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Recent range expansion of brown marmorated stink bug in Europe

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Abstract

A public survey to determine the current distribution of the invasive brown marmortaed stink bug, Halyomorpha halys in Switzerland showed that by the end of 2013, it was present in 11 Cantons, including six newly invaded Cantons (Basel-Landschaft, Aargau, Genève, Solothurn, Ticino, Thurgau, and Bern). In total, H. halys was found in 76 locations in 38 cities across Switzerland with large breading populations being present in the cities Zurich, Basel, Bern, and Lugano. There is now evidence that H. halys was already present in 2004, three years before its first official detection in 2007. Although H. halys has been present in Switzerland for nearly 10 years, its natural spread can be considered slow. Large distribution gaps between Swiss cities Zurich, Basel and Bern indicate that founder populations from Zurich arrived in these locations through human activity and movement of goods along the main motorways connecting the cities. The new list of host plants in Europe contains 51 host plants in 32 families, including many exotic and native plants. High densities of nymphs and adults were observed on Catalpa bignonioides, Sorbus aucuparia, Cornus sanguinea, Fraxinus excelsior, and Parthenocissus quinquefolia. With growing populations in Switzerland, France and Italy H. halys may further extend its distribution and become a nuisance pest in many European cities.
... The brown marmorated stink bug (BMSB), Halyomorpha halys (Stål, 1855) (Hemiptera: Pentatomidae), is native to China, Korea, Taiwan, Japan, and Vietnam (Josifov and Kerzhner 1978;Rider et al. 2002). It has been introduced in North and South America (Hoebeke and Carter 2003;Faúndez and Rider 2017) as well as in Europe, where it was first detected in 2004, in Switzerland (Haye et al. 2014). Halyomorpha halys is an invasive polyphagous species, which is able to cause heavy feeding damage to many cultivated plants of major economic significance, such as apple, pear, peach, citrus fruits, hazelnut, tomato, pepper and sweet corn Leskey et al. 2012; Bariselli et al. 2016;Vétek and Korányi 2017;Bosco et al. 2018;Musolin et al. 2018). ...
... The international flight connections from this airport are available to many cities of continental Europe, such as Athens, Basel, Belgrade, Bucharest, Budapest, Milan and Zurich (Hermes Airports 2020). These are locations where the presence of large populations of H. halys has already been observed (Ciceoi et al. 2017;Gariepy et al. 2015;Haye et al. 2014;Maistrello et al. 2018;Vétek et al. 2018;Vétek personal observation). Also the airport of Paphos, which can be found a few kilometres away from the city harbour popular with tourists, is available from several of these towns (Hermes Airports 2020). ...
... Involvement of citizen scientists has been considered to be extremely useful for early detection of invasive pests ). In the case of H. halys, both approaches (i.e., targeted trapping and the involvement of the public in data collection) have already proved to be suitable for obtaining data quickly, broadly and even relatively inexpensively on the occurrence of this particular pest (Haye et al. 2014;Maistrello et al. 2016;Vétek et al. 2018;Tassini and Mifsud 2019). ...
... It has been introduced in North and South America (Hoebeke and Carter 2003;Faúndez and Rider 2017) as well as in Europe, where it was first detected in Citation: Vétek G, Melifronidou-Pantelidou A, Koukkoularidou D, Martinou A (2021) Initiation of a monitoring programme for early detection of Halyomorpha halys in Cyprus by using pheromone-baited traps and involving citizen science. Management of Biological Invasions 12 (in press) 2004, in Switzerland (Haye et al. 2014). Halyomorpha halys is an invasive polyphagous species, which is able to cause heavy feeding damage to many cultivated plants of major economic significance, such as apple, pear, peach, citrus fruits, hazelnut, tomato, pepper and sweet corn Leskey et al. 2012; Bariselli et al. 2016;Vétek and Korányi 2017;Bosco et al. 2018;Musolin et al. 2018). ...
... The international flight connections from this airport are available to many cities of continental Europe, such as Athens, Basel, Belgrade, Bucharest, Budapest, Milan and Zurich (Hermes Airports 2020). These are locations where the presence of large populations of H. halys has already been observed (Ciceoi et al. 2017;Gariepy et al. 2015;Haye et al. 2014;Maistrello et al. 2018;Vétek et al. 2018;Vétek personal observation). Also the airport of Paphos, which can be found a few kilometres away from the city harbour popular with tourists, is available from several of these towns (Hermes Airports 2020). ...
... Involvement of citizen scientists has been considered to be extremely useful for early detection of invasive pests ). In the case of H. halys, both approaches (i.e., targeted trapping and the involvement of the public in data collection) have already proved to be suitable for obtaining data quickly, broadly and even relatively inexpensively on the occurrence of this particular pest (Haye et al. 2014;Maistrello et al. 2016;Vétek et al. 2018;Tassini and Mifsud 2019). ...
... This pest is native to East Asia [2]. The earliest records of the pest in North America date back to 2001 and that in Europe to 2004 [3,4]. The spread, feeding, and reproduction of the species are highly linked to anthropogenic activities [5][6][7][8]. ...
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Qualitative and quantitative parameters of tomatoes are impaired by Halyomorpha halys Stål (Hemiptera: Pentatomidae), which cause severe economic losses worldwide. Our aims were to assess H. halys-induced tissue damage in tomatoes via computer tomography and to confirm the results of imaging obtained by analytical methods. Our examination confirmed the intensification of the change in the inner structure of damaged tomatoes as a function of time. The tendency of this destruction triggered by bug saliva grew exponentially from the exocarp layer to the inner placenta. The destruction of the plant tissue was aggravated by an increase in the number of bugs, as it was unequivocally evinced by the shell thickness assays. The results of the assessment of the antioxidant capacity of tomato mesocarp showed a distinct decrease in the antioxidant capacity of the samples obtained from H. halys-infested tomatoes. This indicates that the ferric-reducing antioxidant power value was related to the degradation processes of the mesocarp tissue in tomato fruit caused by the watery saliva released by H. halys. The presented experimental method can be suitable for the qualitative control of the vegetable items intended for trade, which can help for the isolation of tomatoes damaged by bugs immediately after harvest.
... The method of Finney 75 was used to determine the lethal time (LT 50 ) of the probit analysis. Calculation of the lethal concentration (LC) and its 95% confidence limits (CL) was performed based on accurate estimation of log (CL) variances 76 . The Kaplan-Meier survival analysis technique was used to describe both, the median lethal time (LT 50 ) (the number of days until 50% of the insects were dead, for each treatment) and the mean survival time (SPSS 23.0). ...
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Dactylopius opuntiae (Cockerell) (Hemiptera: Dactylopiidae) or prickly pear cochineal, is the most damaging pest on cactus species with heavy economic losses worldwide. The efficacy of two Moroccan EPN isolates; Steinernema feltiae (Filipjev) (Rhabditida: Steinernematidae) and Heterorhabditis bacteriophora (Poinar) (Rhabditida: Heterorhabditidae) (applied at 25, 50, and 75 IJs cm−2) against D. opuntiae nymphs and young females were evaluated under both laboratory bioassays and field conditions. Results showed that S. feltiae was more effective, causing higher mortality of nymphs and adult females (98.8% and 97.5%, respectively) after 8 days of exposure, resulting in an LT50 value of 5.9 days (nymph) and 6.0 days (young female). While, H. bacteriophora had lower mortalities (83.8% for nymph and 81.3% for adult females). For the cochineal nymphs and adult females, no significant difference was observed among S. feltiae at 25, 50, and 75 IJs cm−2, and the positive control, D-limonene applied at 0.5 g/L which was used due to its high effectiveness against nymphs and females of D. opuntiae. In the field experiment, D-limonene at 0.5 g/L and S. feltiae applied at 75 IJs cm−2 were effective in reducing nymph and adult female populations by 85.3–93.9% at 12 days of post exposure period. To our knowledge, this work is the first report on the use of EPNs to control D. opuntiae. Thus, in addition to D-limonene, both Moroccan EPN isolates S. feltiae, and H. bacteriophora could be used as part of the integrated pest management strategy against D. opuntiae. Many factors such as temperature can affect the establishment and effectiveness of EPNs under field conditions. Therefore, additional studies under field conditions are needed.
... In addition, adults are very good fliers and can travel distances from a few to more than 100 km (Lee and Leskey, 2015). Haye et al. (2014) reported that the natural spread of H. halys in Switzerland was relatively slow over a period of almost 10 years. However, the results from Croatia indicated the pest has spread quite rapidly only one year after the first detection in 2018 in Zagreb. ...
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The brown marmorated stink bug (Halyomorpha halys (Stål, 1855)) is an extremely polyphagous invasive insect originating from East Asia. It causes damage by feeding on fruit trees and shrubs, legumes, forest trees, and ornamental shrubs and trees. The pest has successfully established in North America and Europe and causes economic damage to agricultural production. The first discovery of H. halys in Croatia occurred in 2017 in the coastal region in Rijeka. In 2018, the pest was sporadically observed in urban areas of Sveta Nedelja, Zagreb and Vukovar, and a total of 22 specimens of H. halys were found in single and multi-family houses in eight locations. The discovery of the species in the continental part of the country is evidence of the spread of this species in Croatia. During 2019, the first mass occurrence of the pest was detected in the rural area of Zagreb (Drenčec) in a soybean field. A total of 723 specimens of H. halys were identified. The average number of stink bugs per 10 plants was 14 specimens, which poses a serious threat to soybean production in the area. The very rapid spread of the pest from urban to rural areas and the establishment of its local populations is evidence of the invasive nature of the species and a warning signal for farmers in Croatia. To prevent the spread and mass occurrence of H. halys on agricultural land and to minimise possible damage to agricultural production, it is necessary to constantly monitor the pest and, if necessary, to take appropriate protective measures in agriculture.
... The same scenario of invasion occurred after its introduction in Europe in 2004 [9]. In 15 years, H. halys managed to colonize almost all climatically suitable areas in Europe [10][11][12][13][14][15][16][17][18][19][20][21][22] and became one of the most serious agriculture pests, as well as a nuisance insect in urban environments [23]. Due to the damage caused by H. halys and subsequent economic losses, the use of insecticides has substantially increased in commercial orchards [24], disrupting established integrated pest management programs for different crops in the USA and Europe [25][26][27]. ...
Article
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Halyomorpha halys (Hemiptera: Pentatomidae), native to East Asia, has become a globally invasive pest, as a serious threat to agricultural production and a notorious nuisance pest in urban areas. Considerable efforts have been made so far to develop effective pest control measures to prevent crop damage. Biological control of this invasive stink bug by egg parasitoids has proven to be the most environmentally sustainable long-term solution. Knowledge of the native egg parasitoid fauna is of key importance when implementing a biological control program. Therefore, the main objective of our study was to detect egg parasitoid species associated with H. halys in the Goriška region (Western Slovenia) and to evaluate their impact on the pest population under field conditions. In the years 2019 and 2020, around 4600 H. halys eggs were collected in the wild and more than 3400 sentinel eggs were exposed to detect parasitoids in the field. Five egg-parasitoid species emerged from H. halys eggs: Anastatus bifasciatus (Hymenoptera: Eupelmidae), Telenomus sp., Trissolcus basalis, Trissolcus mitsukurii (Hymenoptera: Scelionidae) and Ooencyrtus telenomicida (Hymenoptera: Encyrtidae), all of them are new records for Slovenia. The native species, An. bifasciatus, dominated in urban and suburban areas, while non-native Tr. mitsukurii prevailed in agricultural areas. Overall parasitism rates of naturally laid eggs by the parasitoid species complex in 2019 and 2020 was 3.0 and 14.4%, respectively. Rapid recruitment of native parasitoids, early detection of an effective alien parasitoid species and increasing overall parasitism rates are very encouraging results, which need to be followed and verified in future research.
... Since first detected in the USA in 1996 [41], BMSB has invaded many neighbouring countries. In Europe, BMSB was first recorded in Switzerland in 2004 [14,21,42], then spread to many countries such as Germany, France, Italy, Georgia and Hungary [43][44][45]. Therefore, based on the timeline of reports, BMSB invasion might have started in the USA (1996) [2], then Europe (2004) and Chile (2017) [17], though a more transparent history of invasion remains unknown and needs further investigation. ...
Article
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Background Brown marmorated stink bug (BMSB), Halyomorpha halys (Hemiptera: Pentatomidae) is native to East Asia but has invaded many countries in the world. BMSB is a polyphagous insect pest and causes significant economic losses to agriculture worldwide. Knowledge on the genetic diversity among BMSB populations is scarce but is essential to understand the patterns of colonization and invasion history of local populations. Efforts have been made to assess the genetic diversity of BMSB using partial mitochondrial DNA sequences but genetic divergence on mitochondria is not high enough to precisely accurately identify and distinguish various BMSB populations. Therefore, in this study, we applied a ddRAD (double digest restriction-site associated DNA) sequencing approach to ascertain the genetic diversity of BMSB populations collected from 12 countries (2 native and 10 invaded) across four continents with the ultimate aim to trace the origin of BMSBs intercepted during border inspections and post-border surveillance. Result A total of 1775 high confidence single nucleotide polymorphisms (SNPs) were identified from ddRAD sequencing data collected from 389 adult BMSB individuals. Principal component analysis (PCA) of the identified SNPs indicated the existence of two main distinct genetic clusters representing individuals sampled from regions where BMSB is native to, China and Japan, respectively, and one broad cluster comprised individuals sampled from countries which have been invaded by BMSB. The population genetic structure analysis further discriminated the genetic diversity among the BMSB populations at a higher resolution and distinguished them into five potential genetic clusters. Conclusion The study revealed hidden genetic diversity among the studied BMSB populations across the continents. The BMSB populations from Japan were genetically distant from the other studied populations. Similarly, the BMSB populations from China were also genetically differentiated from the Japanese and other populations. Further genetic structure analysis revealed the presence of at least three genetic clusters of BMSB in the invaded countries, possibly originating via multiple invasions. Furthermore, this study has produced novel set of SNP markers to enhance the knowledge of genetic diversity among BMSB populations and demonstrates the potential to trace the origin of BMSB individuals for future invasion events.
... Native to East Asia, the brown marmorated stink bug (BMSB), Halyomorpha halys (Stål) (Rhynchota, Pentatomidae) is an invasive herbivore pest insect, in the USA, Canada, and Europe (Arnold, 2009;CABI/EPPO, 2013;Haye et al., 2014;Haye & Zimmerman, 2017;Lee et al., 2013;Leskey et al., 2012;Zhang et al., 2013). H. halys is highly polyphagous, feeding and damaging over 170 diverse plants, including economically important field crops, vegetables, tree fruits, row crops and ornamentals. ...
... Native to East Asia, the brown marmorated stink bug (BMSB), Halyomorpha halys (Stål) (Rhynchota, Pentatomidae) is an invasive herbivore pest insect, in the USA, Canada, and Europe (Arnold, 2009;CABI/EPPO, 2013;Haye et al., 2014;Haye & Zimmerman, 2017;Lee et al., 2013;Leskey et al., 2012;Zhang et al., 2013). H. halys is highly polyphagous, feeding and damaging over 170 diverse plants, including economically important field crops, vegetables, tree fruits, row crops and ornamentals. ...
Article
Full-text available
The brown marmorated stink bug Halyomorpha halys is one of the most harmful invasive insect species worldwide. Originating from Asia, this species invaded first North America and later the European continent, where it has soon become widely spread. There have been no official data of the presence of H. halys on territory of the Republic of North Macedonia, although the species was recorded in the neighbouring countries: Serbia, Bulgaria, Greece and most recently in Albania. This paper reports the first record of H. halys in two regions of R. North Macedonia: in the town of Gevgelija, situated close to the Greek border and in the capital Skopje. The transport as a stowaway and natural dispersal across borders are discussed as potential pathways of introduction of the pest species in this country. The establishment and further spread of H. halys in R. North Macedonia could be expected in the future.
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