Biological Invasions

, Volume 20, Issue 4, pp 1073–1092 | Cite as

Genetic diversity of the brown marmorated stink bug Halyomorpha halys in the invaded territories of Europe and its patterns of diffusion in Italy

  • Michele Cesari
  • Lara Maistrello
  • Lucia Piemontese
  • Raoul Bonini
  • Paride Dioli
  • Wonhoon Lee
  • Chang-Gyu Park
  • Georgios K. Partsinevelos
  • Lorena Rebecchi
  • Roberto Guidetti
Original Paper


Halyomorpha halys is an invasive stink bug pest originating from East Asia. In Europe, it was first detected in Switzerland in 2004. It is now present in thirteen countries, and seems to be spreading throughout the continent. In Italy, where it has been recorded since 2012, other than being an urban nuisance, it is causing severe damage in commercial fruit orchards. An integrated approach, using current and previous observational data in space and time and molecular information, was used to identify the genetic diversity of this pest in Europe, its invasion history, and the potential pathways of entry and diffusion. The analysis of 1175 bp of mitochondrial DNA cytochrome c oxidase I and II genes (cox1, cox2) led to the identification of twenty previously unknown haplotypes. The European distribution of H. halys is the result of multiple invasions that are still in progress, and, in some cases, it was possible to identify the specific Asian areas of origin. Moreover, secondary invasions could have occurred among European countries by a bridgehead effect. In Italy, the data were more clearly related to their temporal occurrence, allowing for a clearer reading of the patterns of invasion and dispersion. After having successfully established in localized areas, H. halys further expanded its range by an active dispersion process and/or by jump dispersal events due to passive transport. The multiple introductions from different areas of the native range together with the different patterns of diffusion of H. halys, may hamper the pest management strategies for its containment.


Invasive species Haplotype network Agricultural pest Jump dispersal Multiple invasions 



The authors wish to thank Wen-Jun Bu and Zhen Ye (Nankai University, China) for kindly supplying the geographical information for Chinese specimens. We are also indebted to Prof. Aparna Palmer (Colorado Mesa University) for the English revision and her valuable suggestions. The authors wish to thank two anonymous reviewers, whose suggestions helped to improve the manuscript. We are grateful to the following people/groups for providing H. halys specimens: Ronni Paolinelli, Gruppo Modenese Scienze Naturali, M. Agosti, L. Mola, M. Salvetti, Moreno Dutto, researchers, students and trainees of UNIMORE-UNIMI-UNITO-UNIPD, technicians and employees of regional and provincial Plant Protection Services and other institutions (SF-Emilia Romagna, Consorzi Fitosanitari MO-RE-PR-PC, Consorzio Agrario di Ravenna, ASTRA, SF-Bolzano, FEM, SF-Veneto, ERSAF Friuli Venezia Giulia, APOFRUIT, SF-Ticino, CREA), Martino Salvetti (Fondazione Fojanini di Studi Superiori, Sondrio, Italy), Maurizio Pavesi (Museo Civico di Storia Naturale, Milano, Italy), Piero Leo (Cagliari, Italy), Livio Mola (Brescia, Italy)), Moreno Dutto (Azienda sanitaria, Cuneo), Stefano Turolo (Monza, Italy), Alida Piglia (Milano, Italy) for providing specimens. Funding for the research was supported by the ‘Fondazione Cassa di Risparmio di Modena’, grant 2013.0665 “Innovative tools and protocols for monitoring and sustainable control of the alien stink bug H. halys, a new phytosanitary threat, and of other harmful heteropterans for the fruit crops of the territory of Modena”.

Authors’ contributions

MC and RG conceived and designed the research. MC, LP and RB conducted the experiments. LM, PD, GKP collected and identified the specimens. WL and PC provided the sequences and geographical information of Korean and U.S. specimens. MC and LP analysed the data. RG, LR and LM provided the research funds. RG, LR, LP, LM and MC wrote the manuscript. All authors read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animals rights

This research did not contain any studies with human participants or animals (vertebrates) performed by any of the authors.

Informed consent

Informed consent was obtained from all individual participants involved in the study.

Supplementary material

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Supplementary material 1 (DOCX 43 kb)
10530_2017_1611_MOESM2_ESM.docx (34 kb)
Supplementary material 2 (DOCX 33 kb)
10530_2017_1611_MOESM3_ESM.docx (18 kb)
Supplementary material 3 (DOCX 18 kb)


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Copyright information

© Springer International Publishing AG, part of Springer Nature 2017

Authors and Affiliations

  • Michele Cesari
    • 1
  • Lara Maistrello
    • 1
  • Lucia Piemontese
    • 1
  • Raoul Bonini
    • 1
  • Paride Dioli
    • 2
  • Wonhoon Lee
    • 3
  • Chang-Gyu Park
    • 4
  • Georgios K. Partsinevelos
    • 5
  • 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
  3. 3.Department of Plant Medicine and Institute of Agriculture and Life ScienceGyeongsang National UniversityJinjuRepublic of Korea
  4. 4.Crop Protection Division, Department of Crop Life SafetyNational Academy of Agricultural ScienceWanjuRepublic of Korea
  5. 5.Department of Entomology and Agricultural ZoologyBenaki Phytopathological InstituteKifissiaGreece

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