Abstract
Exotic forest insects and pathogens (EFIP) have become regular features of temperate forest ecosystems, yet we lack a long-term perspective on their net impacts on tree mortality, carbon sequestration, and tree species diversity. Here, we analyze 3 decades (1987–2019) of forest monitoring data from the Blue Ridge Mountains ecoregion in eastern North America, including 67 plots totaling 29.4 ha, along with a historical survey from 1939. Over the past century, EFIP substantially affected at least eight tree genera. Tree host taxa had anomalously high mortality rates (≥ 6% year−1 from 2008 to 2019 vs 1.4% year−1 for less-impacted taxa). Following the arrival of EFIP, affected taxa declined in abundance (− 25 to − 100%) and live aboveground biomass (AGB; − 13 to − 100%) within our monitoring plots. We estimate that EFIP were responsible for 21–29% of ecosystem AGB loss through mortality (− 87 g m−2 year−1) from 1991 to 2013 across 66 sites. Over a century, net AGB loss among affected species totaled roughly 6.6–10 kg m−2. The affected host taxa accounted for 23–29% of genera losses at the plot scale, with mixed net effects on α-diversity. Several taxa were lost from our monitoring plots but not completely extirpated from the region. Despite these losses, both total AGB and α-diversity were largely recovered through increases in sympatric genera. These results indicate that EFIP have been an important force shaping forest composition, carbon cycling, and diversity. At the same time, less-affected taxa in these relatively diverse temperate forests have conferred substantial resilience with regard to biomass and α-diversity.
This is a preview of subscription content,
to check access.




Similar content being viewed by others
Data Availability
Data, code, and results associated with this project are archived in Zenodo (Doi: https://doi.org/10.5281/zenodo.3728134). https://doi.org/10.5281/zenodo.3604993 (version of SCBI-ForestGEO data repository used in this analysis, archived on Zenodo). https://scbi-forestgeo.github.io/SCBI-ForestGEO-Data/ (SCBI-ForestGEO data repository on GitHub). https://ctfs.si.edu/datarequest/ (SCBI census data through ForestGEO data portal).
References
Abella SR, Hausman CE, Jaeger JF, Menard KS, Schetter TA, Rocha OJ. 2019. Fourteen years of swamp forest change from the onset, during, and after invasion of emerald ash borer. Biol Invasions 21:3685–96.
Anagnostakis SL. 1987. Chestnut blight: The classical problem of an introduced pathogen. Mycologia 79:23–37.
Anderson-Teixeira KJ, Davies SJ, Bennett AC, Gonzalez-Akre EB, Muller-Landau HC, Joseph Wright S, Abu Salim K, Almeyda Zambrano AM, Alonso A, Baltzer JL, Basset Y, Bourg NA, Broadbent EN, Brockelman WY, Bunyavejchewin S, Burslem DFRP, Butt N, Cao M, Cardenas D, Chuyong GB, Clay K, Cordell S, Dattaraja HS, Deng X, Detto M, Du X, Duque A, Erikson DL, Ewango CEN, Fischer GA, Fletcher C, Foster RB, Giardina CP, Gilbert GS, Gunatilleke N, Gunatilleke S, Hao Z, Hargrove WW, Hart TB, Hau BCH, He F, Hoffman FM, Howe RW, Hubbell SP, Inman-Narahari FM, Jansen PA, Jiang M, Johnson DJ, Kanzaki M, Kassim AR, Kenfack D, Kibet S, Kinnaird MF, Korte L, Kral K, Kumar J, Larson AJ, Li Y, Li X, Liu S, Lum SKY, Lutz JA, Ma K, Maddalena DM, Makana J-R, Malhi Y, Marthews T, Mat Serudin R, McMahon SM, McShea WJ, Memiaghe HR, Mi X, Mizuno T, Morecroft M, Myers JA, Novotny V, de Oliveira AA, Ong PS, Orwig DA, Ostertag R, den Ouden J, Parker GG, Phillips RP, Sack L, Sainge MN, Sang W, Sri-ngernyuang K, Sukumar R, Sun I-F, Sungpalee W, Suresh HS, Tan S, Thomas SC, Thomas DW, Thompson J, Turner BL, Uriarte M, Valencia R, et al. 2015. CTFS-ForestGEO: a worldwide network monitoring forests in an era of global change. Glob Change Biol 21:528–49.
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 60:886–97.
Ayres MP, Lombardero MJ. 2000. Assessing the consequences of global change for forest disturbance from herbivores and pathogens. Sci Total Environ 262:263–86.
Berg LY, Moore RB. 1941. Forest cover types of Shenandoah National Park, Virginia. Luray, Virginia, USA: United States Department of the Interior: National Park Service.
Bonan GB. 2008. Forests and Climate Change: Forcings, Feedbacks, and the Climate Benefits of Forests. Science 320:1444–9.
Bourg NA, McShea WJ, Thompson JR, McGarvey JC, Shen X. 2013. Initial census, woody seedling, seed rain, and stand structure data for the SCBI SIGEO Large Forest Dynamics Plot: Ecological Archives E094-195. Ecology 94:2111–2.
Boyd IL, Freer-Smith PH, Gilligan CA, Godfray HCJ. 2013. The consequence of tree pests and diseases for ecosystem services. Science 342:1235773.
Bradshaw CJA, Leroy B, Bellard C, Roiz D, Albert C, Fournier A, Barbet-Massin M, Salles J-M, Simard F, Courchamp F. 2016. Massive yet grossly underestimated global costs of invasive insects. Nat Commun 7:12986.
Brasier CM. 1991. Ophiostoma novo-ulmi sp. nov., causative agent of current Dutch elm disease pandemics. Mycopathologia 115:151–61.
Brasier CM. 2000. Intercontinental spread and continuing evolution of the Dutch Elm disease pathogens. In: Dunn CP, Ed. The Elms: breeding, conservation, and disease management. Boston, MA: Springer. pp 61–72. https://doi.org/10.1007/978-1-4615-4507-1_4
Bugmann H, Seidl R, Hartig F, Bohn F, Brůna J, Cailleret M, François L, Heinke J, Henrot A-J, Hickler T, Hülsmann L, Huth A, Jacquemin I, Kollas C, Lasch-Born P, Lexer MJ, Merganič J, Merganičová K, Mette T, Miranda BR, Nadal-Sala D, Rammer W, Rammig A, Reineking B, Roedig E, Sabaté S, Steinkamp J, Suckow F, Vacchiano G, Wild J, Xu C, Reyer CPO. 2019. Tree mortality submodels drive simulated long-term forest dynamics: assessing 15 models from the stand to global scale. Ecosphere 10:e02616.
Caetano-Anollés G, Trigiano RN, Windham MT. 2001. Patterns of evolution in Discula fungi and the origin of dogwood anthracnose in North America, studied using arbitrarily amplified and ribosomal DNA. Curr Genet 39:346–54.
Carr DE, Banas LE. 2000. Dogwood anthracnose (Discula destructiva): effects of and consequences for Host (Cornus florida) demography. Am Midl Nat 143:169–77.
Cass W, Hochstedler W, Fisichelli N. 2011. Shenandoah National Park forest vegetation monitoring protocol: Version 2.3. Natural Resource Report NPS/MIDN/NRR—2011/475. :52.
Cass W, Hochstedler WW, Williams AB. 2012. Forest vegetation status in Shenandoah National Park: long-term ecological monitoring summary report 2003–2011. Natural resources data series NPS/MIDN/NRDS-2012/353. Fort Collins, CO: National Park Service.
Chojnacky DC, Heath LS, Jenkins JC. 2014. Updated generalized biomass equations for North American tree species. Forestry 87:129–51.
Cipollini D. 2015. White fringetree as a novel larval host for Emerald Ash Borer. J Econ Entomol 108:370–5.
Conners JA. 1988. Shenandoah National Park: an interpretive guide. Blacksburg, VA: McDonald & Woodward Pub Co.
Dietze MC, Matthes JH. 2014. A general ecophysiological framework for modelling the impact of pests and pathogens on forest ecosystems. Ecol Lett 17:1418–26.
Dukes JS, Pontius J, Orwig D, Garnas JR, Rodgers VL, Brazee N, Cooke B, Theoharides KA, Stange EE, Harrington R, Ehrenfeld J, Gurevitch J, Lerdau M, Stinson K, Wick R, Ayres M. 2009. Responses of insect pests, pathogens, and invasive plant species to climate change in the forests of northeastern North America: what can we predict? Can J For Res 39:231–48.
Ellison AM, Orwig DA, Fitzpatrick MC, Preisser EL. 2018. The past, present, and future of the hemlock woolly adelgid (Adelges tsugae) and its ecological interactions with eastern hemlock (Tsuga canadensis) forests. Insects 9:172.
Fei S, Morin RS, Oswalt CM, Liebhold AM. 2019. Biomass losses resulting from insect and disease invasions in US forests. Proc Natl Acad Sci 116:17371–17376.
Finzi AC, Raymer PCL, Giasson M-A, Orwig DA. 2014. Net primary production and soil respiration in New England hemlock forests affected by the hemlock woolly adelgid. Ecosphere 5:art98.
Flower CE, Knight KS, Gonzalez-Meler MA. 2013. Impacts of the emerald ash borer (Agrilus planipennis Fairmaire) induced ash (Fraxinus spp.) mortality on forest carbon cycling and successional dynamics in the eastern United States. Biol Invasions 15:931–44.
Fraterrigo JM, Ream K, Knoepp JD. 2018. Tree mortality from insect infestation enhances carbon stabilization in Southern Appalachian forest soils. J Geophys Res Biogeosci 123:2121–34.
Friedlingstein P, Cox P, Betts R, Bopp L, von Bloh W, Brovkin V, Cadule P, Doney S, Eby M, Fung I, Bala G, John J, Jones C, Joos F, Kato T, Kawamiya M, Knorr W, Lindsay K, Matthews HD, Raddatz T, Rayner P, Reick C, Roeckner E, Schnitzler K-G, Schnur R, Strassmann K, Weaver AJ, Yoshikawa C, Zeng N. 2006. Climate–carbon cycle feedback analysis: results from the C4MIP model intercomparison. J Clim 19:3337–53.
Gonzalez-Akre E, Meakem V, Eng C-Y, Tepley AJ, Bourg NA, McShea W, Davies SJ, Anderson-Teixeira K. 2016. Patterns of tree mortality in a temperate deciduous forest derived from a large forest dynamics plot. Ecosphere 7:e01595.
Guo Q, Fei S, Potter KM, Liebhold AM, Wen J. 2019. Tree diversity regulates forest pest invasion. Proc Natl Acad Sci 116:7382–7386.
Hanberry BB, Nowacki GJ. 2016. Oaks were the historical foundation genus of the east-central United States. Quat Sci Rev 145:94–103.
Hansen E, Reeser P, Sutton W, Kanaskie A, Navarro S, Goheen EM. 2019. Efficacy of local eradication treatments against the sudden oak death epidemic in Oregon tanoak forests. Woodward S, editor. For Pathol 49:e12530.
Hassan RM, Scholes RJ, Ash N, Millennium Ecosystem Assessment (Program), Eds. 2005. Ecosystems and human well-being: current state and trends: findings of the condition and trends Working Group of the Millennium Ecosystem Assessment. Washington, DC: Island Press.
Herms DA, McCullough DG. 2014. Emerald Ash Borer invasion of North America: history, biology, ecology, impacts, and management. Annu Rev Entomol 59:13–30.
Isbell F, Craven D, Connolly J, Loreau M, Schmid B, Beierkuhnlein C, Bezemer TM, Bonin C, Bruelheide H, Luca E de, Ebeling A, Griffin JN, Guo Q, Hautier Y, Hector A, Jentsch A, Kreyling J, Lanta V, Manning P, Meyer ST, Mori AS, Naeem S, Niklaus PA, Polley HW, Reich PB, Roscher C, Seabloom EW, Smith MD, Thakur MP, Tilman D, Tracy BF, Putten WH van der, Ruijven J van, Weigelt A, Weisser WW, Wilsey B, Eisenhauer N. 2015. Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature 526:574–7.
IUCN. 2019. The IUCN Red List of threatened species. Version 2019-2. https://www.iucnredlist.org. Downloaded on 18 August 2019.
Jacobs DF. 2007. Toward development of silvical strategies for forest restoration of American chestnut (Castanea dentata) using blight-resistant hybrids. Biol Conserv 137:497–506.
Jenkins JC, Chojnacky DC, Heath LS, Birdsey RA. 2003. National-scale biomass estimators for United States tree species. For Sci 49:12–35.
Karban R. 1978. Changes in an oak-chestnut forest since the chestnut blight. Castanea 43:221–8.
Kasbohm JW. 1994. Response of black bears to gypsy moth infestation in Shenandoah National Park, Virginia. https://vtechworks.lib.vt.edu/handle/10919/39530. Accessed 05 June 2018.
Levine JM, D’Antonio CM. 2003. Forecasting biological invasions with increasing international trade. Conserv Biol 17:322–6.
Liebhold AM, McCullough DG, Blackburn LM, Frankel SJ, Holle BV, Aukema JE. 2013. A highly aggregated geographical distribution of forest pest invasions in the USA. Divers Distrib 19:1208–16.
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.
Lovett GM, Weiss M, Liebhold AM, Holmes TP, Leung B, Lambert KF, Orwig DA, Campbell FT, Rosenthal J, McCullough DG, Wildova R, Ayres MP, Canham CD, Foster DR, LaDeau SL, Weldy T. 2016. Nonnative forest insects and pathogens in the United States: impacts and policy options. Ecol Appl 26:1437–55.
Magarey RD, Colunga-Garcia M, Fieselmann DA. 2009. Plant biosecurity in the United states: roles, responsibilities, and information needs. BioScience 59:875–84.
Mahan CG, Diefenbach DR, Cass WB. 2007. Evaluating and revising a long-term monitoring program for vascular plants: lessons from Shenandoah National Park. Nat Areas J 27:16–24.
McCarty EP, Addesso KM. 2019. Hemlock woolly adelgid (Hemiptera: Adelgidae) management in forest, landscape, and nursery production. J Insect Sci 19. 19:iez031. https://doi.org/10.1093/jisesa/iez031.
McGarvey JC, Thompson JR, Epstein HE, Shugart HH. 2014. Carbon storage in old-growth forests of the Mid-Atlantic: toward better understanding the eastern forest carbon sink. Ecology 96:311–7.
Morin RS, Gottschalk KW, Ostry ME, Liebhold AM. 2018. Regional patterns of declining butternut ( Juglans cinerea L.) suggest site characteristics for restoration. Ecol Evol 8:546–59.
Oak SW, Spetich MA, Morin RS. 2016. Oak decline in central hardwood forests: frequency, spatial extent, and scale. In: Greenberg CH, Collins BS, Eds. Natural disturbances and historic range of variation. managing forest ecosystems. Cham: Springer. pp 49–71. https://doi.org/10.1007/978-3-319-21527-3_3. Accessed 21 Jan 2016.
Peltzer DA, Allen RB, Lovett GM, Whitehead D, Wardle DA. 2010. Effects of biological invasions on forest carbon sequestration. Glob Change Biol 16:732–46.
Potter K, Escanferla M, Jetton R, Man G. 2019. Important insect and disease threats to United States tree species and geographic patterns of their potential impacts. Forests 10:304.
Sakalidis ML, Slippers B, Wingfield BD, Hardy GESJ, Burgess TI. 2013. The challenge of understanding the origin, pathways and extent of fungal invasions: global populations of the Neofusicoccum parvum–N. ribis species complex. Divers Distrib 19:873–83.
Sala OE. 2000. Global biodiversity scenarios for the year 2100 . Science 287:1770–4.
Seidl R, Klonner G, Rammer W, Essl F, Moreno A, Neumann M, Dullinger S. 2018. Invasive alien pests threaten the carbon stored in Europe’s forests. Nat Commun 9:1626.
Strayer DL, Eviner VT, Jeschke JM, Pace ML. 2006. Understanding the long-term effects of species invasions. Trends Ecol Evol 21:645–51.
Thompson JR, Carpenter DN, Cogbill CV, Foster DR. 2013. Four centuries of change in northeastern United States forests. PLOS ONE 8:e72540.
Wester HV, Davidson RW, Fowler ME. 1950. Cankers of Linden and Redbud. Plant Dis Rep. 34. https://www.cabdirect.org/cabdirect/abstract/19511100348. Accessed 19 Mar 2019.
Young JG, Fleming W, Cass WB, Lea C. 2009. Vegetation of Shenandoah National Park in relation to environmental gradients, version 2.0. Philadelphia, PA: National Park Service. https://irma.nps.gov/DataStore/DownloadFile/440196. Accessed 30 Mar 2019.
Zhu K, Zhang J, Niu S, Chu C, Luo Y. 2018. Limits to growth of forest biomass carbon sink under climate change. Nat Commun 9:2709.
Acknowledgements
We thank the many researchers who assisted with forest censuses at both SCBI and SNP and local professionals who provided information on pests and pathogens in the region (Rolf Gubler and Dale Meyerhoeffer at SNP; Lori Chamberlin and Katlin Mooneyham at Virginia Department of Forestry). Thank you to Rupert Seidl and anonymous reviewers for helpful comments. This research was funded by Smithsonian’s Forest Global Earth Observatory, the Shenandoah National Park Inventory and Monitoring Program and grants from the Virginia Native Plant Society (n = 2) and the Shenandoah National Park Trust.
Author information
Authors and Affiliations
Corresponding author
Additional information
Authors' contributions: KJAT, WBC, AJT, and VH conceived and designed the study; WBC, EBGA, NAB, AA, FD, and WJM designed and implemented forest monitoring protocols; AW, SJP, RH, EBGA, NAB, CTC, AEF, CK, VM, IRM, MNP, MKS, and ART performed the research; VH and KJAT analyzed the data; KJAT led the writing of the manuscript. All authors reviewed and approved the draft.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Anderson-Teixeira, K.J., Herrmann, V., Cass, W.B. et al. Long-Term Impacts of Invasive Insects and Pathogens on Composition, Biomass, and Diversity of Forests in Virginia’s Blue Ridge Mountains. Ecosystems 24, 89–105 (2021). https://doi.org/10.1007/s10021-020-00503-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10021-020-00503-w