–102CrossRefGoogle Scholar
  44. Simberloff D, Gibbons L (2004) Now you see them, now you don’t! Population crashes of established introduced species. Biol Invasions 6:161–172CrossRefGoogle Scholar
  45. Skinner M, Parker BL, Gouli S, Ashikaga T (2003) Regional responses of hemlock woolly adelgid (Homoptera: Adelgidae) to low temperatures. Environ Entomol 32:523–528CrossRefGoogle Scholar
  46. Stadler B, Müller T, Orwig D, Cobb R (2005) Hemlock woolly adelgid in New England forests: canopy impacts transforming ecosystem processes and landscapes. Ecosystems 8:233–247CrossRefGoogle Scholar
  47. Stephens PA, Sutherland WJ, Freckleton RP (1999) What is the Allee effect? Oikos 87:185–190CrossRefGoogle Scholar
  48. Suarez AV, Holway DA, Case TJ (2001) Patterns of spread in biological invasions dominated by long-distance jump dispersal: insights from Argentine ants. Proc Natl Acad Sci USA 98:1095–1100PubMedCrossRefGoogle Scholar
  49. Tobin PC, Whitmire SL, Johnson DM, Bjørnstad ON, Liebhold AM (2007) Invasion speed is affected by geographic variation in the strength of Allee effects. Ecol Lett 10:36–43PubMedCrossRefGoogle Scholar
  50. Tobin PC, Berec L, Liebhold AM (2011) Exploiting Allee effects for managing biological invasions. Ecol Lett 14:615–624PubMedCrossRefGoogle Scholar
  51. Trotter RT III, Shields KS (2009) Variation in winter survival of the invasive hemlock woolly adelgid (Hemiptera: Adelgidae) across the eastern United States. Environ Entomol 38:577–587PubMedCrossRefGoogle Scholar
  52. Wallace MS, Hain FP (2000) Field surveys and evaluation of native and established predators of the hemlock woolly adelgid (Homoptera: Adelgidae) in the Southeastern United States. Environ Entomol 29:638–644CrossRefGoogle Scholar
  53. Wellborn G, Capps E (2012) Establishment of a new population by a single gravid colonist: implications for Hyalella biogeography and speciation. Evol Ecol. doi: 10.1007/s10682-012-9579-x (in press)
  54. Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666CrossRefGoogle Scholar
  55. Young RF, Shields KS, Berlyn GP (1995) Hemlock woolly adelgid (Homoptera: Adelgidae): stylet bundle insertion and feeding sites. Ann Entomol Soc Am 88:827–835Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht (outside the USA) 2013

Authors and Affiliations

  • Patrick C. Tobin
    • 1
  • Richard M. Turcotte
    • 2
  • Daniel A. Snider
    • 2
  1. 1.Forest Service, United States Department of Agriculture, Northern Research StationMorgantownUSA
  2. 2.Forest Service, United States Department of Agriculture, State and Private Forestry, Northeastern AreaMorgantownUSA

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