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23 October 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
Erica Jean Kistner
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The invasive brown marmorated stink bug, Halyomorpha halys (Stål; Hemiptera: Pentatomidae), has recently emerged as a harmful pest of horticultural crops in North America and Europe. Native to East Asia, this highly polyphagous insect is spreading rapidly worldwide. Climate change will add further complications to managing this species in terms of both geographic distribution and population growth. This study used CLIMEX to compare potential H. halys distribution under recent and future climate models using one emission scenario (A2) with two different global circulation models, CSIRO Mk3.0 and MIROC-H. Simulated changes in seasonal phenology and voltinism were examined. Under the possible future climate scenarios, suitable range in Europe expands northward. In North America, the suitable H. halys range shifts northward into Canada and contracts from its southern temperature range limits in the United States due to increased heat stress. Prolonged periods of warm temperatures resulted in longer H. halys growing seasons. However, future climate scenarios indicated that rising summer temperatures decrease H. halys growth potential compared to recent climatic conditions, which in turn, may reduce mid-summer crop damage. Climate change may increase the number of H. halys generations produced annually, thereby enabling the invasive insect to become multivoltine in the northern latitudes of North America and Europe where it is currently reported to be univoltine. These results indicate prime horticultural production areas in Europe, the northeastern United States, and southeastern Canada are at greatest risk from H. halys under both current and possible future climates.

There is mounting scientific evidence that climate change will exacerbate agricultural losses from insect pests in a number of ways (Porter et al. 1991, Gregory et al. 2009, Ziska et al. 2011). First, numerous crop pests have expanded their range northward since the 1960s due, in part, to rising annual temperatures (Bebber et al. 2013). Second, warmer winter temperatures at higher latitudes are expected to reduce winter die-offs thereby resulting in higher densities of pest insects emerging to feed and reproduce in the spring (Bale et al. 2002). Third, warming induced shifts in phenology may lead to earlier spring emergence and subsequent dispersal of overwintering insects (Bell et al. 2015). Finally, climate change is predicted to increase number of generations produced per year in multivoltine insects which in turn can greatly exacerbate the economic damage caused by these agricultural pests (Tobin et al. 2008, Ziter et al. 2012).

The brown marmorated stink bug, Halyomorpha halys (Stål; Hemiptera: Pentatomidae),an extremely polyphagous insect (Hoebeke and Carter 2003), has recently emerged as a harmful invasive pest in North America and Europe. Originally from East Asia (Lee et al. 2013), H. halys invaded North America in 1996 (Hoebeke and Carter 2003) and Europe around 2004 (Haye et al. 2014). H. halys is capable of being transported very long distances via shipping sea freights, ground transport vehicles, and air transportation (Hoebeke and Carter 2003, Gariepy et al. 2014, Gariepy et al. 2015). In addition, both adult and nymphal stages have a strong dispersal capacity (Lee 2015, Lee and Leskey 2015). Consequently, H. halys has rapidly spread across the United States with detections in 43 states (NIPMC 2017). In Canada, the pest has established breeding populations in southern Ontario including Niagara's apple orchards (Frasier 2016); detections have also been made in the provinces of Quebec, Alberta, and British Colombia (Gariepy et al. 2014, NIPMC 2017). After its initial 2007 detection in Switzerland, H. halys has been spreading across Europe (Haye et al. 2014). Breeding populations are present in Switzerland (Haye et al. 2014), France (Callot and Brua 2013), and Italy (Cesari et al. 2015); individuals have also been detected in Liechtenstein (Arnold 2009), Germany (Heckmann 2012), Hungry (Vétek et al. 2014), Greece (Milonas and Partsinevelos 2014), Serbia (Šeat 2015), Romania (Macavei et al. 2015), Spain (Dioli et al. 2016), and Bulgaria (Simov 2016). In Europe, H. halys appears to be moving eastward given the recent detections in Georgia and Russia (Gapon 2016).

H. halys occurs in a wide range of landscapes, including urban areas, where the insect is considered a nuisance pest (Lee 2015). During winter, H. halys enters a facultative reproductive diapause with adults congregating in protected areas including human-made structures. In its native range of East Asia, H. halys is classified as an outbreak pest of fruit trees (Lee et al. 2013). However, in the United States, H. halys has quickly become a major agricultural pest, especially in fruit tree orchards (Leskey et al. 2012a,b, 2015). This phytophagous pentatomomid has >100 reported host plants including ornamental shrubs, hardwood trees, field crops, as well as a wide range of fruit and vegetable crops (Rice et al. 2014). In 2010, the mid-Atlantic apple industry suffered an estimated ~US$37 million in losses from H. halys feeding damage (USAA 2010). Feeding damage has also been reported in the Pacific Northwest and Midwestern United States (NIPMC 2017). In Europe, H. halys has established in Emilia Romagna, Italy, one of the most important tree fruit and wine producing regions in Europe (Maistrello et al. 2016). In just a few short years after first discovery, H. halys has become a significant fruit pest in Italy, with damages estimated upwards of 40% being reported in fruit orchards where this insect is abundant (Maistrello et al. 2017).

The length and favorability of an insect's growing season impacts agricultural losses by influencing host-crop synchrony and pest densities (Gregory et al. 2009, Ziska et al. 2011). For instance, favorable abiotic conditions, including mild winters and early onset of spring, can lead to massive insect pest outbreaks in some years (Roff 1983, Porter et al. 1991). In the mid-Atlantic region of the United States, H. halys’ growing season aligns well with those of apples and peaches, but pest densities and subsequent economic losses vary both spatially and annually (Leskey et al. 2012a, 2015). Similarly, abiotic conditions during the growing season influence the number of generations produced per year by multivoltine insects like H. halys which in turn can influence crop losses. In northern China and Japan, H. halys has been reported to have one or two generations (reviewed by Lee et al. 2013), while four to six generations per year have been suggested in the southern Chinese province of Guangdong (Hoffman 1933). In the United States, H. halys is reported to be univoltine in Pennsylvania, New Jersey, and New York (Nielsen and Hamilton 2009a) and bivoltine in West Virginia, Virginia, North Carolina (Bakken et al. 2015, Leskey et al. 2015), and California (Ingels et al. 2016). In Europe, H. halys appears to be univoltine in Switzerland (Haye et al. 2014) and bivoltine in Italy (Maistrello et al. 2016).

Climate is often a good predictor for continental scale invasive risk forecasts because invasive species are often limited more by climate than biotic interactions (Dukes and Mooney 1999, Ziska et al. 2011). Kriticos et al. (2017) modeled the potential global distribution of H. halys using the bioclimatic niche model, CLIMEX. This model highlighted several regions at risk for further spread and establishment under current climatic conditions. Climate change will add to the complications of managing such a species because the geographic distribution of H. halys is primarily driven by climate although the non-climatic factors likely influence population densities (Venugopal et al. 2016). Projected rising temperatures may enhance H. halys development and survival particularly in the northern latitudes where winter minimum temperatures are predicted to rise disproportionally faster (Nakicenovic and Swart 2000, Musolin 2007). For instance, mean January and February temperatures influence H. halys overwintering mortality and Kiritani (2006) estimated that each 1°C rise above 4°C would reduce winter mortality by 13.5% in Japan. However, climate change may also negatively impact H. halys distribution and abundance in more southern latitudes where average daily temperatures are likely to rise above H. halys’ upper temperature threshold (Zhu et al. 2016). To date, several ecological niche models have been used to predict the potential global distribution of H. halys under current climatic conditions (Zhu et al. 2012, Haye et al. 2015, Zhu et al. 2017, Kriticos et al. 2017) and possible mid-century climate scenarios (Zhu et al. 2016). However, none of these models address potential changes in H. halys voltinism and phenology that may occur under a changing global climate.

To address this shortcoming, CLIMEX (Hearne Scientific Software Pty Ltd, South Yarra, Australia), a process-based bioclimatic niche modeling package (Kriticos et al. 2015a), was used to compare the potential global geographic distribution and abundance of the invasive H. halys under recent baseline climate and possible future climate scenarios. CLIMEX was chosen because it has a proven track record of reliably modeling the potential distribution of invasive species (Sutherst and Maywald 2005, Kriticos et al. 2015b, Yonow et al. 2016) and can be used to inform biosecurity planning and pest management in light of a changing global climate (Sutherst et al. 2000, Kriticos and Brunel 2016, Olfert et al. 2016). This approach identifies areas suitable for H. halys and could serve as a potential framework to quantify the impacts of climate change by incorporating multiple future climatic scenarios to examine shifts in suitable areas. CLIMEX model output was also used to assess how climate change may influence H. halys phenology and voltinism across representative locations in its non-native range.

Materials and Methods

The CLIMEX Model

In this study, the CLIMEX bioclimatic model for H. halys developed by Kriticos et al. (2017) was used to evaluate distribution and population dynamics (Table 1). This model's range projections are consistent with the known global distribution of this species and exhibits higher sensitivity compared to previous attempts to estimate the potential distribution of H. halys (Zhu et al. 2012; Haye et al. 2015; Zhu et al. 2017). CLIMEX is a process-based niche modeling package that estimates suitable areas based on a combination of long-term meteorological data and parameter values describing the lspecies' abiotic preferences (Kriticos et al. 2015a). Unlike correlative niche models, CLIMEX model parameters can be calibrated inferentially, utilizing species occurrence data and phenological observations, as well as deductively, drawing upon experimental observations of species behavior under laboratory conditions to inform parameter section. CLIMEX uses weekly and annual Growth Indices, (GIW) and (GIA) respectively, to describe the potential for population growth as a function of optimal Soil Moisture (MI) and Temperature (TI) indices. A second set of parameters, Stress Indices (cold, wet, hot, dry), depict what extreme temperature and moisture conditions limit species distribution and survival. As a result, the CLIMEX model better matches observed northern latitudinal occurrences in North America and China by clearly defining H. halys tolerance to cold temperatures (Zhu et al. 2017). In addition, Kriticos and colleagues' (2017) model defines this insect's dry range limit more realistically whereas previous MaxEnt models overestimated suitable habitat in arid regions of North America and the Middle-East (Haye et al. 2015). Nevertheless, there are some important discrepancies between the aforementioned niche models concerning their estimations of H. halys establishment potential in Africa that should be noted. For instance, Zhu and colleagues' (2012) GARP model and Haye and colleagues' (2015) MaxEnt model underestimate suitability in sub-tropic regions of southern Africa given H. haly's presence in the subtropical regions of south eastern China and Taiwan. However, Kriticos and colleagues' (2017) CLIMEX model overestimates suitability in large tropical regions of equatorial Africa including DR Congo, Congo Republic, and Uganda.

Table 1.

CLIMEX parameter values for Halyomorpha halys


Climate Data

The global climate datasets used in the CLIMEX modeling all had a spatial resolution of 10 arc minutes (Kriticos et al. 2012). Two sets of climate data were used in this study. First, the CM10_1975H_V1.2 dataset, comprised of 30-yr averages centered on 1975 of monthly values for daily minimum and maximum temperature (°C), relative humidity (%) at 09:00 and 15:00 (local time), as well as monthly precipitation total (mm), was used to represent the baseline climate. The sample period for temperature, humidity, and precipitation is 1961–1990, but the precipitation sampling period was extended to 1951–2000 for some stations that were otherwise poorly sampled (Hijmans et al. 2005). This dataset was used to project the potential distribution of H. halys under recent historical climate conditions. Second, the potential distribution and general abundance of H. halys under possible future climate was modeled using two Global Climate Models (GCMs), CSIRO Mk3.0 (CSIRO, Australia) and MIROC-H (Centre for Climate Change, Japan), available as part of the CliMond datasets (Kriticos et al. 2012). Data from these GCMs were pattern-scaled to develop individual change scenarios relative to the base climatology. The two GCMs represent different climate sensitivities, defined as the amount of global warming for a doubling CO2 concentration compared to 1990s levels (Kriticos and Brunel 2016). For instance, CSIRO Mk3.0 predicts a global mean temperature increase of 2.11°C while MIROC-H predicts an increase of 4.31°C by 2100 (Kriticos et al. 2012). There are also differences in global mean precipitation projections. The CSIRO Mk3.0 model predicts a 14% decrease in future mean precipitation compared to the 1% decrease predicted by the MIROC-H model.

The A2 SRES scenario (Nakicenovic and Swart 2000) was selected to characterize possible future climatic conditions for the years 2050 and 2100. To date, the A family of SRES scenarios represents the best future climate scenarios available in CLIMEX format; the 2010 Representative Concentration Pathways (RCPs) are currently unavailable (Moss et al. 2010). Comparing carbon dioxide concentrations and global temperature change between the SRES and RCP scenarios, the SRES A2 scenario is similar to the RCP scenario 8.5 (Walsh et al. 2014). The A2 scenario was chosen because it represents the “worst case” scenario (i.e., no reductions in greenhouse gas emissions). In this study, no lower emissions scenarios were run given that ongoing greenhouse gas emissions are consistent with the most extreme SRES scenarios (Manning et al. 2010).

Potential Distribution

The known distribution was assembled from the Invasive Species Compendium (CABI 2017), the Early Detection and Distribution Mapping System (EDDMapS 2017), and the literature. A total of 6,083 occurrence localities were found with 358 in Asia (e.g., North Korea, China and Japan), 28 in Europe, and 5,702 in North America. The large number of detections in the United States is largely due to increased public awareness, citizen science, and the ease of digital reporting a potential specimen (EDDMapS 2017, NIPMC 2017).

To better understand how climate change may influence potential H. halys distribution, Ecoclimatic Index (EI) was evaluated under both recent historical and future climate scenarios. The EI is the net effect of the annual growth and total stress indices of a given species (Kriticos et al. 2015a). Essentially, the EI represents the overall climatic suitability of a given geographic location for the persistence of a given species. The EI is scaled from 0 to 100 with EI values < 1 indicating that a species cannot survive in that region (Kriticos et al. 2015a). Since the EI represents the annual climatic suitability of a given organism, species that undergo diapause (i.e., a dormancy period in which no growth occurs due to unfavorable abiotic conditions) tend to have lower EI values compared to species that are active year round at the same given location (Kriticos et al. 2015a). EI values were displayed in map format with four categories: “unsuitable” (EI < 1), “marginal” (EI = 1–5), “suitable” (EI = 6–15), and “highly suitable” (EI > 15). All H. halys occurrence data and EI values generated from CLIMEX were then mapped using ArcGIS 10.3.1 (Esri 2015).

Phenology and Voltinism

Twelve representative locations with established non-native H. halys populations (EDDMapS 2017, NIPMC 2017) were selected to assess H. halys sensitivity to different possible future climates. Representative locations in the invaded range included ten locations in North America (eight in the United States and two in Canada) and two locations in Europe (Table 2). The latitude, longitude, and elevation of each representative 10′ grid cell location are shown in Supplementary Table 1. Rural and urban irrigation practices in Walla Walla, Portland, and Sacramento, United States were simulated by assuming that 2.5 mm of water was applied to farms and urban gardens daily to better match observed H. halys’ densities at these drier sites (Hansen 2015, Leskey et al. 2015, Ingels et al. 2016, Kriticos et al. 2017). Essentially, in any week which had <21 mm of precipitation, the model would make up the deficit as an irrigation supplement. To examine the impact of climate change on H. halys phenology, shifts in the weekly growth index (GIw) were predicted under the two GCMs for the years 2050 and 2100. The number of weeks where GIw > 0 (0 = no growth and 1 = optimal growth) provided an estimation of the total growing season length for H. halys. Therefore, GIw is a decent indicator of population growth and this “modeled seasonal suitability” was found to match accurately observed trends in insect seasonal phenology based on trap counts (De Villiers et al. 2013, Kriticos et al. 2015b, Yonow et al. 2016). In addition, the simulated number of generations predicted based on the CLIMEX model, using a value of 595 degree-days above 12°C, was utilized to compare recent historical and possible future climates.

Table 2.

Ecoclimatic Index values (% of total continental areas) for Halylomorpha halys based on recent historical climate (1975H), 2050 and 2100 with two general circulation models (CSIRO Mk3.0 and MIROC-H) under the SRES A2 for the World, North America, and Europe



Potential Distribution Under Possible Future Climate Scenarios

Overall, the modeled potential global distribution under recent historical climate agrees well with the known distribution of this species in both its native and invaded ranges (see Kriticos et al. 2017 for model validation). In the Southern Hemisphere, model output indicates that portions of eastern South America, central and southern Africa, and Australia's eastern coast and New Zealand's North Island are highly suitable for H. halys establishment (Fig. 1). Modeled climatic suitably estimates in the Southern Hemisphere are consistent with the known geographic distribution of H. halys with the exception of equatorial Africa where the CLIMEX model projects an excessive capability of H. halys to cope with wet tropical climates. There is also potential for further range expansions in both North America (Fig. 2) and Europe (Fig. 3). Compared to recent historical climate conditions, the suitable H. halys range was shown to shift poleward and to contract from its known southern range limits in North America and Asia beginning in 2050 and continuing into 2100 (Fig. 4). In the Northern Hemisphere, China and the United States become less favorable for H. halys while Europe, Eastern Russia, and Canada become more susceptible to H. halys establishment and spread under both GCM scenarios by the end of the 21st century (Fig. 4). In East Asia, southern Russia constitutes a steep cold stress gradient that limits northward range expansion under future climate scenarios (Fig. 4). In contrast, potential suitable ranges in the Southern Hemisphere contract in South America, Africa, and Australia under both GCM scenarios (Fig. 4). On a global scale, the percentage of highly suitable range declined under future climate scenarios, but more so under the CSIRO Mk3.0 scenarios (Table 2).

Fig. 1.

The modeled global climatic suitability (CLIMEX Ecoclimatic Index) for Halyomorpha halys under recent historical climate. Blue circles designate recorded occurrences of H. halys.


Fig. 2.

Modeled climatic suitability (CLIMEX Ecoclimatic Index) for Halyomorpha halys under recent historical climate in North America. Blue circles designate recorded occurrences of H. halys.


Fig. 3.

Modeled climatic suitability (CLIMEX Ecoclimatic Index) for Halyomorpha halys under recent historical climate in Europe. Blue circles designate recorded occurrences of H. halys.


In North America, potential H. halys range expanded northward into Canada as cold limitations were overcome while substantial range contraction occurred in the southeastern United States under future climate scenarios (Fig. 5). These range contractions were more pronounced under the MIROC-H model, but overall projected changes in climatic suitability (EI values) were similar between the two GCMs (Table 2). Projected range losses in the southern latitudes (EI < 1) and reduced climatic suitability in the northern latitudes were associated with increased heat stress (HS) (Table 3). Accumulated heat stress > 100 indicated that stress was sufficient to eliminate the majority of potential H. halys range in Texas, Oklahoma, Kansas, Missouri, Tennessee, Kentucky, Arkansas, Louisiana, South Carolina, Mississippi, and Florida by 2100 under both GCMs (Fig. 5). By 2050, much of inland California would no longer be suitable for H. halys, including Sacramento, due to heat stress (Fig. 5) (Table 3). By 2100, the two GCM outputs indicated that Walla Walla, United States would also no longer be able to support year round H. halys populations as a result of increased heat stress levels (Table 3). However, positive annual growth indices at Sacramento and Walla Walla (Supplementary Table 2) and high rates of weekly spring and fall growth rates (Supplementary Fig. 1) under future climate scenarios indicate the possibility of transient H. halys populations at these increasingly hot sites. In Canada, large portions of Ontario, Quebec, New Brunswick, and Nova Scotia become suitable or highly suitable for H. halys establishment by 2100 under both GCMs (Fig. 5). Under future climate scenarios, suitable to highly suitable areas increased substantially across Europe (Table 2) and considerable range expansion was observed in northern Europe as cold stress limits were overcome (Fig 6). EI values rose more under the MIROC-H model compared to the CSIRO Mk3.0 model (Table 2). Under the CSIRO Mk3.0 model, suitable areas increased more than highly suitable areas compared to recent historical conditions (Table 2). The MIROC-H model indicated that the percentage of highly suitable areas, including large proportions of the United Kingdom, France, Belgium, the Netherlands, Germany, Poland, and Denmark, would undergo a 30-fold increase by 2100 compared to projections under the recent historical climate data (Table 2). In southern Europe, EI values declined in portions of Spain, Italy, Serbia, and Greece under both GCMs by 2100 due to rising heat stress levels (Fig. 6).

Fig. 4.

The modeled global climatic suitability (CLIMEX Ecoclimatic Index) for Halyomorpha halys based on CSIRO Mk3.0 and MIROC-H general circulation model projections under the A2 SRES emission scenario for 2050 and 2100.


Fig. 5.

The modeled climatic suitability (CLIMEX Ecoclimatic Index) for Halyomorpha halys based on CSIRO Mk3.0 and MIROC-H general circulation model projections in North America under the A2 SRES emission scenario for 2050 and 2100.


Table 3.

CLIMEX indices for Halyomorpha halys based on recent historical climate (1975H) and general circulation model CSIRO Mk3.0 and MICRO-H at 12 representative locations in North America and Europe


Fig. 6.

The modeled climatic suitability (CLIMEX Ecoclimatic Index) for Halyomorpha halys based on CSIRO Mk3.0 and MIROC-H general circulation model projections in Europe under the A2 SRES emission scenario for 2050 and 2100.



The number of potential generations modeled using the baseline climate dataset (1975H) and Kriticos and colleagues' (2017) degree day requirements for H. halys (595°C-days above 12°C for a single generation) are fairly consistent with field observations for this species at each representative location (Table 3) with the exception of two locations in North America (Allentown and Sacramento, United States). Under future climate scenarios, longer growing seasons resulted in the potential for two or more generations per year (Table 3). Overall, modeled increases in the number of weeks where growth occurs (GIw) and in turn, the number of generations per year were more pronounced under the MIROC-H model compared to the CSIRO Mk3.0. By 2050, all but one North American H. halys population become capable of producing two or more complete generations per year under the MIROC-H model. In Europe, Zurich-Obefleden, Switzerland gained a partial second generation by 2050 and became completely bivoltine by 2100, while Emilia-RomognazModena, Italy gained a full third and fourth generation by 2050 and 2100, respectively.


Weekly growth indices for H. halys were plotted for 6 out of the 12 representative locations selected based on available H. halys phenology records and the presence of vulnerable crops (Fig. 7). Weekly growth indices for the other six representative locations are shown in Supplementary Fig. 1. Overall, the number of weeks where the growth index was positive (GIw) increased, resulting in longer growing seasons under both GCMs (Table 3). Rising spring temperatures resulted in early spring emergence while warming fall temperatures led to later fall activity (Fig. 7). However, these increased opportunities for growth were often negated by weeks where the average maximum temperature exceeded H. halys’ limiting high temperature threshold (DV3 = 33°C) (Table 1). Overall, excessively warm weeks in June through August reduced weekly growth rates at all representative locations with the exception of Zurich-Obefleden, Switzerland (Fig. 7A–E). At Zurich-Obefleden, Switzerland, observed recent historical weekly growth rates doubled in July-August (CSIRO Mk3.0) and September (MIROC-H) by 2100, respectively (Fig. 7F). By 2100, the projected timing of peak and minimal growth periods varied greatly between the GCMs. For many locations, model output using MIROC-H resulted in lower EI values compared to CSIRO Mk3.0 (Table 3) due to decreased mid-summer growth rates for 2100, including Allentown, United States (Fig. 7A), Asheville, United States (Fig. 7B), and Emilia-Romogna-Modena, Italy (Fig. 7E). When an irrigation scenario was applied, Portland, United States exhibited 5 additional weeks of positive H. halys growth (Fig. 7D), which in turn, doubled the climatic suitable (EI) rating at this site under the recent historical climate (Table 3). Sacramento and Walla Walla, United States also exhibited enhanced growth and climatic suitability when an irrigation scenario was applied (Table 3) (Supplementary Fig. 1E and F). Under future climate scenarios, weekly growth indices at Portland, Walla Walla, and Sacramento were enhanced by the inclusion of an irrigation scenario (Table 3), which also neutralized any potential dry stress accumulation at these sites (Supplementary Table 2).

Fig. 7.

Weekly growth index (GIw) for Halyomorpha halys based on recent historical climate and general circulation model outputs for (A) Allentown, United States, (B) Asheville, United States, (C) Niagara-Fonthill, Canada, (D) Portland, United States under top-up irrigation scenario, (E) Emilia-Romagna-Modena, Italy, and (F) Zurich-Obefelden, Switzerland.



In the context of this study, the global potential range of H. halys expanded polewards and contracted from its southern temperature range limits under future climate scenarios. The future climate scenarios explored here suggest that the invasion threat posed to Europe and Canada will greatly intensify. Overall, H. halys exhibited longer growing seasons as well as enhanced population growth in the spring, and more possible generations per year. However, summer growth was greatly reduced in all but one representative location. Therefore, the effect of climate change on H. halys is complex with both positive and negative impacts varying both spatially and temporally. This study highlights some areas of emerging or increasing threat of invasion by H. halys under possible future climates. It also identifies areas where H. halys abundance and subsequent pest outbreaks may decline. Nevertheless, these range suitability and relative abundance projections are only potential distributions in which pest outbreaks may occur based on climatic factors and not predicted future distributions.

In the United States, prime horticultural areas in the Northeast, Pacific Northwest, Upper Midwest, and portions of California remained suitable or became more suitable for H. halys in terms of future climate scenarios. Although soil moisture was not a limiting factor for H. halys persistence across the majority of sites examined in this study, the inclusion of a moderate irrigation scenario did enhance H. halys growth potential and climatic suitability at representative locations in California and the Pacific Northwest under both baseline and future climate scenarios. Given that many horticultural production regions are heavily irrigated, current ecological niche models may be underestimating the threat H. halys poses to horticultural crops grown in more arid regions (Zhu et al. 2012, Kriticos et al. 2017). Therefore, U.S. pest managers in these regions should continue to monitor changes in H. halys densities and be prepared for the possibility of pest outbreaks in the future. At present, H. halys has very limited distribution in Canada and no agricultural losses have been reported. However, future climate scenarios indicate that key fruit and vegetable growing regions in Ontario, Quebec, and British Columbia will become increasingly suitable for H. halys (Statistics Canada 2012). Therefore, it would seem prudent to consider the feasibility of coordinated containment strategies to prevent the future spread of this pest into Canada's prime horticultural regions.

In terms of the future climate scenarios explored here, substantial northward range expansions are indicated across Europe. The large decrease in climatic suitability in southern Spain by the end of the century is encouraging, although much of the country's northern boundaries remain climatically suitable. By 2100, Modena, Italy, which is located within a key fruit growing region in Europe, became marginal to completely unsuitable for H. halys due to increases in summer temperatures above its upper temperature threshold. However, the majority of Emilia-Romagna region remained suitable for H. halys particularly in areas east of Modena where orchards and vineyards are abundant (Maistrello et al. 2016). Since H. halys is capable of travelling >5 km per day (Lee and Leskey 2015), it is plausible that the pest will disperse from sites like Modena during the summer and seek temporary refuge in cooler land types especially forests and mountains (Bakken et al. 2015). Thus, Italy's horticultural regions will likely remain at risk from H. halys in the future, but the timing and intensity of infestations will likely vary depending on land type. Given that future climate scenarios indicate that the risks for Europe are likely to increase in conjunction with the present risk of further spread (Kriticos et al. 2017), European countries may want to consider which biosecurity measures are needed to reduce further spread of H. halys across Europe. Preventing its entry into high-risk countries may be the most cost-effective response.

Changes in weekly growth indices (GIw) for Allentown and Asheville, United States under recent historical conditions closely conformed to results of phenological studies conducted at these locations (Nielsen and Hamilton 2009a, Bakken et al. 2015). Unfortunately, the literature did not provide much data on H. halys phenology in European countries and Canada, but the simulated weekly growth indices for Zurich-Obefleden, Switzerland were consistent with a phenology study conducted by Haye et al. (2014) in nearby Zurich-Wollishofen, Switzerland. In this study, future climate scenarios resulted in longer growing seasons. However, both GCM projections suggest that rising mid-summer temperatures could restrict H. halys population growth. These results are consistent with Olfert et al. (2016) who also found mid-summer declines in weekly growth rates of the parasitoid, Peristenus digoneutis (Loan; Hemeoptera: Braconidae), across Canada under similar future climate scenarios. Dramatic shifts in H. halys phenology could have important management implications in terms of chemical control. In the mid-Atlantic region of the United States, H. halys is reported to feed on tree fruit over the entire growing season with the majority of feeding damage occurring late in the growing season (August–early September) by first-generation adults (Nielsen and Hamilton 2009b). In response, growers in this region have increased the frequency of costly insecticide applications (Leskey et al. 2012a) which have inadvertently decreased natural occurring predator and parasitoid densities. In turn, secondary pest outbreaks of the woolly apple aphid and San Jose scale have been reported in several mid-Atlantic apples orchards that employ insecticides to control H. halys (Leskey et al. 2012b). In the absence of their natural enemies, these once minor pests are now able to grow to economically damaging levels (Hardin et al. 1995) indicating that current chemical control strategies are not financially and ecologically sustainable in the long run. Given that the modeled decreases in mid-summer H. halys growth across this region coincides with late season tree fruit development, climate change may reduce mid- to late season fruit damage, thereby lessening the need for late season insecticide applications. However, the possible future climates explored here also indicated earlier spring activity and enhanced spring growth potential. Earlier spring emergence coupled with reduced over-wintering mortality (Kiritani 2006) could increase the risk of early season feeding damage in some horticultural crops.

Although model projections for voltinism were fairly consistent with numbers reported in the literature, these estimates should be approached with some caution. The number of generations predicted by Kriticos and colleagues' (2017) CLIMEX model was based off of a degree day model with a relaxed minimal developmental threshold (DV0) of 12°C. Since estimated temperature thresholds for complete development are 14.17°C for U.S. populations (Nielsen et al. 2008) and 12.97°C for Swiss populations (Haye et al. 2014), Kriticos and colleagues' (2017) CLIMEX model parameters may be overestimating the number of annual generations possible. For instance, an additional generation was projected in Sacramento, United States, under recent historical climate than has actually been observed (Ingels et al. 2016). In the northeastern United States, the completion of a partial to full second generation in Pennsylvania and New York, as projected in this study's model output, is plausible based on previous H. halys voltinism model estimations conducted by (Nielsen et al. 2016), but have yet to be confirmed at these locations. Unfortunately, captures in pheromone traps commonly used to monitor H. halys phenology do not necessarily provide clear estimates pertaining to the number of generations per season as generations often overlap (Leskey et al. 2015). Regardless, projected changes in H. halys voltinism under different possible future climates were consistent with similar studies examining the impact of climate change on insect voltinism (Tobin et al. 2008, Ziter et al. 2012, Olfert et al. 2016). Rising global temperatures are expected to increase the number of annual generations in multivoltine insects, including stinkbugs (Kiritani 2006), and this study suggests that H. halys may become multivoltine throughout much of its non-native range over the next 30 to 80 yr.

Overall, the projected changes in global H. halys distribution and relative abundance were similar between mid-century GCM scenarios. In contrast, CSIRO Mk3.0 and MIROC-H model outputs for 2100 differed greatly, which highlights the uncertainties associated with current climate modeling projections. However, it should be noted that variance the between the two GCMs (under a single high emission scenario) does not represent the full range of uncertainties associated with climate change modeling. The use of additional GCMs would cover a wider range of climatic sensitives in relation to climate change (Kriticos and Brunnel 2016). Future studies should also consider employing more moderate greenhouse gas emission scenarios given the dynamic nature of global policy in regards to climate change.

In addition to the uncertainties related to future global greenhouse gas emission patterns, CLIMEX itself makes several assumptions that introduce further uncertainty to model projections. First, CLIMEX utilizes a baseline climate data set that is centered on 1975 (Kriticos et al. 2012). Given the increase in global temperatures since 1975 (Rahmstorf et al. 2012) and the ongoing observed shifts in insect pest distributions (Bebber et al. 2013), up-to-date global climatologies for ecological niche and species distribution modeling packages are greatly needed. Second, CLIMEX does not account for potential changes in the frequency and intensity of extreme short-term weather events predicted under future climate change scenarios (Kriticos et al. 2012, Walsh et al. 2014), which could have important management implications for H. halys. Third, the CLIMEX model parameters used in this study assume that the existing invasive populations have the same adaptive potential as their native counterparts in East Asia. However, North American populations are likely the result of a single introduction event comprising of individuals originating from the Beijing region in China (Gariepy et al. 2014, Xu et al. 2014). In contrast, there have been multiple introductions in Europe resulting in dominant haplotypes differing between countries (Gariepy et al. 2015). Given the differences in genetic diversity across native and invaded ranges, it is reasonable to assume invasive populations may respond differently to climate change compared to their more genetically diverse East Asian counterparts. Finally, CLIMEX's projected changes in H. halys distribution and abundance are based solely on its response to climate. Non-climatic factors, such as land use type, host plant distribution, and biotic interactions, have been shown to influence H. halys distribution and densities at regional spatial scales (Haye et al. 2014, Rice et al. 2014, Venugopal et al. 2016). In the mid-Atlantic United States, Bakken et al. (2015) found greater H. halys abundance at high altitudes, a surrogate for decreasing temperature. Thus, mountainous terrains, like the Appalachian Mountains, may act as a temperature refuge for H. halys during the increasingly hot summer months that are likely to occur under future climate change. The relationship between host plants and H. halys development is an important component of this pest's population dynamics. Despite its broad host range, H. halys is only reported to complete its life cycle on a few select host plants (Bergmann et al. 2016). For example, H. halys survival on apples (Malus domestica Borkh) is low (Funayama 2002) while peach (Prunus persica L.) is able to support all H. halys life stages (Rice et al. 2014). Similarly, Acebes-Doria et al. (2016) found that H. halys fitness was enhanced by feeding on multiple host plants and higher pest densities are often associated with orchards neighboring unmanaged woodland (Bakken et al. 2015, Venugopal et al. 2016). Crop phenology is also likely driving H. halys movement between host plants as H. halys prefers to feed on reproductive structures of many economically important crop species (Rice et al. 2014). Climate change may influence these seasonal feeding patterns by shifting the availably of preferred host plant life stages.

In the instance of H. halys, global climate change directly influenced this lspecies' potential distribution and abundance. Concurrently, climate change may also influence pest-crop outcomes (Bale et al. 2002), thereby indirectly influencing pest dynamics. To better address future economic risks associated with H. halys under global climate change, host plant responses to a changing climate also need to be considered (Gregory et al. 2009). Earlier spring emergence is likely to occur across much of this pest's range in the future, which may result in a crop-pest mismatch if H. halys responds more strongly to rising temperatures than their preferred host plants. For instance, Funayama (2013) found that higher maximum spring temperatures in northern Japan were associated with lower H. halys densities as the insect emerged weeks before suitable host plants were available. It is plausible that such phenological desynchronization could ultimately lead to decreased crop damage if H. halys emerges before preferred crops are available.

In conclusion, the results of this study provide an indication of the possible change in potential future distribution and abundance of H. halys in light of climate change. Regardless of CLIMEX's limitations and uncertainties related to future greenhouse gas emission scenarios, it would seem prudent to assess the feasibility of a coordinated containment strategy in Europe and Canada as both current (Zhu et al. 2012, 2017; Haye et al. 2015; Kriticos et al. 2017) and future climate scenarios (Zhu et al. 2016) indicate suitable climatic conditions for further spread. The most sensible response in light of uncertainties associated with climate change may be to educate the general public about the threats caused by this species and organize an efficient early warning system through citizen science (Maistrello et al. 2016) in regions currently under high risk of H. halys establishment as well as areas that are projected to become suitable for this species in the future.


I thank Darren Kriticos, John Kean, and Hernando Acosta for giving me permission to use their H. halys CLIMEX model parameters for this study. Dennis Todey, Jerry Hatfield, Darren Kriticos, and Clayton Thomas provided valuable feedback in the preparation of the manuscript.

Supplementary Data

Supplementary data are available at Environmental Entomology online.

References Cited


Acebes-Doria, A. L., T. C. Leskey, and C. J. Bergh. 2016. Host plant effects on Halyomorpha halys (Hemiptera: Pentatomidae) nymphal development and survivorship. Environ. Entomol 45: 663–670. Google Scholar


Arnold, K. 2009. Halyomorpha halys (Stål, 1855), eine für die europäische Fauna neu nachgewiesene Wanzenart (Insecta: Heteroptera: Pentatomidae: Cappaeini). Mitt. Thüringer Entomol. 16: 19. Google Scholar


Bakken, A. J., S. C. Schoof, M. Bickerton, K. L. Kamminga, J. C. Jenrette, S. Malone, M. A. Abney, D. A. Herbert Jr , D. Reisig, T. P. Kuhar, et al. 2015. Occurrence of brown marmorated stink bug (Hemiptera: Pentatomidae) on wild hosts in nonmanaged woodlands and soybean fields in North Carolina and Virginia. Environ. Entomol. 44: 1011–1021. Google Scholar


Bale, J. S., G. J. Masters, I. D. Hodkinson, C. Awmack, T. M. Bezemer, V. K. Brown, J. Butterfield, A. Buse, J. C. Coulson, J. Farrar, et al. 2002. Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glo. Change Biol. 8: 1–6. Google Scholar


Bebber, D. P., M. A. Ramotowski, and S. J. Gurr. 2013. Crop pests and pathogens move polewards in a warming world. Nat. Clim. Change 3: 985–988. Google Scholar


Bell, J. R., L. Alderson, D. Izera, T. Kruger, S. Parker, J. Pickup, C. R. Shortall, M. S. Taylor, P. Verrier, and R. Harrington. 2015. Long-term phenological trends, species accumulation rates, aphid traits and climate: five decades of change in migrating aphids. J. Anim. Ecol. 84: 21–34. Google Scholar


Bergmann, E., K. M. Bernhard, G. Bernon, M. Bickerton, S. Gill, C. Gonzales, G. C. Hamilton, C. Hedstrom, K. Kamminga, C. Koplinka-Loehr, et al. 2016. Host plants of the brown marmorated stink bug. (accessed 30 August 2016). Google Scholar


Cesari, M., L. Maistrello, F. Ganzerli, P. Doili, L. Rebecchi, and R. Guidetti. 2015. A pest alien invasion in progress: potential pathways of origin of the brown marmorated stink bug Halyomorpha halys populations in Italy. J. Pest Sci. 88: 1–7. Google Scholar


CABI. 2017. Halyomorpha halys. In: Invasive species compendium . CAB International, Wallingford, UK. (accessed 24 January 2017). Google Scholar


Callot, H., and C. Brua. 2013. Halyomorpha halys (Stål, 1855), la Punaise diabolique, nouvelle espe`ce pour la faune de France (Heteroptera: Pentatomidae). L'Entomologiste 69: 69–71. Google Scholar


De Villiers, M., V. Hattingh, and D. J. Kriticos. 2013. Combining field phenological observations with distribution data to model the potential distribution of the fruit fly Ceratitis rosa Karsch (Diptera: Tephritidae). Bull. Entomol. Res. 103: 60–73. Google Scholar


Dioli, P., P. Leo, and L. Maistrello. 2016. Prime segnalazioni in Spagna e in Sardegna della specie aliena Halyomorpha halys (Stål, 1855) e note sulla sua distribuzione in Europa (Hemiptera, Pentatomidae). Revista gaditana de Entomología 7: 539–548. Google Scholar


Dukes, J. S. and H. A. Mooney. 1999. Does global change increase the success of biological invaders? Trends Ecol. Evol. 14: 135–139. Google Scholar


EDDMapS. 2017. Early detection & distribution mapping system. The University of Georgia - Center for Invasive Species and Ecosystem Health. (accessed 12 February 2017) Google Scholar


ESRI. 2015. ArcGIS 10.3.1. Environmental Systems Research Institute, Redlands, CA. Google Scholar


Frasier. 2016. BMSB update. Ontario Ministry of Agriculture, Food, and Rural Affairs. (accessed 5 November 2016). Google Scholar


Funayama, K. 2002. Oviposition and development of Halyomorpha halys (Stål) and Homalogonia obtuse (Walker) in apple trees. Japn. J. Appl. Entomol. Zool. 46: 1–6. Google Scholar


Funayama, K. 2013. Effect of climate change on annual fluctuations in the population density of the brown marmorated stink bug (Hemiptera: Pentatomidae) in Northern Japan. J. Econ. Entomol. 106: 2141–2143. Google Scholar


Gapon, D. A. 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. Google Scholar


Gariepy, T. D., A. Bruin, T. Haye, P. Milonas, and G. Vetek. 2015. Occurrence and genetic diversity of new populations of Halyomorpha halys in Europe. J. Pest. Sci. 88: 451–460. Google Scholar


Gariepy, T. D., T. Haye, H. Fraser, and J. Zhang. 2014. Occurrence, genetic diversity, and potential pathways of entry of Halyomorpha halys in newly invaded areas of Canada and Switzerland. J. Pest Sci. 87: 17–28. Google Scholar


Gregory, P. J., S. N. Johnson, A. C. Newton, and J. S. Ingram. 2009. Integrating pests and pathogens into the climate change/food security debate. J. Exp. Bot. 60: 2827–2838. Google Scholar


Hansen, M. 2015. Stink bug continues its spread: Northwest growers should be on the lookout for brown marmorated stink bug. Good Fruit Grower. (accessed 23 September 2016). Google Scholar


Hardin, M. R., B. Benrey, M. Coll, W. O. Lamp, G. K. Roderick, and P. Barbosa. 1995. Arthropod pest resurgence: an overview of potential mechanisms. Crop Prot. 14: 3–18. Google Scholar


Haye, T., S. Abdallah, T. Gariepy, and D. Wyniger. 2014. Phenology, life table analysis and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys, in Europe. J. Pest Sci. 87: 407–418. Google Scholar


Haye, T., T. Gariepy, K. Hoelmer, J.-P. Rossi, J.-C. Streito, X. Tassus, and N. Desneux. 2015. Range expansion of the invasive brown marmorated stinkbug, Halyomorpha halys: an increasing threat to field, fruit and vegetable crops worldwide. J. Pest Sci 88: 665–673. Google Scholar


Heckmann, R. 2012. Erster Nachweis von Halyomorpha halys (STÅL,1855) (Heteroptera: Pentatomidae) für Deutschland. Heteropteron 36: 17–18. Google Scholar


Hijmans, R. J., S. E. Cameron, J. L. Parra, P.G. Jones, and A. Jarvis. 2005. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25: 1965–1978. Google Scholar


Hoebeke, E. R., and M. E. Carter. 2003. Halyomorpha halys (Stål) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proc. Entomol. Soc. Wash. 105: 225–237. Google Scholar


Hoffman, W. E. 1933. A pentatomid pest of growing beans in South China. Peking Nat. His. Bull. 5: 25–26. Google Scholar


Ingels, C., L. Varela, R. Elkins, and C. Hurley. 2016. Phenology of brown marmorated stink bugs and distribution near California pear orchards. Technical report for California Pear Pest Management Research Fund. (accessed 2 December 2016). Google Scholar


Kiritani, K. 2006. Predicting impact of global warming on population dynamics and distribution of arthropods in Japan. Popul. Ecol. 48: 5–12. Google Scholar


Kriticos, D. J., and S. Brunel. 2016. Assessing and managing the current and future pest risk from water hyacinth, (Eichhornia crassipes), an invasive aquatic plant threatening the environment and water security. PloS one 11: e0120054. Google Scholar


Kriticos, D. J., J. M. Kean, C. B. Phillips, S. Senay, H. Acosta, and T. Haye. 2017. The potential global distribution of the brown marmorated stink bug, Halyomorpha halys Stål (Hemiptera: Pentatomidae): a critical threat to plant biosecurity. J. Pest. Sci. 90: 1033–1043. DOI: 10.1007/s10340-017-0869-5. Google Scholar


Kriticos, D. J., G. F. Maywald, T. Yonow, E. J. Zurcher, N. I. Herrmann, and R. W. Sutherst. 2015a. CLIMEX Version 4: exploring the effects of climate on plants, animals and diseases. CSIRO, Canberra, Australia. Google Scholar


Kriticos, D. J., O. Noboru, H. D. William, J. Beddow, T. Walsh, W. T. Tay, D. M. Borchert, S. V. Paula-Moreas, C. Czepak, and M. P. Zalucki. 2015b. The potential distribution of invading Helicoverpa armigera in North America: is it just a matter of time. PLoS One 10: e0119618. Google Scholar


Kriticos, D. J., B. L. Webber, A. Leriche, N. Ota, J. Bathols, I. Macadam, and J. K. Scott. 2012. CliMond: global high resolution historical and future scenario climate surfaces for bioclimatic modelling. Methods Ecol. Evol. 3: 53–64. Google Scholar


Lee, D.-H. 2015. Current status of research progress on the biology and management of Halyomorpha halys (Hemiptera: Pentatomidae) as an invasive species. Appl. Entomol. Zool. 50: 277–290. Google Scholar


Lee, D.-H., and T. C. Leskey. 2015. Flight behavior of foraging and overwintering brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae). Bull. Entomol. Res. 105: 566–573. Google Scholar


Lee, D.-H., B. D. Short, S. V. Joseph, J. C. Bergh, and T. C. Leskey. 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. Google Scholar


Leskey, T. C., A. Agnello, J. C. Bergh, G. P. Dively, G. C. Hamilton, P. Jentsch, A. Khrimian, G. Krawczyk, T. P. Kuhar, D.-H. Lee, et al. 2015. Attraction of the invasive Halyomorpha halys (Hemiptera: Pentatomidae) to traps baited with semiochemical stimuli across the United States. Environ. Entomol. 44: 746–756. Google Scholar


Leskey, T. C., B. D. Short, B. R. Butler, and S. E. Wright. 2012a. Impact of the invasive brown marmorated stink bug, Halyomorpha halys (Stål), in mid-Atlantic tree fruit orchards in the United States: case studies of commercial management. Psyche J. Entomol. 105: 535062. Google Scholar


Leskey, T. C., D. H. Lee, B. D. Short, and S. E. Wright. 2012b. Impact of insecticides on the invasive Halyomorpha halys (Stål) (Hemiptera: Pentatomidae): analysis on the insecticide lethality. J. Econ. Entomol. 105: 1726–1735. Google Scholar


Manning, M. R., J. Edmonds, S. Emori, A. Grubler, K. Hibbard, F. Joos, M. Kainuma, R. F. Keeling, T. Kram, A. C. Manning, et al. 2010. Misrepresentation of the IPCC CO2 emission scenarios. Nat Geosci 3: 376–377. Google Scholar


Macavei, L., R. Bfi01_1212.gifţan, I. Oltean, T. Florean, M. Varga, E. Costi, and L. Maistrello. 2015. First detection of Halyomorpha halys, a new invasive species with a high potential of damage on agricultural crops in Romania. Lucrari Stiintifice Seria Agronomie 58: 105–400. Google Scholar


Maistrello, L., P. Dioli, M. Bariselli, G. L. Mazzoli, and I. Giacalone-Forini. 2016. Citizen science and early detection of invasive species: phenology of first occurrences of Halyomorpha halys in Southern Europe. Biol. Invasions 18: 3109–3116. Google Scholar


Maistrello, L., G. Vaccari, S. Caruso, E. Costi, S. Bortolini, L. Macavei, G. Foca, A. Ulrici, P. P. Bortolotti, R. Nannini, et al. 2017. Monitoring of the invasive Halyomorpha halys, a new key pest of fruit orchards in northern Italy. J. Pest Sci. 90: 1231–1244. DOI: 10.1007/s10340-017-0896-2. Google Scholar


Milonas, P., and G. Partsinevelos. 2014. First report of brown marmorated stink bug Halyomorpha halys Stål (Hemiptera: Pentatomidae) in Greece. EPPO Bulletin 44: 183–186. Google Scholar


Moss, R.H., J. A. Edmonds, K. A. Hibbard, M. R. Manning, S.K. Rose, D. P. van Vuuren, T. R. Carter, S. Emori, M. Kainuma, T. Kram, et al. 2010. The next generation of scenarios for climate change research and assessment. Nature 463: 747–756. Google Scholar


Musolin, D. L. 2007. Insects in a warmer world: ecological, physiological and life-history responses of true bugs (Heteroptera) to climate change. Glob. Chang. Biol 13: 1565–1585. Google Scholar


Nakicenovic, N. and R. Swart. 2000. Special report on emissions scenarios, pp. 612. In N. Nakicenovic and R. Swart (eds.), A Special Report of Working Group III of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge UK. Google Scholar


Nielsen, A. L., G. C. Hamilton, and D. Matadha. 2008. Developmental rate estimation and life table analysis for Halyomorpha halys (Hemiptera: Pentatomidae). Environ. Entomol. 37: 348–355. Google Scholar


Nielsen, A. L., and G. C. Hamilton. 2009a. Life history of the invasive species Halyomorpha halys (Hemiptera: Pentatomidae) in northeastern United States. Ann. Entomol. Soc. Am. 102: 608–616. Google Scholar


Nielsen, A. L., and G. C. Hamilton. 2009b. Seasonal Occurrence and Impact of Halyomorpha halys (Hemiptera: Pentatomidae) in Tree Fruit. J. Econ. Entomol 102: 1133–1140. Google Scholar


Nielsen, A. L., S. Chen, and S. J. Fleischer. 2016. Coupling developmental physiology, photoperiod, and temperature to model phenology and dynamics of an invasive Heteropteran, Halyomorpha halys. Front. Physiol. 7: 165. Google Scholar


Northeastern IPM Center [NIPMC]. 2017. BMSB State-by-State Map. (accessed 15 January 2017). Google Scholar


Olfert, O., T. Haye, R. Weiss, D. Kriticos, and U. Kuhlmann. 2016. Modelling the potential impact of climate change on future spatial and temporal patterns of biological control agents: Peristenus digoneutis (Hymenoptera: Braconidae) as a case study. Can. Entomol 148: 579–594. Google Scholar


Porter, J. H., M. L. Parry, and T. R. Carter. 1991. The potential effects of climatic change on agricultural insect pests. Agr. Forest. Meteorol. 57: 221–240. Google Scholar


Rahmstorf, S., G. Foster, and A. Cazenave. 2012. Comparing climate projections to observations up to 2011. Environ. Res. Lett. 7: 044035. Google Scholar


Rice, K.B., C. J. Bergh, E. J. Bergmann, D. J. Biddinger, C. Dieckhoff, G. Dively, H. Fraser, T. Gariepy, G. Hamilton, T. Haye, et al. 2014. Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). J. Integ. Pest Manage. 5: 1–13. Google Scholar


Roff, D., 1983. Diapause and Life Cycle Strategies in Insects, pp 253–220. In V. K. Brown and I. Hodek, (eds), Phenological adaptation in a seasonal environment: a theoretical perspective. Kluwer Academic Publishers, Dordrecht, Netherlands. Google Scholar


Šeat, J. 2015. Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) a new invasive species in Serbia. Acta Entomologica Serbica 20: 167–171. Google Scholar


Simov, N. 2016. The invasive brown marmorated stink bug Halyomorpha halys (Stål, 1855) (Heteroptera: Pentatomidae) already in Bulgaria. Ecologica Montenegrina. 9: 51–53. Google Scholar


Sutherst, R. W., and G. Maywald. 2005. A climate model of the red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae): implications for invasion of new regions, particularly Oceania. Environ. Entomol. 34: 317–335. Google Scholar


Sutherst, R. W., G. F. Maywald, and B. L. Russel. 2000. Estimating vulnerability under global change: modular modelling of pests. Agric. Ecosyst. Environ. 82: 303–319. Google Scholar


Statistics Canada. Agriculture Division Crops Section. 2012. Fruit and Vegetable Production. v80: 1–40 (accessed 1 September 2016). Google Scholar


Tobin, P. C., S. Nagarkatti, G. Loeb, and M. C. Saunders. 2008. Historical and projected interactions between climate change and insect voltinism in a multivoltine species. Glo. Change Biol. 14: 951–957. Google Scholar


United States Apple Association [USAA]. 2010. Asian pest inflicting substantial losses, raising alarm in eastern apple orchards. Apple News 41: 488. Google Scholar


Venugopal, P. D., G. P. Dively, A. Herbert, S. Malone, J. Whalen, and W. O. Lamp. 2016. Contrasting role of temperature in structuring regional patterns of invasive and native pestilential stink bugs. PloS One 11: e0150649. Google Scholar


Vétek, G., V. Papp, A. Haltrich, and D. Rédei. 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. Google Scholar


Walsh, J., D. Wuebbles, K. Hayhoe, J. Kossin, K. Kunkel, G. Stephens, P. Thorne, R. Vose, M. Wehner, J. Willis, et al. 2014. Our Changing Climate, pp 19–67. In M. Melillo, T. C. Richmond, and G. W. Yohe, (eds). Climate change impacts in the United States: The Third National Climate Assessment. U.S. Global Change Research Program, Washington, DC. Google Scholar


Xu J., D. M. Fonseca, G. C. Hamilton, K. A. Hoelmer, and A. L. Nielsen. 2014. Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys. Biol. Invasions 16: 153–166. Google Scholar


Yonow, T., D. J. Kriticos, N. Ota, J. Van Den Berg, and W. D. Hutchison. 2016. The potential global distribution of Chilo partellus, including consideration of irrigation and cropping patterns. J. Pest Sci. 90: 459–477. Google Scholar


Zhu, G., W. Bu, Y. Gao, and G. Liu. 2012. Potential geographic distribution of brown marmorated stink bug invasion (Halyomorpha halys). PLoS One 7: e31246. Google Scholar


Zhu, G., Z. Ye, J. Du, D. Zhang, Y. Zhen, C. Zheng, L. Zhao, and W. Bu. 2016. Range wide molecular data and niche modeling revealed the Pleistocene history of a global invader (Halyomorpha halys). Sci. Rep. 6: 23192. Google Scholar


Zhu, G., T. D. Gariepy, T. Haye, W. Bu. 2017. Patterns of niche filling and expansion across the invaded ranges of Halyomorpha halys in North America and Europe. J. Pest Sci. 90: 1045–1057. doi:10.1007/s10340-016-0786-z Google Scholar


Ziska, L. H., D. M. Blumenthal, G. B. Runion, E. R. Hunt Jr , and H. DiazSoltero. 2011. Invasive species and climate change: an agronomic perspective. Clim. Change 105: 13–42. Google Scholar


Ziter, C., E. A. Robinson, and J. A. Newman. 2012. Climate change and voltinism in Californian insect pest species: sensitivity to location, scenario and climate model choice. Glo. Change Biol. 18: 2771–2780. Google Scholar
Published by Oxford University Press on behalf of Entomological Society of America 2017. This work is written by (a) US Government employee(s) and is in the public domain in the US. This Open Access article contains public sector information licensed under the Open Government Licence v2.0 (
Erica Jean Kistner "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, (23 October 2017).
Received: 23 May 2017; Accepted: 31 August 2017; Published: 23 October 2017

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