Biological Invasions

, Volume 12, Issue 2, pp 389–405 | Cite as

Direct and indirect effects of alien insect herbivores on ecological processes and interactions in forests of eastern North America

  • Kamal J. K. Gandhi
  • Daniel A. HermsEmail author
Original Paper


Alien invasive insects such as gypsy moth, hemlock woolly adelgid, and emerald ash borer continue to disturb the mixed deciduous and hemlock forests of eastern North America by causing wide-scale defoliation, decline and/or mortality of their hosts. Some of the most devastating species are spreading in “defense free space”, causing extensive mortality of hosts that are inherently susceptible, perhaps due to their lack of coevolutionary history with the invader. These disturbances have altered the dynamics of canopy gaps, coarse woody debris, biogeochemical cycling, and ecological interactions among organisms in terrestrial and aquatic systems, with consequent effects on forest composition, structure, and function. Populations of indigenous species specialized to particular habitats and/or host trees are most likely to decrease, while some generalist and opportunistic species may increase in invaded forests, including exotic plants as their facilitation by alien insects sparks an “invasional meltdown”. Although poorly documented, alien insects may induce positive feedback effects on ecological processes and interactions. For example, effects of herbivory on foliar chemistry may indirectly alter tri-trophic interactions of indigenous herbivores on their shared hosts, slow rates of terrestrial nutrient cycling, and decrease productivity of aquatic habitats based on allochthonous inputs. Tactics used to eradicate or suppress alien insects in forests such as insecticide applications, biological control, and silvicultural prescriptions can also have ecological impacts. As alien insects continue to establish and spread in forests of eastern North America, their already pervasive effects on ecological interactions and ecosystem processes will continue to magnify.


Invasive species Invasional meltdown Defense free space Disturbance Nutrient cycling Gap ecology Forest succession Nontarget effects 



We thank Catherine P. Herms (The Ohio State University) and two anonymous reviewers for their helpful comments on earlier drafts of this manuscript, and Lee A. Odgen (The University of Georgia) for formatting the manuscript. Financial support was provided by the USDA Forest Service, Northern Research Station, Morgantown, West Virginia, and Delaware, Ohio, and by state and federal funds appropriated to the Daniel B. Warnell School of Forestry and Natural Resources, The University of Georgia, Athens, and to the Ohio Agricultural Research and Development Center, The Ohio State University, Wooster.


  1. Barber NA, Marquis RJ, Tori WP (2008) Invasive prey impacts the abundance and distribution of native predators. Ecology 89:2678–2683PubMedGoogle Scholar
  2. Barnes BV (1976) Succession in deciduous swamp communities of southern Michigan formerly dominated by American elm. Can J Bot 54:19–24Google Scholar
  3. Becker DA, Brittingham MC, Goguen CB (2008) Effects of hemlock woolly adelgid on breeding birds at Fort Indiantown Gap, Pennsylvania. Northeast Nat 15:227–240Google Scholar
  4. Bell JL, Whitmore RC (2000) Bird nesting ecology in a forest defoliated by gypsy moths. Wilson Bull 112:524–531Google Scholar
  5. Boettner GH, Elkinton JS, Boettner CJ (2000) Effects of a biological control introduction on three nontarget native species of saturniid moths. Conserv Biol 14:1798–1806Google Scholar
  6. Brooks RT (2001) Effects of the removal of overstory hemlock from hemlock-dominated forests on eastern redback salamanders. For Ecol Manage 2001:197–204Google Scholar
  7. Bryant JP, Reichardt JB, Clausen TP, Werner RA (1993) Effects of mineral nutrition on delayed inducible resistance in Alaska paper birch. Ecology 74:2072–2084Google Scholar
  8. Butler L, Chrislip GA, Kondo VA, Townsend EC (1997) Effect of diflubenzuron on nontarget canopy arthropods in closed, deciduous watersheds in a central Appalachian forest. J Econ Entomol 90:784–794Google Scholar
  9. Campbell RW, Sloan RJ (1977) Forest stand responses to defoliation by the gypsy moth. For Sci Monogr 19:1–34Google Scholar
  10. Canham CD, Denslow JS, Platt WJ, Runkle JR, Spies TA, White PS (1990) Light regimes beneath closed canopies and tree-fall gaps in temperate and tropical forests. Can J For Res 20:620–631Google Scholar
  11. Canham CD, Papaik MJ, Latty EF (2001) Interspecific variation in susceptibility to windthrow as a function of tree size and storm severity for northern temperate tree species. Can J For Res 31:1–10Google Scholar
  12. Cappaert D, McCullough DG, Poland TM, Siegert NW (2005) Emerald ash borer in North America: a research and regulatory challenge. Am Entomol 51:152–165Google Scholar
  13. Chornesky EA, Bartuska AM, Aplet GH, Britton KO, Cummings-Carlson J, Davis FW, Eskow J, Gordon DR, Gottschalk KW, Haack RA, Hansen AJ, Mack RN, Rahel FJ, Shannon MA, Wainger LA, Wigley TB (2005) Science priorities for reducing the threat of invasive species to sustainable forestry. Bioscience 55:335–348Google Scholar
  14. Choudhury D (1988) Herbivore induced changes in leaf-litter resource quality: a neglected aspect of herbivory in ecosystem nutrient dynamics. Oikos 51:389–393Google Scholar
  15. Christenson LM, Lovett GM, Mitchell MJ, Groffman PM (2002) The fate of nitrogen in gypsy moth frass deposited to an oak forest floor. Oecologia 131:444–452Google Scholar
  16. Ciesla WM (2003) European woodwasp: a potential threat to North America’s conifer forests. J For 101:18–23Google Scholar
  17. Cleavitt NL, Eschtruth AK, Battles JJ, Fahey TJ (2008) Bryophyte response to eastern hemlock decline caused by hemlock woolly adelgid infestation. J Torr Bot Soc 135:12–25Google Scholar
  18. Cobb RC, Orwig DA (2002) Impacts of hemlock woolly adelgid infestation on decomposition: an overview. In: Onken B, Reardon R (eds) Third symposium on hemlock woolly adelgid in the eastern United States. Asheville, NC. FHTET-2005-01, pp 317–323Google Scholar
  19. Cooper RJ, Dodge KM, Martinat PJ, Donahoe SB, Whitmore RC (1990) Effect of diflubenzuron application on eastern deciduous forest birds. J Wildl Manage 54:486–493Google Scholar
  20. Dale VH, Lannom KO, Tharp ML, Hodges DG, Fogel J (2009) Effects of climate change, land-use change, and invasive species on the ecology of the Cumberland forests. Can J For Res 39:467–480Google Scholar
  21. 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
  22. DeSelm HR, Boner RR (1984) Understory changes in spruce-fir during the first 16–20 years following the death of fir. In: White PS (ed) The southern Appalachian spruce-fir ecosystem: its biology and threats. USDA National Park Service, Atlanta, GA, pp 51–69Google Scholar
  23. Dunbar DM, Stephens GR (1975) Association of twolined chestnut borer and shoestring fungus with mortality of defoliated oak in Connecticut. For Sci 21:169–174Google Scholar
  24. Eisler R (1992) Diflubenzuron hazards to fish, wildlife, and invertebrates: a synoptic review. U.S. Department of Interior Fish and Wildlife Service, Contaminant Hazard Reviews 25, Biological Report 4Google Scholar
  25. Elkinton JS, Liebhold AM (1990) Population dynamics of gypsy moth in North America. Annu Rev Entomol 35:571–596Google Scholar
  26. Ellison AM, Bank MS, Clinton BD, Colburn EA, Elliott K, Ford CR, Foster DR, Kloeppel BD, Knoepp JD, Lovett GM, Mohan J, Orwig DA, Rodenhouse NL, Sobczak WV, Stinson KA, Stone JK, Swan CM, Thompson J, Von Holle B, Webster JR (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol 3:479–486Google Scholar
  27. Eschtruth AK, Battles JJ (2009) Assessing the relative importance of disturbance, herbivory, diversity, and propagule pressure in exotic plant invasions. Ecol Monogr 79:265–280Google Scholar
  28. 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 36:1435–1450Google Scholar
  29. Fajvan MA, Wood JM (1996) Stand structure and development after gypsy moth defoliation in the Appalachian plateau. For Ecol Manage 89:79–88Google Scholar
  30. Findlay S, Carreiro M, Krischik V, Jones CG (1996) Effects of damage to living plants on leaf litter quality. Ecol Appl 6:269–275Google Scholar
  31. Ford CR, Vose JM (2007) Tsuga canadensis (L.) Carr. mortality will impact hydrologic processes in southern Appalachian forest ecosystems. Ecol Appl 17:1156–1167PubMedGoogle Scholar
  32. Gandhi KJK, Gilmore DW, Katovich SA, Mattson WJ, Spence JR, Seybold SJ (2007) Physical effects of weather disturbances on the abundance and diversity of forest insects in North American forests. Environ Rev 15:113–152Google Scholar
  33. Gandhi KJK, Smith A, Long RA, Taylor RAJ, Herms DA (2008) Three-year progression of emerald ash borer induced ash decline and mortality in the forests of southeastern Michigan. In: Mastro V, Lance D, Reardon R, Parra G (eds) Proceedings of the emerald ash borer and Asian longhorned beetle research and technology development meeting, Pittsburgh, Pennsylvania, 23–24 Oct 2007. USDA Forest Health Technology Enterprise Team, FHTET-2008-07, p 27Google Scholar
  34. Gilliam FS (2007) The ecological significance of the herbaceous layer in temperate forest ecosystems. Bioscience 57:845–858Google Scholar
  35. Glasgow LS, Matlack GR (2007) The effects of prescribed burning and canopy openness on establishment of two non-native plant species in a deciduous forest, southeast Ohio, USA. For Ecol Manage 238:31–329Google Scholar
  36. Gómez-Aparicio L, Canham CD (2008) Neighborhood models of the effects of invasive tree species on ecosystem processes. Ecol Monogr 78:69–86Google Scholar
  37. Grace JR (1986) The influence of gypsy moth on the composition and nutrient content of litter fall in a Pennsylvania oak forest. For Sci 32:855–870Google Scholar
  38. Grady AE, Scanlon TM, Galloway JN (2007) Declines in dissolved silica concentrations in western Virginia streams (1988–2003): gypsy moth defoliation stimulates diatoms? J Geophys Res 112:1–11Google Scholar
  39. Griffith MB, Barrows EM, Perry SA (2000) Effect of diflubenzuron on flight of adult aquatic insects (Plecoptera, Trichoptera) following emergence during the second year after aerial application. J Econ Entomol 93:1695–1700PubMedGoogle Scholar
  40. Haack RA (2006) Exotic bark- and wood-boring Coleoptera in the United States: recent establishments and interceptions. Can J For Res 36:269–288Google Scholar
  41. Hammons DL, Kurtural SK, Newman MC, Potter DA (2009) Invasive Japanese beetles facilitate aggregation and injury by a native scarab pest of ripening fruits. Proc Nat Acad Sci USA 106:3686–3691PubMedGoogle Scholar
  42. Hanula JL, Berisford CW (1984) Seasonal flight activity of the smaller European elm bark beetle, Scolytus multistriatus (Coleoptera: Scolytidae), and associates in Georgia. Can Entomol 116:1251–1258Google Scholar
  43. Hanula JL, Mayfield AE, Fraedrich SW, Rabaglia RJ (2008) Biology and host associations of redbay ambrosia beetle (Coleoptera: Curculionidae: Scolytinae), exotic vector of laurel wilt killing redbay trees in the southeastern United States. J Econ Entomol 101:1276–1286PubMedGoogle Scholar
  44. Harmon ME, Franklin JF, Swanson FJ, Sollins P, Gregory SV, Lattin JD, Anderson NH, Cline SP, Aumen NG, Sedell JR, Lienkaemper GW, Cromack K Jr, Cummins KW (1986) Ecology of coarse woody debris in temperate ecosystems. Adv Ecol Res 15:133–302Google Scholar
  45. Hättenschwiler S, Vitousek PM (2000) The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol Evol 15:238–243PubMedGoogle Scholar
  46. Haugen DA, Hoebeke ER (2005) Sirex woodwasp—Sirex noctilio F. (Hymenoptera: Siricidae). USDA-Forest Service, Pest Alert NA-PR-07-05Google Scholar
  47. Haukioja E (1990) Induction of defenses in trees. Annu Rev Entomol 36:25–42Google Scholar
  48. Hausman CE, Rocha OJ, Jaeger JF (2008) How emerald ash borer facilitates a secondary spread of invasive plant species: impacts of emerald ash borer eradication and tree mortality. In: Mastro V, Lance D, Reardon R, Parra G (eds) Proceedings of the emerald ash borer and Asian longhorned beetle research and technology development meeting, Pittsburgh, Pennsylvania, Oct 23–24 2007. USDA Forest Health Technology Enterprise Team, FHTET-2008-07, pp 14–15Google Scholar
  49. 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 99:195–203Google Scholar
  50. Hawkins BA, Marino PC (1997) The colonization of native phytophagous insects in North America by exotic parasitoids. Oecologia 112:566–571Google Scholar
  51. Herms DA (2003) Assessing management options for gypsy moth. Pestic Outlook 14:14–18Google Scholar
  52. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Quart Rev Biol 67:283–335Google Scholar
  53. Herms DA, Stone AK, Chatfield JA (2004) Emerald ash borer: the beginning of the end of ash in North America? In: Chatfield JA, Draper EA, Mathers HM, Dyke DE, Bennett PJ, Boggs JF (eds) Ornamental plants: annual reports and research reviews 2003, OARDC/OSU Extension Special Circular 193, pp 62–71Google Scholar
  54. Herms DA, Gandhi KJK, Cardina J, Long RP, Knight KS, Smith A, McCullough DG (2008) Impacts of emerald ash borer-induced gap formation on forest communities. In: Mastro V, Lance D, Reardon R, Parra G (eds) Proceedings of the emerald ash borer and Asian longhorned beetle research and technology development meeting, Pittsburgh, Pennsylvania, 23–24 Oct 2007, p 10Google Scholar
  55. Hollingsworth RG, Hain FP (1991) Balsam woolly adelgid (Homoptera: Adelgidae) and spruce-fir decline in the southern Appalachians: assessing pest relevance in a damaged ecosystem. Fla Entomol 74:179–187Google Scholar
  56. Horner JD, Gosz JR, Cates RG (1988) The role of carbon-based plant secondary metabolites in decomposition in terrestrial ecosystems. Am Nat 132:869–883Google Scholar
  57. Horvitz CC, Pascarella JB, McMann S, Freedman A, Hofstetter RH (1998) Functional roles of invasive non-indigenous plants in hurricane-affected subtropical hardwood forests. Ecol Appl 8:947–974Google Scholar
  58. Houston DR (1975) Beech bark disease: the aftermath forests are structured for a new outbreak. J For 73:660–663Google Scholar
  59. Houston DR (1987) Forest tree declines of past and present: current understanding. Can J Plant Pathol 9:349–360Google Scholar
  60. Houston DR (1994) Major new tree disease epidemics: beech bark disease. Annu Rev Phytopathol 32:75–87Google Scholar
  61. Hunter JC, Mattice JA (2002) The spread of woody exotics into the forests of a northeastern landscape, 1938–1999. J Torr Bot Soc 129:220–227Google Scholar
  62. Hutchens JJ Jr, Benfield EF (2000) Effects of forest defoliation by the gypsy moth on detritus processing in southern Appalachian streams. Am Midl Nat 143:397–404Google Scholar
  63. Irons JG III, Bryant JP, Oswood MW (1991) Effects of moose browsing on decomposition rates of birch leaf litter in a subarctic stream. Can J Fish Aquat Sci 48:442–444Google Scholar
  64. Jedlicka J, Vandermeer J, Aviles-Vazquez K, Barros O, Perfecto I (2004) Gypsy moth defoliation of oak trees and a positive response of red maple and black cherry: an example of indirect interaction. Am Midl Nat 152:231–236Google Scholar
  65. Jenkins JC, Aber JD, Canham CD (1999) Hemlock woolly adelgid impacts on community structure and N cycling rates in eastern hemlock forests. Can J For Res 29:630–645Google Scholar
  66. Johnson KS, Scriber JM, Nitao JK, Smitley DR (1995) Toxicity of Bacillus thuringiensis var. kurstaki to three nontarget Lepidoptera in field studies. Environ Entomol 24:288–297Google Scholar
  67. Jones CG, Ostfeld RS, Richard MP, Schauber EM, Wolff JO (1998) Chain reactions linking acorns to gypsy moth outbreaks and Lyme disease risk. Science 279:1023–1026PubMedGoogle Scholar
  68. Karnosky DF (1979) Dutch elm disease: a review of the history, environmental implications, control, and research needs. Environ Conserv 6:311–322Google Scholar
  69. Kasbohm JW, Vaughan MR, Kraus JG (1996) Effects of gypsy moth infestation on black bear reproduction and survival. J Wildl Manage 60:408–416Google Scholar
  70. Kellogg SK, Fink LS, Brower LP (2003) Parasitism of native luna moths, Actias luna (L.) (Lepidoptera: Saturniidae) by the introduced Compsilura concinnata (Meigen) (Diptera: Tachnidae) in central Virginia, their hyperparasitism by trigonalid wasp (Hymenoptera: Trigonalidae). Environ Entomol 32:1019–1027Google Scholar
  71. Kenis M, Auger-Rozenberg M, Roques A, Timms L, Péré C, Cock MJW, Settele J, Augustin S, Lopez-Caamonde C (2009) Ecological effects of invasive alien insects. Biol Invasions 11:21–45Google Scholar
  72. Kizlinski ML, Orwig DA, Cobb RC, Foster DR (2002) Direct and indirect ecosystem consequences of an invasive pest on forests dominated by eastern hemlock. J Biogeogr 29:1489–1503Google Scholar
  73. Knapp LB, Canham CD (2000) Invasion of old-growth forests by Ailanthus altissima: sapling growth and recruitment in canopy gaps. J Torr Bot Soc 127:307–315Google Scholar
  74. Koh LP, Dunn RR, Sodhi NS, Colwell RK, Proctor HC, Smith VS (2004) Species coextinctions and the biodiversity crisis. Science 305:1632–1634PubMedGoogle Scholar
  75. Krasny ME, DiGregorio LM (2001) Gap dynamics in Allegheny northern hardwood forests in the presence of beech bark disease and gypsy moth disturbances. For Ecol Manage 144:265–274Google Scholar
  76. Lautenschlager RA, Kircher CH, Podgwaite JD (1977) Effect of nucleopolyhedrosis virus on selected mammalian predators of the gypsy moth. USDA Forest Service, Northeastern Research Station, Res Pap NE-377Google Scholar
  77. Levine JM, Vila M, D’Antonio CM, Dukes JS, Grigulis K, Lavorel S (2003) Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc Lond B 270:775–781Google Scholar
  78. Lewis GP, Likens GE (2007) Changes in stream chemistry associated with insect defoliation in a Pennsylvania hemlock-hardwoods forest. For Ecol Manage 238:199–211Google Scholar
  79. Liebhold AM, MacDonald WL, Bergdahl D, Mastro VC (1995) Invasion by exotic forest pests: a threat to forest ecosystems. For Sci Monogr 30:1–49Google Scholar
  80. Lovett GM, Ruesink AE (1995) Carbon and nitrogen mineralization from decomposing gypsy moth frass. Oecologia 104:133–138Google Scholar
  81. Lovett GM, Christenson LM, Groffman PM, Jones CG, Hart JE, Mitchell MJ (2002) Insect defoliation and nitrogen cycling in forests. Bioscience 52:335–341Google Scholar
  82. Lovett GM, Canham CD, Arthur MA, Weathers KC, Fitzhugh RD (2006) Forest ecosystem responses to exotic pests and pathogens in eastern North America. Bioscience 56:395–405Google Scholar
  83. Marco A, Quilchano C, Blaustein AR (1999) Sensitivity to nitrate and nitrite in pond-breeding amphibians from the Pacific Northwest, USA. Environ Toxicol Chem 18:2836–2839Google Scholar
  84. Martinat PJ, Coffman CC, Dodge K, Cooper RJ, Whitmore RC (1988) Effect of diflubenzuron on the canopy arthropod community in a central Appalachian forest. J Econ Entomol 81:261–267Google Scholar
  85. Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161Google Scholar
  86. Mattson WJ (1997) Exotic insects in North American forests: ecological systems forever altered. In: Britton KO (ed) Exotic pests of eastern forests, conference proceedings, Nashville, TN, 8–10 April 1997. USDA Forest Service and UN Exotic Pest CouncilGoogle Scholar
  87. Mattson WJ, Addy ND (1975) Phytophagous insects as regulators of forest primary production. Science 190:515–522Google Scholar
  88. Mattson WJ, Herms DA, Witter JA, Allen DA (1991) Woody plant grazing systems: North American outbreak folivores and their host plants. In: Baranchikov YO, Mattson WJ, Hain F, Payne TL (eds) Forest insect guilds: patterns of interaction with host trees. USDA General Technical Report NE-153, pp 53–84Google Scholar
  89. Mattson WJ, Niemelä P, Millers I, Inguanzo Y (1994) Immigrant phytophagous insects on woody plants in the United States and Canada: an annotated list. USDA Forest Service, General Technical Report NC-169Google Scholar
  90. Mattson WJ, Vanhanen H, Veteli T, Sivonen S, Niemelä P (2007) Few immigrant phytophagous insects on woody plants in Europe: legacy of the European crucible? Biol Invasions 9:957–974Google Scholar
  91. McCullough DG, Work TT, Cavey JF, Liebhold AM, Marshall D (2006) Interceptions at nonindigenous plant pests at US ports of entry and border crossings over a 17-year period. Biol Invasions 8:611–630Google Scholar
  92. McEwan RW, Rieske LK, Arthur MA (2009) Potential interactions between invasive woody shrubs and the gypsy moth (Lymantria dispar), an invasive insect herbivore. Biol Invasions 11:1053–1058Google Scholar
  93. McShea WJ (2000) The influence of acorn production on annual variation in rodent and bird populations. Ecology 81:228–238Google Scholar
  94. McShea WJ, Healy WM, Devers P, Fearer T, Koch FH, Stauffer D, Waldon J (2007) Forestry matters: decline of oaks will impact wildlife in hardwood forests. J Wildl Manage 71:1717–1728Google Scholar
  95. Miller JC (1990) Field assessment of the effects of a microbial pest control agent on nontarget Lepidoptera. Am Entomol 36:135–139Google Scholar
  96. Morin RS, Liebhold AM, Tobin PC, Gottschalk KW, Luzader E (2007) Spread of beech bark disease in the eastern United States and its relationship to regional forest composition. Can J For Res 37:726–736Google Scholar
  97. Muzika RM, Liebhold AM (1999) Changes in radial increment of host and non-host tree species with gypsy moth defoliation. Can J For Res 29:1365–1373Google Scholar
  98. Muzika RM, Liebhold AM (2001) A critique of silvicultural approaches to managing defoliating insects in North America. Agric For Entomol 2:97–105Google Scholar
  99. Muzika RM, Twery MJ (1995) Regeneration in defoliated and thinned hardwood stands of north-central West Virginia. In: Gottschalk KW, Fosbroke SLC (eds) Proceedings, 10th Central Hardwood Forest Conference, Radnor, Pennsylvania, General Technical Report NE-197, U.S. Department of Agriculture, Forest Service, Northeastern Forest Experiment Station, pp 326–340Google Scholar
  100. Muzika RM, Grusheckyb ST, Liebhold AM, Smith RL (2004) Using thinning as a management tool for gypsy moth: the influence on small mammal abundance. For Ecol Manage 192:349–359Google Scholar
  101. Nagel TA, Svoboda M (2008) Gap disturbance regime in an old-growth Fagus-Abies forest in Dinaric Mountains, Bosnia-Herzegovina. Can J For Res 38:2728–2737CrossRefGoogle Scholar
  102. Naidoo R, Lechowicz MJ (2001) Effects of gypsy moth on radial growth of deciduous trees. For Sci 47:338–348Google Scholar
  103. Niemelä P, Mattson WJ (1996) Invasion of North American forests by European phytophagous insects. Bioscience 46:741–753Google Scholar
  104. Nowacki GJ, Abrams MD (1992) Community, edaphic, and historical analysis of mixed oak forests of the Ridge and Valley Province in central Pennsylvania. Can J For Res 22:790–800Google Scholar
  105. Orwig DA (2002) Stand dynamics associated with chronic hemlock woolly adelgid infestations in southern New England. In: Reardon RC, Onken BP, Lashomb J (eds) Symposium on the Hemlock Woolly adelgid in eastern North America. New Jersey Agricultural Experiment Station Publication, New Brunswick, New Jersey, pp 36–47Google Scholar
  106. Orwig DA, Foster DR (1998) Forest response to the introduced hemlock woolly adelgid in southern New England, USA. J Torr Bot Soc 125:60–73Google Scholar
  107. Orwig DA, Kittredge D (2005) Silvicultural options for managing hemlock forests threatened by hemlock woolly adelgid. In: Onken B, Reardon R (eds) Third symposium on Hemlock Woolly adelgid in the eastern United States. Asheville, North Carolina, FHTET-2005-01, pp 106–118Google Scholar
  108. Orwig DA, Kizlinski ML (2002) Vegetation response following hemlock woolly adelgid infestation, hemlock decline, and hemlock salvage logging. In: Reardon RC, Onken BP, Lashomb J (eds) Proceedings: symposium on Hemlock Woolly adelgid in the eastern United States. New Jersey Agricultural Experiment Station Publication, New Brunswick, New Jersey, pp 106–117Google Scholar
  109. Orwig DA, Foster DR, Mausel DL (2002) Landscape patterns of hemlock decline in New England due to the introduced hemlock woolly adelgid. J Biogeogr 29:1475–1487Google Scholar
  110. Orwig DA, Cobb RC, D’Amato AW, Kizlinski ML, Foster DR (2008) Multi-year ecosystem response to hemlock woolly adelgid infestation in southern New England. Can J For Res 38:834–843Google Scholar
  111. Ostfield RS, Jones CG, Wolff JO (1996) Of mice and mast. Bioscience 46:323–330Google Scholar
  112. Owens AK, Moseley KR, McCay TS, Castleberry SB, Kilgo JC, Ford WM (2008) Amphibian and reptile community response to coarse woody debris manipulations in upland loblolly pine (Pinus taeda) forests. For Ecol Manage 256:2078–2083Google Scholar
  113. Parendes LA, Jones JA (2000) Role of light availability and dispersal in exotic plant invasion along roads and streams in the H. J. Andrews Experimental Forest, Oregon. Conserv Biol 14:64–75Google Scholar
  114. Parker IM, Simberloff D, Lonsdale WM, Goodell K, Wonham M, Karieva PM, Williamson MH, Von Holle B, Moyle PB, Byers JE, Goldwasser L (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19Google Scholar
  115. Parry D (2009) Beyond Pandora’s box: quantitatively evaluating non-target effects of parasitoids in classical biological control. Biol Invasions 11:47–58Google Scholar
  116. Pauley EF, Clebsch EEC (1990) Patterns of Abies fraseri regeneration in a Great Smokey Mountains spruce-fir forest. Bull Torr Bot Club 117:375–381Google Scholar
  117. Penrod KA, McCormick LH (1997) Hay-scented fern spore production following clearcutting. In: Pallardy SG, Cecich RA, Garrett HG, Johnson PS (eds) Proceedings of the 11th Central Hardwood Forest Conference, General Technical Report NC-188, U.S. Department of Agriculture, Forest Service, North Central Forest Experimental Station, St. Paul, Minnesota, pp 401Google Scholar
  118. Perry WB, Christiansen TA, Perry SA (1997) Response of soil and leaf litter microarthropods to forest application of diflubenzuron. Ecotoxicology 6:87–99Google Scholar
  119. Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs associated with non-indigenous species in the United States. Bioscience 50:53–65Google Scholar
  120. Poland T, McCullough D (2006) Emerald ash borer: invasion of the urban forest and the threat to North America’s ash resource. J For 104:118–124Google Scholar
  121. Preisser EL, Elkinton JS (2008) Exploitative competition between invasive herbivores benefits a native host plant. Ecology 89:2671–2677PubMedGoogle Scholar
  122. Rabenold KN, Fauth PT, Goodner BW, Sadowski JA, Parker PG (1998) Response of avian communities to disturbance by an exotic insect in spruce-fir forests of the Southern Appalachians. Conserv Biol 12:177–189Google Scholar
  123. Rastall K, Kondo V, Strazanac JS, Butler L (2003) Lethal effects of biological insecticide applications on non-target lepidopterans in two Appalachian forests. Environ Entomol 32:1364–1369Google Scholar
  124. Rebek EJ, Herms DA, Smitley DR (2008) Interspecific variation in resistance to emerald ash borer (Coleoptera: Buprestidae) among North American and Asian ash (Fraxinus spp.). Environ Entomol 37:242–246PubMedGoogle Scholar
  125. Redman AM, Scriber JM (2000) Competition between the gypsy moth, Lymantria dispar, and the northern tiger swallowtail, Papilio canadensis: interactions mediated by host plant chemistry, pathogens, and parasitoids. Oecologia 125:218–228Google Scholar
  126. Runkle JR (1982) Patterns of disturbance in some old-growth mesic forests of eastern North America. Ecology 63:1533–1546Google Scholar
  127. Runkle JR (1990) Gap dynamics in an Ohio Acer-Fagus forest and speculation on the geography of disturbance. Can J For Res 20:632–641Google Scholar
  128. Runkle JR (1998) Changes in southern Appalachian canopy tree gaps sampled thrice. Ecology 79:1768–1780CrossRefGoogle Scholar
  129. Runkle JR (2000) Canopy tree turnover in old-growth mesic forests of eastern North America. Ecology 81:554–567CrossRefGoogle Scholar
  130. Runkle JR (2005) Twenty-four years of change in an old Tsuga canadensis woods affected by beech bark disease. J Torr Bot Soc 132:483–491Google Scholar
  131. Runkle JR (2007) Impacts of beech bark disease and deer browsing on the old-growth forest. Am Midl Nat 157:241–249Google Scholar
  132. Russell EWB, Davis RB (2001) Five centuries of changing forest vegetation in the northeastern United States. Plant Ecol 155:1–13Google Scholar
  133. Sample BE, Butler L, Zivkovich C, Whitmore RC, Reardon R (1996) Effects of Bacillus thuringiensis Berliner var. kurstaki and defoliation by the gypsy moth (Lymantria dispar (L.), Lepidoptera: Lymantriidae) on native arthropods in West Virginia. Can Entomol 128:573–592CrossRefGoogle Scholar
  134. Scharenbroch BC, Bockheim JG (2008a) The effects of gap disturbance on nitrogen cycling and retention in late-successional northern hardwood-hemlock forests. Biogeochemistry 87:231–248Google Scholar
  135. Scharenbroch BC, Bockheim JG (2008b) Gaps and soil C dynamics in old growth northern hardwood-hemlock forests. Ecosystems 11:426–441Google Scholar
  136. Schowalter TD, Hargrove WW, Crossley DA Jr (1986) Herbivory in forested ecosystems. Annu Rev Entomol 31:177–196Google Scholar
  137. Schultz JC, Baldwin IT (1982) Oak leaf quality declines in response to defoliation by gypsy moth larvae. Science 217:149–151PubMedGoogle Scholar
  138. Schweitzer JA, Bailey JK, Hart SC, Wimp GM, Chapman SK, Whitham TG (2005) The interaction of plant genotype and herbivory decelerate leaf litter decomposition and alter nutrient dynamics. Oikos 110:133–145Google Scholar
  139. Scriber JM (2004) Non-target impacts of forest defoliator management options: decision for no spraying may have worse impacts on non-target Lepidoptera than Bacillus thuringiensis insecticides. J Insect Conserv 8:241–261Google Scholar
  140. Selfridge JA, Parry D, Boettner GH (2007) Parasitism of barrens buck moth Hemileuca maia Drury in early and late successional pine barrens habitats. J Lepid Soc 61:213–221Google Scholar
  141. Shang Z, He HS, Lytle DE, Shifley SR, Crow TR (2007) Modeling the long-term effects of fire suppression on central hardwood forests in Missouri Ozarks, using LANDIS. For Ecol Manage 242:776–790Google Scholar
  142. Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32Google Scholar
  143. Small MJ, Small CJ, Dreyer GD (2005) Changes in a hemlock-dominated forest following woolly adelgid infestation in southern New England. J Torr Bot Soc 132:458–470Google Scholar
  144. Snitzer JL, Boucher DH, Kyde KL (2005) Response of exotic invasive plant species to forest damage caused by Hurricane Isabel. In: Sellner KG (ed) Hurricane Isabel in perspective. Chesapeake Research Consortium, CRC Publication 05-160, Edgewater, Maryland, pp 209–214Google Scholar
  145. Stadler B, Müller T, Orwig D (2006) The ecology of energy and nutrient fluxes in hemlock forests invaded by hemlock woolly adelgid. Ecology 87:1792–1804PubMedGoogle Scholar
  146. Strand RM, Herms DA, Ayres MP, Kubiske ME, Kaufman MG, Walker ED, Pregitzer PS, Merritt RW (1999) Effects of atmospheric CO2, light availability, and tree species on the quality of leaf detritus as a resource for treehole mosquitoes. Oikos 84:277–283Google Scholar
  147. Strazanac JS, Butler L (eds) (2005) Long-term evaluation of the effects of Bacillus thuringiensis kurstaki, gypsy moth nucleohedrosis virus product Gypchek, and Entomophaga maimaiga on nontarget organisms in mixed broadleaf-pine forests in the central Appalachians. USDA Forest Service Forest Health Technology Publication FHTET-2004-14Google Scholar
  148. Swank WT, Waide JB, Crossley DA Jr, Todd RL (1981) Insect defoliation enhances nitrate export from forest ecosystems. Oecologia 51:297–299Google Scholar
  149. Sydnor TD, Bumgardner M, Todd A (2007) The potential economic impacts of emerald ash borer (Agrilus planipennis) on Ohio, U.S., communities. Arbor Urban For 33:48–54Google Scholar
  150. Thurber DK, McLain WR, Whitmore RC (1994) Indirect effects of gypsy moth defoliation on nest predation. J Wildl Manage 58:493–500Google Scholar
  151. Tingley MW, Orwig DW, Field R, Motzkin G (2002) Avian response to removal of a forest dominant: consequences of hemlock woolly adelgid infestations. J Biogeogr 29:1505–1516Google Scholar
  152. Townsend Peterson A, Sachetti-Pereira R (2004) Potential geographic distribution of Anoplophora glabripennis (Coleoptera: Cerambycidae) in North America. Am Midl Nat 151:170–178Google Scholar
  153. Tuomi J, Niemelä P, Haukioja E, Sirén S, Neuvonen S (1984) Nutrient stress: an explanation for plant anti-herbivore responses to defoliation. Oecologia 61:208–210Google Scholar
  154. Twery MJ (1990). Effects of defoliation by gypsy moth. In: Gottschalk KW, Twery MJ, Smith SI (eds) USDA gypsy moth research review, USDA Forest Service, Northeast Forest Experiment Station General Technical Report NE-146, pp 27–39Google Scholar
  155. Wagner DL (2007) Emerald ash borer threatens ash-feeding Lepidoptera. News Lepid Soc 49:10–11Google Scholar
  156. Walker ED, Kaufman MG, Ayres MP, Riedel MH, Merritt RW (1997) Effects of variation in quality of leaf detritus on growth of the eastern tree-hole mosquito, Aedes triseriatus (Diptera: Culicidae). Can J Zool 75:706–718Google Scholar
  157. Wallner WE (1996) Invasive pests (‘biological pollutants’) and US forests: whose problem, who pays? Bull OEPP/EPPO Bull 26:167–180Google Scholar
  158. Wargo PM (1977) Armillariella mellea and Agrilus bilineatus and mortality of defoliated oak trees. For Sci 23:485–492Google Scholar
  159. Webb SL (1999) Disturbance by wind in temperate-zone forests. In: Walker LR (ed) Ecosystems of disturbed ground. Ecosystems of the world 16. Elsevier, Amsterdam, The Netherlands, pp 187–222Google Scholar
  160. Webb JR, Cosby BJ, Deviney FA, Eshleman KN, Galloway JN (1995) Change in the acid–base status of an Appalachian mountain catchment following forest defoliation by the gypsy moth. Water Air Soil Pollut 85:535–540Google Scholar
  161. Webster CR, Nelson K, Wangen SR (2005) Stand dynamics of an insular population of an invasive tree, Acer platanoides. For Ecol Manage 208:85–99Google Scholar
  162. Weston PA, Desurmont G, Hoebeke ER (2007) Viburnum leaf beetle (Coleoptera: Chrysomelidae): biology, invasion history in North America, and management options. Am Entomol 53:96–101Google Scholar
  163. Witter JA, Ragenovich IR (1986) Regeneration of Fraser fir at Mt. Mitchell, North Carolina, after depredations by the balsam woolly adelgid. For Sci 32:585–594Google Scholar
  164. Work TT, McCullough DG (2000) Lepidopteran communities in two forest ecosystems during the first gypsy moth outbreaks in northern Michigan. Environ Entomol 29:884–900Google Scholar
  165. Work TT, McCullough DG, Cavey JG, Komsa R (2005) Arrival rate of nonindigenous insect species into the United States through foreign trade. Biol Invasions 7:323–332Google Scholar
  166. Yorks TE, Jenkins JC, Leopold DJ, Raynal DJ, Orwig DA (1999) Influences of eastern hemlock mortality on nutrient cycling. In: McManus KA, Shields KS, Souto DR (eds) Proceedings: symposium on sustainable management of hemlock ecosystems in eastern North America. 22–23 June, 100, Durham, NH, USDA Forest Service, General Technical Report NE-267, pp 126–133Google Scholar
  167. Zak DR, Groffman PM, Pregitzer KS, Christensen S, Tiedje JM (1990) The vernal dam: plant-microbe competition for nitrogen in northern hardwood forests. Ecology 71:651–656Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Daniel B. Warnell School of Forestry and Natural ResourcesThe University of GeorgiaAthensUSA
  2. 2.Department of EntomologyThe Ohio State University, Ohio Agricultural Research and Development CenterWoosterUSA

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