Skip to main content

Advertisement

Log in

Occurrence, genetic diversity, and potential pathways of entry of Halyomorpha halys in newly invaded areas of Canada and Switzerland

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

Halyomorpha halys has recently established in countries outside of its Asian area of origin. In the North Eastern USA, this pest causes severe economic loss in agricultural crops. Breeding populations have been confirmed in Switzerland and Canada; however, their pathways of entry and genetic diversity remain unknown. To determine invasion pathways and source population(s), the diversity of specimens from Asia, North America, and Europe was investigated. Genetic diversity in Asia was higher than that in the Canada and Switzerland. Although three haplotypes were detected among Canadian H. halys, one haplotype dominated. In contrast, two out of three haplotypes were found frequently among Swiss samples. Based on molecular data and interception records it appears likely that H. halys in Canada is derived from the movement of established US populations. Further, North American populations likely originated from the Hebei/Beijing regions of China. The area of origin of the Swiss samples remains unclear. Although the dominant haplotype in Switzerland was consistent with Asian samples collected in the Hebei and Beijing provinces, it was not the dominant haplotype in these regions and further sampling is necessary to its confirm the distribution and abundance in the area of origin. The remaining two haplotypes were unique to Switzerland and no matches were found among our Asian samples. Interestingly, no haplotypes were shared between the North American and Swiss samples, indicating that the two invasions were separate and distinct events and did not result from the movement of goods and materials between USA and Europe.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aldrich JR, Khrimian A, Chen X, Camp MJ (2009) Semiochemically based monitoring of the invasion of the brown marmorated stink bug and unexpected attraction of the native green stink bug (Heteroptera: Pentatomidae) in Maryland. Fla Entomol 92:483–491

    Article  CAS  Google Scholar 

  • Arnold K (2009) Halyomorpha halys (Stål, 1855), eine für die europäische Fauna neu nachgewiesene Wanzenart (Insecta: Heteroptera: Pentatomidae: Cappaeini). Mitt Thüringer Entomol 16:19

    Google Scholar 

  • Auger-Rozenberg MA, Boivin T, Magnoux E, Courtin C, Roques A, Kerdelhué C (2012) Inferences on population history of a seed chalcid wasp: invasion success despite a severe founder effect from an unexpected source population. Mol Ecol 21:6086–6103

    Article  PubMed  Google Scholar 

  • Australian Department of Agriculture, Fisheries and Forestry (2012a) Operational science program bulletin December 2011/January 2012. http://www.daff.gov.au/__data/assets/pdf_file/0004/2160481/PDF_version_Jan_2012_OSP_Bulletin.pdf. Accessed 21 Jan 2013

  • Australian Department of Agriculture, Fisheries and Forestry (2012b) Operational science program bulletin February 2012. http://www.daff.gov.au/__data/assets/pdf_file/0007/2160817/osp-bulletin-feb12.pdf. Accessed 21 Jan 2013

  • Avise JC (1995) Mitochondrial DNA polymorphism and a connection between genetics and demography of relevance to conservation. Conserv Biol 9:686–690

    Article  Google Scholar 

  • Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522

    Google Scholar 

  • Barr NB (2009) Pathway analysis of Ceratitis capitata (Diptera: Tephritidae) using mitochondrial DNA. J Econ Entomol 102:401–411

    Article  CAS  PubMed  Google Scholar 

  • Blanchet S (2012) The use of molecular tools in invasion biology: an emphasis on freshwater ecosystems. Fish Manag Ecol 19:120–132

    Article  Google Scholar 

  • Callot H, Brua C (2013) Halyomorpha halys (Stål, 1855), la Punaise diabolique, nouvelle espèce pour la faune de France (Heteroptera Pentatomidae). L’Entomologiste 69:69–71

    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 

  • Corin SE, Lester PJ, Abbott KL, Ritchie PA (2007) Inferring historical introduction pathways with mitochondrial DNA: the case of introduced Argentine ants (Linepithema humile) into New Zealand. Divers Distrib 13:510–518

    Article  Google Scholar 

  • Cuituan Z, Daluan L, Haifeng S, Guoliang X (1993) A study on the biological characteristics of Halyomorpha picus and Erthesina fullo. For Res 3:5

    Google Scholar 

  • deLeón JH, Sétamou M, Gastaminza GA, Buenahora J, Cáceres S, Yamamoto PT, Bouvet JP, Logarzo GA (2011) Two separate introductions of Asian citrus psyllid populations found in the American continents. Ann Entomol Soc Am 104:1392–1398

    Article  Google Scholar 

  • Duthie C (2012) Risk analysis of Halyomorpha halys (Brown Marmorated Stink Bug) on all pathways. Ministry for Primary Industries, Wellington, p 57

    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  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

    CAS  Google Scholar 

  • Fogain R, Graff S (2011) First records of the invasive pest, Halyomorpha halys (Hemiptera: Pentatomidae), in Ontario and Quebec. J Entomol Soc Ont 142:45–48

    Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Franks SJ, Pratt PD, Tsutsui ND (2011) The genetic consequences of a demographic bottleneck in an introduced biological control insect. Conserv Genet 12:201–211

    Article  Google Scholar 

  • Freers A (2012) Blinde Passagiere: Stinkwanzen, Marmorierte Baumwanze–Halyomorpha halys. https://ssl.bremen.de/lmtvet/sixcms/media.php/13/Blinde_Passagiere_Stinkwanze_3_2012.pdf. Accessed 11 March 2013

  • Funayama K (2003) Outbreak and control of stink bugs in apple orchard. Jpn Agric Technol 47:35–39

    Google Scholar 

  • Grapputo A, Boman S, Lindstroem L, Lyytinen A, Mappes J (2005) The voyage of an invasive species across continents: genetic diversity of North American and European Colorado potato beetle populations. Mol Ecol 14:4207–4219

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa H, Umeya K (1974) Outbreak of stink bugs in fruit trees. Plant Prot 28:279–286

    Google Scholar 

  • Haye T, Wyniger D (2013) Current distribution of Halyomorpha halys in Europe. http://www.halyomorphahalys.com. Accessed April 2013

  • He YB, Wan XW, Liu YH, Sun GM, Zhan RL (2012) Mitochondrial COI from Dysmicoccus brevipes (Hemiptera: Pseudococcidae) suggests cryptic lineage and pinpoints the source of the introduction to China. Fla Entomol 95:183–191

    Article  CAS  Google Scholar 

  • Heckmann R (2012) Erster Nachweis von Halyomorpha halys (STÅL, 1855) (Heteroptera: Pentatomidae) für Deutschland. Heteropteron 36:17–18

    Google Scholar 

  • Hoebeke ER, Carter ME (2003) Halyomorpha halys (Stål) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. P Entomol Soc Wash 105:225–237

    Google Scholar 

  • Hoelmer KA, Kirk AA (2005) Selecting arthropod biological control agents against arthropod pests: can the science be improved to decrease the risk of releasing ineffective agents? Biol Control 34:255–264

    Article  Google Scholar 

  • Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18

    Article  Google Scholar 

  • Hulme PE, Bacher S, Kenis M, Klotz S, Kühn I, Minchin D, Nentwig W, Olenin S, Panov V, Pergl J (2008) Grasping at the routes of biological invasions: a framework for integrating pathways into policy. J Appl Ecol 45:403–414

    Article  Google Scholar 

  • Kaňuch P, Berggren Å, Cassel-Lundhagen A (2012) Colonization history of Metrioptera roeselii in northern Europe indicates human-mediated dispersal. J Biogeogr 40:977–987

    Google Scholar 

  • Kavar T, Pavlovcic P, Susnik S, Meglic V, Virant-Doberlet M (2006) Genetic differentiation of geographically separated populations of the southern green stink bug Nezara viridula (Hemiptera: Pentatomidae). Bull Entomol Res 96:117–128

    Article  CAS  PubMed  Google Scholar 

  • Leskey TC, Short BD, Butler BR, Wright SE (2012a) Impact of the invasive brown marmorated stink bug, Halyomorpha halys (Stål), in Mid-Atlantic tree fruit orchards in the United States: case studies of commercial management. Psyche 2012:1–14

    Article  Google Scholar 

  • Leskey TC, Wright SE, Short BD, Khrimian A (2012b) Development of behaviorally based monitoring tools for the brown marmorated stink bug, Halyomorpha halys (Stål)(Heteroptera: Pentatomidae) in commercial tree fruit orchards. J Entomol Sci 47:76–85

    Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Mayr E (1954) Change of genetic environment and evolution. In: Huxley J, Hardy A, Ford E (eds) Evolution as a process. Allen and Unwin, London, pp 157–180

    Google Scholar 

  • Miller N, Estoup A, Toepfer S, Bourguet D, Lapchin L, Derridj S, Kim KS, Reynaud P, Furlan L, Guillemaud T (2005) Multiple transatlantic introductions of the western corn rootworm. Science 310:992

    Article  CAS  PubMed  Google Scholar 

  • Mueller G, Luescher IL, Schmidt M (2011) New data on the incidence of household arthropod pests and new invasive pests in Zurich (Switzerland). In: Proceedings of the seventh international conference on urban pests: 99–104

  • Muraji M, Kawasaki K, Shimizu T (2000) Phylogenetic utility of nucleotide sequences of mitochondrial 16S ribosomal RNA and cytochrome b genes in anthocorid bugs (Hemiptera: Anthocoridae). Appl Entomol Zool 35:293–300

    Article  CAS  Google Scholar 

  • Nielsen AL (2011) Invasion biology and seasonality of BMSB in Pennsylvania and New Jersey (presentation 0020). In: Proceedings of the 59th annual meeting of the entomological society of America, 13–16 Nov 2011

  • Nielsen AL, Hamilton GC (2009a) Life history of the invasive species Halyomorpha halys (Hemiptera: Pentatomidae) in Northeastern United States. Ann Entomol Soc Am 102:608–616

    Article  Google Scholar 

  • Nielsen AL, Hamilton GC (2009b) Seasonal occurrence and impact of Halyomorpha halys (Hemiptera: Pentatomidae) in tree fruit. J Econ Entomol 102:1133–1140

    Article  PubMed  Google Scholar 

  • Nielsen AL, Hamilton GC, Shearer PW (2011) Seasonal phenology and monitoring of the non-native Halyomorpha halys(Stål) (Hemiptera: Pentatomidae) in soybean. Environ Entomol 40:231–238

    Article  Google Scholar 

  • Park D-S, Foottit R, Maw E, Hebert PDN (2011) Barcoding bugs: DNA-based identification of the true bugs (Insecta: Hemiptera: Heteroptera). PloS One 6:e18749

  • Piel F, Gilbert M, De Cannière C, Grégoire JC (2008) Coniferous round wood imports from Russia and Baltic countries to Belgium. A pathway analysis for assessing risks of exotic pest insect introductions. Divers Distrib 14:318–328

    Article  Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

  • Sax DF, Brown JH (2000) The paradox of invasion. Global Ecol Biogeogr 9:363–371

    Article  Google Scholar 

  • Smith KF, Stefaniak L, Saito Y, Gemmill CEC, Cary SC, Fidler AE (2012a) Increased inter-colony fusion rates are associated with reduced COI haplotype diversity in an invasive colonial ascidian Didemnum vexillum. PLoS One 7:e30473

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Smith KF, Thia J, Gemmill CEC, Cary SC, Fidler AE (2012b) Barcoding of the cytochrome oxidase I (COI) indicates a recent introduction of Ciona savignyi into New Zealand and provides a rapid method for Ciona species discrimination. Aquat Invasions 7:305–313

    Article  Google Scholar 

  • Song H, Buhay JE, Whiting MF, Crandall KA (2008) Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proc Natl Acad Sci USA 105:13486–13491

    Article  CAS  PubMed  Google Scholar 

  • Stephens JD, Santos SR, Folkerts DR (2011) Genetic Differentiation, structure, and a transition zone among populations of the pitcher plant moth Exyra semicrocea: implications for conservation. PLoS One 6:e22658

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Szűcs M, Eigenbrode SD, Schwarzländer M, Schaffner U (2012) Hybrid vigor in the biological control agent, Longitarsus jacobaeae. Evol Appl 5:489–497

    Article  PubMed Central  PubMed  Google Scholar 

  • Teske PR, Rius M, McQuaid CD, Styan CA, Piggott MP, Benhissoune S, Fuentes-Grünewald C, Walls K, Page M, Attard CRM (2011) “Nested” cryptic diversity in a widespread marine ecosystem engineer: a challenge for detecting biological invasions. BMC Evol Biol 11:1–13

    Article  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Walker K (2009) Brown marmorated stink bug (Halyomorpha halys). PaDIL. http://www.padil.gov.au. Accessed 21 Jan 2013

  • Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506

    CAS  PubMed  Google Scholar 

  • Watanabe M, Arakawa R, Shinagawa Y, Okazawa T (1994) Anti-invading methods against the brown marmorated stink bug, Halyomorpha mista, in houses. Jpn J Sanit Zool 45:311–317

    Google Scholar 

  • Wermelinger B, Wyniger D, Forster B (2008) First records of an invasive bug in Europe: Halyomorpha halys Stal (Heteroptera: Pentatomidae), a new pest on woody ornamentals and fruit trees? Mitt Schweiz Entomol Ges 81:1–8

    Google Scholar 

  • Wyniger D, Kment P (2010) Key for the separation of Halyomorpha halys (Stål) from similar-appearing pentatomids (Insecta: Heteroptera: Pentatomidae) occurring in Central Europe, with new Swiss records. Mitt Schweiz Entomol Ges 83:261–270

    Google Scholar 

  • Xu J, Fonseca DM, Hamilton GC, Hoelmer KA, Nielsen AL (2013) Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys. Biol Invasions (in press)

  • Zhu G, Bu W, Gao Y, Liu G (2012) Potential geographic distribution of brown marmorated stink bug invasion (Halyomorpha halys). PLoS One 7:e31246

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful to all Swiss homeowners who kindly provided us with specimens, particularly A. Knup, A. Six, R. Burtscher, W. and T. Rüesch, E. Roschet, and K. Häberlin. We would like to thank the team of the MoA-CABI Joint Lab for Biosafety for their assistance and Dr. Y. Lu for kindly giving us access to his light traps at the Langfang Experimental Station. The authors would like to thank Allison Bruin for technical assistance, and the Canadian Food Inspection Agency and the Canadian National Collection, particularly O. Lonsdale, for providing intercepted specimens in shipments and cargo.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. D. Gariepy.

Additional information

Communicated by M. Traugott.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 120 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gariepy, T.D., Haye, T., Fraser, H. et al. Occurrence, genetic diversity, and potential pathways of entry of Halyomorpha halys in newly invaded areas of Canada and Switzerland. J Pest Sci 87, 17–28 (2014). https://doi.org/10.1007/s10340-013-0529-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-013-0529-3

Keywords

Navigation