Skip to main content
Log in

Range expansion of the invasive brown marmorated stinkbug, Halyomorpha halys: an increasing threat to field, fruit and vegetable crops worldwide

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

Abstract

The brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae), has emerged as a harmful invasive insect pest in North America and Europe in the 1990s and 2000s, respectively. Native to eastern Asia, this highly polyphagous pest (>120 different host plants) is spreading rapidly worldwide, notably through human activities. The increasing global importance of the pest suggests that more coordinated actions are needed to slow its spread and mitigate negative effects in invaded areas. Prevention of large-scale outbreaks will require accurate identification and effective mitigation tools to be rapidly developed and widely implemented. In this short review, we update the current distribution of H. halys, discuss potential geographic range expansion based on passive and active dispersal and provide insight on the economic, environmental and social impact associated with H. halys.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Abram P, Gariepy TD, Boivin G, Brodeur J (2009) An invasive stink bug as an evolutionary trap for an indigenous egg parasitoid. Biol Invasions. doi:10.1007/s10530-013-0576-y

    Google Scholar 

  • ANSES (2014) https://www.anses.fr/sites/default/files/documents/SVEG2013sa0093Ra.pdf. Accessed 10 Jan 2015

  • 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 

  • Bae SD, Kim HJ, Lee GH, Park ST, Lee SW (2008) Susceptibility of stink bugs collected in soybean fields in Milyang to some insecticides. Korean J Appl Entomol 47:413–419

    Article  Google Scholar 

  • Bae SD, Kim HJ, Yoon YN, Park ST, Choi BR, Jung JK (2009) Effects of mungbean cultivar, Jangannodgu on nymphal development, adult longevity and oviposition of soybean stink bugs. Korean J Appl Entomol 48:311–318

    Article  Google Scholar 

  • Baldwin RL, Zhang A, Fultz SW, Abubeker S, Harris C, Connor EE, Van Hekken DL (2014) Brown marmorated stink bug odor compounds do not transfer into milk by feeding bug-contaminated corn silage to lactating dairy cattle. J Dairy Sci 97:1877–1884

    Article  CAS  PubMed  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 

  • Cesari M, Maistrello L, Ganzerli F, Dioli P, Rebecchi L, Guidetti R (2014) A pest alien invasion in progress: potential pathways of origin of the brown marmorated stink bug Halyomorpha halys populations in Italy. J Pest Sci. doi:10.1007/s10340-014-0634-y

    Google Scholar 

  • Ciosi M, Miller NJ, Kim KS, Giordano R, Estoup A, Guillemaud T (2008) Invasion of Europe by the western corn rootworm, Diabrotica virgifera virgifera: multiple transatlantic introductions with various reductions of genetic diversity. Mol Ecol 17:3614–3627

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

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

    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 9 Dec 2014

  • Fukuoka T, Yamakage H, Niiyama T (2002) Sucking injury to vegetables by the brown marmorated stink bug, Halyomorpha halys (Stål). Ann Rep Plant Prot N Jpn 53:229–231

    Google Scholar 

  • Funayama K (2002) Comparison of the susceptibility to injury of apple cultivars by stink bugs. Jpn J Appl Entomol Zool 46:37–40

    Article  Google Scholar 

  • Gariepy TD, Fraser H, Scott-Dupreea CD (2014a) Brown marmorated stink bug (Hemiptera: Pentatomidae) in Canada: recent establishment, occurrence, and pest status in southern Ontario. Can Entomol. doi:10.4039/tce.2014.4

    Google Scholar 

  • Gariepy TD, Haye T, Fraser H, Zhang J (2014b) 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

    Article  Google Scholar 

  • Garrouste R, Haye T, Streito JC, Dioli P, Maistrello L (2014) Halyomorpha halys (Hemiptera, Pentatomidae): Ten years after in Europe. In: Proceedings of the 5th quadrennial meeting of the international heteropterists’ society, 21–25 July, Washington, 28–29

  • Hamilton GC (2009) Brown marmorated stink bug. Am Entomol 55:19–20

    Article  Google Scholar 

  • Haye T, Abdallah S, Gariepy T, Wyniger D (2014a) Phenology, life table analysis, and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys, in Europe. J Pest Sci 87:407–418

    Article  Google Scholar 

  • Haye T, Wyniger D, Gariepy T (2014b) Recent range expansion of brown marmorated stink bug in Europe. In: Müller G, Pospischil R, Robinson WH (eds.) Proceedings of the eighth international conference on Urban Pests, 20–23 July, Zurich: 309–314

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

    Google Scholar 

  • Hedstrom CS, Shearer PW, Miller JC, Walton VM (2014) The effects of kernel feeding by Halyomorpha halys (Hemiptera: Pentatomidae) on commercial hazelnuts. J Econ Entomol 107:1858–1865

    Article  CAS  PubMed  Google Scholar 

  • Hoebeke ER (2002) Brown marmorated stink bug, Halyomorpha halys (Stal). Pennsyl. Dept. Agric., Bur. Plant Industry, Regulatory Hortic. 28:35–37

    Google Scholar 

  • 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 105:225–237

    Google Scholar 

  • Inkley DB (2012) Characteristics of home invasion by the brown marmorated stink bug (Hemiptera: Pentatomidae). J Entomol Sci 47:125–130

    Google Scholar 

  • Jacobs S, Bernhard KM (2009) (Revised January 2014) Brown Marmorated Stink Bug. Penn State Entomological Notes. http://www.ento.psu.edu/extension/factsheets/brownMarmoratedstinkbug.htm. Accessed 9 Dec 2014

  • Kobayashi T, Hasegawa T, Kegasawa K (1972) Major insect pests of leguminous crops in Japan. Trop Agric Res Series 6:109–126

    Google Scholar 

  • Kriticos DJ, Webber BL, Leriche A, Ota N, Macadam I, Bathols J, Scott JK (2012) CliMond: global high resolution historical and future scenario climate surfaces for bioclimatic modelling. Methods Ecol Evol 3:53–64

    Article  Google Scholar 

  • Kuhar TP, Kamminga KL, Whalen J, Dively GP, Brust G, Hooks CRR, Hamilton G, Herbert DA (2012) The pest potential of brown marmorated stink bug on vegetable crops. Plant Health Progress. doi:10.1094/PHP-2012-0523-01-BR

    Google Scholar 

  • Lawson Handley LJ, Estoup A, Evans DM, Thomas CE, Lombaert E, Facon B, Aebi A, Roy HE (2011) Ecological genetics of invasive alien species. Biocontrol 56:409–428

    Article  Google Scholar 

  • Lee DH, Short BD, Joseph SV, Bergh JC, Leskey TC (2013) Review of the biology, ecology, and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea. Environ Entomol 42:627–641

    Article  PubMed  Google Scholar 

  • Leskey TC, Short BD, Wright SE, Brown MW (2009) Diagnosis and variation in appearance of brown stink bug (Hemiptera: Pentatomidae) injury on apple. J Entomol Sci 44:314–322

    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 (2012a) Pest status of the brown marmorated stink bug, Halyomorpha halys in the USA. Outlooks Pest Manag 23:218–226. doi:10.1564/23oct07

    Article  Google Scholar 

  • Leskey TC, Short BD, Butler BR, Wright SE (2012b) 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, Hamilton G, Biddinger DJ, Buffington ML, Dieckhoff C, Fraser H, Gariepy TD, Herbert DA, Hoelmer KA, Hooks CRR, Inkley D, Krawczyk G, Kuhar TP, Lee DH, Nielsen AL, Pfeiffer DG, Rodriguez-Saona C, Shearer PW, Talamas E, Tomasino E, Tooker J, Venugopal PD, Whalen J, Walton V, Wiman N (2014) Datasheet Halyomorpha halys, CABI Invasive Species Compendium. http://www.cabi.org/isc/datasheet/27377. Accessed 17 Aug 2014

  • Maistrello L, Dioli P, Vaccari G, Nannini R, Bortolotto 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 1:283–288

    Google Scholar 

  • McPherson JE, McPherson RM (2000) Stink bugs of economic importance in America North of Mexico. CRC Press, Boca Raton

    Book  Google Scholar 

  • Mertz TL, Jacobs SB, Craig TJ, Ishmael FT (2012) The brown marmorated stinkbug as a new aeroallergen. J Allergy Clin Immun 130:999–1001

    Article  CAS  PubMed  Google Scholar 

  • Milonas PG, Partsinevelos GK (2014) First report of brown marmorated stink bug Halyomorpha halys Stål (Hemiptera: Pentatomidae) in Greece. EPPO Bull 44:183–186

    Article  Google Scholar 

  • Mohekar P, Lapis T, Lim J, Tomasino E (2013) Retronasal detection and consumer rejection threshold of “brown marmorated stink bug taint” in commercial Pinot Noir. 64th ASEV National Conference, Monterey, California, June 24–28

  • 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, pp 99–104

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

    Article  PubMed  Google Scholar 

  • Northeastern IPM Center (2014a) Where is BMSB? http://www.stopbmsb.org/where-is-bmsb/host-plants/. Accessed Mar 2015

  • Northeastern IPM Center (2014b) Host plants of the brown marmorated stink bug in the US. http://www.stopbmsb.org/where-is-bmsb/host-plants/. Accessed July 2014

  • Northeastern IPM Center (2014c) Stink bug detectives. http://www.stopbmsb.org/stink-bug-bulletin/stink-bug-detectives/Accessed. Accessed Mar 2015

  • Pansa MG, Asteggiano L, Costamagna C, Vittone G, Tavella L (2013) First discovery of Halyomorpha halys in peach orchards in Piedmont. Informatore Agrario 69:60–61

    Google Scholar 

  • Rice K, Bergh C, Bergman E, Biddinger D, Dieckhoff C, Dively G, Fraser H, Gariepy T, Hamilton G, Haye T, Herbert A, Hoelmer K, Hooks C, Jones A, Krawczyk G, Kuhar T, Mitchell W, Nielsen A, Pfeiffer D, Raupp M, Rodriguez-Saona C, Shearer P, Shrewsbury P, Venugopal PD, Whalen J, Wiman N, Leskey T, Tooker J (2014) Biology, ecology, and management of brown marmorated stink bug (Halyomorpha halys). J Integr Pest Manag. doi:10.1603/IPM14002

    Google Scholar 

  • Rider DA, Zheng LY, Kerzhner IM (2002) Checklist and nomenclatural notes on the Chinese Pentatomidae (Heteroptera). II. Pentatominae. Zoosyst Rossica 11:135–153

    Google Scholar 

  • Sauer C. (2012) Die Marmorierte Baumwanze tritt neu im Deutschschweizer Gemüsebau auf. Extension Gemüsebau, Forschungsanstalt Agroscope Changins-Wädenswil, Gemüsebau Info 28/12:4–5

  • Solomon D, Dutcher D, Raymond T (2013) Characterization of Halyomorpha halys (brown marmorated stink bug) biogenic volatile organic compound emissions and their role in secondary organic aerosol formation. J Air Waste Manag Assoc 63:1264–1269

    Article  CAS  PubMed  Google Scholar 

  • Tomasino E, Wiman N, Osborne J, Hedstrom C, Walton V (2013a) Impact of brown marmorated stink bug on Pinot Noir quality. In: 64th ASEV National Conference, Monterey, California, June 24–28

  • Tomasino E, Mohekar P, Lapis T, Wiman N, Walton V, Lim J (2013b) Effect of brown marmorated stink bug on wine—impact to Pinot Noir quality and threshold determination of taint compound trans-2-decenal. The 15th Australian Wine Industry Technical Conference, Sydney, Australia, July 13–18

  • United States Apple Association (2010) Asian pest inflicting substantial losses, raising alarm in eastern apple orchards. Apple News 41:488

    Google Scholar 

  • United States Department Agriculture (2002) Brown marmorated stink bug, Halyomorpha halys in US (Pennsylvania). USDA-APHIS NAPPO Alert, 2 October 2002

  • Vétek G, Papp V, Haltrich A, Rédei 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 3780:194–200

    Article  PubMed  Google Scholar 

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

  • Watanabe M (1980) Study of the life cycle of the brown marmorated stink bug, Halyomorpha mista, by observing ovary development. Insectarium 17:168–173

    Google Scholar 

  • Watanabe M, Arakawa R, Shinagawa Y, Okazawa T (1994) Antiinvading methods against the brown marmorated stink bug, Halyomorpha mista, in houses. Jpn Soc Med Entomol Zool 45:311–317

    Google Scholar 

  • Weber DC, Leskey TC, Cabrera Walsh G, Khrimian A (2014) Synergy of aggregation pheromone with Methyl (E, E, Z)-2,4,6-Decatrienoate in attraction of Halyomorpha halys (Hemiptera: Pentatomidae). J Econ Entomol 107:1061–1068

    Article  CAS  PubMed  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 

  • Wiman NG, Walton VM, Shearer PW, Rondon SI, Lee JC (2014) Factors affecting flight capacity of brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae). J Pest Sci. doi:10.1007/s10340-014-0582-6

    Google Scholar 

  • Xu J, Fonseca DM, Hamilton GC, Hoelmer KA, Nielsen AL (2014) Tracing the origin of US brown marmorated stink bugs Halyomorpha halys. Biol Invasions. doi:10.1007/s10530-013-0510-3

    Google Scholar 

  • Yu GY, Zhang JM (2007) The brown marmorated stink bug, Halyomorpha halys (Heteroptera: Pentatomidae) in P.R. China. In: Yun W, Xiao-yi W (compilers) International workshop on biological control of invasive species of forests, 20–25 September 2007, Beijing, P. R. China, FHTET-2008-04, pp 58–62

  • 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  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank the French Agency for Food, Environmental and Occupational Health & Safety (ANSES) for supporting this review.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tim Haye.

Additional information

Communicated by M. Traugott.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Haye, T., Gariepy, T., Hoelmer, K. et al. Range expansion of the invasive brown marmorated stinkbug, Halyomorpha halys: an increasing threat to field, fruit and vegetable crops worldwide. J Pest Sci 88, 665–673 (2015). https://doi.org/10.1007/s10340-015-0670-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-015-0670-2

Keywords

Navigation