Abstract
Halyomorpha halys is a harmful invasive species of heteropteran insects. We identified the ecological and geographical distribution boundaries of the species by analyzing the occurrences of H. halys in its native range (East Asia) and its invasive range (North America and Europe) and subsequently comparing these occurrences with maps of environmental factors. The limits of its ecological tolerance towards the primary limiting environmental factors affecting its distribution have been refined. The longer history of the invasion of this species in North America, the features of the spatial distribution of environmental factors, and the location of the initial penetration allowed H. halys to occupy its potential ecological niche more fully in North America compared to Europe. A comparative ecogeographical analysis of the current distribution of H. halys in North America has enabled an assessment of the species’ near-term prospects for distribution in Europe. The spread of the invader into Europe under contemporary climatic conditions may occur in an eastern direction—through the territory of Ukraine, the southern regions of Belarus, and the southwestern part of the Russian Federation. The boundaries of this advancement are primarily linked with the ability of H. halys to adapt to harsh overwintering conditions. Within large cities acting as heat islands, the formation of self-sustaining populations of H. halys up to 55° N latitude cannot be ruled out. However, significant territories in Eastern Europe are characterized by pessimal values for H. halys across multiple environmental factors simultaneously. This might contain the further spread of the species in Europe, hinder its naturalization, and reduce the occurrence of H. halys in these regions.
REFERENCES
Afonin, A.N., Kulakova, Yu.Yu., and Fedorova, Yu.A., Technologies of ecological niche modeling as a tool for phytosanitary risk analysis, Vestn. Zashch. Rast., 2021, vol. 104, no. 1, pp. 40–52. https://doi.org/10.31993/2308-6459-2021-104-1-14422
Afonin, A.N., Milyutina, E.A., and Musolin, D.L., Methods of calculating sums of effective temperatures using average monthly temperature data and compiling global maps for ecological-geographical modeling, Meteorol. Gidrol. (in press).
Afonin, A.N. and Sokolova, Yu.V., Ecological-Geographical Analysis and Modeling of the Distribution of Biological Objects Using GIS, St. Petersburg: VVM, 2018.
Andrew, N.R. and Hughes, L., Arthropod community structure along a latitudinal gradient: implications for future impacts of climate change, Austral Ecology, 2005, vol. 30, pp. 281–297. https://doi.org/10.1111/j.1442-9993.2005.01464.x
Arnold, K., Halyomorpha halys (Stål, 1855), eine für die europäische Fauna neu nachgewiesene Wanzenart (Insecta: Heteroptera, Pentatomidae, Pentatominae, Cappaeini), Mitteilungen des Thüringer Entomologenverbandes, 2009, vol. 16, no. 1, p. 19.
Booth, T.H., Nix, H.A., Busby, J.R., and Hutchinson, M.F., Bioclim: The first species distribution modelling package, its early applications and relevance to most current MaxEnt studies, Diversity and Distribution, 2014, vol. 20, pp. 1–9. https://doi.org/10.1111/ddi.12144
Cira, T.M., Venette, R.C., Aigner, J., Kuhar, T., Mullins, D.E., Gabbert, S.E., and Hutchison, W.D., Cold tolerance of Halyomorpha halys (Hemiptera: Pentatomidae) across geographic and temporal scales, Environ. Entomol., 2016, vol. 45, pp. 484–491. https://doi.org/10.1093/ee/nvv220
Deutsch, C.A., Tewksbury, J.J., Huey, R.B., Sheldon, K.S., Ghalambor, C.K., Haak, D.C., and Martin, P.R., Impacts of climate warming on terrestrial ectotherms across latitude, Proc. Natl. Acad. Sci. U. S. A., 2008, vol. 105, pp. 6668–6672. https://doi.org/10.1073/pnas.0709472105
Didan, K., MOD13C2 MODIS, Terra Vegetation Indices Monthly L3 Global 0.05Deg CMG V006, NASA EOSDIS Land Processes DAAC, 2015.
Eastman, J.R., IDRISI Guide to GIS and Image Processing Accessed in IDRISI Selva, Worcester: Clark University, 2009, pp. 182–185.
EcoMaps_Hh, https://drive.google.com/drive/folders/1KgEIRC1OANQ56A32hMmPF4kEnlIqZ8rK. Accessed September 15, 2023.
Fogain, R. and Graff, S., First records of the invasive pest, Halyomorpha halys (Hemiptera: Pentatomidae), in Ontario and Quebec, J. Entomol. Soc. Ontario, 2011, vol. 142, no. 1, pp. 45–48.
Gandjaeva, L.A., Hudayberdieva, M.O., Abdullaev, I.I., Mirzayeva, G.S., and Yusupboev, E.K., First record of Halyomorpha halys (Heteroptera: Pentatomidae) from Uzbekistan, Zoosyst. Ross., 2022, vol. 31, no. 2, pp. 329–331. https://doi.org/10.31610/zsr/2022.31.2.329
Gaspar, H., Castro, S., Grosso-Silva, J.M., van der Heyden, T., and Loureiro, J., Exponential outspread of Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae) in Portugal, Arq. Entomol., 2023, vol. 26, pp. 13–18.
Gierlasiński, G. and Taszakowski, A., Pluskwiaki różnoskrzydłe (Hemiptera: Heteroptera) Polski, 2013–2023. http://www.heteroptera.us.edu.pl/mapy/halyomorpha-halys.html. Accessed September 15, 2023.
Hamilton, G.C., Ahn, J.J., Bu, W., Leskey, T.C., Nielsen, A.L., Park, Y.-L., Rabitsch, W., and Hoelmer, K.A., Halyomorpha halys (Stål), in Invasive Stink Bugs and Related Species (Pentatomoidea): Biology, Higher Systematics, Semiochemistry and Management, McPherson, J.E., Ed., : CRC, 2018, pp. 243–292.
Hartung, V., Heller, M., and Husemann, M., First record of the invasive true bug (Heteroptera) Halyomorpha halys (Stål, 1855) from Hamburg with other records from Northern Germany and possible implications for its range expression, Evol. Syst., 2022, vol. 6, no. 1, pp. 57–64. https://doi.org/10.3897/evolsyst.6.80744
Hh_Euro occurrence.tif, https://drive.google.com/file/d/1x7VbN68HSHL_xzik9xuheawQpMFR4j1c/view?pli=1. Accessed September 15, 2023.
Hoebeke, E.R. and Carter, M.E., Halyomorpha halys (Stål) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America, Proc. Entomol. Soc. Wash., 2003, vol. 105, pp. 225–237.
iNaturalist. https://www.inaturalist.org/taxa/81923-Halyomorpha-halys. Accessed March 5, 2022.
Kibar, A., Mansur, U., and Celal, T., Distribution and population density of Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae) in Black Sea Region of Türkiye, Turk. J. Zool., 2023, vol. 47, pp. 120–129. https://doi.org/10.55730/1300-0179.3122
Kriticos, D.J., Kean, J.M., Phillips, C.B., Senay, S.D., Acosta, H., and Haye, T., The potential global distribution of the brown marmorated stink bug, Halyomorpha halys, a critical threat to plant biosecurity, J. Pest Sci., 2017, vol. 90, pp. 1033–1043.
Lee, D.H., Current status of research progress on the biology and management of Halyomorpha halys (Hemiptera: Pentatomidae) as an invasive species, Appl. Entomol. Zool., 2015, vol. 50, no. 3, pp. 277–290. https://doi.org/10.1007/s13355-015-0350-y
Lee, D.H. and Leskey, T.C., Flight behavior of foraging and overwintering brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae), Bull. Entomol. Res., 2015, vol. 105, no. 5, pp. 566–573. https://doi.org/10.1017/S0007485315000462
Lee, D.H., Short, B.D., Joseph, S.V., Bergh, J.C., and Leskey, T.C., Review of the biology, ecology, and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea, Environ. Entomol., 2013, vol. 4, no. 4, pp. 627–641. https://doi.org/10.1603/EN13006
Musolin, D.L., Insects in a warmer world: Ecological, physiological and life-history responses of true bugs (Heteroptera) to climate change, Global Change Biol., 2007, vol. 13, no. 8, pp. 1565–1585. https://doi.org/10.1111/j.1365-2486.2007.01395.x
Musolin, D.L., Dolgovskaya, M.Yu., Protsenko, V.Ye., Karpun, N.N., Reznik, S.Ya., and Saulich, A.Kh., Photoperiodic and temperature control of nymphal growth and adult diapause induction in the invasive Caucasian population of the brown marmorated stink bug, Halyomorpha halys, J. Pest Sci., 2019, vol. 92, no. 2, pp. 621–631. https://doi.org/10.1007/s10340-019-01080-1
Musolin, D.L., Kirichenko, N.I., Karpun, N.N., Aksenenko, E.V., Golub, V.B., Kerchev, I.A., Mandelshtam, M.Y., Vasaitis, R., Volkovitsh, M.G., Zhuravleva, E.N. and Selikhovkin, A.V., Invasive insect pests of forests and urban trees in Russia: Origin, pathways, damage, and management, Forests, 2022, vol. 13, no. 4, p. 521. https://doi.org/10.3390/f13040521
Musolin, D.L. and Saulich, A.K., Responses of insects to current climate changes: from physiology and behavior to range shifts, Entomol. Rev., 2012, vol. 92, no. 7, pp. 715–740. https://doi.org/10.1134/S0013873812070019
Nielsen, A.L., Hamilton, G.C., and Matadha, D., Developmental rate estimation and life table analysis for Halyomorpha halys (Hemiptera: Pentatomidae), Environ. Entomol., 2008, vol. 27, pp. 348–355.
Nix, H.A., A biogeographic analysis of Australian elapid snakes, in Atlas of Elapid Snakes of Australia, Longmore, R., Ed., Canberra: Australian Government Publishing Service, 1986, no. 7, pp. 4–15.
Parmesan, C., Ecological and evolutionary responses to recent climate change, Annu. Rev. Ecol., Evol., Syst., 2006, vol. 37, pp. 637–669. https://doi.org/10.1146/annurev.ecolsys.37.091305.110100
Saulich, A.Kh. and Musolin, D.L., Seasonal cycles of Pentatomoidea, in Invasive Stink Bugs and Related Species (Pentatomoidea): Biology, Higher Systematics, Semiochemistry and Management, McPherson, J.E., Ed., Boca Raton: CRC, 2018, pp. 565–607. https://doi.org/10.1201/9781315371221-12
Small, C. and Center for International Earth Science Information Network (CIESIN), Columbia University, VIIRS Plus DMSP Change in Lights (VIIRS + DMSP dLIGHT), Palisades, NY: NASA Socioeconomic Data and Applications Center (SEDAC), 2020. Accessed April 9, 2022.https://doi.org/10.7927/9ryj-6467
Small, C., Sousa, D., Yetman, G., Elvidge, C., and MacManus, K., Decades of urban growth and development on the Asian megadeltas, Global Planet. Change, 2018, vol. 165, pp. 62–89. https://doi.org/10.1016/j.gloplacha.2018.03.005
Streito, J.C., Chartois, M., Pierre, É., et al., Citizen science and niche modeling to track and forecast the expansion of the brown marmorated stinkbug Halyomorpha halys (Stål, 1855), Sci. Rep., 2021, vol. 11, p. 11421. https://doi.org/10.1038/s41598-021-90378-1
Szanyi, S., Ősz, A., Szanyi, K., Potish, L., and Nagy, A., The distribution of brown marmorated stink bug (Halyomorpha halys (Stål, 1855); Hemiptera: Pentatomidae) in the Northeast part of the Carpathian Lowland (West Ukraine), Acta Agrar. Debrecen., 2022, vol. 1, pp. 191–194. https://doi.org/10.34101/actaagrar/1/10831
Tougou, D., Musolin, D.L., and Fujisaki, K., Some like it hot! Rapid climate change promotes changes in distribution ranges of Nezara viridula and Nezara antennata in Japan, Entomol. Exp. Appl., 2009, vol. 130, no. 3, pp. 249–258. https://doi.org/10.1111/j.1570-7458.2008.00818.x
von Liebig, J., Die organische Chemie in ihrer Anwendung auf Agricultur und Physiologie, Braunschweig, 1840.
Wan, Z., Hook, S., and Hulley, G., MOD11C3 MODIS, Terra Land Surface Temperature, Emissivity Monthly L3 Global 0.05Deg CMG V006, NASA EOSDIS Land Processes DAAC, 2015. Accessed December 12, 2022.https://doi.org/10.5067/MODIS/MOD11C3.006
Wiman, N.G., Walton, V.M., Shearer, P.W., Rondon, S.I., and Lee, J.C., Factors affecting flight capacity of brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae), J. Pest Sci., 2015, vol. 88, pp. 37–47. https://doi.org/10.1007/s10340-014-0582-6
Yanagi, T. and Hagihara, Y., Ecology of the brown marmorated stink bug, Shokubutsu Boeki, 1980, vol. 34, pp. 315–321.
Zhu, G., Bu, W., Gao, Y., and Liu, G., Potential geographic distribution of brown marmorated stink bug invasion (Halyomorpha halys), PLoS One, 2012, vol. 7, p. e31246. https://doi.org/10.1371/journal.pone.0031246
ACKNOWLEDGMENTS
We are grateful to anonymous reviewers for their constructive comments and suggestions.
Funding
The study was supported by a grant from the Russian Science Foundation, no. 21-16-00050 (https://rscf.ru/project/21-16-00050/).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
ETHICS APPROVAL AND CONSENT TO PARTICIPATE
This work does not contain any studies involving human and animal subjects.
CONFLICT OF INTEREST
The authors of this work declare that they have no conflicts of interest.
Additional information
Publisher’s Note.
Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Afonin, A.N., Musolin, D.L. The Potential of Distribution of the Brown Marmorated Stink Bug Halyomorpha halys (Heteroptera: Pentatomidae) in Europe Determined on the Basis of the Comparative Analysis of the Ecogeographical Borders of Its Range. Russ J Biol Invasions 15, 11–25 (2024). https://doi.org/10.1134/S207511172401003X
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S207511172401003X