Abstract
The unintentional transport of insects beyond their native ranges has greatly increased with globalization over the past century, leading to higher propagule pressure in non-native ranges of many species. Knowledge about the prevalence of a species in international invasion pathways is important for predicting invasions and taking appropriate biosecurity measures. We investigated the spatiotemporal patterns and drivers of interceptions—detections of at least one individual with imported goods that potentially serve as a proxy for arrival rates—for a tree-killing bark beetle, the European spruce bark beetle (Ips typographus L.; Coleoptera: Curculionidae: Scolytinae), in the USA from 1914 to 2008. Across the study period, there were 505 interceptions of I. typographus with shipments originating from > 25 countries at ports in 22 US states. Interceptions first occurred in 1938, peaked at 33 and 25 in 1984 and 1996, respectively, and declined after the mid-1990s. Interceptions of I. typographus did not have a statistically detectable relationship with outbreak levels in the native range, were inversely related to annual import volume (an artifact likely driven by changes in inspection policies), and were more frequent during the winter. Thus, while interceptions of I. typographus are challenging to predict, we found evidence that (i) biosecurity practices against this beetle could be increased during winter but not in response to outbreaks in source regions and (ii) the overall abundance of this beetle in invasion pathways has recently decreased, probably because strengthened phytosanitary protocols have reduced contamination levels and/or decreased the perceived need for inspections.
This is a preview of subscription content, access via your institution.
Data availability
Data reported and analyzed were collected by the US Department of Agriculture, Animal and Plant Health Inspection Service (APHIS) and are subject to data agreements. For details of the data and how to request access contact Phytosanitary.Advanced.Analytics.Team@usda.gov.
References
Anderbrant O (1989) Reemergence and second brood in the bark beetle Ips typographus. Holarct Ecol 12:494–500. https://doi.org/10.1111/j.1600-0587.1989.tb00927.x
Aukema JE, McCullough DG, Von Holle B et al (2010) Historical accumulation of nonindigenous forest pests in the continental United States. Bioscience 60:886–897. https://doi.org/10.1525/bio.2010.60.11.5
Barton K (2022) MuMIn: Multi-model inference. R package version 1.46.0. https://CRAN.R-project.org/package=MuMIn
Bentz BJ, Jönsson AM, Schroeder M et al (2019) Ips typographus and Dendroctonus ponderosae models project thermal suitability for intra- and inter-continental establishment in a changing climate. Front For Glob Change 2:1–17. https://doi.org/10.3389/ffgc.2019.00001
Bertelsmeier C, Ollier S, Liebhold A, Keller L (2017) Recent human history governs global ant invasion dynamics. Nat Ecol Evol. https://doi.org/10.1038/s41559-017-0184
Bertelsmeier C, Ollier S, Liebhold AM et al (2018) Recurrent bridgehead effects accelerate global alien ant spread. Proc Natl Acad Sci U S A 115:5486–5491. https://doi.org/10.1073/pnas.1801990115
Bivand R, Keitt T, Rowlingson B (2019) rgdal: bindings for the “Geospatial” data abstraction library. R package version 1.4-8. https://CRAN.R-project.org/package=rgdal
Branco M, Nunes P, Roques A et al (2019) Urban trees facilitate the establishment of non-native forest insects. NeoBiota 52:25–46. https://doi.org/10.3897/neobiota.52.36358
Brockerhoff EG, Bain J, Kimberley M, Knížek M (2006) Interception frequency of exotic bark and ambrosia beetles (Coleoptera: Scolytinae) and relationship with establishment in New Zealand and worldwide. Can J for Res 36:289–298. https://doi.org/10.1139/x05-250
Brockerhoff EG, Kimberley M, Liebhold AM et al (2014) Predicting how altering propagule pressure changes establishment rates of biological invaders across species pools. Ecology 95:594–601. https://doi.org/10.1890/13-0465.1
Brockerhoff EG, Liebhold AM (2017) Ecology of forest insect invasions. Biol Invasions 19:3141–3159. https://doi.org/10.1007/s10530-017-1514-1
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer
Cavey J, Passoa S (1993) Possible new introduction—European spruce bark beetle. United States Department of Agriculture, Forest Service, Northeastern Area, NA–TP–18–93 https://www.barkbeetles.org/marchaddition/PAlertES/PAlertES.html. Accessed 17 Sep 2019. 3–5
CERIS (2013) Ips typographus (Linnaeus), fact sheet from Center for Environmental and Regulatory Information Systems (CERIS). Accessed 19 Sep 2019. 1–7
Chapman D, Purse BV, Roy HE, Bullock JM (2017) Global trade networks determine the distribution of invasive non-native species. Glob Ecol Biogeogr 26:907–917. https://doi.org/10.1111/geb.12599
Christiansen E, Bakke A (1988) The spruce bark beetle of Eurasia. In: Berryman AA (ed) Dynamics of forest insect populations. Population ecology. Springer, Boston, pp 479–503. https://doi.org/10.1007/978-1-4899-0789-9_23
Colunga-Garcia M, Haack RA, Adelaja AO (2009) Freight transportation and the potential for invasions of exotic insects in urban and periurban forests of the United States. J Econ Entomol 102:237–246. https://doi.org/10.1603/029.102.0133
Colunga-Garcia M, Haack RA, Magarey RA, Margosian ML (2010) Modeling spatial establishment patterns of exotic forest insects in urban areas in relation to tree cover and propagule pressure. J Econ Entomol 103:108–118. https://doi.org/10.1603/EC09203
Doležal P, Sehnal F (2007) Effects of photoperiod and temperature on the development and diapause of the bark beetle Ips typographus. J Appl Entomol 131:165–173. https://doi.org/10.1111/j.1439-0418.2006.01123.x
Drake JM, Lodge DM (2006) Allee effects, propagule pressure and the probability of establishment: risk analysis for biological invasions. Biol Invasions 8:365–375. https://doi.org/10.1007/s10530-004-8122-6
Duncan RP, Blackburn TM, Rossinelli S, Bacher S (2014) Quantifying invasion risk: the relationship between establishment probability and founding population size. Methods Ecol Evol 5:1255–1263. https://doi.org/10.1111/2041-210X.12288
Eriksson M, Pouttu A, Roininen H (2005) The influence of windthrow area and timber characteristics on colonization of wind-felled spruces by Ips typographus (L.). For Ecol Manage 216:105–116. https://doi.org/10.1016/j.foreco.2005.05.044
Essl F, Bacher S, Blackburn TM et al (2015) Crossing frontiers in tackling pathways of biological invasions. Bioscience 65:769–782. https://doi.org/10.1093/biosci/biv082
Faulkner KT, Robertson MP, Rouget M, Wilson JRU (2016) Border control for stowaway alien species should be prioritised based on variations in establishment debt. J Environ Manage 180:301–309. https://doi.org/10.1016/j.jenvman.2016.05.023
Faulkner KT, Robertson MP, Wilson JRU (2020) Stronger regional biosecurity is essential to prevent hundreds of harmful biological invasions. Glob Change Biol 26:2449–2462. https://doi.org/10.1111/gcb.15006
Flø D, Norli HR, Økland B, Krokene P (2018) Successful reproduction and pheromone production by the spruce bark beetle in evolutionary naïve spruce hosts with familiar terpenoid defences. Agric For Entomol 20:476–486. https://doi.org/10.1111/afe.12280
GBIF (2022) GBIF.org (24 March 2022) GBIF Occurrence Download. https://doi.org/10.15468/dl.eq7whx
Gippet JM, Liebhold AM, Fenn-Moltu G, Bertelsmeier C (2019) Human-mediated dispersal in insects. Curr Opin Insect Sci 35:96–102. https://doi.org/10.1016/j.cois.2019.07.005
Göthlin E, Schroeder LM, Lindelöw A (2000) Attacks by Ips typographus and Pityogenes chalcographus on windthrown spruces (Picea abies) during the two years following a storm felling. Scand J For Res 15:542–549. https://doi.org/10.1080/028275800750173492
Gray DR (2010) Hitchhikers on trade routes: a phenology model estimates the probabilities of gypsy moth introduction and establishment. Ecol Appl 20:2300–2309. https://doi.org/10.1890/09-1540.1
Gregoire JC, Raffa KF, Lindgren BS (2015) Economics and politics of bark beetles. In: Vega F, Hofstetter R (eds) Bark beetles: biology and ecology of native and invasive species. Academic Press, pp 585–613. https://doi.org/10.1016/B978-0-12-417156-5.00015-0
Haack RA (2001) Intercepted Scolytidae (Coleoptera) at U.S. ports of entry: 1985–2000. Integr Pest Manag Rev 6:253–282. https://doi.org/10.1023/A:1025715200538
Haack RA (2006) Exotic bark- and wood-boring Coleoptera in the United States: recent establishments and interceptions. Can J For Res 36:269–288. https://doi.org/10.1139/x05-249
Haack RA, Britton KO, Brockerhoff EG et al (2014) Effectiveness of the international phytosanitary standard ISPM No. 15 on reducing wood borer infestation rates in wood packaging material entering the United States. PLoS ONE 9:e96611. https://doi.org/10.1371/journal.pone.0096611
Hijmans RJ (2020) raster: geographic data analysis and modeling. R package version 3.1-5. https://CRAN.R-project.org/package=raster
Hroššo B, Mezei P, Potterf M et al (2020) Drivers of spruce bark beetle (Ips typographus) infestations on downed trees after severe windthrow. Forests 11:1–15. https://doi.org/10.3390/f11121290
Humphreys N, Allen E (1999) Eight-spined spruce bark beetle—Ips typographus. Exot For Pest Advis 3:1–4
Jackson L, Molet T (2014) Exotic wood borer/bark beetle national survey guidelines. Revised 2014 Manual. http://download.ceris.purdue.edu/file/3290. Accessed Mar 2021
Katsar CS, Hong S, Kim BJ, Griffin RL (2017) Risk-based sampling: the United States NPPO (USDA-APHIS-PPQ) Perspective. In: “Proceedings international symposium for riskbased sampling” North American Plant Protection Organization. https://nappo.org/application/files/4215/8746/3813/RBS_Symposium_Proceed. 18–21
Krishnankutty S, Nadel H, Taylor AM et al (2020) Identification of tree genera used in the construction of solid wood-packaging materials that arrived at U.S. Ports infested with live wood-boring insects. J Econ Entomol 113:1183–1194. https://doi.org/10.1093/jee/toaa060
Lantschner MV, Corley JC, Liebhold AM (2020) Drivers of global Scolytinae invasion patterns. Ecol Appl 30:1–12. https://doi.org/10.1002/eap.2103
Lawson SA, Carnegie AJ, Cameron N et al (2018) Risk of exotic pests to the Australian forest industry. Aust For 81:3–13. https://doi.org/10.1080/00049158.2018.1433119
Liebhold AM, Brockerhoff EG, Kimberley M (2017) Depletion of heterogeneous source species pools predicts future invasion rates. J Appl. https://doi.org/10.1111/1365-2664.12895
Liebhold AM, Mccullough DG, Blackburn LM et al (2013) A highly aggregated geographical distribution of forest pest invasions in the USA. Divers Distrib 19:1208–1216. https://doi.org/10.1111/ddi.12112
Liebhold AM, Work TT, McCullough DG, Cavey JF (2006) Airline baggage as a pathway for alien insect species invading the United States. Am Entomol 52:48–54. https://doi.org/10.1093/ae/52.1.48
Lombaert E, Guillemaud T, Cornuet JM et al (2010) Bridgehead effect in the worldwide invasion of the biocontrol Harlequin ladybird. PLoS ONE 5:e9743. https://doi.org/10.1371/journal.pone.0009743
Marini L, Økland B, Jönsson AM et al (2017) Climate drivers of bark beetle outbreak dynamics in Norway spruce forests. Ecography 40:1426–1435. https://doi.org/10.1111/ecog.02769
Marini L, Zalucki MP (2017) Density-dependence in the declining population of the monarch butterfly. Sci Rep 7:1–8. https://doi.org/10.1038/s41598-017-14510-w
McCullough DG, Work TT, Cavey JF et al (2006) Interceptions of nonindigenous plant pests at US ports of entry and border crossings over a 17-year period. Biol Invasions 8:611–630. https://doi.org/10.1007/s10530-005-1798-4
Meurisse N, Rassati D, Hurley BP et al (2019) Common pathways by which non-native forest insects move internationally and domestically. J Pest Sci 92:13–27. https://doi.org/10.1007/s10340-018-0990-0
Morris JL, Cottrell S, Fettig CJ et al (2018) Bark beetles as agents of change in social–ecological systems. Front Ecol Environ 16:S34–S43. https://doi.org/10.1002/fee.1754
Nahrung HF, Carnegie AJ (2021) Border interceptions of forest insects established in Australia: intercepted invaders travel early and often. NeoBiota 64:69–86. https://doi.org/10.3897/neobiota.64.60424
Nelson WA, Lewis MA (2008) Connecting host physiology to host resistance in the conifer-bark beetle system. Theor Ecol 1:163–177. https://doi.org/10.1007/s12080-008-0017-1
Økland B, Erbilgin N, Skarpaas O et al (2011) Inter-species interactions and ecosystem effects of non-indigenous invasive and native tree-killing bark beetles. Biol Invasions 13:1151–1164. https://doi.org/10.1007/s10530-011-9957-2
Poland TM, McCullough DG (2006) Emerald ash borer: invasion of the urban forest and the threat to North America’s ash resource. J For 104:118–124. https://doi.org/10.1093/jof/104.3.118
R Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rabaglia RJ, Cognato AI, Hoebeke ER et al (2019) Early Detection and Rapid Response: a 10-year summary of the USDA Forest Service program of surveillance for non-native bark and ambrosia beetles. Am Entomol 65:29–42. https://doi.org/10.1093/ae/tmz015
Saccaggi DL, Karsten M, Robertson MP et al (2016) Methods and approaches for the management of arthropod border incursions. Biol Invasions 18:1057–1075. https://doi.org/10.1007/s10530-016-1085-6
Saul WC, Roy HE, Booy O et al (2017) Assessing patterns in introduction pathways of alien species by linking major invasion data bases. J Appl Ecol 54:657–669. https://doi.org/10.1111/1365-2664.12819
Schebeck M, Hansen EM, Schopf A et al (2017) Diapause and overwintering of two spruce bark beetle species. Physiol Entomol 42:200–210. https://doi.org/10.1111/phen.12200
Seebens H, Bacher S, Blackburn TM et al (2020) Projecting the continental accumulation of alien species through to 2050. Glob Change Biol. https://doi.org/10.1111/gcb.15333
Seebens H, Blackburn TM, Dyer EE et al (2018) Global rise in emerging alien species results from increased accessibility of new source pools. Proc Natl Acad Sci 115:201719429. https://doi.org/10.1073/pnas.1719429115
Sikes BA, Bufford JL, Hulme PE et al (2018) Import volumes and biosecurity interventions shape the arrival rate of fungal pathogens. PLoS Biol 16:1–16. https://doi.org/10.1371/journal.pbio.2006025
Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Syst 40:81–102. https://doi.org/10.1146/annurev.ecolsys.110308.120304
Sinclair JS, Lockwood JL, Hasnain S et al (2020) A framework for predicting which non-native individuals and species will enter, survive, and exit human-mediated transport. Biol Invasions 22:217–231. https://doi.org/10.1007/s10530-019-02086-7
Strutt A, Turner JA, Haack RA, Olson L (2013) Evaluating the impacts of an international phytosanitary standard for wood packaging material: global and United States trade implications. For Policy Econ 27:54–64. https://doi.org/10.1016/j.forpol.2012.11.003
Turner RM, Brockerhoff EG, Bertelsmeier C et al (2021) Worldwide border interceptions provide a window into human-mediated global insect movement. Ecol Appl. https://doi.org/10.1002/eap.2412
Turner RM, Plank MJ, Brockerhoff EG et al (2020) Considering unseen arrivals in predictions of establishment risk based on border biosecurity interceptions. Ecol Appl 30:eap.2194. https://doi.org/10.1002/eap.2194
UK Forestry Commission (2021) Larger eight-toothed European spruce bark beetle (Ips typographus) https://www.gov.uk/guidance/eight-toothed-european-spruce-bark-beetle-ips-typographus. Accessed 16 Nov 2021
Wagenmakers E-J, Farrell S (2004) AIC model selection using Akaike weights. Psychon Bull Rev 11:192–196. https://doi.org/10.3758/BF03206482
Waltz RD, Washington W (1996) European spruce bark beetle (Ips typographus (L.)) interceptions in Indiana 1995. Proc Indiana Acad Sci 105:225–231
Ward SF, Fei S, Liebhold AM (2019) Spatial patterns of discovery points and invasion hotspots of non-native forest pests. Purdue University Research Repository. https://doi.org/10.4231/7YT5-ET33
Wickham H, Averick M, Bryan J et al (2019) Welcome to the Tidyverse. J Open Source Softw 4:1686. https://doi.org/10.21105/joss.01686
Wilson BT, Lister AJ, Riemann RI, Griffith DM (2013) Live tree species basal area of the contiguous United States (2000–2009). Newtown Square, PA: USDA Forest Service, Rocky Mountain Research Station. https://doi.org/10.2737/RDS-2013-0013
Zahradník P, Zahradníková M (2019) Salvage felling in the Czech Republic’s forests during the last twenty years. Cent Eur For J 65:12–20. https://doi.org/10.2478/forj-2019-0008
Zeileis A, Hothorn T (2002) Diagnostic checking in regression relationships. R News 2:7–10
Acknowledgements
The authors thank port inspectors, biosecurity specialists, and insect identifiers that contributed to the collection of invasion pathway data. USDA-APHIS conducted a pre-submission review of this work, through which Tewodros Wakie and two anonymous reviewers provided several helpful comments that improved the manuscript; we thank Barney Caton for facilitating the USDA-APHIS review. Additionally, we thank an anonymous reviewer and Dr. Davina Saccaggi for their insightful reviews and suggestions.
Funding
This research was supported by the National Science Foundation MacroSystems Biology grant 1638702, USDA Forest Service International Programs 21-IG-11132762-241, Grant EVA4.0, No. CZ.02.1.01/0.0/0.0/16_019/0000803 financed by Czech Operational Programme Science, Research, and Education, New Zealand MBIE core funding (C04X1104) to Scion, and the HOMED project (http://homed-project.eu/), which received funding from the European Union’s Horizon 2020 research and innovation program under grant agreement No. 771271. This publication is a contribution of the Mississippi Agricultural and Forestry Experiment Station and based upon work supported by the National Institute of Food and Agriculture, US Department of Agriculture, Hatch project under Accession Number 1025843.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interests
The authors have no relevant financial or non-financial interests to disclose.
Consent to participate
Not applicable.
Consent to publish
Not applicable.
Ethical approval
Not applicable.
Additional information
Communicated by Jon Sweeney.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ward, S.F., Brockerhoff, E.G., Turner, R.M. et al. Prevalence and drivers of a tree-killing bark beetle, Ips typographus (Coleoptera, Scolytinae), in international invasion pathways into the USA. J Pest Sci 96, 845–856 (2023). https://doi.org/10.1007/s10340-022-01559-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-022-01559-4