Biological Invasions

, Volume 15, Issue 12, pp 2667–2679 | Cite as

Changes in the regional abundance of hemlock associated with the invasion of hemlock woolly adelgid (Adelges tsugae Annand)

  • R. Talbot TrotterIIIEmail author
  • Randall S. Morin
  • Sonja N. Oswalt
  • Andrew Liebhold
Original Paper


Since its introduction, the non-native hemlock woolly adelgid (Adelges tsugae) has spread to infest hemlock (Tsuga spp.) in at least 18 states in the eastern USA. Previous studies have documented highly variable rates of hemlock mortality among infested stands making it difficult to estimate regional impacts. Here data from the US Forest Service Forest Inventory and Analysis program collected from 432 eastern U.S. counties reveals several surprising and conflicting regional patterns. First, median live and dead hemlock basal area has generally increased over the last two decades across the eastern U.S. This has generally been the case in both infested and uninfested counties. Second, the median percentage of hemlock which is alive has decreased over the past ~20 years, again in both infested and uninfested counties. Third, the ages of infestations are negatively correlated with the percentage of live hemlock, as might be expected given the known impact adelgids can have on a stand through time; however this relationship depends on the exclusion of uninfested counties, as counties infested >12 years and uninfested counties have similar percentages of live hemlock. Combined, these data suggest increasing tree density associated with the past century of reforestation and succession in the eastern U.S. may currently be overwhelming the negative impacts of the adelgid at the regional scale, however, the long-term stability of this situation is not known, and data from long-infested counties suggest the landscape may be at a “tipping point”.


Invasive species Forest insects Forest Inventory and Analysis Succession 



We thank Timothy Gregoire and Jonathan Reuning-Scherer for statistical recommendations. We thank Nathan Havill, Mike Montgomery, and two anonymous reviewers for critical reviews of the manuscript. This work was supported by the USDA Forest Service, Northern and Southern Research Stations.


  1. Davidson CB, Gottschalk KW, Johnson JE (1999) Tree mortality following defoliation by the European gypsy moth (Lymantria dispar L.) in the United States: a review. For Sci 45:74–84Google Scholar
  2. Eschtruth AK, Cleavitt NL, Battles JJ, Evans RA, Fahey TJ (2006) Vegetation dynamics in declining eastern hemlock stands: 9 years of forest response to hemlock woolly adelgid infestation. Can J For Res 36:1435–1450CrossRefGoogle Scholar
  3. Evans AM, Gregoire TG (2007) A geographically variable model of hemlock woolly adelgid spread. Biol Invasions 9:369–382CrossRefGoogle Scholar
  4. Foster DR (1992) Land-use history (1730–1990) and vegetation dynamics in central New England, USA. J Ecol 80:19Google Scholar
  5. Gansner DA, Herrick OW (1987) Impact of gypsy moth on the timber resource. In: Fosbroke S, Hicks RR Jr (eds) Coping with the gypsy moth in the new frontier. West Virginia University Books, Morgantown, WVGoogle Scholar
  6. Garnas JR, Ayres MP, Liebhold AM, Evans C (2011) Subcontinental impacts of an invasive tree disease on forest structure and dynamics. J Ecol 99:532–541Google Scholar
  7. Gouger RJ (1971) Control of Adelges tsugae on hemlock in Pennsylvania. Sci Tree Topics 3:9Google Scholar
  8. Havill NP, Foottit RG (2007) Biology and evolution of Adelgidae. Annu Rev Entomol 52:325–349Google Scholar
  9. Havill NP, Montgomery ME, 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
  10. Holmes TP, Aukema JE, Von Holle B, Liebhold A, Sills E (2009) Economic impacts of invasive species in forests: Past, present, and future. Ann NY Acad Sci 1162:18–38PubMedCrossRefGoogle Scholar
  11. Ingwell LL, Preisser EL (2011) Using citizen science programs to identify host resistance in pest-invaded forests. Conserv Biol 25:182–188PubMedCrossRefGoogle Scholar
  12. Inouye M (1953) Monographische Studie uber die japanischen Koniferen-Gallenlause (Adelgidae). Bull Sapporo Branch Gov For Exp Stn 15:1–91Google Scholar
  13. Keever C (1953) Present composition of some stands of the former oak-chestnut forest in the southern Blue Ridge Mountains. Ecology 34:44–54CrossRefGoogle Scholar
  14. Kohler GR, Stiefel VL, Wallin KF, Ross DW (2008) Predators associated with the hemlock woolly adelgid (Hemiptera: Adelgidae) in the Pacific Northwest. Environ Entomol 37:494–504PubMedCrossRefGoogle Scholar
  15. Krapfl KJ, Holzmueller EJ, Jenkins MA (2011) Early impacts of hemlock woolly adelgid in Tsuga canadensis forest communities of the southern Appalachian Mountains. J Torrey Bot Soc 138:93–106CrossRefGoogle Scholar
  16. Kuhlman HM (1971) Effects of insect defoliation on growth and mortality of trees. Annu Rev Entomol 16:289–324CrossRefGoogle Scholar
  17. Liebhold AM, Macdonald WL, Bergdahl D, Mastro VC (1995) Invasion by exotic forest pests: a threat to forest ecosystems. For Sci Monogr 30:1–54Google Scholar
  18. Loo JA (2009) Ecological impacts of non-indigenous invasive fungi as forest pathogens. Biol Invasions 11:81–96CrossRefGoogle Scholar
  19. McCormick JF, Platt RB (1980) Recovery of an Appalachian forest following the chestnut blight. Am Midl Nat 104:264–273CrossRefGoogle Scholar
  20. Montgomery ME, Lyon SM (1996) Natural enemies of adelgids in North America: their prospect for biological control of Adelges tsugae (Homoptera: Adelgidae). In: Salom SM, Tigner TC, Reardon RC (eds) First hemlock woolly adelgid review. United States Department of Agriculture, Forest Health Technology Enterprise Team, Charlottesville, VAGoogle Scholar
  21. Morin RS, Liebhold AM, Tobin PC, Gottschalk KW, Luzander E (2007) Spread of beech bark disease in the Eastern United States and its relationship to regional forest composition. Can J For Res 37:726–736CrossRefGoogle Scholar
  22. Morin RS, Liebhold AM, Gottschalk KW (2009) Anisotropic spread of hemlock woolly adelgid in the eastern United States. Biol Invasions 11:2341–2350CrossRefGoogle Scholar
  23. Morin RS, Oswalt SN, Trotter III RT, Liebhold AW (2011) Status of hemlock in the Eastern United States forest inventory and analysis factsheet. In: U.S. Department of Agriculture FS, Southern Research Station (ed), Asheville, NCGoogle Scholar
  24. Orwig DA, Foster DR (1998) Forest response to the introduced hemlock woolly adelgid in southern New England, USA. J Torrey Bot Soc 125:60–73CrossRefGoogle Scholar
  25. Orwig DA and Foster DR (2000) Stand, landscape, and ecosystem analysis of hemlock woolly adelgid outbreaks in southern New England: an overview. In: McManus KA, Shields KS and Souto DR (eds) Symposium on sustainable management of hemlock ecosystems in Eastern North America, pp 123–125Google Scholar
  26. 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
  27. 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
  28. Parker BL, Skinner M, Gouli S, Ashikaga T, Teillon HB (1998) Survival of hemlock woolly adelgid (Homoptera: Adelgidae) at low temperatures. Forest Science 44:414–420Google Scholar
  29. Parker BL, Skinner M, Gouli S, Ashikaga T, Teillon HB (1999) Low lethal temperature for hemlock woolly adelgid (Homoptera: Adelgidae). Environ Entomol 28:1085–1091Google Scholar
  30. Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65CrossRefGoogle Scholar
  31. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288CrossRefGoogle Scholar
  32. Preisser EL, Lodge AG, Orwig DA, Elkinton JS (2008) Range expansion and population dynamics of co-occurring invasive herbivores. Biol Invasions 10:201–213CrossRefGoogle Scholar
  33. Preisser EL, Miller-Pierce MR, Vansant J, Orwig DA (2011) Eastern hemlock (Tsuga canadensis) regeneration in the presence of hemlock woolly adelgid (Adelges tsugae) and elongate hemlock scale (Fiorinia externa). Can J For Res 41:2433–2439CrossRefGoogle Scholar
  34. Remington RD, Schork MA (1985) Statistics with applications to the biological and health sciences. Prentice-Hall Inc, Englewood Cliffs 415 ppGoogle Scholar
  35. 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
  36. 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
  37. Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478Google Scholar
  38. 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
  39. Woudenberg SW, Conkling BL, O’Connel BM, LaPoint EB, Turner JA and Waddell KL (2010) The Forest Inventory and Analysis Database: database description and users manual version 4.0 for phase 2. In: U.S. Department of Agriculture FS, Rocky Mountain Research Station (ed), Fort Collins, COGoogle Scholar

Copyright information

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

Authors and Affiliations

  • R. Talbot TrotterIII
    • 1
    Email author
  • Randall S. Morin
    • 2
  • Sonja N. Oswalt
    • 3
  • Andrew Liebhold
    • 4
  1. 1.Northern Research StationUSDA Forest ServiceHamdenUSA
  2. 2.Northern Research Station Forest Inventory and AnalysisUSDA Forest ServiceNewtown SquareUSA
  3. 3.Southern Research Station Forest Inventory and AnalysisUSDA Forest ServiceKnoxvilleUSA
  4. 4.Northern Research StationUSDA Forest ServiceMorgantownUSA

Personalised recommendations