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The potential global distribution of the brown marmorated stink bug, Halyomorpha halys, a critical threat to plant biosecurity

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Abstract

The brown marmorated stinkbug, Halyomorpha halys is a highly polyphagous invasive insect, which has more than 300 reported hosts, including important horticultural crops. It has spread to every Northern Hemisphere continent, most recently to Europe. Whilst there have been no reports of incursions into Southern Hemisphere countries, there have been many interceptions associated with trade and postal goods. We modelled the potential distribution of H. halys using CLIMEX, a process-oriented bioclimatic niche model. The model was validated with independent widespread distribution data in the USA, and more limited data from Europe. The model agreed with all credible distribution data. The few exceptions in the distribution dataset appeared to be transient observations of hitchhikers, or were found at the edge of the range, in regions with topographic relief that was not captured in the climatic datasets used to fit and project the model. There appears to be potential for further spread in North America, particularly in central and southern states of the USA. In Europe, there is substantial potential for further spread, though under historical climate the UK, Ireland, Scandinavia and the Baltic states of Estonia, Lithuania and Latvia appear not to be at risk of establishment of H. halys. In the Southern Hemisphere, regions with moist tropical, sub-tropical, Mediterranean and warm-temperate climates appear to be at substantial risk on each continent. The threats are greatest in prime horticultural production areas.

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References

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

  • Bergmann EJ, Venugopal PD, Martinson HM, Raupp MJ, Shrewsbury PM (2016) Host plant use by the invasive Halyomorpha halys (Stål) on woody ornamental trees and shrubs. PLoS ONE 11:e0149975

    Article  PubMed  PubMed Central  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 (2015) A pest alien invasion in progress: potential pathways of origin of the brown marmorated stink bug Halyomorpha halys populations in Italy. J Pest Sci 88:1–7. doi:10.1007/s10340-014-0634-y

    Article  Google Scholar 

  • Chamberlin TC (1965) The method of multiple working hypotheses. Science 148:754–759. doi:10.1126/science.148.3671.754

    Article  CAS  PubMed  Google Scholar 

  • Cira TM, Venette RC, Aigner J, Kuhar T, Mullins DE, Gabbert SE, Hutchison W (2016) Cold tolerance of Halyomorpha halys (Hemiptera: Pentatomidae) across geographic and temporal scales. Environ Entomol 45:484–491

    Article  PubMed  Google Scholar 

  • De Villiers M et al (2016) The potential distribution of Bactrocera dorsalis: considering phenology and irrigation patterns. Bull Entomol Res 106:19–33

    Article  PubMed  Google 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). Revista gaditana de Entomología 7:539–548

    Google Scholar 

  • Duthie C (2012) Risk analysis of Halyomorpha halys (brown marmorated stink bug) on all pathways. Ministry for Primary Industries, Wellington

    Google Scholar 

  • Elith J, Phillips SJ, Hastie T, Dudik M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Div Distrib 17:43–57

    Article  Google Scholar 

  • Gapon DA (2016) First records of the brown marmorated stink bug Halyomorpha halys (Stål, 1855) (Heteroptera, Pentatomidae) in Russia, Abkhazia, and Georgia. Entomol Rev 96:1086–1088

    Article  Google Scholar 

  • 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 87:17–28. doi:10.1007/s10340-013-0529-3

    Article  Google Scholar 

  • Gariepy TD, Bruin A, Haye T, Milonas P, Vetek G (2015) Occurrence and genetic diversity of new populations of Halyomorpha halys in Europe J. Pest Sci 88:451–460. doi:10.1007/s10340-015-0672-0

    Article  Google Scholar 

  • 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 87:407–418. doi:10.1007/s10340-014-0560-z

    Article  Google Scholar 

  • Haye T, Gariepy T, Hoelmer K, Rossi JP, Streito JC, Tassus X, Desneux N (2015) 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. doi:10.1007/s10340-015-0670-2

    Article  Google Scholar 

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

    Google Scholar 

  • Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Article  Google Scholar 

  • Hiruki C (1997) Paulownia witches’-broom disease important in East Asia. In: International symposium on urban tree health 496, pp 63–68. doi:10.17660/ActaHortic.1999.496.6

  • 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 

  • Hoffman WE (1931) A pentatomid pest of growing beans in South China. Peking Nat Hist Bull 5:25–26

    Google Scholar 

  • Jones JR, Lambdin PL (2009) New county and state records for Tennessee of an exotic pest, Halyomorpha halys (Hemiptera: Pentatomidae), with potential economic and ecological implications. Fla Entomol 92:177–178. doi:10.1653/024.092.0132

    Article  Google Scholar 

  • Julien MH, Skarratt B, Maywald GF (1995) Potential geographical distribution of alligator weed and its biological control by Agasicles hygrophila. J Aquat Plant Manag 33:55–60

    Google Scholar 

  • Kiritani K (2007) The impact of global warming and land-use change on the pest status of rice and fruit bugs (Heteroptera) in Japan. Glob Change Biol 13:1586–1595

    Article  Google Scholar 

  • Kriticos DJ (2016) Climex publications up until April 2015. CSIRO, Canberra

    Google Scholar 

  • Kriticos DJ, Randall RP (2001) A comparison of systems to analyse potential weed distributions. In: Groves RH, Panetta FD, Virtue JG (eds) Weed risk assessment. CSIRO Publishing, Melbourne, pp 61–79

    Google Scholar 

  • Kriticos DJ, Leriche A (2009) The effects of spatial data precision on fitting and projecting species niche models. Ecography 33:115–127. doi:10.1111/j.1600-0587.2009.06042.x

    Article  Google Scholar 

  • Kriticos DJ, Brunel S (2016) Assessing and managing the current and future pest risk from water hyacinth, (Eichornia crassipes), an invasive aquatic plant threatening food and water security. PLoS ONE 11:e0120054

    Article  PubMed  PubMed Central  Google Scholar 

  • Kriticos DJ, Sutherst RW, Brown JR, Adkins SA, Maywald GF (2003) Climate change and biotic invasions: a case history of a tropical woody vine. Biol Invasions 5:145–165

    Article  Google Scholar 

  • Kriticos DJ, Webber BL, Leriche A, Ota N, Bathols J, Macadam I, Scott JK (2012) CliMond: global high resolution historical and future scenario climate surfaces for bioclimatic modelling. Methods Ecol Evol 3:53–64. doi:10.1111/j.2041-210X.2011.00134.x

    Article  Google Scholar 

  • Kriticos DJ, Maywald GF, Yonow T, Zurcher EJ, Herrmann NI, Sutherst RW (2015a) CLIMEX Version 4: exploring the effects of climate on plants, animals and diseases. CSIRO, Canberra

    Google Scholar 

  • Kriticos DJ et al (2015b) The potential distribution of invading Helicoverpa armigera in North America: Is it just a matter of time? PLoS ONE 10:e0119618. doi:10.1371/journal.pone.0119618

    Article  PubMed  PubMed Central  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 Environmental. Entomology 42:627–641. doi:10.1603/En13006

    Google Scholar 

  • Leskey TC et al (2012a) Pest status of the brown marmorated stink bug, Halyomorpha halys in the USA. Outlooks Pest Manag 23:218–226

    Article  Google Scholar 

  • Leskey TC, Lee DH, Short BD, Wright SE (2012b) Impact of insecticides on the invasive Halyomorpha halys (Hemiptera: Pentatomidae): analysis of insecticide lethality. J Econ Entomol 105:1726–1735

    Article  CAS  PubMed  Google Scholar 

  • Macavei L, Bǎeţan R, Oltean I, Florean T, Varga M, Costi E, Maistrello L (2015) First detection of Halyomorpha halys, a new invasive species with a high potential of damage on agricultural crops in Romania. Lucrari Stiintifice Seria Agronomie 58:105–108

    Google Scholar 

  • Mesgaran MB, Cousens RD, Webber BL (2014) Here be dragons: a tool for quantifying novelty due to covariate range and correlation change when projecting species distribution models. Div Distrib. doi:10.1111/ddi.12209

    Google Scholar 

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

    Article  Google Scholar 

  • Mitchell TD, Carter TR, Jones PD, Hulme M, New M (2004) A comprehensive set of climate scenarios for Europe and the globe: the observed record (1900–2000) and 16 scenarios (2000–2100). University of East Anglia, Norwich

    Google Scholar 

  • Mityushev IM (2016) First record of marmorated bug detection in Russia. Zashchita Karantin Rasteniĭ 3:48

    Google Scholar 

  • Nielsen AL, Hamilton GC (2009) Life history of the invasive species Halyomorpha halys (Hemiptera: Pentatomidae) in northeastern United States. Ann Entomol Soc Am 102:608–616. doi:10.1603/008.102.0405

    Article  Google Scholar 

  • Nielsen AL, Hamilton GC, Matadha D (2008a) Developmental rate estimation and life table analysis for Halyomorpha halys (Hemiptera: Pentatomidae). Environ Entomol 37:348–355

    Article  PubMed  Google Scholar 

  • Nielsen AL, Shearer PW, Hamilton GC (2008b) Toxicity of insecticides to Halymorpha halys (Hemiptera: Pentatomidae) using glass-vial bioassays. J Econ Entomol 101:1439–1442

    Article  CAS  PubMed  Google Scholar 

  • Niva CC, Takeda M (2003) Effects of photoperiod, temperature and melatonin on nymphal development, polyphenism and reproduction in Halyomorpha halys (Heteroptera: Pentatomidae). Zool Sci 20:963–970. doi:10.2108/zsj.20.963

    Article  CAS  PubMed  Google Scholar 

  • Nystrom Santacruz E, Venette R, Dieckhoff C, Hoelmer K, Koch RL (2017) Cold tolerance of Trissolcus japonicus and T. cultratus, potential biological control agents of Halyomorpha halys, the brown marmorated stink bug. Biol Control 107:11–20. doi:10.1016/j.biocontrol.2017.01.004

    Article  Google Scholar 

  • Pigato M, Tang W (2015) China and Africa: expanding economic ties in an evolving global context. World Bank, Washington

    Google Scholar 

  • Rice KB et al (2014) Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). J Integr Pest Manag 5:A1–A13

    Article  Google Scholar 

  • Šeat J (2015) Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) a new invasive species in Serbia. Acta Entomologica Serbica 20:167–171

    Google Scholar 

  • Shelford VE (1963) The ecology of North America. University of Illinois Press, Urbana

    Google Scholar 

  • Simov N (2016) The invasive brown marmorated stink bug Halyomorpha halys (Stål 1855 (Heteroptera: Pentatomidae) already in Bulgaria. Ecologica Montenegrina 9:51–53

    Google Scholar 

  • Sutherst RW, Maywald GF (1985) A computerised system for matching climates in ecology Agriculture. Ecosyst Environ 13:281–299

    Article  Google Scholar 

  • Sutherst RW, Bourne AS (2009) Modelling non-equilibrium distributions of invasive species: a tale of two modelling paradigms. Biol Invasions 11:1231–1237

    Article  Google Scholar 

  • Teulon DAJ, Leskey TC, Duthie C (2016) Brown marmorated stink bug—current or planned research to prevent its establishment and to reduce its impact in New Zealand. NZ Plant Prot 69:323

    Google Scholar 

  • van der Ploeg RR, Böhm W, Kirkham MB (1999) On the origin of the theory of mineral nutrition of plants and the law of the minimum. Soil Sci Soc Am J 63:1055–1062

    Article  Google Scholar 

  • 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 

  • Vink CJ, Derraik JGB, Phillips CB, Sirvid PJ (2011) The invasive Australian redback spider, Latrodectus hasseltii Thorell 1870 (Araneae: Theridiidae): current and potential distributions, and likely impacts. Biol Invasions 13:1003–1019. doi:10.1007/s10530-010-9885-6

    Article  Google Scholar 

  • Watanabe M, Kamimura K, Koizumi Y (1978) The annual life cycle of Halyomorpha mista and ovarian development process. Toyama J Rural Med 9:95–99

    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

    Article  Google Scholar 

  • Watt MS, Ganley RJ, Kriticos DJ, Manning LK (2011) Dothistroma needle blight and pitch canker: the current and future potential distribution of two devastating diseases of Pinus species. For Ecol Manag 41:412–424. doi:10.1139/X10-204

    Google Scholar 

  • Webber BL et al (2011) Modelling horses for novel climate courses: insights from projecting potential distributions of native and alien Australian acacias with correlative and mechanistic models. Div Distrib 17:978–1000. doi:10.1111/j.1472-4642.2011.00811.x

    Article  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? Mitteilungen-Schweizerische Entomologische Gesellschaft 81:1

    Google Scholar 

  • Wiman NG, Walton VM, Shearer PW, Rondon SI, Lee JC (2015) Factors affecting flight capacity of brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae). J Pest Sci 88:37–47

    Article  Google Scholar 

  • Yonow T, Kriticos DJ, Medd RW (2004) The potential geographic range of Pyrenophora semeniperda. Phytopathology 94:805–812

    Article  PubMed  Google Scholar 

  • Yonow T, Hattingh V, de Villiers M (2013) CLIMEX modelling of the potential global distribution of the citrus black spot disease caused by Guignardia citricarpa and the risk posed to Europe. Crop Prot 44:18–28. doi:10.1016/j.cropro.2012.10.006

    Article  Google Scholar 

  • Yonow T, Kriticos DJ, Ota N, Van den Berg J, Hutchison WD (2016) The potential global distribution of Chilo partellus, including consideration of irrigation and cropping patterns. J Pest Sci. doi:10.1007/s10340-016-0801-4

    Google Scholar 

  • Yu G, Zhang J (2007) The brown marmorated stink bug, Halyomorpha halys (Heteroptera: Pentatomidae) in PR China. In: International workshop on biological control of invasive species of forests. Beijing, China, Citeseer, 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. doi:10.1371/journal.pone.0031246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu G, Gariepy TD, Haye T, Bu W (2016) Patterns of niche filling and expansion across the invaded ranges of Halyomorpha halys in North America and Europe. J Pest Sci. doi:10.1007/s10340-016-0786-z

    Google Scholar 

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Acknowledgements

All authors read and approved the manuscript. This project is a component of the International Pest Risk Research Group’s “Project Stinky” (www.pestrisk.org/project_stinky).

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Correspondence to Darren J. Kriticos.

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Communicated by M. Traugott.

Special issue: The brown marmorated stink bug Halyomorpha halys an emerging pest of global concern.

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Kriticos, D.J., Kean, J.M., Phillips, C.B. et al. The potential global distribution of the brown marmorated stink bug, Halyomorpha halys, a critical threat to plant biosecurity. J Pest Sci 90, 1033–1043 (2017). https://doi.org/10.1007/s10340-017-0869-5

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