Published January 18, 2024
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Distribution and genetic diversity of the invasive pest Halyomorpha halys (Hemiptera, Pentatomidae) in Belgium
Authors/Creators
- 1. Ghent University, Ghent, Belgium
- 2. Crops and Forest Health Unit, Life Sciences Department, Walloon Agricultural Research Centre, Gembloux, Belgium
- 3. Zoology Department, Research Centre for Fruit Cultivation, Sint-Truiden, Belgium
Description
The brown marmorated stink bug, Halyomorpha halys, native to East Asia, is an invasive pest of economic importance. It has invaded North America and many European countries and is further expanding its range. In Belgium, it was first observed in 2011. Halyomorpha halys is known to cause severe damage in commercial fruit orchards and vegetable crops. A dramatic and unmitigated expansion of H. halys in its adventive range could lead to significant economic implications for agricultural production. In this study, occurrence data of H. halys since its first observation in Belgium was analysed together with molecular information to map the populations and evaluate the genetic diversity of this pest. The genetic diversity of H. halys in Belgium was compared to data from other invaded and native countries reported in previous studies to identify possible invasion routes. The analysis of 1176-bp of mitochondrial DNA cytochrome c oxidase I and II genes (COI and COII) led to the discovery of two novel COI-COII haplotype combinations currently unique to Belgium. The invasion of H. halys in Belgium is likely the result of multiple and ongoing introductions from its native region and from already invaded countries in Europe, particularly Italy. The expansion of the brown marmorated stink bug populations in Belgium is recent and ongoing. Presently, it appears to thrive best in northern Belgium.
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References
- Aukema B, Bieman den K, Lommen G, Maat van de G, Troisfontaine L, Vossen P (2019) Nieuwe en interessante nederlandse Wantsen VI (Hemiptera: Heteroptera). Nederlandse Faunistische Mededelingen 46: 57–86.
- Berteloot OH, Vervaet L, Huayan C, Talamas EJ, Van Leeuwen T, De Clercq P (2021) First record in Belgium of Trissolcus basalis (Hymenoptera, Scelionidae), an egg parasitoid of economically important stink bugs (Hemiptera, Pentatomidae). Belgian Journal of Zoology 151: 139–148. https://doi.org/10.26496/bjz.2021.90
- Bodenhofer U, Bonatesta E, Horejs-Kainrath C, Hochreiter S (2015) msa: An R package for multiple sequence alignment. Bioinformatics 31(24): 3997–3999. https://doi.org/10.1093/bioinformatics/btv494
- Bowler DE, Callaghan CT, Bhandari N, Henle K, Barth MB, Koppitz C, Klenke R, Winter M, Bruelheide H, Bonn A (2022) Temporal trends in the spatial bias of species occurrence records. Ecography 8(8): e06219. https://doi.org/10.1111/ecog.06219
- Bras A, Avtzis DN, Kenis M, Li H, Vétek G, Bernard A, Courtin C, Rousselet J, Roques A, Auger-Rozenberg M-A (2019) A complex invasion story underlies the fast spread of the invasive box tree moth (Cydalima perspectalis) across Europe. Journal of Pest Science 92(3): 1187–1202. https://doi.org/10.1007/s10340-019-01111-x
- Bulgarini G, Badra Z, Leonardi S, Maistrello L (2020) The predatory ability of generalist predators on eggs, young nymphs and adults of the invasive Halyomorpha halys in southern Europe. BioControl 66(3): 355–366. https://doi.org/10.1007/s10526-020-10066-3
- 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. Journal of Pest Science 88(1): 1–7. https://doi.org/10.1007/s10340-014-0634-y
- Cesari M, Maistrello L, Piemontese L, Bonini R, Dioli P, Lee W, Park C, Partsinevelos GK, Rebecchi L, Guidetti R (2018) Genetic diversity of the brown marmorated stink bug Halyomorpha halys in the invaded territories of Europe and its patterns of diffusion in Italy. Biological Invasions 20(4): 1073–1092. https://doi.org/10.1007/s10530-017-1611-1
- Claerebout S, Haye T, Olafsson E, Pannier E, Bultot J (2018) Premières occurrences de Halyomorpha halys (Stål, 1855) pour la Belgique et actualisation de sa répartition en Europe (Hemiptera: Heteroptera: Pentatomidae). Bulletin de la Société Royale Belge d'Entomologie 154: 205–227.
- Commission EU (2022a) The apple market in the EU: Production, yields and areas. EU Fruit and Vegetables market observatory, pip fruit subgroup. https://agriculture.ec.europa.eu/system/files/2022-10/apples-production_en.pdf
- Commission EU (2022b) The pear market in the EU: Production, yields and areas. EU Fruit and Vegetables market observatory, pip fruit subgroup. https://agriculture.ec.europa.eu/system/files/2022-10/pears-production_en.pdf
- Cristescu ME (2016) Genetic reconstructions of invasion history. In: Barret SCH, Colautti RI, Dlugosch KM, Rieseberg LH (Eds) Invasion Genetics. John Wiley & Sons, Ltd., Chichester, 267–282. https://doi.org/10.1002/9781119072799.ch15
- Dlugosch KM, Parker IM (2008) Founding events in species invasions: Genetic variation, adaptive evolution, and the role of multiple introductions. Molecular Ecology 17(1): 431–449. https://doi.org/10.1111/j.1365-294X.2007.03538.x
- Faúndez EI, Rider DA (2017) The brown marmorated stink bug Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) in Chile. Arquivos Entomolóxicos, 305–307.
- Ficetola GF, Bonin A, Miaud C (2008) Population genetics reveals origin and number of founders in a biological invasion. Molecular Ecology 17(3): 773–782. https://doi.org/10.1111/j.1365-294X.2007.03622.x
- Folmer O, Black M, Hoeh W, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3(5): 294–299.
- Frank SD, Backe KM (2023) Effects of urban heat islands on temperate forest trees and arthropods. Current Forestry Reports 9(1): 48–57. https://doi.org/10.1007/s40725-022-00178-7
- Gapon DA (2016) First records of the brown marmorated stink bug Halyomorpha halys (Stål, 1855) (Heteroptera, Pentatomidae) in Russia, Abkhazia, and Georgia. Entomological Review 96(8): 1086–1088. https://doi.org/10.1134/S001387381608011X
- 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. Journal of Pest Science 87(1): 17–28. https://doi.org/10.1007/s10340-013-0529-3
- Gariepy TD, Musolin DL, Konjević A, Karpun NN, Zakharchenko VY, Zhuravleva EN, Tavella L, Bruin A, Haye T (2021) Diversity and distribution of cytochrome oxidase I (COI) haplotypes of the brown marmorated stink bug, Halyomorpha halys Stål (Hemiptera, Pentatomidae), along the eastern front of its invasive range in Eurasia. NeoBiota 68: 53–77. https://doi.org/10.3897/neobiota.68.68915
- Geldmann J, Heilmann-Clausen J, Holm TE, Levinsky I, Markussen B, Olsen K, Rahbek C, Tøttrup AP (2016) What determines spatial bias in citizen science? Exploring four recording schemes with different proficiency requirements. Biodiversity Research 22(11): 1139–1149. https://doi.org/10.1111/ddi.12477
- Girardello M, Chapman A, Dennis R, Kaila L, Borges PAV, Santangeli A (2019) Gaps in butterfly inventory data: A global analysis. Biological Conservation 236: 289–295. https://doi.org/10.1016/j.biocon.2019.05.053
- Güncan A, Gümüş E (2019) Brown marmorated stink bug, Halyomorpha halys (Stål, 1855) (Hemiptera: Heteroptera, Pentatomidae), a new and important pest in Turkey. Entomological News 128(2): 204–210. https://doi.org/10.3157/021.128.0208
- Hamelin RC, Roe AD (2019) Genomic biosurveillance of forest invasive alien enemies: A story written in code. Evolutionary Applications 13(1): 95–115. https://doi.org/10.1111/eva.12853
- Hamilton GC, Ahn JJ, Bu W, Leskey TC, Nielsen AL, Park YL, Rabitsch W, Hoelmer KA (2018) Halyomorpha halys (Stål). In: McPherson JE (Ed.) Invasive Stink Bugs and Related Species (Pentatomoidea): Biology, Higher Systematics, Semiochemistry, and Management. CRC Press, Taylor & Francis, Boca Raton, 243–292. https://doi.org/10.1201/9781315371221-4
- Hartung V, Heller M, Husemann M (2022) 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 expansion. Evolutionary Systematics 6(1): 57–64. https://doi.org/10.3897/evolsyst.6.80744
- Haye T, Gariepy T, Hoelmer K, Rossi J-P, Streito J-C, 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. Journal of Pest Science 88(4): 665–673. https://doi.org/10.1007/s10340-015-0670-2
- Hoebeke ER, Carter ME (2003) Halyomorpha halys (Stål) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proceedings of the Entomological Society of Washington 105: 225–237.
- Horwood M, Milnes JM, Cooper WR (2019) Brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae), detections in Western Sidney, New South Wales, Australia. Austral Entomology 58(4): 857–865. https://doi.org/10.1111/aen.12421
- Jombart T (2008) adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24(11): 1403–1405. https://doi.org/10.1093/bioinformatics/btn129
- Kaiser A, Merckx T, Van Dyck H (2016) The Urban Heat Island and its special scale dependent impact on survival and development in butterflies of different thermal sensitivity. Ecology and Evolution 6(12): 4129–4140. https://doi.org/10.1002/ece3.2166
- Kapantaidaki DE, Evangelou VI, Morrison WR III, Leskey TC, Brodeur J, Milonas P (2019) Halyomorpha halys (Hemiptera: Pentatomidae) Genetic diversity in North America and Europe. Insects 10(6): e174. https://doi.org/10.3390/insects10060174
- Kelling S, Fink D, La Sorte FA, Johnston A, Bruns NE, Hochachka WM (2015) Taking a 'Big Data' approach to data quality in a citizen science project. Ambio 44(S4): 601–611. https://doi.org/10.1007/s13280-015-0710-4
- Kistner EJ (2017) Climate change impacts on the potential distribution and abundance of the brown marmorated stink bug (Hemiptera: Pentatomidae) with special reference to North America and Europe. Environmental Entomology 46(6): 1212–1224. https://doi.org/10.1093/ee/nvx157
- 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 13(1): 1–41. https://doi.org/10.1094/PHP-2012-0523-01-BR
- Lahr EC, Dun RR, Frank SD (2018) Getting ahead of the curve: Cities as surrogates for global change. Proceedings of the Royal Society B, Biological Sciences 285(1882): e20180643. https://doi.org/10.1098/rspb.2018.0643
- 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. Environmental Entomology 42(4): 627–641. https://doi.org/10.1603/EN13006
- Lee W, Guidetti R, Cesari M, Gariepy TD, Park Y-L, Park C-G (2018) Genetic diversity of Halyomorpha halys (Hemiptera, Pentatomidae) in Korea and Comparison with COI sequence datasets from East Asia, Europe, and North America. The Florida Entomologist 101(1): 49–54. https://doi.org/10.1653/024.101.0110
- Leskey TC, Hamilton GC, Nielsen AL, Polk DF, Rodriguez SC, Bergh JC, Herbert DA, Kuhar TP, Pfeiffer D, Dively GP, Hooks CRR, Raupp MJ, Shrewsbury PM, Krawczyk G, Shearer PW, Whalen J, Koplinka LC, Myers E, Inkley D, Hoelmer KA, Lee D-H, Wright SE (2012) Pest status of the brown marmorated stink bug, Halyomorpha halys in the USA. Outlooks on Pest Management 23(5): 218–226. https://doi.org/10.1564/23oct07
- Lombaert E, Guillemaud T, Comuet J-M, Malausa T, Facon B, Estoup A (2010) Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. PLoS ONE 5(3): e9743. https://doi.org/10.1371/journal.pone.0009743
- Macavei LI, Baetan 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 58: e2015.
- Maistrello L, Dioli P, Vaccari G, Nannini R, Bortolotti P, Caruso S, Costi E, Montermini A, Casoli L, Bariselli M (2014) Primi rinvenimenti in Italia della cimice esotica Halyomorpha halys, una nuova minaccia per la frutticoltura. Giornate Fitopatologiche 1: 283–288.
- Maistrello L, Dioli P, Bariselli M, Mazzoli GL, Giacalone-Forini L (2016) Citizen science and early detection of invasive species: Phenology of first occurrences of Halyomorpha halys in Southern Europe. Biological Invasions 18(11): 3109–3116. https://doi.org/10.1007/s10530-016-1217-z
- Milonas PG, Partsinevelos GK (2014) First report of brown marmorated stink bug Halyomorpha halys Stål (Hemiptera: Pentatomidae) in Greece. Bulletin OEPP. EPPO Bulletin. European and Mediterranean Plant Protection Organisation 44(2): 183–186. https://doi.org/10.1111/epp.12129
- Observation International and local partners (2022) Observation International and local partners [waarnemingen.be/observations.be dataset Halyomorpha halys]. [retrieved June 5, 2023, from] https://waarnemingen.be/species/197583/
- Outhwaite CL, Gregory RD, Chandler RE, Collen B, Isaac NJB (2020) Complex long-term biodiversity change among invertebrates, bryophytes and lichens. Nature Ecology & Evolution 4(3): 384–392. https://doi.org/10.1038/s41559-020-1111-z
- Paradis E (2010) pegas: An R package for population genetics with an integrated-modular approach. Bioinformatics 26(3): 419–420. https://doi.org/10.1093/bioinformatics/btp696
- Powney GD, Carvell C, Edwards M, Morris RKA, Roy HE, Woodcock BA, Isaac NJB (2019) Widespread losses of pollinating insects in Britain. Nature Communications 10(1): e1018. https://doi.org/10.1038/s41467-019-08974-9
- QGIS Development Team (2023) QGIS Geographic Information System. Open Source Geospatial Foundation Project. http://qgis.osgeo.org
- R Core Team (2020) R: A Language and Environment for statistical Computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
- Rabitsch W, Friebe G (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: 115–139.
- Rice KB, Bergh CJ, Bergmann EJ, Biddinger DJ, Dieckhoff C, Dively G, Fraser H, Gariepy T, Hamilton G, Haye T, Herbert A, Hoelmer K, Hooks CR, Jones A, Krawczyk G, Kuhar T, Martinson H, Mitchell W, Nielsen AL, Pfeiffer DG, Raupp MJ, Rodriguez-Saona C, Shearer P, Shrewsbury P, Venugopal PD, Whalen J, Wiman NG, Leskey TC, Tooker JF (2014) Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). Journal of Integrated Pest Management 5(3): 1–13. https://doi.org/10.1603/IPM14002
- Rollins LA, Woolnough AP, Sinclair R, Mooney NJ, Sherwin WB (2011) Mitochondrial DNA offers unique insights into invasion history of the common starling: Mitochondrial DNA in invasive populations. Molecular Ecology 20(11): 2307–2317. https://doi.org/10.1111/j.1365-294X.2011.05101.x
- Rot M, Devetak M, Carlevaris B, Žežlina J, Žežlina I (2018) First record of brown marmorated stink bug (Halyomorpha halys Stål, 1855) (Hemiptera: Pentatomidae) in Slovenia. Acta Entomologica Slovenica 26: 5–12. https://doi.org/10.3390/insects12060505
- Ryan SF, Lombaert E, Espeset A, Vila R, Talavera G, Dincă V, Doellman MM, Renshaw MA, Eng MW, Hornett EA, Li Y, Pfrender ME, Shoemaker D (2019) Global invasion history of the agricultural pest butterfly Pieris rapae revealed with genomics and citizen science. Proceedings of the National Academy of Sciences of the United States of America 116(40): 20015–20024. https://doi.org/10.1073/pnas.1907492116
- Schuler H, Elser D, Fischnaller S (2020) Population genetics of the brown marmorated stink bug Halyomorpha halys in the early phase of invasion in South Tyrol (Northen Italy). Bulletin of Entomological Research 111(4): 394–401. https://doi.org/10.1017/S0007485320000553
- Šeat J (2015) Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) a new invasive species in Serbia. Acta Entomologica Serbica 20: 167–171.
- Sheard JK, Rahbek C, Dunn RR, Sanders NJ, Isaac NJB (2021) Long-term trends in the occupancy of ants revealed through use of multi-sourced datasets. Biology Letters 17(10): e20210240. https://doi.org/10.1098/rsbl.2021.0240
- Stoeckli S, Felber R, Haye T (2020) Current distribution and voltinism of the brown marmorated stink bug, Halyomorpha halys, in Switzerland and its response to climate change using a high-resolution CLIMEX model. International Journal of Biometeorology 64(12): 2019–2032. https://doi.org/10.1007/s00484-020-01992-z
- Streito J-C, Chartois M, Pierre E, Dusoulier F, Armand J-M, Gaudin J, Rossi J-P (2021) Citizen science and niche modeling to track and forecast the expansion of the brown marmorated stinkbug Halyomorpha halys (Stål, 1855). Scientific Reports 11(1): e11421. https://doi.org/10.1038/s41598-021-90378-1
- Valentin RE, Nielsen AL, Wiman NG, Lee D-H, Fonseca DM (2017) Global invasion network of the brown marmorated stink bug, Halyomorpha halys. Scientific Reports 7(1): e9866. https://doi.org/10.1038/s41598-017-10315-z
- Verbond van Belgische Tuinbouwcoöperaties (2022) Verbond van Belgische Tuinbouwcoöperaties. Annual report. https://www.vbt.eu/en/annual-reports
- 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. https://doi.org/10.11646/zootaxa.3780.1.8
- Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10: 506–513.
- Xu J, Fonseca DM, Hamilton GC, Hoelmer KA, Nielsen AL (2014) Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys. Biological Invasions 16(1): 153–166. https://doi.org/10.1007/s10530-013-0510-3
- Yan J, Pal C, Anderson D, Vétek G, Farkas P, Burne A, Fan Q-H, Zhang J, Gunawardana DN, Balan RK, George S, Li D (2021) Genetic diversity analysis of brown marmorated stink bug, Halyomorpha halys based on mitochondrial COI and COII haplotypes. BMC Genomic Data 22(1): 1–7. https://doi.org/10.1186/s12863-021-00961-8
- Zattara EE, Aizen MA (2021) Worldwide occurrence records suggest a global decline in bee species richness. One Earth 4(1): 114–123. https://doi.org/10.1016/j.oneear.2020.12.005
- Zhu G-P, Ye Z, Du J, Zhang D-L, Zhen Y, Zheng C, Zhao L, Li M, Bu W-J (2016) Range wide molecular data and niche modeling revealed the Pleistocene history of a global invader (Halyomorpha halys). Scientific Reports 6(1): e23192. https://doi.org/10.1038/srep23192