Abstract
Halyomorpha halys is native to Asia, but was recently accidentally introduced to North America and Europe. This species was recorded for the first time in Russia in 2013 (2014) and in both Serbia and Abkhazia in 2015. In 2015–2017, we conducted surveys in Russia, Serbia, and Abkhazia and found that H. halys had not only successfully survived its first winters in new regions, but also started to establish locally, spread, increase populations, and damage local crops. In Sochi (Russia) and Abkhazia, H. halys was recorded to feed on 32 species and cultivars from 16 plants families. In Serbia, it has so far been observed on only four species from four plant families. H. halys is already widely spread in Abkhazia and causes serious damage to many crops: in 2016, the yield of peach, mandarin orange, persimmon and other crops fell down by 13.2–87.4% if compared to the long-term means of yield. The losses are likely to be mostly caused by feeding of H. halys. We conclude that H. halys was accidentally introduced to Russia in 2012–2013 most likely with woody plants imported to Sochi from Italy or Greece for urban landscaping before the 2014 Winter Olympics. The species established in Sochi and quickly moved to Krasnodar (Russia), Abkhazia, and beyond—to Georgia. Populations in Serbia most likely arrived in 2015 traveling on railway cars or in commodities on the Bucharest–Belgrade railway line. We discuss phenology and prospects of further expansion of H. halys in Europe.
Similar content being viewed by others
References
Arnold K (2009) Halyomorpha halys (Stål, 1855), eine für die europäische fauna neu nachgewiesene wanzenart (Insecta: Heteroptera: Pentatomidae: Cappaeini). Mitteilungen des Thüringer Entomologenverbandes 16:19
Ciceoi R, Mardare E, Teodorescu E, Dobrin I (2016) The status of brown marmorated stink bug, Halyomorpha halys, in Bucharest area. J Hortic Biotechnol 20(4):18–25
Dioli P, Leo P, Maistrello L (2016) First records in Spain and Sardinia of the alien species Halyomorpha halys (Stål, 1855), with notes on its distribution in Europe (Hemiptera, Pentatomidae). Rev gaditana de Entomología 7:539–548
Esenbekova PA (2017) First record of Halyomorpha halys (Stål, 1855) (Heteroptera, Pentatomidae) from Kazakhstan. Eurasian Entomol J 16(1):23–24
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
Gariepy TD, Fraser H, Scott-Dupree CD (2014) Brown marmorated stink bug (Hemiptera: Pentatomidae) in Canada: recent establishment, occurrence, and pest status in southern Ontario. Can Entomol 146:579–582
Hamilton GC, Ahn JJ, Bu W, Leskey TC, Nielsen AL, Park Y-L, Rabitsch W, Hoelmer KA (2017) Halyomorpha halys (Stål). In: McPherson JE (ed) Invasive stink bugs and related species (Pentatomoidea): biology, higher systematics, semiochemistry, and management. CRC Press, Boca Raton, pp 243–292
Haye T, Abdallah S, Gariepy T, Wyniger D (2014) Phenology, lifetable analysis, and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys, in Europe. J Pest Sci 87:407–418
Haye T, Gariepy T, Hoelmer K, Rossi J-P, Streito J-C, Tassus X, Desneux N (2015) Range expansion of the invasive brown marmorated stink bug, Halyomorpha halys: an increasing threat to field, fruit and vegetable crops worldwide. J Pest Sci 88:665–673
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
Hoffman WE (1931) A pentatomid pest of growing beans in south China. Peking Nat Hist Bull 4:25–27
Jimerikin VN, Guliy VV (2014) Marmorated stink bug. Zashita i Karantine Rasteniy [Prot Quar Plants] (Moscow) 4:40–43 (Russian)
Karpun NN, Ignatova AYe, Zhuravleva EN (2015) Species of pests on ornamental woody plants in humid subtropics new for Krasnodar Kray (Russia). Izvestia Sankt-Peterburgskoj Lesotehniceskoj Akademii [Trans Saint Petersburg Forest Tech Acad] 211:189–203 (Russian with English summary)
Karpun NN, Zhuravleva EN, Protsenko VYe (2016) To the fauna of pests of plants in humid subtropics new for Krasnodar Kray (Russia). In: Musolin DL, Selikhovkin AV (eds) The Kataev memorial readings—IX. Dendrobiotic invertebrates and fungi and their role in forest ecosystems (Proceedings of the international conference). Saint Petersburg State Forest Technical University, Saint Petersburg (Russia), p 47
Karpun NN, Zhuravleva NYe, Volkovitsh МG, Procenko (Protsenko) VYe, Musolin DL (2017) To the fauna and biology of new alien insect pest species of woody plants in humid subtropics of Russia. Izvestia Sankt-Peterburgskoj Lesotehniceskoj Akademii [Trans Saint Petersburg Forest Tech Acad] 220:169–185. https://doi.org/10.21266/2079-4304.2017.220.169-185 (Russian with English summary)
Kereši T, Sekulić R, Protić L, Milovac Ž (2012) Pojava stenice Nezara viridula L. (Heteroptera: Pentatomidae) u Srbiji [Occurrence of Nezara viridula L. (Heteroptera: Pentatomidae) in Serbia]. Biljni lekar [Plant Doctor] 40:296–304 (Serbian with English summary)
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 Prog. https://doi.org/10.1094/PHP-2012-0523-01-BR
Lee D-H, 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
Leskey TC, Hamilton GC (2010a) Brown marmorated stink bug working group meeting report, June 2010. http://projects.ipmcenters.org/Northeastern/FundedProjects/ReportFiles/Pship2010/Pship2010-Leskey-ProgressReport-237195.pdf. Accessed November 2016
Leskey TC, Hamilton GC (2010b) Brown marmorated stink bug working group meeting report, November 2010. http://projects.ipmcenters.org/Northeastern/FundedProjects/ReportFiles/Pship2010/Pship2010-Leskey-ProgressReport-237195-Meeting-2010_11_17.pdf. Accessed November 2016
Leskey TC, Hamilton GC (2011) Brown marmorated stink bug working group meeting report, November 2011. http://projects.ipmcenters.org/Northeastern/FundedProjects/ReportFiles/Pship2011/Pship2011-Leskey-ProgressReport-4681655.pdf. Accessed November 2016
Leskey TC, Hamilton GC (2015) Brown marmorated stink bug working group meeting report, June 2015. http://www.northeastipm.org/neipm/assets/File/BMSB-Working-Group-Meeting-Report-Jun-2015.pdf. Accessed November 2016
Leskey TC, Hamilton GC, Nielsen AL, Polk DF, Rodriguez-Saona C, Bergh JC, Herbert DA, Kuhar TP, Pfeiffer D, Dively G, Hooks CRR, Raupp MJ, Shrewsbury PM, Krawczyk G, Shearer PW, Whalen J, Koplinka-Loehr C, Myers E, Inkley D, Hoelmer KA, Lee D-Y, and Wright SE (2012) Pest status of the brown marmorated stink bug, Halyomorpha halys (Stål), in the USA. Outlooks Pest Manag 23:218–226
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 ser Agronomie 58:105–108
Maistrello L, Dioli P, Bariselli M (2013) Trovata una cimice esotica dannosa per i frutteti. Agricoltura 6:67–68
Maistrello L, Dioli P, Bariselli M, Mazzoli GL, Giacalone-Forini I (2016) Citizen science and early detection of invasive species: phenology of first occurrences of Halyomorpha halys in Southern Europe. Biol Invasions 18:3109–3116
Malumphy C (2014) Second interception of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) in Britain. Het News 3:4–5
Milonas PG, Partsinevelos GK (2014) First report of brown marmorated stink bug Halyomorpha halys Stål (Hemiptera: Pentatomidae) in Greece. Bull OEPP/EPPO Bull 44:183–186
Mityushev IM (2016) The first record of Brown marmorated stink bug in Russia. Zashita I Karantin Rasteniy [Prot Quar Plants] 3:48 (Russian)
Musolin DL, Saulich AKh (2017) Diapause in Pentatomoidea. In: McPherson JE (ed) Invasive stink bugs and related species (Pentatomoidea): biology, higher systematics, semiochemistry, and management. CRC Press, Boca Raton, pp 497–564
Nielsen AL, Hamilton GC (2009) Seasonal occurrence and impact of Halyomorpha halys (Hemiptera: Pentatomidae) in tree fruit. J Econ Entomol 102:1133–1140
Protić LJ (2011) New Heteroptera for the fauna of Serbia. Bull Nat Hist Mus 4:119–125
Rice KB, Bergh JC, Bergmann EJ, 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 D, Whalen J, Wiman N, Leskey TC, Tooker J (2014) Biology, ecology, and management of brown marmorated stink bug (Halyomorpha halys). J Integr Pest Manag 5:1–13
Saulich AKh, Musolin DL (2017) Seasonal cycles of Pentatomoidea. In: McPherson JE (ed) Invasive stink bugs and related species (Pentatomoidea): biology, higher systematics, semiochemistry, and management. CRC Press, Boca Raton, pp 565–607
Šeat J (2015) Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) a new invasive species in Serbia. Acta Entomol Serbica 20:161–171
Shiryeva (Shiriaeva) NV (2015) New pests of trees and shrubs in Sochi Park “Arboretum”. Izvestia Sankt-Peterburgskoj Lesotehniceskoj Akademii [Trans Saint Petersburg Forest Tech Acad] 211:243–253 (Russian with English summary)
Vétek G, Papp V, Haltrich A, Redei D (2014) First record of the brown marmorated stink bug (Hemiptera: Heteroptera: Pentatomidae), in Hungary, with description of the genitalia of both sexes. Zootaxa 3780:194–200
Wang H-J, Liu G-Q (2005) Hemiptera: Scutelleridae, Tessaratomidae, Dinindoridae and Pentatomidae. In: Tang K-K (ed) Insect fauna of middle-west Quinling range and south mountains of Gansu Province. Science Press, Beijing, pp 279–292
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
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 Schweizerischen Entomol Gesellschaft 81:1–8
Wyniger D, Kment P (2010) Key for the separation of Halyomorpha halys (Stål) from similar-appearing pentatomids (Insecta: Heteroptera: Pentatomidae) occurring in Central Europe, with new Swiss records. Bull Soc Entomol Suisse 83:261–270
Yanagi T, Hagihara Y (1980) Ecology of the brown marmorated stink bug. Plant Prot 34:315–321 (Japanese)
Zhu G, Bu W, Gao Y, Liu G (2012) Potential geographic distribution of brown marmorated stink bug invasion (Halyomorpha halys). PLoS ONE 7:e31246
Acknowledgements
The present study was partially supported by the Russian Foundation for Basic Research (Grant No. 17-04-01486 for DLM) and the EU COST Action FP1401 Global Warning (A global network of nurseries as early warning system against alien tree pests; http://www.cost.eu/COST_Actions/fps/FP1401). Survey conducted during 2016 in Serbia was supported by the Serbian Ministry of Agriculture and Environmental Protection, Plant Protection Directorate. We sincerely thank Dr. D. Gillespie (AAFC Agassiz, retired), Dr. K. Tsytsulina and two anonymous reviewers for critical reading of the MS and helpful correction.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Heikki Hokkanen.
Rights and permissions
About this article
Cite this article
Musolin, D.L., Konjević, A., Karpun, N.N. et al. Invasive brown marmorated stink bug Halyomorpha halys (Stål) (Heteroptera: Pentatomidae) in Russia, Abkhazia, and Serbia: history of invasion, range expansion, early stages of establishment, and first records of damage to local crops. Arthropod-Plant Interactions 12, 517–529 (2018). https://doi.org/10.1007/s11829-017-9583-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-017-9583-8