Journal of Pest Science

, Volume 88, Issue 1, pp 1–7 | Cite as

A pest alien invasion in progress: potential pathways of origin of the brown marmorated stink bug Halyomorpha halys populations in Italy

  • Michele Cesari
  • Lara Maistrello
  • Francesco Ganzerli
  • Paride Dioli
  • Lorena Rebecchi
  • Roberto Guidetti
Rapid Communication


The brown marmorated stink bug, Halyomorpha halys, is an agricultural and household pest native of far East. In the last years, it has spread to and established in countries outside its area of origin, most notably in North America (United States and Canada), causing severe economic losses in agricultural crops. Recently, H. halys has been found in Europe (Switzerland, Germany, France, Hungary, and Greece) and since September 2012, it has also been found in Italy. However, the modalities of introduction and spreading of this pest on the Italian territory are unknown. Tracing back the diffusion modes of the species by analyzing the genetic structure and composition of populations in their initial phase of colonization could be useful also in the view to implement better pest control strategies. The present study aimed to identify the potential pathways of entry of H. halys by detecting the genetic diversity of specimens collected from Northern Italy and Canton Ticino (Southern Switzerland). The analyses of 1,175 base pairs of mtDNA cytochrome c oxidase I and II genes (cox1 and cox2) on 42 specimens led to the identification of four combined haplotypes: one, found in Emilia Romagna region, is the same found in China and North America but never observed before in Europe. The other combined haplotypes are new but consistent in part with haplotypes previously found in Switzerland. Present data indicate that the Italian invasion may have occurred from two different pathways, both from Switzerland and from Asia and/or North America.


Heteroptera Pentatomidae Invasive species Haplotype network Agricultural pest DNA barcoding 



This research was supported by the Grant “Innovative tools and protocols for monitoring and sustainable control of the alien stink bug Halyomorpha halys, a new phytosanitary threat, and of other harmful heteropterans for the fruit crops of the territory of Modena” (2013.065) of “Fondazione Cassa di Risparmio di Modena,” Modena, Italy. We want to thank all the people who provided us the H. halys specimens.

Supplementary material

10340_2014_634_MOESM1_ESM.docx (15 kb)
Table S1 Sequences retrieved from GenBank and BOLD Systems for appropriate comparisons (DOCX 16 kb)
10340_2014_634_MOESM2_ESM.pdf (16 kb)
Table S2 Uncorrected p-distance (below the diagonal) and Kimura 2-parameters (above the diagonal) distances computed among all specimens. The analysis was carried out on 657 bp of cox1 gene (PDF 17 kb)
10340_2014_634_MOESM3_ESM.docx (44 kb)
Table S3 Uncorrected p-distance (below the diagonal) and Kimura 2-parameters (above the diagonal) distances computed among all specimens. The analysis was carried out on 518 bp of cox2 gene (DOCX 44 kb)
10340_2014_634_MOESM4_ESM.docx (19 kb)
Table S4 Uncorrected p-distance (below the diagonal) and Kimura 2-parameters (above the diagonal) distances computed among all specimens. The analysis was carried out on 1,175 bp of both cox1 and cox2 genes (DOCX 20 kb)


  1. Arnold K (2009) Halyomorpha halys (Stål, 1855), eine für die europäische Fauna neu nachgewiesene Wanzenart (Insecta: Heteroptera, Pentatomidae, Pentatominae, Cappaeini). Mitt Thür Entomologenverband e. 16(1):19Google Scholar
  2. Callot H, Brua C (2013) Halyomorpha halys (Stål, 1855), la Punaise diabolique, nouvelle espèce pour la faune de France (Heteroptera Pentatomidae). L’Entomologiste 69(2):69–71Google Scholar
  3. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660Google Scholar
  4. EPPO (2013) First report of Halyomorpha halys in Italy. EPPO Reporting Service, Pest & Diseases 5:10–11Google Scholar
  5. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochromec oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  6. Gariepy TD, Haye T, Fraser H, Zhang J (2014) Occurrence, genetic diversity, and potential pathways of entry of Halyomorpha halys in newly invaded areas of Canada and Switzerland. J Pest Sci 87(1):17–28CrossRefGoogle Scholar
  7. Haye T, Abdallah S, Gariepy T, Wyniger D (2014) Phenology, life table analysis and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys, in Europe. J Pest Sci 87(3):1–12CrossRefGoogle Scholar
  8. Hebert PDN, Cywinska A, Ball SL, DeWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–321Google Scholar
  9. Heckmann R (2012) Erster Nachweis von Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) für Deutschland. Heteropteron 36:17–18Google Scholar
  10. Hoebeke ER, Carter ME (2003) Halyomorpha halys (Stål) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proc Entomol Soc Wash 105:225–237Google Scholar
  11. Kirk H, Dorn S, Mazzi D (2013) Molecular genetics and genomics generate new insights into invertebrate pest invasions. Evol Appl 6(5):842–856CrossRefGoogle Scholar
  12. Lee W, Kang J, Jung C, Hoelmer K, Lee SH, Lee S (2009) Complete mitochondrial genome of brown marmorated stink bug Halyomorpha halys (Hemiptera: Pentatomidae), and phylogenetic relationships of Hemipteran suborders. Mol Cells 28:155–165CrossRefPubMedGoogle Scholar
  13. Lee D-H, Short BD, Joseph SV et al (2013) Review of the biology, ecology, and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea. Environ Entomol 42:627–641CrossRefPubMedGoogle Scholar
  14. Leskey TC, Hamilton GC, Nielsen AL et al (2012) Pest status of the brown marmorated stink bug, Halyomorpha halys in the USA. Outlooks Pest Manag 23:218–226CrossRefGoogle Scholar
  15. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  16. Maistrello L, Dioli P, Bariselli M (2013) Trovata una cimice esotica dannosa per i frutteti. Agricoltura 6:67–68Google Scholar
  17. Maistrello L, Dioli P, Vaccari G et al (2014) Primi rinvenimenti in Italia della cimice esotica Halyomorpha halys, una nuova minaccia per la frutticoltura. Atti Giornate Fitopatologiche CLUEB, Bologna, pp 283–288Google Scholar
  18. Milonas PG, Partsinevelos GK (2014) First report of brown marmorated stink bug Halyomorpha halys Stål (Hemiptera: Pentatomidae) in Greece. EPPO Bull 44(2):183–186CrossRefGoogle Scholar
  19. Pansa MG, Asteggiano L, Costamagna C, Vittone G, Tavella L (2013) First discovery of Halyomorpha halys in peach orchards in Piedmont. L’Informatore Agrario 69(37):60–61Google Scholar
  20. Tamura K, Peterson D, Peterson N, Stechler G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739Google Scholar
  21. USDA-NIFA SCRI (2014) Stop BMSB. Biology, ecology, and management of brown marmorated stink bug in specialty crop. In: Stop BMSB. Accessed 25 Jul 2014
  22. Vétek G, Papp V, Haltrich A, Redei D (2014) First record of the brown marmorated stink bug, Halyomorpha halys (Hemiptera: Heteroptera: Pentatomidae), in Hungary, with description of the genitalia of both sexes. Zootaxa 3780(1):194–200CrossRefPubMedGoogle Scholar
  23. Wermelinger B, Wyniger D, Forster B (2008) First records of an invasive bug in Europe: Halyomorpha halys Stål (Heteroptera: Pentatomidae), a new pest on woody ornamentals and fruit trees? Mitt Schweiz Entomol Ges 81:1–8Google Scholar
  24. Xia X, Xie Z (2001) DAMBE: data analysis in molecular biology and evolution. J Hered 92:371–373CrossRefPubMedGoogle Scholar
  25. Xu J, Fonseca DM, Hamilton GC, Hoelmer KA, Nielsen AL (2014) Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys. Biol Invasions 16(1):153-166Google Scholar
  26. Zhu G, Bu W, Gao Y, Liu G (2012) Potential geographic distribution of brown marmorated stink bug invasion (Halyomorpha halys). PLoS ONE 7(2):e31246CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Michele Cesari
    • 1
  • Lara Maistrello
    • 1
  • Francesco Ganzerli
    • 1
  • Paride Dioli
    • 2
  • Lorena Rebecchi
    • 1
  • Roberto Guidetti
    • 1
  1. 1.Department of Life SciencesUniversity of Modena and Reggio EmiliaModenaItaly
  2. 2.Museo Civico di Storia Naturale di MilanoMilanItaly

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