Genetic diversity of the brown marmorated stink bug Halyomorpha halys in the invaded territories of Europe and its patterns of diffusion in Italy
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.
KeywordsInvasive 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”.
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 was obtained from all individual participants involved in the study.
- Arnold K (2009) Halyomorpha halys (Stål, 1855), eine für die europäische Fauna neu nachgewiesene Wanzenart (Insecta: Heteroptera, Pentatomidae, Pentatominae, Cappaeini). Mitt Thür Entomologenverbande e 16(1):19Google 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(2):69–71Google Scholar
- Dioli P, Leo P, Maistrello L (2016) Prime segnalazioni in Spagna e in Sardegna della specie aliena Halyomorpha halys (Stål, 1855) e note sulla sua distribuzione in Europa (Hemiptera, Pentatomidae). Revta gad Entom 7(1):539–548Google Scholar
- Duthie CD, Michael T, Stephenson B, Yamoah E, McDonald B (2012) Risk analysis of Halyomorpha halys (brown marmorated stink bug) on all pathways. Biosecurity Risk Analysis Group, Ministry of Agriculture and Forestry of New Zealand, WellingtonGoogle Scholar
- Fanfani R, Pieri R (2016) Il sistema agro-alimentare dell’Emilia-Romagna. Rapporto 2015. Unione regionale delle Camere di commercio dell’Emilia-Romagna Regione Emilia-Romagna, Assessorato agricoltura, caccia e pesca, BolognaGoogle Scholar
- Heckmann R (2012) Erster Nachweis von Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) für Deutschland. Heteropteron 36:17–18Google Scholar
- Hoebeke ER, Carter EM (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
- Lee W, Guidetti R, Cesari M, Gariepy TD, Park YR, Park CG (2017) Genetic diversity of Halyomorpha halys (Hemiptera, Pentatomidae) in Korea, comparing with COI sequence dataset of East Asia, Europe, and North America. Fla Entomol (in press) Google Scholar
- Leskey TC, Hamilton GC, Nielsen AL, Polk DF, Rodriguez-Saona C, Bergh JC, Herbert DA, Kuhar TP, Pfeiffer D, Dively GP, Hooks CRR, Raupp MJ, Shrewsbury PM, Krawczyk G, Shearer PW, Whalen J, Koplinka-Loehr C, Myers E, Inkley D, Hoelmer KA, Lee DH, Wright SE (2012) Pest status of the brown marmorated stink bug, Halyomorpha halys in the USA. Outlooks Pest Manag 23:218–226CrossRefGoogle Scholar
- Macavei LI, Bâeţan R, Oltean I, Florian T, Varga M, Costi E, Maistrello L (2015) First detection of Halyomorpha halys Stål, a new invasive species with a high potential of damage on agricultural crops in Romania. Lucrări Ştiinţifice seria Agronomie 58(1):105–108Google Scholar
- MacLellan R (2013) Brown marmorated stink bug: a potential threat to New Zealand. Surveillance (Wellington NZ) 40:3Google Scholar
- Maistrello L, Dioli P, Vaccari G, Nannini R, Bortolotti P, Caruso S, Costi E, Montermini A, Casoli L, Bariselli M (2014) First records in Italy of the Asian stinkbug Halyomorpha halys a new threat to fruit crops. Atti Giornate Fitopatologiche 1:283–288Google Scholar
- Maistrello L, Costi E, Caruso S, Vaccari G, Bortolotti P, Nannini R, Casoli L, Montermini A, Bariselli M, Guidetti R (2016a) Halyomorpha halys in Italy: first results of field monitoring in fruit orchards. Integrated protection of fruit crops subgroups “pome fruit arthropods” and “stone fruits”. IOBC-WPRS Bull 112:1–5Google Scholar
- Maistrello L, Vaccari G, Caruso S, Costi E, Bortolini S, Macavei L, Foca G, Ulrici A, Bortolotti PP, Nannini R, Casoli L, Fornaciari M, Mazzoli GL, Dioli P (2017) Monitoring of the invasive Halyomorpha halys, a new key pest of fruit orchards in northern Italy. J Pest Sci 90:1231–1244CrossRefGoogle Scholar
- Malumphy C (2014) Second interception of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) in Britain. Het News 21:4–5Google Scholar
- Maurel JP, Blaye G, Valladares L, Roinel É, Cochard PO (2016) Halyomorpha halys (Stål, 1855), la punaise diabolique en France, à Toulouse (Heteroptera; Pentatomidae). Carnets Nat 3:21–25Google Scholar
- Mityushev IM (2016) First record of Halyomorpha halys detection in Russia. Zashchitai Karantin Rasteniĭ 3:48Google Scholar
- Moore A (2014) Brown marmorated stink bug Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae). Guam new invasive species alert No. 2014-01. University of Guam, Guam. http://guaminsects.net/anr/sites/default/files/brownMarmoratedStinkBug.pdf
- Nikam KN, More SV (2016) Diversity of Insects from Jangamhatti area, Chandgad, Kolhapur district of Maharashtra. Biolife 4(1):209–212Google Scholar
- Novak SJ, Mack RN (2005) Genetic bottlenecks in alien plant species. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution and biogeography. Sinauer Associates Inc, Sunderland, pp 201–228Google Scholar
- Rabitsch W, Griebe GJ (2015) From the west and from the east? First records of Halyomorpha halys (Stål, 1855) (Hemiptera: Heteroptera: Pentatomidae) in Vorarlberg and Vienna, Austria. Beiträge zur Entomofaunistik 16:115–139Google Scholar
- Rice KB, Troyer RR, Watrous KM, Tooker JF, Fleischer SJ (2016) Landscape factors influencing stink bug injury in Mid-Atlantic tomato fields. J Econ Entomol 110:94–100Google Scholar
- Šeat J (2015) Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) a new invasive species in Serbia. Acta Entomol Serb 20:167–171Google Scholar
- Simov N (2016) The invasive brown marmorated stink bug Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) already in Bulgaria. Ecologica Montenegrina 9:51–53Google Scholar
- Walker K (2009) Brown marmorated stink bug (Halyomorpha halys). Updated on 11/25/2011. http://www.padil.gov.au
- Wallner AM, Hamilton GC, Nielsen AL, Hahn N, Green EJ, Rodriguez-Saona CRR (2014) Landscape factors facilitating the invasive dynamics and distribution of the Brown Marmorated Stink Bug, Halyomorpha halys (Hemiptera: Pentatomidae), after arrival in the United States. PLoS ONE 9(5):e95691CrossRefPubMedPubMedCentralGoogle Scholar
- Ward N (2013) Plants and environment investigation. Surveillance (Wellington NZ) 40:1Google Scholar
- 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
- Wright S (1969) Evolution and genetics of natural populations. The theory of gene frequencies, vol 2. University Chicago Press, ChicagoGoogle Scholar