Advertisement

Biological Invasions

, Volume 20, Issue 3, pp 695–707 | Cite as

Forest decline after a 15-year “perfect storm” of invasion by hemlock woolly adelgid, drought, and hurricanes

  • Scott R. Abella
Original Paper

Abstract

Invasions by introduced pests can interact with other disturbances to alter forests and their functions, particularly when a dominant tree species declines. To identify changes after invasion by the insect hemlock woolly adelgid (Adelges tsugae; HWA), coinciding with severe droughts and hurricanes, this study compared tree species composition of eastern hemlock (Tsuga canadensis) forests on 11 plots before (2001) and 15 years after (2016) invasion in the southern Appalachian Mountains, USA. Losses of hemlock trees after HWA invasion were among the highest reported, with a 90% decline in density, 86% decline in basal area, and 100% mortality for individuals ≥ 60 cm in diameter. In contrast to predictions of theoretical models, deciduous tree density declined after HWA invasion, while basal area changed little, at least during the initial 15 years after invasion. Overall, forest density declined by 58%, basal area by 25%, and tree species richness by 8%. Factors additional to HWA likely exacerbating forest decline included: droughts before (1999–2001) and after HWA invasion (2006–2008); tree uprooting from hurricane-stimulated winds in 2004; pest-related declines of deciduous tree species otherwise likely benefitting from hemlock’s demise; death of deciduous trees when large hemlocks fell; and competition from aggressive understory plants including doghobble (Leucothoe fontanesiana), rosebay rhododendron (Rhododendron maximum), and Rubus spp. Models of forest change and ecosystem function should not assume that deciduous trees always increase during the first decades after HWA invasion.

Keywords

Deciduous forest Introduced forest pest Jocassee Gorges Rhododendron Southern Appalachian Mountains Tsuga canadensis 

Notes

Acknowledgements

The 2016 remeasurement was funded by start-up funds managed by S.R. Abella and provided by the University of Nevada Las Vegas, and by funds donated by S.R. Abella via Natural Resource Conservation LLC. The 2001 data collection was supported by grants to V.B. Shelburne from the South Carolina Department of Natural Resources (SCDNR) and the U.S. Fish and Wildlife Service’s Wildlife Conservation and Restoration Program. The 2001 study was performed in partial fulfillment of the requirements for a M.Sc. for S.R. Abella at Clemson University, under advisement by V.B. Shelburne. The SCDNR and Duke Power Company provided access to establish the plots and supported the research; H. Douglass (Foothills Trail Conference), V.B. Shelburne, and D. Chastain provided helpful information on recent forest changes in the study area; S. Altman prepared the figures; and two anonymous reviewers provided helpful comments on the manuscript.

Supplementary material

10530_2017_1568_MOESM1_ESM.pdf (32.5 mb)
Supplementary material 1 (PDF 33328 kb)
10530_2017_1568_MOESM2_ESM.pdf (19 kb)
Supplementary material 2 (PDF 18 kb)

References

  1. Abella SR (2003) Quantifying ecosystem geomorphology of the southern Appalachian Mountains. Phys Geogr 24:488–501CrossRefGoogle Scholar
  2. Abella SR (2014) Impacts and management of hemlock woolly adelgid in national parks of the eastern United States. Southeast Nat 13:16–45Google Scholar
  3. Abella SR (2015) Conserving America’s national parks. CreateSpace, CharlestonGoogle Scholar
  4. Abella SR, Shelburne VB (2004) Ecological species groups of South Carolina’s Jocassee Gorges, southern Appalachian Mountains. J Torrey Bot Soc 131:220–231CrossRefGoogle Scholar
  5. Abella SR, Shelburne VB, MacDonald NW (2003) Multifactor classification of forest landscape ecosystems of Jocassee Gorges, southern Appalachian Mountains, South Carolina. Can J For Res 33:1933–1946CrossRefGoogle Scholar
  6. Abella SR, Gering LR, Shelburne VB (2004) Slope correction of plot dimensions for vegetation sampling in mountainous terrain. Nat Area J 24:348–350Google Scholar
  7. Aukema JE, McCullough DG, Von Holle B, Liebhold AM, Britton K, Frankel SJ (2010) Historical accumulation of nonindigenous forest pests in the continental United States. Bioscience 60:886–897CrossRefGoogle Scholar
  8. Beckage B, Clark JS, Clinton BD, Haines BL (2000) A long-term study of tree seedling recruitment in southern Appalachian forests: the effects of canopy gaps and shrub understories. Can J For Res 30:1617–1631CrossRefGoogle Scholar
  9. Benton E, Grant JF, Cowles R, Webster J, Nichols R, Lagalante A, Coots C (2016) Assessing relationships between tree diameter and long-term persistence of imidacloprid and olefin to optimize imidacloprid treatments on eastern hemlock. For Ecol Manag 370:12–21CrossRefGoogle Scholar
  10. Bevins SN, Pedersen K, Lutman MW, Gidlewski T, Deliberto TJ (2014) Consequences associated with the recent range expansion of nonnative feral swine. Bioscience 64:291–299CrossRefGoogle Scholar
  11. Birt AG, Zeng Y, Tchakerian MD, Coulson RN, Lafon CW, Cairns DM, Waldron J, Xi W, Chen S, Street DA (2014) Evaluating southern Appalachian forest dynamics without eastern hemlock: consequences of herbivory by the hemlock woolly adelgid. Open J For 4:91–99Google Scholar
  12. Blake ES, Landsea CW, Gibney EJ (2011) The deadliest, costliest, and most intense United States tropical cyclones from 1851 to 2010. NOAA technical memorandum NWS NHC-6. National Hurricane Center, Miami, FloridaGoogle Scholar
  13. Boyle MF, Abella SR, Shelburne VB (2014) An ecosystem classification approach to assessing forest change in the southern Appalachian Mountains. For Ecol Manag 323:85–97CrossRefGoogle Scholar
  14. Brockerhoff EG, Liebhold AM (2017) Ecology of forest insect invasions. Biol Invasions. doi: 10.1007/s10530-017-1514-1
  15. Cooper AW, Hardin JW (1970) Floristics and vegetation of the gorges of the southern Blue Ridge Escarpment. In: Holt PC, Paterson RA (eds) The distributional history of the biota of the southern Appalachians. Part II: Flora. Research division monograph, vol 2. Virginia Polytechnic Institute and State University, Blacksburg, pp 291–330Google Scholar
  16. Dietze MC, Clark JS (2008) Changing the gap dynamics paradigm: vegetative regeneration control on forest response to disturbance. Ecol Monogr 78:331–347CrossRefGoogle Scholar
  17. Elliott KJ, Swank WT (2008) Long-term changes in forest composition and diversity following early logging (1919–1923) and the decline of American chestnut (Castanea dentata). Plant Ecol 197:155–172CrossRefGoogle Scholar
  18. Elliott KJ, Vose JM (2011) The contribution of the Coweeta Hydrologic Laboratory to developing an understanding of long-term (1934–2008) changes in managed and unmanaged forests. For Ecol Manag 261:900–910CrossRefGoogle Scholar
  19. Ellison AM, Bank MS, Clinton BD et al (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 9:479–486CrossRefGoogle Scholar
  20. Ellison AM, Barker Plotkin AA, Khalid S (2016) Foundation species loss and biodiversity of the herbaceous layer in New England forests. Forests 7:9CrossRefGoogle Scholar
  21. 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
  22. Eschtruth AK, Evans RA, Battles JJ (2013) Patterns and predictors of survival in Tsuga canadensis populations infested by the exotic pest Adelges tsugae: 20 years of monitoring. For Ecol Manag 305:195–203CrossRefGoogle Scholar
  23. Fisichelli NA, Abella SR, Peters M, Krist FJ (2014) Climate, trees, pests, and weeds: change, uncertainty, and biotic stressors in eastern U.S. national park forests. For Ecol Manag 327:31–39CrossRefGoogle Scholar
  24. Ford CR, Elliott KJ, Clinton BD, Kloeppel BD, Vose JM (2012) Forest dynamics following eastern hemlock mortality in the southern Appalachians. Oikos 121:523–536CrossRefGoogle Scholar
  25. Foster DR (ed) (2014) Hemlock: a forest giant on the edge. Yale University Press, New HavenGoogle Scholar
  26. Gómez S, Gonda-King L, Orians CM, Orwig DA, Panko R, Radville L, Soltis N, Thornber CS, Preisser EL (2015) Interactions between invasive herbivores and their long-term impact on New England hemlock forests. Biol Invasions 17:661–673CrossRefGoogle Scholar
  27. Havill NP, Shiyake S, Lamb Galloway A, Foottit RG, Yu G, Paradis A, Elkinton J, Montgomery ME, Sano M, Caccone A (2016) Ancient and modern colonization of North America by hemlock woolly adelgid, Adelges tsugae (Hemiptera: Adelgidae), an invasive insect from East Asia. Mol Ecol 25:2065–2080CrossRefPubMedGoogle Scholar
  28. Holzmueller EJ, Jose S, Jenkins MJ (2010) Ecological consequences of an exotic fungal diease in eastern U.S. hardwood forests. For Ecol Manag 259:1347–1353CrossRefGoogle Scholar
  29. 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
  30. Langor DW, DeHaas LJ, Foottit RG (2009) Diversity of non-native terrestrial arthropods on woody plants in Canada. Biol Invasions 11:5–19CrossRefGoogle Scholar
  31. Liebhold AM, Brockerhoff EG, Kalisz S et al (2017) Biological invasions in forest ecosystems. Biol Invasions. doi: 10.1007/s10530-017-1458-5
  32. Lorimer CG (1980) Age structure and disturbance history of a southern Appalachian virgin forest. Ecology 61:1169–1184CrossRefGoogle Scholar
  33. Lovett GM, Canham CD, Arthur MA, Weathers KC, Fitzhugh RD (2006) Forest ecosystem responses to exotic pests and pathogens in eastern North America. Bioscience 56:395–405CrossRefGoogle Scholar
  34. Lovett GM, Weiss M, Liebhold AM et al (2016) Nonnative forest insects and pathogens in the United States: impacts and policy options. Ecol Appl 26:1437–1455CrossRefPubMedGoogle Scholar
  35. Mallik AU (2003) Conifer regeneration problems in boreal and temperate forests with ericaceous understory: role of disturbance, seedbed limitation, and keystone species change. Crit Rev Plant Sci 22:341–366CrossRefGoogle Scholar
  36. Martin KL, Goebel PC (2012) Decline in riparian Tsuga canadensis forests of the central Appalachians across an Adelges tsugae invasion chronosequence. J Torrey Bot Soc 139:367–378CrossRefGoogle Scholar
  37. McClure MS (2002) The elongate hemlock scale, Fiorinia externa Ferris (Homoptera: Diaspididae): a new look at an old nemesis. In: Reardon RC, Onken BP, Lashomb L (eds) Proceedings: hemlock woolly adelgid in the eastern United States symposium. New Jersey Agricultural Experiment Station, New Brunswick, pp 248–253Google Scholar
  38. McCune B, Mefford MJ (1999) PC-ORD: multivariate analysis of ecological data. User’s guide. MjM Software Design, Gleneden Beach, OregonGoogle Scholar
  39. McNab WH (1993) A topographic index to quantify the effect of mesoscale landform on site productivity. Can J For Res 23:1100–1107CrossRefGoogle Scholar
  40. Morin RS, Liebhold AM, Gottschalk KW (2009) Anisotropic spread of hemlock woolly adelgid in the eastern United States. Biol Invasions 11:2341–2350CrossRefGoogle Scholar
  41. Mowbray TB, Oosting HJ (1968) Vegetation gradients in relation to environment and phenology in a southern Blue Ridge gorge. Ecol Monogr 38:309–344CrossRefGoogle Scholar
  42. Natural Resources Conservation Service (2016) The PLANTS database. http://plants.usda.gov. Accessed 15 Oct 2016
  43. 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
  44. 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
  45. Orwig DA, Thompson JR, Povak NA, Manner M, Niebyl D, Foster DR (2012) A foundation tree at the precipice: Tsuga canadensis health after the arrival of Adelges tsugae in central New England. Ecosphere 3(1):10CrossRefGoogle Scholar
  46. Oten KLF, Merkle SA, Jetton RM, Smith BC, Talley ME, Hain FP (2014) Understanding and developing resistance in hemlocks to the hemlock woolly adelgid. Southeast Nat 13:147–167Google Scholar
  47. Rankin WT, Tramer EJ (2002) The gap dynamics of canopy trees of a Tsuga canadensis forest community. Northeastern Nat 9:391–406CrossRefGoogle Scholar
  48. Roques A, Auger-Rozenberg M, Blackburn TM et al (2016) Temoral and interspecific variation in rates of spread for insect species invading Europe during the last 200 years. Biol Invasions 18:907–920CrossRefGoogle Scholar
  49. Runkle JR (1998) Changes in Southern Appalachian canopy tree gaps sampled thrice. Ecology 79:1768–1780CrossRefGoogle Scholar
  50. Small MJ, Small CJ, Dreyer GD (2005) Changes in a hemlock-dominated forest following woolly adelgid infestation in southern New England. J Torrey Bot Soc 132:458–470CrossRefGoogle Scholar
  51. Spaulding HL, Rieske LK (2010) The aftermath of an invasion: structure and composition of central Appalachian hemlock forests following establishment of the hemlock woolly adelgid, Adelges tsugae. Biol Invasions 12:3135–3143CrossRefGoogle Scholar
  52. Stewart SR (2004) Tropical cyclone report: Hurricane Ivan. National Hurricane Center, MiamiGoogle Scholar
  53. Vose JM, Wear DN, Mayfield AE, Nelson CD (2013) Hemlock woolly adelgid in the southern Appalachians: control strategies, ecological impacts, and potential management responses. For Ecol Manag 291:209–219CrossRefGoogle Scholar
  54. Willeford Bair M (2002) Eastern hemlock (Tsuga canadensis) mortality in Shenandoah National Park. In: Reardon RC, Onken BP, Lashomb L (eds) Proceedings: hemlock woolly adelgid in the eastern United States symposium. New Jersey Agricultural Experiment Station, New Brunswick, pp 61–66Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.School of Life SciencesUniversity of Nevada Las VegasLas VegasUSA

Personalised recommendations