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The rapid spread of Leptoglossus occidentalis in Europe: a bridgehead invasion

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Abstract

Retracing the routes of invasions and determining the origins of invading species is often critical in understanding biological invasions. The Western conifer seed bug, Leptoglossus occidentalis, an insect native of western North America, was first accidentally introduced to eastern North America and then to Europe. The colonization of the entire European continent occurred in ca. 10–15 years, probably promoted by independent introductions in different parts of Europe. A multi-marker approach (mtDNA and microsatellites) combined with approximate Bayesian computation analyses was used to track the origin of European populations and to determine whether this rapid invasion was caused by multiple introductions. Our results show that at least two independent introductions of L. occidentalis have occurred in Europe. Moreover, the analyses showed a stronger genetic similarity of European invasive populations with the eastern North American populations than with those of the native range, suggesting that invasive North American population acted as a bridgehead for European invasion. The results also revealed that natural dispersal as well as human-mediated transportations as hitchhikers probably enhanced the rapid spread of this invasive pest across Europe. This study illustrates the complexity of a rapid invasion and confirms that bridgehead and multiple introductions have serious implications for the success of invasion.

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References

  • Ahn SJ, Son D, Choo HY, Park CG (2013) The first record on Leptoglossus occidentalis (Hemiptera: Coreidae) in Korea, a potential pest of the pinaceous tree species. J Asia Pac Entomol 16:281–284

    Article  Google Scholar 

  • Aukema B, Libeer R (2007) Eerste waarneming van Leptoglossus occidentalis in België (Heteroptera: Coreidae). Bull Soc R Belg Entomol 143:92–93

    Google Scholar 

  • Aukema JE, Leung B, Kovacs K, Chivers C, Britton KO, Englin J, Frankel SJ, Haight RG, Holmes TP, Liebhold AM, McCullough DG, Bv Holle (2011) Economic impacts of non-native forest insects in the continental United States. PLoS ONE 6(9):e24587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barta M (2016) Biology and temperature requirements of the invasive seed bug Leptoglossus occidentalis (Heteroptera: Coreidae) in Europe. J Pest Sci 89:31–44

    Article  Google Scholar 

  • Bates SL, Borden JH (2005) Life table for Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae) and prediction of damage in lodgepole pine seed orchards. Agric For Entomol 7:145–151

    Article  Google Scholar 

  • Beaumont MA, Zhang WY, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025–2035

    PubMed  PubMed Central  Google Scholar 

  • Ben Jamaa ML, Mejri M, Naves P, Sousa E (2013) Detection of Leptoglossus occidentalis Heidemann, 1910 (Heteroptera: Coreidae) in Tunisia. Afr Entomol 21:165–167

    Article  Google Scholar 

  • Binazzi F, Benassai D, Peverieri GS, Roversi PF (2013) Effects of Leptoglossus occidentalis Heidemann (Heteroptera Coreidae) egg age on the indigenous parasitoid Ooencyrtus pityocampae Mercet (Hymenoptera Encyrtidae). Redia 96:79–84

    Google Scholar 

  • Blatt SE (1994) An unusually large aggregation of the western conifer seed bug, Leptoglossus occidentalis (Hemiptera: Coreidae), in a man-made structure. J Entomol Soc B C 91:71–72

    Google Scholar 

  • Boheemen LA, Lombaert E, Nurkowski KA, Gauffre B, Rieseberg LH, Hodgins KA (2017) Multiple introductions, admixture and bridgehead invasion characterize the introduction history of Ambrosia artemisiifolia in Europe and Australia. Mol Ecol 26:5421–5434

    Article  PubMed  Google Scholar 

  • Boissin E, Hurley B, Wingfield M, Vasaitis R, Stenlid J, Davis C, Groot Pd, Ahumada R, Carnegie A, Goldarazena A (2012) Retracing the routes of introduction of invasive species: the case of the Sirex noctilio woodwasp. Mol Ecol 21:5728–5744

    Article  CAS  PubMed  Google Scholar 

  • Bracalini M, Benedettelli S, Croci F, Terreni P, Tiberi R, Panzavolta T (2013) Cone and seed pests of Pinus pinea: assessment and characterization of damage. J Eco Entomol 106:229–234

    Article  Google Scholar 

  • Cavalli-Sforza LL, Edward AWF (1967) Phylogenetic analysis. Models and estimation procedures. Am J Hum Genet 19:233–257

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    Article  CAS  PubMed  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  CAS  PubMed  Google Scholar 

  • Cornuet JM, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M, Leblois R, Marin J-M, Estoup A (2014) DIYABC v2.0: a software to make approximate Bayesian Computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30:1187–1189

    Article  CAS  PubMed  Google Scholar 

  • Crandall KA, Templeton AR (1993) Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134:959–969

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dempster A, Laird M, Rubin D (1977) Maximum likelihood from incompletedata via the EM algorithm. J R Stat Soc 39:1–38

    Google Scholar 

  • Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449

    Article  CAS  PubMed  Google Scholar 

  • Dusoulier F, Lupoli R, Aberlenc HP, Streito JC (2007) L’invasion orientale de Leptoglossus occidentalis en France: bilan de son extension biogéographique en 2007 (Hemiptera Coreidae). L’Entomologiste 63:303–308

    Google Scholar 

  • Earl DA, Vonholdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: Why, how and so what? Mol Ecol 19:4113–4130

    Article  PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50

    Article  CAS  Google Scholar 

  • Farinha AO, Branco M, Pereira MF, Auger-Rozenberg MA, Maurício A, Yart A, Guerreiro V, Sousa EM, Roques A (2017) Micro X-ray computed tomography suggests cooperative feeding among adult invasive bugs Leptoglossus occidentalis on mature seeds of stone pine Pinus pinea. Agric For Entomol 20:18–27

    Article  Google Scholar 

  • Faúndez EI, Rocca JR (2017) La chinche de las coníferas occidental, Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae) en Chile; rápida expansión, posibles impactos y desafíos. Rev Chil Entomol 42:25–27

    Google Scholar 

  • Fent M, Kment P (2011) First record of the invasive western conifer seed bug Leptoglossus occidentalis (Heteroptera: Coreidae) in Turkey. North West J Zool 7:72–80

    Google Scholar 

  • Gall WK (1992) Further eastern range extension and host records for Leptoglossus occidentalis (Heteroptera: Coreidae): well-documented dispersal of a household nuisance. Great Lakes Entomol 25:159–171

    Google Scholar 

  • Gandhi KJK, Herms DA (2010) North American arthropods at risk due to widespread Fraxinus mortality caused by the alien emerald ash borer. Biol Inv 12:1839–1846

    Article  Google Scholar 

  • Gapon DA (2012) First records of the western conifer seed bug Leptoglossus occidentalis Heid. (Heteroptera, Coreidae) from Russia and Ukraine, regularities in its distribution and possibilities of its range expansion in the Palaearctic region. Entomol Rev 93:174–181

    Article  Google Scholar 

  • Gapon DA (2015) First record of Leptoglossus occidentalis (Heteroptera: Coreidae) in Morocco. Heteropterus Rev Entomol 15:161–163

    Google Scholar 

  • Garnas JR, Auger-Rozenberg M-A, Roques A, Bertelsmeier C, Wingfield MJ, Saccaggi DL, Roy HE, Slippers B (2016) Complex patterns of global spread in invasive insects: eco-evolutionary and management consequences. Biol Inv 18:935–952

    Article  Google Scholar 

  • Goudet J (2002) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). Updated from Goudet (1995). Available from http://www2.unil.ch/popgen/softwares/fstat.htm

  • Guillemaud T, Beaumont MA, Ciosi M, Cornuet JM, Estoup A (2010) Inferring introduction routes of invasive species using approximate Bayesian computation on microsatellite data. Heredity 104:88–99

    Article  CAS  PubMed  Google Scholar 

  • Harry M, Solignac M, Lachaise D (1998) Molecular evidence for parallel evolution of adaptative syndromes in fig-breeding Lissocephala (Drosophilidae). Mol Phylogenet Evol 9:542–551

    Article  CAS  PubMed  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332

    Article  PubMed  PubMed Central  Google Scholar 

  • Ishikawa T, Kikuhara Y (2009) Leptoglossus occidentalis Heidemann (Hemiptera: Coreidae), a presumable recent invader to Japan. Jpn J Entomol 12:115–116

    Google Scholar 

  • Javal M, Roques A, Haran J, Hérard F, Keena M, Roux G (2017) Complex invasion history of the Asian long-horned beetle: fifteen years after first detection in Europe. J Pest Sci. https://doi.org/10.1007/s10340-017-0917-1.

    Article  Google Scholar 

  • Jermiin LS, Crozier RH (1994) The cytochrome b region in the mitochondrial DNA of the ant Tetraponera rufoniger: sequence divergence in Hymenoptera may be associated with nucleotide content. J Mol Evol 38:282–294

    Article  CAS  PubMed  Google Scholar 

  • Juliano SA, Lounibos LP (2005) Ecology of invasive mosquitoes: effects on resident species and on human health. Ecol Lett 8:558–574

    Article  PubMed  PubMed Central  Google Scholar 

  • Kenis M, Branco M (2010) Impact of alien terrestrial arthropods in Europe. In: Roques A, Kenis M, Lees D et al (eds) Alien terrestrial arthropods of Europe. Pensoft, Sofia, pp 51–71

    Google Scholar 

  • Kenis M, Roques A, Santini A, Liebhold AM (2017) Impact of non-native invertebrates and pathogens on market forest tree resources. In: Vila M, Hulme PE (eds) Impact of biological invasions on ecosystem services. Springer, Cham, pp 103–117

    Chapter  Google Scholar 

  • Kirk H, Dorn S, Mazzi D (2013) Molecular genetics and genomics generate new insights into invertebrate pest invasions. Evol Appl 6:842–856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koerber TW (1963) Leptoglossus occidentalis (Hemiptera, Coreidae), a newly discovered pest of coniferous seed. An Entomol Soc Am 56:229–234

    Article  Google Scholar 

  • Langella O (1999) Populations, Ver. 1.2.3. a population genetic software. Available from: http://bioinformatics.org/~tryphon/populations/

  • Lesieur V (2014) Invasion de la punaise américaine Leptoglossus occidentalis en Europe: une contribution à la compréhension des invasions fulgurantes. Dissertation, University of Orléans

  • Lesieur V, Courtial B, Roques A, Auger-Rozenberg MA (2014a) Isolation and characterization of 11 polymorphic microsatellite markers in the highly invasive Western conifer seed bug, Leptoglossus occidentalis (Heteroptera, Coreidae). Conserv Genet Resour 6:617–619

    Article  Google Scholar 

  • Lesieur V, Yart A, Guilbon S, Lorme P, Auger-Rozenberg M-A, Roques A (2014b) The invasive Leptoglossus seed bug, a threat for commercial seed crops, but for conifer diversity? Biol Inv 16:1833–1849

    Article  Google Scholar 

  • Lombaert E, Guillemaud T, Cornuet J-M, Malausa T, Facon B, Estoup A (2010) Bridgehead effect in the worldwide Invasion of the biocontrol Harlequin ladybird. PLoS ONE 5:e9743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lombaert E, Guillemaud T, Lundgren J, Koch R, Facon B, Grez A, Loomans A, Malausa T, Nedved O, Rhule E (2014) Complementarity of statistical treatments to reconstruct worldwide routes of invasion: the case of the Asian ladybird Harmonia axyridis. Mol Ecol 23:5979–5997

    Article  PubMed  Google Scholar 

  • Malumphy C, Botting J, Bantock T, Reid S (2008) Influx of Leptoglossus occidentalis Heidemann (Coreidae) in England. Het News 2:7–9

    Google Scholar 

  • McPherson JE, Packauskas RJ, Taylor SJ, O’Brien MF (1990) Eastern range extension of Leptoglossus occidentalis with a key to Leptoglossus species of America north of Mexico (Heteroptera:Coreidae). Great Lakes Entomol 23:99–104

    Google Scholar 

  • Niccoli A, Benassai D, Croci F, Roversi P (2009) Anastatus bifasciatus ooparassitoide di Leptoglossus occidentalis. In: Proceedings XXII Congresso Nazionale Italiano di Entomologia

  • Paap T, Burgess TI, Wingfield MJ (2017) Urban trees: bridge-heads for forest pest invasions and sentinels for early detection. Biol Inv 19:3515–3526

    Article  Google Scholar 

  • Page RDC (1996) Tree view: an application to display phylogenetic trees on personal computers. Bioinformatics 12:357–358

    Article  CAS  Google Scholar 

  • Pérez Valcárcel J, Prieto Piloña F (2010) La contribución de registros fotográficos en internet para estudios faunísticos: el caso de la expansión iberobalear de la especie invasora Leptoglossus occidentalis Heidemann, 1910 (Hemiptera, Coreidae). Arq Entomol 4:45–52

    Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

  • Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rabitsch W, Heiss E (2005) Leptoglossus occidentalis Heidemann, 1910, eine amerikanische Adventivart auch in Österreich aufgefunden (Heteroptera: Coreidae). Berichte des naturwissenschaftlich-medizinischen Verein Innsbruck 92:131–135

    Google Scholar 

  • Ribes J, Escolà O (2005) Leptoglossus occidentalis Heidemann, 1910, a Nearctic bug (Hemiptera, Heteroptera, Coreidae) found in Catalonia, Spain. Sessio Conjucta d’Entomologia ICHN-SCL 13:47–50

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–226

    Article  PubMed  Google Scholar 

  • Ridge-O’Connor GE (2001) Distribution of the western conifer seed bug, Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae) in Connecticut and parasitism by a tachinid fly, Trichopoda pennipes (F.) (Diptera: Tachinidae). Proc Entomol Soc Wash 103:364–366

    Google Scholar 

  • Rius M, Darling JA (2014) How important is intraspecific genetic admixture to the success of colonising populations? Trends Ecol Evol 29:233–242

    Article  PubMed  Google Scholar 

  • Roques A (2010) Taxonomy, time and geographic patterns. In: Roques A, Kenis M, Lees D et al (eds) Alien terrestrial arthropods of Europe. Pensoft, Sofia, pp 11–26

    Google Scholar 

  • Roques A, Auger-Rozenberg M-A, Blackburn TM, Garnas J, Pyšek P, Rabitsch W, Richardson DM, Wingfield MJ, Liebhold AM, Duncan RP (2016) Temporal and interspecific variation in rates of spread for insect species invading Europe during the last 200 years. Biol Inv 18:907–920

    Article  Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Rossi J-P, Garcia J, Roques A, Rousselet J (2016a) Trees outside forests in agricultural landscapes: spatial distribution and impact on habitat connectivity for forest organisms. Landsc Ecol 31:243–254

    Article  Google Scholar 

  • Rossi J-P, Imbault V, Lamant T, Rousselet J (2016b) A citywide survey of the pine processionary moth Thaumetopoea pityocampa spatial distribution in Orléans (France). Urban For Urban Green 20:71–80

    Article  Google Scholar 

  • Rousset F (2008) GENEPOP ‘ 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Schaffner JC (1967) The occurrence of Theognis occidentalis in the midwestern United States (Hemiptera; Coreidae). J Kansas Entomol Soc 40:141–142

    Google Scholar 

  • Scudder G (2008) New provincial and state records for Heteroptera (Hemiptera) in Canada and the United States. J Entomol Soc B C 105:3–18

    Google Scholar 

  • Seebens H, Blackburn TM, Dyer EE, Genovesi P, Hulme PE, Jeschke JM, Pagad S, Pyšek P, Winter M, Arianoutsou M (2017) No saturation in the accumulation of alien species worldwide. Nat Commun 8:14435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Evol Syst 40:81–102

    Article  Google Scholar 

  • Simov N (2008) Western conifer seed bug, Leptoglossus occidentalis Heidemann, 1910 (Heteroptera: Coreidae) already in Bulgaria. Hist Nat Bulgarica 19:179–180

    Google Scholar 

  • Strong W (2016) Lodgepole pine seedset increase by mesh bagging is due to Leptoglossus occidentalis (Hemiptera: Coreidae) exclusion. J Entomol Soc B C 112:3–18

    Google Scholar 

  • Tamburini M, Maresi G, Salvadori C, Battisti A, Zottele F, Pedrazzoli F (2012) Adaptation of the invasive western conifer seed bug Leptoglossus occidentalis to Trentino, an alpine region (Italy). Bull Insectol 65:161–170

    Google Scholar 

  • Taylor SJ, Tescari G, Villa M (2001) A nearctic pest of pinaceae accidentally introduced into Europe: Leptoglossus occidentalis (Heteroptera : Coreidae) in northern Italy. Entomol News 112:101–103

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van der Heyden T (2018) First record of Leptoglossus occidentalis Heidemann, 1910 (Hemiptera: Heteroptera: Coreidae: Coreinae: Anisoscelini) in the Golan Heights. Rev Gaditana Entomol 9:1–3

    Google Scholar 

  • Westphal MI, Browne M, MacKinnon K, Noble I (2008) The link between international trade and the global distribution of invasive alien species. Biol Inv 10:391–398

    Article  Google Scholar 

  • Zhu WB (2010) Exotic coreid bugs introduced into China. In: Proceeding of the 4th meeting of the international heteropterist’s society. Nankai University, Tianjin, China, July 12–17, 2010, Nankai University, Tianjin, p 71

  • Zhu G-P, Rédei D, Kment P, Bu W-J (2013) Effect of geographic background and equilibrium state on niche model transferability: predicting areas of invasion of Leptoglossus occidentalis. Biol Inv 16:1069–1081

    Article  Google Scholar 

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Acknowledgements

We are indebted to C. Carvalho and N. Gillette (Institute of Forest Genetics, Placerville, USA), N. Wihelmi (Washington Department of Natural Resources, USA), B. Slonecker and S. Cook (University of Idaho, USA), K. Gibson and A. Gannon (Montana Department of Natural Resources and Conservation, USA), J. Egan, S. Kegley, T. Steel and B. Steed (USDA Forest Service, USA), W. Cranshaw (Colorado State University, USA), R. Campos (Universidad Autonoma Chapingo), H. Russell (Michigan State University, USA), J. Hahn (University of Minnesota, USA), S. Passoa (APHIS—USDA, Ohio State University, USA), C. Sclar and B. Landhuis (Longwood Gardens Inc., USA), O. Lonsdale (Agriculture and Agri-Food Canada, Ottawa, Canada), J. Sweeney (Natural Resources Canada Canadian Forest Service, Canada), M. Giroux (Insectarium de Montreal, Canada), C. Briet (Vivarmor, France), C. Brua (Société Alsacienne d’Entomologie, France), C. Blazy (ONF, France), C. Kerdelhué (CBGP, France), E. de Sousa (National Institute of Biological Resources, Portugal), M. Á. Gómez de Dios (Agencia de Medio Ambiente y Agua de Andalucía, Spain), Antonio Muñoz Risueño (Spain), G. Sanchez Peña (ICP Forest, Spain), S. Chiesa (Italy), A. Battisti (University of Padova, Italy), C. Stauffer (University of Natural Resources and Applied Life Sciences, Vienna, Austria) N. Simov (National Museum of Natural History, Sofia, Bulgaria), M. Düzbastilar (University of Izmir, Turkey), G. Popov and A. Gubin (Donetsk Botanical Garden, Ukraine) and D. Musolin (University of Saint Petersburg, Russia) who provided bug samples. We greatly acknowledge support from the European project ISEFOR (Increasing Sustainability of European Forests: Modelling for Security Against Invasive Pests and Pathogens under Climate Change—collaborative project 245268), Cost action PERMIT (Pathway Evaluation and pest Risk Management In Transport) and the French Ministry of Agriculture, Food, Fisheries, Rural Affairs and Spatial Planning (convention DGFAR 01/09). We gratefully thank C. Bertheau (University of Franche-Comté, France) and J. Rousselet (INRA, Orléans) for their helpful advices. We are grateful to T. Bourgeois and C. Courtin for technical assistance. We thank S. Raghu (CSIRO Brisbane) and A. Sheppard (CSIRO Canberra) for their comments and suggestions on an early version of the manuscript. We also thank three anonymous reviewers for their helpful comments.

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  1. V. Lesieur

    Present address: Montpellier-SupAgro, UMR CBGP, 755 Avenue du Campus Agropolis, 34980, Montferrier sur Lez, France

  2. V. Lesieur

    Present address: CSIRO European Laboratory, 830, Avenue du Campus Agropolis, 34980, Montferrier sur Lez, France

Authors and Affiliations

  1. INRA UR633 Zoologie Forestière, 2163 Avenue de la pomme de pin, CS 40001 Ardon, 45075, Orléans Cedex 2, France

    V. Lesieur, B. Courtial, A. Roques & M.-A. Auger-Rozenberg

  2. INRA, CNRS, Université Côte d’Azur, ISA, 400 Route des Chappes, BP 167-06903, Sophia Antipolis Cedex, France

    E. Lombaert & T. Guillemaud

  3. BC Ministry of Forests, Lands, Mines and Natural Resource Operations, Kalamalka Forestry Centre, 3401 Reservoir Rd, Vernon, BC, V1B 2C7, Canada

    W. Strong

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Likewise, collection on public lands was conducted in compliance with existing regulations for insects defined as non-commercial, as determined by local offices. Furthermore, for sampling carried out on private lands, we had permission from the owners. Additionally, these field studies did not involve endangered or protected species.

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Special Issue on Invasive Pests of Forests and Urban Trees.

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Lesieur, V., Lombaert, E., Guillemaud, T. et al. The rapid spread of Leptoglossus occidentalis in Europe: a bridgehead invasion. J Pest Sci 92, 189–200 (2019). https://doi.org/10.1007/s10340-018-0993-x

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