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Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys

Authors:
  • Ragon Institute of MGH, MIT and Harvard & Havard Medical School

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Identifying the origin of a biological invasion has important applications to the effective control of the invaders. This is more critical for invasive agricultural pests that cause severe economic losses. The brown marmorated stink bug, Halyomorpha halys, originally from East Asia, has become a principal agricultural pest in the US since its first detection in Pennsylvania in 1996. This species is responsible for crop failures on many mid-Atlantic farms and current control efforts rely on heavy insecticide applications because no other options are available. To examine the genetic diversity and identify the source region of the US introductions, we sequenced portions of the mitochondrial cytochrome c oxidase subunit II gene, 12S ribosomal RNA gene and control region in populations from the US, China, South Korea and Japan. We detected high genetic divergence among native populations and traced the origin of US H. halys to the Beijing area in China. We observed much lower genetic diversity in exotic compared to native populations—two mitochondrial haplotypes in 55 US specimens versus 43 haplotypes in 77 native specimens. A single introduction of small propagule size matches the invasion history in the US. For the effective control of the US population, we suggest that surveys on egg parasitoids and insecticide resistance in natives should focus on the Beijing area in China.
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... Over the last few decades, methods to reconstruct the invasion history of biological invasions , and in particular of human mediated invasions (Lombaert et al., 2011), using molecular markers have improved substantially (Cristescu, 2015). Using the cytochrome oxidase 2 and a fragment starting on the 12S ribosomal RNA and spanning part of the control region, Xu et al. (2013) detected only two haplotypes in BMSB collected in the northeastern U.S. From this, the authors concluded that BMSB might be introduced from the Bejing area in China. In the present study, we investigated the geographic origins of BMSB in the western U.S. (California, Oregon and Washington states) following the same approach as Xu et al. (2013). ...
... Using the cytochrome oxidase 2 and a fragment starting on the 12S ribosomal RNA and spanning part of the control region, Xu et al. (2013) detected only two haplotypes in BMSB collected in the northeastern U.S. From this, the authors concluded that BMSB might be introduced from the Bejing area in China. In the present study, we investigated the geographic origins of BMSB in the western U.S. (California, Oregon and Washington states) following the same approach as Xu et al. (2013). In total, 125 individuals were collected from the field, preserved in ethanol and shipped to EBCL for DNA extraction and subsequent genetic analysis. ...
... In total, 125 individuals were collected from the field, preserved in ethanol and shipped to EBCL for DNA extraction and subsequent genetic analysis. We detected a total of five haplotypes, two of them being already found in the eastern U.S. by Xu et al. (2013). While the eastern U.S. pest populations match a single source in the Bejing region in China, the overall genetic structure observed in the western U.S. suggested a more complex invasion scenario, encompassing several introduction events from different sources in China, including the Beijing area and also potentially from Japan. ...
Chapter
Full-text available
This proceedings contains papers dealing with issues affecting biological control, particularly pertaining to the use of parasitoids and predators as biological control agents. This includes all approaches to biological control: conservation, augmentation, and importation of natural enemy species for the control of arthropod targets, as well as other transversal issues related to its implementation. It has 14 sessions addressing the most relevant and current topics in the field of biological control of arthropods: (i) Accidental introductions of biocontrol agens: positive and negative aspects; (ii) The importance of pre and post release genetics in biological control; (iii) How well do we understand non-target impacts in arthropod biological control; (iv) Regulation and access and benefit sharing policies relevant for classical biological control approaches; (v) The role of native and alien natural enemy diversity in biological control; (vi) Frontiers in forest insect control; (vii) Biocontrol marketplace I; (viii) Weed and arthropod biological control: mutual benefits and challenges; (ix) Maximizing opportunities for biological control in Asia's rapidly changing agro-environments; (x) Biological control based integrated pest management: does it work?; (xi) Exploring the compatibility of arthropod biological control and pesticides: models and data; (xii) Successes and uptake of arthropod biological control in developing countries; (xiii) Socio-economic impacts of biological control; (xiv) Biocontrol marketplace II.
... Over the last few decades, methods to reconstruct the invasion history of biological invasions , and in particular of human mediated invasions (Lombaert et al., 2011), using molecular markers have improved substantially (Cristescu, 2015). Using the cytochrome oxidase 2 and a fragment starting on the 12S ribosomal RNA and spanning part of the control region, Xu et al. (2013) detected only two haplotypes in BMSB collected in the northeastern U.S. From this, the authors concluded that BMSB might be introduced from the Bejing area in China. In the present study, we investigated the geographic origins of BMSB in the western U.S. (California, Oregon and Washington states) following the same approach as Xu et al. (2013). ...
... Using the cytochrome oxidase 2 and a fragment starting on the 12S ribosomal RNA and spanning part of the control region, Xu et al. (2013) detected only two haplotypes in BMSB collected in the northeastern U.S. From this, the authors concluded that BMSB might be introduced from the Bejing area in China. In the present study, we investigated the geographic origins of BMSB in the western U.S. (California, Oregon and Washington states) following the same approach as Xu et al. (2013). In total, 125 individuals were collected from the field, preserved in ethanol and shipped to EBCL for DNA extraction and subsequent genetic analysis. ...
... In total, 125 individuals were collected from the field, preserved in ethanol and shipped to EBCL for DNA extraction and subsequent genetic analysis. We detected a total of five haplotypes, two of them being already found in the eastern U.S. by Xu et al. (2013). While the eastern U.S. pest populations match a single source in the Bejing region in China, the overall genetic structure observed in the western U.S. suggested a more complex invasion scenario, encompassing several introduction events from different sources in China, including the Beijing area and also potentially from Japan. ...
Chapter
This proceedings contains papers dealing with issues affecting biological control, particularly pertaining to the use of parasitoids and predators as biological control agents. This includes all approaches to biological control: conservation, augmentation, and importation of natural enemy species for the control of arthropod targets, as well as other transversal issues related to its implementation. It has 14 sessions addressing the most relevant and current topics in the field of biological control of arthropods: (i) Accidental introductions of biocontrol agens: positive and negative aspects; (ii) The importance of pre and post release genetics in biological control; (iii) How well do we understand non-target impacts in arthropod biological control; (iv) Regulation and access and benefit sharing policies relevant for classical biological control approaches; (v) The role of native and alien natural enemy diversity in biological control; (vi) Frontiers in forest insect control; (vii) Biocontrol marketplace I; (viii) Weed and arthropod biological control: mutual benefits and challenges; (ix) Maximizing opportunities for biological control in Asia's rapidly changing agro-environments; (x) Biological control based integrated pest management: does it work?; (xi) Exploring the compatibility of arthropod biological control and pesticides: models and data; (xii) Successes and uptake of arthropod biological control in developing countries; (xiii) Socio-economic impacts of biological control; (xiv) Biocontrol marketplace II.
... (pears), Prunus spp. (cherries, apricots, peaches, plums) (Yanagi & Hagihara, 2008;Xu et al., 2014). el tráfico comercial en los países de la ribera norte del Mediterráneo conectados vía puertos. ...
... (peras), Prunus spp. (cerezas, albaricoques, melocotones, ciruelas) (Yanagi & Hagihara, 2008;Xu et al., 2014). ...
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In the last decades the Asiatic brown marmorated stink bug Halyomorpha halys (Stål, 1855) (BMSB) infested North America and recently Europe, where it was recorded in many countries. The new record from Algeria is recent (2021) and concerns an adult photographed in the city of Skikda at the Mediterranean coast of the country. There is a penetration of pests in Algeria by commercial business, mainly from Spain and Morocco, probably in the area of the port. Skikda is connected to other Mediterranean ports from coast to coast on a daily basis.
... PCR priming sites are, therefore, at best, only conserved enough for very closely related species. Consequently, the effort and resources to develop the method by species have been constrained to those pests considered very high-risk based on their economic, environmental, or social impact and global invasion patterns [9][10][11][12][13][14]. Unfortunately, a lot of exotic insects which arrive, and those which may become established, do not have this status but represent potential hazards nonetheless, for which populationlevel data would be beneficial [15]. ...
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Biosecurity responses to post-border exotic pest detections are more effective with knowledge of where the species may have originated from or if recurrent detections are connected. Population genetic markers for this are typically species-specific and not available in advance for any but the highest risk species, leaving other less anticipated species difficult to assess at the time. Here, new degenerate PCR primer sets are designed for within the Lepidoptera and Diptera for the 3′ COI, ND3, ND6, and 3′ plus 5′ 16S gene regions. These are shown to be universal at the ordinal level amongst species of 14 and 15 families across 10 and 11 dipteran and lepidopteran superfamilies, respectively. Sequencing the ND3 amplicons as an example of all the loci confirmed detection of population-level variation. This supported finding multiple population haplotypes from the publicly available sequences. Concatenation of the sequences also confirmed that higher population resolution is achieved than for the individual genes. Although as-yet untested in a biosecurity situation, this method is a relatively simple, off-the-shelf means to characterise populations. This makes a proactive contribution to the toolbox of quarantine agencies at the time of detection without the need for unprepared species-specific research and development.
... Populations subsequently spread and became established in most eastern and midwestern states and in at least four western states (StopBMSB.org). Low genetic diversity among H. halys in the eastern USA suggests these populations are the result of a single introduction from near Beijing, China, into eastern Pennsylvania (Xu et al. 2014;Valentin et al. 2017). Greater genetic diversity among western US populations suggest separate and multiple introductions from China (Valentin et al. 2017). ...
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Brown marmorated stink bug, Halyomorpha halys (Stål), is an invasive pest of Asian origin first detected in North Carolina in 2009. By 2015, it became an important pest in the mountain and Piedmont regions, but its population densities have remained low in the eastern plains regions. Starting with a cohort of diapausing adults in January of 2018 and 2019, semi-field cage studies were used to document the phenology and reproductive capacity of H. halys through October of each year at Mills River (mountains) and Goldsboro (Southeastern Plains) sites, which have the same photoperiod, but different temperature profiles. Halyomorpha halys was univoltine in the cooler mountain site, but bivoltine in the warmer plains site, leading to earlier emergence from overwintering diapause, greater heat unit accumulations, and a F1 adult generation that emerged before on-set of diapause-inducing conditions, which allowed for an F2 generation. However, only 17.2% of ovipositing F1 females laid egg masses that hatched, compared to > 90% of overwintered females. Poor establishment of H. halys in the plains versus mountains was attributed to heat stress that contributed to a higher percentage of overwintered adults that emerged early and did not oviposit, a truncated oviposition pattern by overwintered adults, and poor F2 egg hatch. Quadratic equations fit relationships between cumulative degree-days from biofix and proportional oviposition and adult eclosion of respective generations. Utility of the phenology model on a wider scale will depend on how well H. halys populations in other areas conform to North Carolina population’s response to photoperiod and temperature.
... The mitochondrial Cytochrome Oxidase I (COI) gene has shown utility in species identification and separation of genetic lineages (Bucklin et al. 2011;Stephens et al. 2011), in particular as it relates to reconstructing routes of invasion (Auger-Rozenberg et al. 2012;Chapman et al. 2015). Although the Cytochrome Oxidase II (COII) gene of H. halys has also been sequenced (Xu et al. 2014;Cesari et al. 2015Cesari et al. , 2018Yan et al. 2021), the COI gene has been used more extensively in the characterisation of the invasion history, diversity and identity of H. halys haplotypes in both native and invaded regions Cesari et al. 2015Cesari et al. , 2018Zhu et al. 2016;Morrison et al. 2017;Valentin et al. 2017;Lee et al. 2018;Horwood et al. 2019;Schuler et al. 2020;Yan et al. 2021). Based on the COI haplotype analysis of H. halys, it has been suggested that multiple invasion events took place in the initial / early stages of invasion in Europe (2007)(2008)(2009)(2010)(2011)(2012), with the population in Switzerland (primarily haplotype H3 and H8) resulting from the establishment of individuals that arrived directly from China; the population in Italy (primarily H1) resulting from the establishment of individuals from the invasive population in the USA; and the population in Greece (predominantly haplotype H33) resulting from a separate establishment of H. halys from China (Cesari et al. 2015;Gariepy et al. 2015;Valentin et al. 2017). ...
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The arrival, establishment and pest status of Halyomorpha halys in Europe and non-native countries in Asia have been well-documented, with thorough characterisation of the genetic diversity and occurrence of cytochrome oxidase I (COI) haplotypes in Switzerland, France, Hungary, Italy and Greece. However, a number of gaps exist in terms of the characterisation of the haplotype diversity and occurrence of H. halys along the invasion front that covers eastern Europe, western and central Asia. To contribute towards filling this gap, the COI haplotype diversity and distribution were investigated for H. halys collected in Serbia, Ukraine, Russia, Georgia and Kazakhstan. A total of 646 specimens were analysed and five haplotypes were found (H1, H3, H8, H33 and H80). Haplotype H1 was present in all five countries investigated and was the only haplotype detected amongst > 500 specimens collected from Ukraine, Russia and Georgia. H1 (82%) was the dominant haplotype found in Kazakhstan, alongside H3 (18%). In contrast to the low or no diversity observed in these four countries, Serbia had higher haplotype diversity and was represented by five haplotypes. Although H3 was dominant (47%) in Serbia, H1 was also prevalent (40%); the remaining haplotypes (H8, H33 and H80) were minor contributors (1–11%) to the haplotype composition. The results are discussed in context with other known populations in neighbouring countries and patterns of haplotype diversity indicate the movement of successful invasive populations in Europe to generate secondary invasions along the eastern front of the invasion in Eurasia. Possible scenarios regarding the spread of particular haplotypes in these regions are discussed, along with suggestions for future research to fill existing gaps.
... For those countries that have not been invaded, effective biosurveillance tools are of great importance. This is especially relevant in light of research confirming that initial populations within the USA originated from a single incursion from Beijing, China, with a predicated propagule size of two gravid females (Xu et al., 2014), indicating that a high level of sensitivity and precision is necessary for biosecurity programs. Moreover, uninvaded southern hemisphere countries such as New Zealand have experienced a noticeable increase in H. halys interceptions over recent years from northern hemisphere regions with invasive populations present, these are particularly prevalent during the insects' overwintering period (Duthie et al., 2012). ...
Article
The brown marmorated stink bug, Halyomorpha halys Stål (Hemiptera: Pentatomidae), is an invasive pest in America, Europe and Asia and causes serious economic loss to crops, and nuisance problems during overwintering. Uninvaded southern hemisphere countries, such as New Zealand and Australia, see an increase in H. halys border interceptions during the northern hemisphere populations’ overwintering period as large aggregations of H. halys can settle to diapause in items for export, e.g. vehicles, containers, etc. Here, we explored aspects of diapausing H. halys behaviour relative to release and perception of defensive odour compounds. First, to determine whether group size and agitation affect the release of defensive odours, diapausing H. halys were confined in glass tubes as individuals or in varying group sizes and mechanically agitated or remained stationary and the presence or absence of defensive odours was recorded. Using gas chromatography-mass spectrometry, we also established if exposure to individual defensive odour components (tridecane, (E)-2-decenal, 4-oxo-(E)-2-hexenal, and dodecane) induced individuals to release defensive compounds. Additionally, H. halys dispersal was measured in the laboratory following exposure to individual components of their defensive odour or their natural blend. We found that agitating individual bugs did not induce the release of defensive odours. The release of human-detectable odours was only found in groups of mechanically agitated H. halys, whereas non-agitated bugs did not emit odour. Exposure to 4-oxo-(E)-2-hexenal was the only odour component that resulted in individual H. halys releasing defensive compounds. Diapausing H. halys exposure to the natural blend of defensive compounds resulted in increased horizontal distance moved and velocity, while tridecane exposure increased distance moved, velocity and angular velocity, and (E)-2-decenal exposure increased distance moved. Our behavioural and chemical data suggest that defensive compounds released by diapausing H. halys act as an alarm pheromone, particularly when adults are in aggregations.
... The mitochondrial Cytochrome Oxidase I (COI) gene has shown utility in species identification and separation of genetic lineages (Bucklin et al. 2011;Stephens et al. 2011), in particular as it relates to reconstructing routes of invasion (Auger-Rozenberg et al. 2012;Chapman et al. 2015). Although the Cytochrome Oxidase II (COII) gene of H. halys has also been sequenced (Xu et al. 2014;Cesari et al. 2015Cesari et al. , 2018Yan et al. 2021), the COI gene has been used more extensively in the characterisation of the invasion history, diversity and identity of H. halys haplotypes in both native and invaded regions Cesari et al. 2015Cesari et al. , 2018Zhu et al. 2016;Morrison et al. 2017;Valentin et al. 2017;Lee et al. 2018;Horwood et al. 2019;Schuler et al. 2020;Yan et al. 2021). Based on the COI haplotype analysis of H. halys, it has been suggested that multiple invasion events took place in the initial / early stages of invasion in Europe (2007)(2008)(2009)(2010)(2011)(2012), with the population in Switzerland (primarily haplotype H3 and H8) resulting from the establishment of individuals that arrived directly from China; the population in Italy (primarily H1) resulting from the establishment of individuals from the invasive population in the USA; and the population in Greece (predominantly haplotype H33) resulting from a separate establishment of H. halys from China (Cesari et al. 2015;Gariepy et al. 2015;Valentin et al. 2017). ...
Article
The arrival, establishment and pest status of Halyomorpha halys in Europe and non-native countries in Asia have been well-documented, with thorough characterisation of the genetic diversity and occurrence of cytochrome oxidase I (COI) haplotypes in Switzerland, France, Hungary, Italy and Greece. However, a number of gaps exist in terms of the characterisation of the haplotype diversity and occurrence of H. halys along the invasion front that covers eastern Europe, western and central Asia. To contribute towards filling this gap, the COI haplotype diversity and distribution were investigated for H. halys collected in Serbia, Ukraine, Russia, Georgia and Kazakhstan. A total of 646 specimens were analysed and five haplotypes were found (H1, H3, H8, H33 and H80). Haplotype H1 was present in all five countries investigated and was the only haplotype detected amongst > 500 specimens collected from Ukraine, Russia and Georgia. H1 (82%) was the dominant haplotype found in Kazakhstan, alongside H3 (18%). In contrast to the low or no diversity observed in these four countries, Serbia had higher haplotype diversity and was represented by five haplotypes. Although H3 was dominant (47%) in Serbia, H1 was also prevalent (40%); the remaining haplotypes (H8, H33 and H80) were minor contributors (1–11%) to the haplotype composition. The results are discussed in context with other known populations in neighbouring countries and patterns of haplotype diversity indicate the movement of successful invasive populations in Europe to generate secondary invasions along the eastern front of the invasion in Eurasia. Possible scenarios regarding the spread of particular haplotypes in these regions are discussed, along with suggestions for future research to fill existing gaps.
... Halyomorpha halys adult body size varies from 12 to 17 mm long and 7-10 mm wide (Hoebeke and Carter 2003). Adults and nymphs (except the 1 st instar) have two white Halyomorpha halys is native to East Asia, particularly China, Taiwan, Japan, and South Korea (Xu et al. 2014), and has become an invasive pest outside of this range, where it occurs in the rest of the world. Halyomorpha halys was first detected in the eastern United States in the late 1990s (Hoebeke and Carter 2003) and has spread to over 47 U.S. states and 4 Canadian provinces (Stop BMSB 2021). ...
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