General Enquiries on the form should be made to: Defra, Strategic Evidence and Analysis E-mail: [email protected]

Evidence Project Final Report

⚫ Note In line with the Freedom of Information Project identification Act 2000, Defra aims to place the results of its completed research projects in the public domain wherever possible. 1. Defra Project code PH04100 The Evidence Project Final Report is designed to capture the information on 2. Project title the results and outputs of Defra-funded UK Monitoring for Brown Marmorated Stink Bug research in a format that is easily publishable through the Defra website An Evidence Project Final Report must be completed for all projects. 3. Contractor • This form is in Word format and the organisation(s) NIAB EMR boxes may be expanded, as appropriate. East Malling, Kent ⚫ ACCESS TO INFORMATION ME19 6BJ The information collected on this form will be stored electronically and may be sent to any part of Defra, or to individual £ 9,625 researchers or organisations outside 54. Total Defra project costs Defra for the purposes of reviewing the (agreed fixed price) project. Defra may also disclose the information to any outside organisation 5. Project: start date ...... 01/07/2020 acting as an agent authorised by Defra to process final research reports on its behalf. Defra intends to publish this form end date...... 30/11/2020 on its website, unless there are strong reasons not to, which fully comply with exemptions under the Environmental Information Regulations or the Freedom of Information Act 2000. Defra may be required to release information, including personal data and commercial information, on request under the Environmental Information Regulations or the Freedom of Information Act 2000. However, Defra will not permit any unwarranted breach of confidentiality or act in contravention of its obligations under the Data Protection Act 1998. Defra or its appointed agents may use the name, address or other details on your form to contact you in connection with occasional customer research aimed at improving the processes through which Defra works with its contractors.

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6. It is Defra’s intention to publish this form. Please confirm your agreement to do so...... YES NO (a) When preparing Evidence Project Final Reports contractors should bear in mind that Defra intends that they be made public. They should be written in a clear and concise manner and represent a full account of the research project which someone not closely associated with the project can follow. Defra recognises that in a small minority of cases there may be information, such as intellectual property or commercially confidential data, used in or generated by the research p roject, which should no t b e disclosed. In these cases, such information should be detailed in a separate annex (not to be published) so that the Evidence Project Final Report can be placed in the public domain. Where it is impossible to complete the Final Report without including references to any sensitive or confidential data, the information should be included and section (b) completed. NB: only in exceptional circumstances will Defra expect contractors to give a "No" answer. In all cases, reasons for withholding information must be fully in line with exemptions under the Environmental Information Regulations or the Freedom of Information Act 2000. (b) If you have answered NO, please explain why the Final report should not be released into public domain

Executive Summary 7. The executive summary must not exceed 2 sides in total of A4 and should be understandable to the intelligent non-scientist. It should cover the main objectives, methods and findings of the research, together with any other significant events and options for new work. Surveillance activities targeting brown marmorated stink bug (Halyomorpha halys) were carried out between May and November 2020. Reports of UK interceptions at ports date back to 2010, but more recently (since 2018) adults have been observed free in the environment within England. Previous sentinel pheromone traps deployed in England and Wales during 2018 and 2019 (work funded by AHDB) caught no H. halys. However, two adult males (in Essex and London) were caught during this Defra-funded work in 2020. These catches were followed up with active sampling of foliage around the trap sites, using the beating tray technique, but no further signs of the pest were detected. Active sampling was also carried out at locations close to transport hubs and ports in South East England, but H. halys were not detected.

Only adults have been detected so far in the UK. Other life stages would be required to demonstrate reproduction and provide evidence for an established population. CLIMEX modelling based on UK climate parameters (using both historical data and projected future climate) was carried out in collaboration with SRUC, and predicts that H. halys already has the potential to establish in localised areas (particularly Greater London), with a much larger area of suitability for establishment across South East and Eastern England predicted by 2050. Based on this modelling, and on patterns of initial urban establishment of the pest in other countries, it is recommended that future UK surveillance efforts should include a greater number of pheromone traps within the Greater London area.

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Project Report to Defra 8. As a guide this report should be no longer than 20 sides of A4. This report is to provide Defra with details of the outputs of the research project for internal purposes; to meet the terms of the contract; and to allow Defra to publish details of the outputs to meet Environmental Information Regulation or Freedom of Information obligations. This short report to Defra does not preclude contractors from also seeking to p ublish a f ull, formal scientific report/paper in an appropriate scientific or other journal/publication. Indeed, Defra actively encourages such publications as part of the contract terms. The report to Defra should include: ⚫ the objectives as set out in the contract; ⚫ the extent to which the objectives set out in the contract have been met; ⚫ details of methods used and the results obtained, including statistical analysis (if appropriate); ⚫ a discussion of the results and their reliability; ⚫ the main implications of the findings; ⚫ possible future work; and ⚫ any action resulting from the research (e.g. IP, Knowledge Exchange).

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The agreed activities comprised: • Co-ordination of a pheromone-based trapping programme, hosted by volunteers at multiple (between 15 and 20) sites in England and Wales. • Field visits to suspected areas of BMSB population establishment for active searching for life stages of the invasive pest in mid- and late-summer, using established beating tray and net sampling methods. The following report is a modification of a manuscript accepted for publication (Powell et al., 2020) on 30th November 2020.

INTRODUCTION Halyomorpha halys (Stål) (brown marmorated stink bug) (: ) is an invasive shieldbug native to East Asia, where it occurs in regions of China, Japan, and Korea (Haye et al., 2015). The global range of this species has expanded considerably within the last three decades and it is now well established in North America and Europe (Haye et al., 2015; Leskey & Nielsen, 2018). Populations initially established in the USA during the late 1990s (Rice et al., 2014) and the species subsequently also colonised parts of Canada (Gariepy et al., 2014; Abram et al., 2017). Records in Europe date back to 2004 in Liechtenstein and Switzerland, followed by significant establishment and spread within Switzerland (Haye et al., 2015). Subsequent records followed in many European countries including (in 2012) France (Callot & Brua, 2013) and Italy (Maistrello et al., 2014) and later (2013) in Hungary (Vétek et al., 2014). Climate-based niche models indicate that regions of Europe between latitudes 40 and 50oN show particularly high risk of H. halys invasion and establishment (Zhu et al., 2012). Regions beyond 50oN (e.g. most of the UK) appear to have marginal suitability for establishment when historic climatic data are used to predict potential distribution, but small amounts of inter-annual climate variability, or future global warming, could change this scenario substantially (Kriticos et al., 2017; Kistner, 2017). Establishment in the Southern Hemisphere has been more limited but H. halys is also recorded in Chile (Faúndez & Rider, 2017). Halyomorpha halys has a very wide host range and is capable of feeding on many crop species in addition to exotic ornamental woody plants. The uses its piercing mouth parts to imbibe plant sap and particularly targets developing fruits, causing deformities (Fig. 1e) and internal staining that can render crops unmarketable. Tree fruit crops such as apple, pear, and peach (Leskey et al., 2012; Leskey & Nielsen, 2018) as well as soft fruits such as raspberry (Haye et al., 2015) are susceptible to damage. Glasshouse and field crops including tomatoes, peppers, sweetcorn, crucifers, and legumes may also be attacked and damaged (Rice et al., 2014). Following arrival in a new region, H. halys can spread rapidly and have agricultural impacts very soon after establishment. For example, the pest was first detected in Georgia in 2015 (Gapon, 2016) and caused US$24 million losses in hazelnut production in the first full year it was demonstrated to be present, whereas significant damage to Italian fruit crops occurred within two years of the first report of the species in Northern Italy (Maistrello et al., 2016). Like most other pentatomid species, H. halys pass the winter as adults. In the autumn, individuals move from food plants to sheltered over-wintering sites (Nielsen & Hamilton, 2009). Release of an aggregation pheromone by males (Weber et al., 2017), combined with vibration and tactile cues from conspecifics, may result in large clusters of adults (of both sexes) forming outside and inside buildings at this time of the year. The large numbers of aggregating , coupled with their distinct odour, can lead to significant urban nuisance problems in homes and businesses. The insects also crawl inside house contents,

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manufactured products, and packaging materials at this time of year, leading to a propensity for global passive dispersal (“hitch-hiking”) with exported cargo and passenger luggage. H. halys adults are capable of moving several kilometres via sustained flight, and flights exceeding 100 km are possible (Lee & Leskey, 2015). However, field (Zhang et al., 1993) and laboratory (Wiman et al., 2014; Lee & Leskey, 2015) studies suggest that most single flights are limited to distances of less than 5 km The increased global distribution of the species has instead been driven largely by the human-associated transport that occurs as a consequence of autumnal sheltering and aggregation behaviour. Live adults have been intercepted entering Britain with passenger luggage and imported commodities on several occasions (e.g. in 2010 and 2013; Malumphy, 2014). More recently (from 2018), live adults have been observed free in the UK environment and not obviously associated with imported materials. Halyomorpha halys also release their pheromone signal and are attractive to conspecifics during spring and summer, contributing to aggregation during feeding (Fig. 1a) in addition to over-wintering. This natural behaviour can be exploited for monitoring and surveillance purposes, as commercial traps and lures are available based on synthetic pheromone components. During the summer of 2020, adults were caught in pheromone traps for the first time in South East England. We describe these interceptions and use CLIMEX modelling and localised degree-day analyses to assess the likelihood of establishment across the UK and Ireland and at specific local sites of interception. Based on these approaches, we discuss the provenance of the recently-intercepted insects and the current and likely future status of H. halys in the UK.

RECENT INLAND RECORDS WITHIN THE UK Halyomorpha halys adults (Fig. 1a) can be distinguished from similar species found in Europe (Wyniger & Kment, 2010) based on features including absence of fine hairs covering the body (unlike Dolycoris baccarum (L.)), lack of a ventral spine (unlike Rhaphigaster nebulosa (Poda)), unique patterns of pale areas of the scutellum, pronotum and antennae (Powell, 2018), and a relatively rectangular-shaped head. In addition to interceptions of the pest with imported goods and luggage at UK borders since 2010 (Malumphy, 2014; Malumphy & Eyre, 2015), we are aware of three occasions when live adult H. halys were reported and identified following chance observations in the UK interior (Table 1). The first insect was sheltering within a rodent bait box at a business premises in Hampshire and was found and identified by a pest control specialist (Davies, 2018). This insect was collected and confirmed to be a male adult H. halys. In April 2019, a second adult was observed near Farnham (at a site in Hampshire, close to the Surrey border and within 30 km of the location of the November 2018 insect). This individual was photographed and images uploaded to iNaturalist.org (Rockhill, 2019). The images were sufficient for later identification to species, but the insect was not collected, and the sex is unknown. In August 2020, another live adult was spotted and photographed in a suburban garden in the Rowley Fields area of Leicester (Cann, 2020). The images of this insect (naturespot.org.uk) also allow identification to species but the sex cannot be determined. In 2018, 2019 and 2020, sentinel pheromone traps were deployed at several sites in England and Wales as part of a H. halys surveillance programme co-ordinated by NIAB EMR. “Pherocon BMSB STKY” rectangular (30 x 15 cm) double-sided clear sticky traps with high-dose 12-week pheromone lures (Trece Inc., USA) were used, releasing a chemical component of the H. halys aggregation pheromone (murgantiol) and a synergist (methyl (E,E,Z)-2,4,6-decatrienoate). These pheromone traps provide effective, long-lasting detection of H. halys when populations of the pest are present (Weber et al., 2017).

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Traps were located in a variety of regions and habitats (10 sites in 2018 and 2019, 19 sites in during the 2020 Defra study; Fig. 2), including urban parks and gardens, business premises and rural sites of commercial fruit production. Each trap was fixed to a horizontal tree branch (Fig. 3) approximately 2.5 m from ground level. Traps were initially installed between late May and early June of each year when possible, with the aim of checking weekly for signs of captured shieldbugs (adults or nymphs, as the aggregation pheromone may potentially attract any mobile life stages). The sticky traps and lures were replaced after 12 weeks (in late August / early September) and the trapping continued for a second 12- week period (until November). No H. halys were caught during 2018 or 2019, and pentatomids of other species were very rarely reported on the traps during any of the three field seasons. On 14th August 2020, a male H. halys (Fig. 4a,b) was observed stuck to the sticky surface of a trap located at RSPB Rainham Marshes, Essex. The insect was alive at the time of interception and therefore very likely flew to the trap within a day or two of this finding. On 18th August, a second insect (also a male, Fig. 4c) was recovered from the trap located in the Natural History Museum Wildlife Garden at South Kensington, London. This insect was dead at the time of interception, and as it had not been possible to check this trap since 31st July, may have been attracted to the lure up to 17 days previously (date of capture was recorded as 1-17/08/20). Both insects were damaged during removal from the surface of the sticky trap (Fig. 4). It should be noted that, although traps were installed by early June at most sites, Covid-19-related lockdown, and restrictions delayed installation at both the Natural History Museum and the Rainham Marshes sites. The Museum trap was put up on 30th June, and the Rainham Marshes one on 27th July. Both pheromone catches were followed up with targeted active sampling at both sites during August and September, beating foliage to search for other signs of the invasive species, but no further individuals were found.

CURRENT AND FUTURE LIKELIHOOD OF UK ESTABLISHMENT CLIMEX (a process-oriented climate-based niche modelling software package) has been widely used to model the potential distribution of many invasive pests, including H. halys (Kriticos et al., 2017). Access to this model allowed use of UK data to assess the risk of H. halys establishment. The CliMond CM10 World (1975H V1.2) climate dataset was used for model fitting (Kriticos et al., 2012). This global climatological dataset has a spatial resolution of 10 arc minutes and consists of long-term (30 year) monthly averages of daily minimum and maximum temperature, relative humidity at 09:00 and 15:00 h and monthly rainfall totals. As well as assessing recent historical climate for the establishment of H. halys, climate projections for 2050 based on IPCC IV SRES Scenario A1B (medium emissions) were also evaluated, using data from the CSIRO Mk3.0 Global Climate Model (Harris et al., 2014). The CLIMEX parameter values used were those developed by Kriticos et al. (2017) and the International Pest Risk Research Group (IPRRG- https://pestrisk.org/) for H. halys and included a development threshold of 12 oC, 595 degree days required per generation, an optimal temperature range of 27 - 30 oC, and diapause induction below 12 h day length and 5 oC. Spatial outputs from the CLIMEX model under historical average climate values are shown in Fig. 5a. Only restricted regions of South East England (in areas of Greater London and North Norfolk) are highlighted as suitable for supporting H. halys populations. These areas may support one generation at the most and should therefore be considered at least marginally suitable for establishment during the years captured by this data set (1961 – 1990). All other areas of the UK did not have sufficient degree days during this period to allow H. halys to complete a generation

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Applying climate projections for 2050 using the CLIMEX model highlighted a much larger area within England as likely to become suitable for establishment, indicating that between 1 and 1.5 generations a year would be possible in outdoor conditions (Fig. 5b). In addition, analysis of individual recent years and locations was carried out, based on the degree days accumulated at various specific sites of interest (data obtained from https://degreedays.io/) to assess suitability for establishment. At the sites of recent records in Hampshire, Essex and London, the local climate data recorded during the year of interception always indicated that sufficient degree days for completion of at least one full generation occurred (Table 2). This was not the case for the location of the adult recorded in Leicester following partial (to October) analysis of 2020 data, but a full generation may have been possible at this location during one of the previous years analysed (2018) using full-year data sets.

PROVENANCE OF 2020 PHEROMONE CATCHES The two interceptions of male H. halys during the late summer of 2020 represent very different situations to the previous UK reports based on chance observations (Table 1). Flight to these pheromone-baited traps indicates that the individuals caught in Essex and London were actively searching for conspecifics during the time of the season when aggregation occurs on host plants. The timing of these catches makes it very unlikely that they were adults that had developed overseas during the 2020 season and been imported shortly before capture. Movements of live over-wintered H. halys with imports (hitch-hiker interceptions at borders) start from September and are most likely to occur between November and January (e.g. Australian Department of Agriculture, 2019). The adults found in South East England and Leicester during August 2020 would have therefore spent the spring and summer feeding within the UK. They either developed overseas before being imported during the 2019-20 winter or may have developed undetected in small local populations. In order to examine this second possibility, assuming that the insects developed locally and moulted to adult shortly before capture, 2020 degree-day data were obtained for the specific sites of interception. These analyses were based on published egg-to-adult thermal requirements from European H. halys populations (Haye et al., 2014; 588 degree days required above a critical temperature of 12oC to complete development). Extrapolating back from each date of capture indicated that only eggs deposited before 10 th April at the Rainham Marshes site and 25th May at the South Kensington site would have been exposed to sufficient degree days for full development locally. It seems very unlikely that oviposition would have occurred before the end of May within small, undetected UK populations. At more southern latitudes in Europe and the USA, reproductive diapause by over-wintered adults continues well into the spring. Oviposition starts in late May / early June but most eggs are deposited during June and July (data from the USA, Switzerland and Italy: Nielsen & Hamilton, 2009; Nielsen et al., 2017; Haye et al., 2014; Costi et al., 2017). Although CLIMEX modelling (Fig. 5a) and analysis of specific, localised degree-day data (Table 2) indicate that H. halys has potential to complete at least one generation and establish small populations in parts of the UK, we conclude that the individuals intercepted in August 2020 were probably imported as diapausing adults several months earlier, during the 2019-20 winter. Survival curves of H. halys adults collected from over-wintering sites and contained with food sources (in cages, provided with shelter from the rain but exposed to external conditions in Switzerland; Haye et al., 2014) indicate that approximately 30% of such over-wintered adults remain alive in mid-August. It therefore seems feasible that the South Kensington, Rainham Marshes and Leicester adults were imported as hitch-hikers having developed to

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adult and sought over-wintering shelter overseas. With more numerous UK interceptions anticipated in the future, it should be possible to dissect adults to investigate their stage of reproductive development and assess whether individuals are pre-reproductive (in diapause), reproductive or post-reproductive at the time of interception (Nielsen et al., 2017).

ACTIVE SAMPLING FOR THE PEST DURING 2020 In addition to pheromone-based monitoring, active sampling was carried out at locations considered to be likely establishment sites. These included locations in Hampshire where adults were reported in 2018 and 2019, in addition to sites close to transport hubs and ports. Vegetation was sampled using the beating tray method. Numerous other species of UK shieldbugs were observed during this sampling work, confirming the efficacy of the sampling method. However, no H. halys were found.

The sites sampled were New Alresford, Hampshire (8th July), Alice Holt and Birdworld, Hampshire (23rd July), Southampton Docks and City Centre (11th August), Rainham Marshes Nature Reserve, Essex (20th August), Dover Ferry Port and Town Centre, Kent (11th September), Natural History Museum Wildlife Garden, South Kensington (14th September), perimeter of Eurotunnel terminal near Folkestone, Kent (15th September) and Ashford International Station and Town Centre parkland, Kent (21st September).

CONCLUSIONS AND LIKELY FUTURE COLONISATION PATTERNS Recent observations and catches at pheromone traps confirm that adult H. halys are present within the UK. As a pest of global concern, particularly in fruit and vegetable-growing regions, it will be important to continue to monitor the movement and establishment of the species. The absence of significant cross- attraction and by-catch of other species makes pheromone-based surveillance a useful approach for continuing future monitoring and early detection. In the UK this species will remain classified as migrant (recorded occasionally but without established colonies) rather than colonist (recently settled and with established colonies) (Hawkins, 2003) until other life stages (nymphs and egg masses) are reported. Nymphs of H. halys have striking features that are not shared with other pentatomid species present in Europe (including lateral spines on the pronotum and head, Fig. 1b,c,d) and are likely to be spotted and reported.

CLIMEX modelling based on recent climate data predicts regions of suitability for H. halys establishment localised to Greater London, with potential to spread to a much larger area of Eastern and South East England by 2050. However, the modelling does not account for the increases in frequency and intensity of short-term extreme weather events predicted under future climate scenarios (Kriticos et al., 2012; Kistner, 2017). At specific locations of recent interceptions, the model prediction (based on recent historical climate data) was marginally short of a full generation per year, whereas degree-day data recorded during 2018- 20 indicated that at least one generation could be completed (Table 2). Short-term patterns of climate variability may allow build-up of significant populations in future, possibly leading to sporadic outbreaks with potential for urban nuisance problems and crop damage. In the UK, tree fruit crops such as apple and pear are likely to be at particular risk of damage, but field crops including sweetcorn and brassicas may also be affected. While the climate-based modelling in this study and previous work is based on outdoor conditions, the enhanced temperatures provided under protected cropping conditions may contribute to increased risk of damage to susceptible glasshouse and polytunnel crops such as tomatoes, peppers and soft fruit. CLIMEX modelling using temperature data collected from polytunnels in Scotland (K.A. Evans,

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SRUC, unpublished) has demonstrated the potential for at least two generations of H. halys a season depending on when the pest is introduced into the tunnel and the stage of its development (egg, nymph or adult). The urban “heat island” effect has played a key role in the establishment of other invasive pentatomid species (Tougou et al., 2009; Musolin & Saulich, 2012). In the UK, the impact of this effect has likely influenced initial establishment of both Nezara viridula (L.) (Barclay, 2004; Salisbury et al., 2009) and R. nebulosa (Bantock et al., 2011) in the Greater London area during the last two decades, with both species subsequently expanding their distribution to other areas. Both R. nebulosa and N. viridula have been noted in the Natural History Museum garden, and overwintering in the NHM building, and NHM pest monitoring will pay attention to overwintering pentatomids in future to see if H. halys are detected. Halyomorpha halys also shows a pattern of initial urban colonisation, e.g. early reports in Europe included initial population growth in Zurich (Haye et al., 2015) and Paris (Maurel et al., 2016). Recent records of the species in Berlin (the 139 confirmed observations recorded on iNaturalist.org to 30th November 2020 are all from 2018-2020) include numerous images of early-, mid- and late-instar nymphs, indicating that H. halys is currently colonising this area. Future UK surveillance efforts should therefore include a higher density of pheromone traps within Greater London and other urban sites within the South East.

ACKNOWLEDGEMENTS We thank the volunteers who have hosted H. halys pheromone traps in England and Wales as part of this surveillance work. At RSPB Rainham Marshes, Andrew Gouldstone (Senior Site Manager) and Jamie Smith (Warden) agreed to host traps and assisted with setting them up. Caroline Ware and other staff at Natural History Museum enabled the placement of traps in the NHM garden. Melvin Knapp, Jaime Rockhill, Robert Sayer and Jack Vasey kindly shared information relevant to their observations of adults in Hampshire and Leicester, and Tim Haye (CABI) and Debbie Evans (Feltons Orchards) gave permission for use of photographs. We also thank Brian Garms (Department of Agriculture and Water Resources, Australia), Tania Yonow (CSIRO, Australia) and Michelle Fountain (NIAB EMR) for helpful comments and advice during preparation of the report.

REFERENCES

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Leskey, T.C & Nielsen, A.L. 2018. Impact of the invasive brown marmorated stink bug in North America and Europe: history, biology, ecology and management. Annual Review of Entomology 63: 599- 618. Leskey, T.C., Short, B.D., Butler, B.R & Wright, S.E. 2012. 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 2012: 1–14. Maistrello, L., Dioli P., Vaccari, G., Nannini, R., Bortolotto, P., Caruso, S., Costi, E., Montermini, A., Casoli, L. & Bariselli, M. 2014 First records in Italy of the Asian stinkbug Halyomorpha halys, a new threat

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to fruit crops. ATTI Giornate Fitopatologiche 1: 283–288. Maistrello, L., Costi, E., Caruso, S., Vaccari1, G., Bortolotti, P., Nannini, R., Casoli, L., Montermini, A., Bariselli, M. & Guidetti, R. 2016. Halyomorpha halys in Italy: first results of field monitoring in fruit orchards. Integrated Protection of Fruit Crops Subgroups “Pome fruit ” and “Stone fruits” IOBC-WPRS Bulletin 112: 1-5. Malumphy, C. 2014. Second interception of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) in Britain. Het News, 3rd Series 21: 4–5. Malumphy, C; Eyre, D (2015) Plant pest factsheet, Brown marmorated stink bug Halyomorpha halys. Department of Environment Food and Rural affairs (DEFRA) (https://planthealthportal.defra.gov.uk/assets/factsheets/halyomorpha-halys-defra-pest-factsheet- v3.pdf) Maurel, J.-P., Blaye, G., Valladares, L., Roinel, É Cochard, P.-O. 2016. Halyomorpha halys (Stål, 1855), la punaise diabolique en France, à Toulouse (Heteroptera; Pentatomidae). Carnets natures 3: 21-25. Musolin, D.L., Saulich, A.K. 2012. Responses of insects to the current climate changes: from physiology and behavior to range shifts. Entomological Review 92: 715–740. Nielsen, A.L., Hamilton, G.C. 2009. Seasonal occurrence and impact of Halyomorpha halys (Hemiptera: Pentatomidae) in tree fruit. Journal of Economic Entomology 102: 1133–1140. Nielsen, A.L., Fleischer, S., Hamilton, G., Hancock, T., Krawczyk, G., Lee, J.C., Ogburn, E., Pote, J.M., Raudenbush, A., Rucker, A., Saunders, M., Skillman, V.P., Sullivan, J., Timer, J., Walgenbach, J., Wiman, N.G. & Leskey, T.C. 2017. Phenology of brown marmorated stink bug described using female reproductive development. Ecology and Evolution 7: 6680–6690. Powell, G. 2018. Brown marmorated stink bug Halyomorpha halys: species alert. British Journal of Entomology and Natural History 31: 2672. Powell, G., Barclay, M.V.L., Couch, Y. & Evans, K.A. 2021. Current invasion status and potential for UK establishment of the brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae). British Journal of Entomology and Natural History (in press). Rice, K.B., Bergh, C.J., Bergmann, E.J., Biddinger, D.J., Dieckhoff, C. et al. 2014. Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). Journal of Integrated Pest Management 5: 1-13. Rockhill, J. 2019 Brown marmorated stink bug (Halyomorpha halys) report on iNaturalist. (https://www.inaturalist.org/observations/23382471) Salisbury, A., Barclay, M.V.L., Reid, S. & Halstead, A. 2009. The current status of the southern green shield bug, Nezara viridula (Hemiptera: Pentatomidae), an introduced pest species recently established in South-East England. British Journal of Entomology and Natural History 22: 189-194. Tougou, D., Musolin, D.L. & Fujisaki, K. 2009. Some like it hot! Rapid climate change promotes shifts in distribution ranges of Nezara viridula and N. antennata in Japan. Entomologia Experimentalis et Applicata 30: 249–258. Vétek, G., Papp, V., Haltrich, A., Rédei, D. 2014. First record of the brown marmorated stink bug, Halyomorpha halys (Hemiptera: Heteroptera: Pentatomidae), in Hungary, with description of the genitalia of both sexes. Zootaxa 3780: 194–200. Weber, D.C., Morrison, W.R., Khrimian, A., Rice, K.B., Leskey, T.C., Rodriguez-Saona, C., Nielsen, A. & Blaauw, B.R. 2017. Chemical ecology of Halyomorpha halys: discoveries and applications. Journal of Pest Science 90: 989–1008.

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Wiman, N.G., Walton, V.M., Shearer, P.W., Rondon, S.I. & Lee, J.C. 2014. Factors affecting flight capacity of brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae). Journal of Pest Science 88: 37-47. Wyniger, D. & Kment, P. 2010. Key for the separation of Halyomorpha halys (Stål) from similar appearing pentatomids (Insecta: Heteroptera: Pentatomidae) occurring in Central Europe, with new Swiss records. Bulletin de la Société Entomologique Suisse 83: 261–270. Zhang, C.T., Li, D.L., Su, H.F. & Xu, G.L. 1993. Study on the biological characteristics of Halyomorpha picus and (in Chinese). Forest Research 6: 271-275. Zhu, G., Bu, W., Gao, Y. & Liu, G. 2012. Potential geographic distribution of brown marmorated stink bug invasion (Halyomorpha halys). PLoS ONE 7: e31246.

Table 1 Records of Halyomorpha halys (all single adults) found in the UK, other than insects intercepted in imported luggage and goods described elsewhere (Malumphy, 2014) Location OS grid Date Method Reference reference New Alresford, SU5933 21/11/18 Observation Davies, 2018 Hampshire Alice Holt, SU810431 27/04/19 Observation Rockhill, 2019 Hampshire Rainham TQ551791 14/08/20 Pheromone trap Couch & Powell, 2020; Marshes, Essex Powell et al., 2020 Natural History TQ265790 17/08/20 Pheromone trap Powell et al., 2020 Museum, London Rowley Fields, SK573027 20/08/20 Observation Cann, 2020 Leicester

Table 2 Cumulative degree days above a 12°C base temperature for Halyomorpha halys development (595° days required to complete a generation) at five English locations where adults have been found (see Table 1 for grid references). Values in parentheses show predicted number of generations that can b e completed. Actual data for 2018, 2019 and 2020, based on accumulated degree days only, rather than full model parameters (*up to 7th Oct 2020), and predictions from the full model based on thirty-year average (centred around 1975) and projected 2050 climate. Values in bold show the degree days and number of possible generations for the particular year of H. halys interception at each location. Location 2018 2019 2020* 30-year 2050 average projection (from (from model) model) New Alresford, 815.32 575.82 627.65 494 637 Hampshire (1.37) (0.97) (1.05) (0.83) (1.07) Alice Holt, 869.88 605.24 644.11 510 655 Hampshire (1.46) (1.02) (1.08) (0.86) (1.1) Rainham 1138.69 870.78 816.48 570 732 Marshes, (1.91) (1.46) (1.37) (0.96) (1.23) Essex Natural History 1315.54 1036.52 976.49 570 736 Museum, (2.21) (1.74) (1.64) (0.96) (1.24) London Rowley Fields, 750.43 520.79 523.98 495 625 Leicester (1.26) (0.88) (0.88) (0.83) (1.05)

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Fig. 1. Halyomorpha halys life stages and damage to fruit (not to scale). a) Adults; b) last immature stage (fifth-instar nymphs); c) mid-instar nymph; d) first-instar nymphs clustered around empty egg cases; e) feeding damage to apple. All images kindly provided by Tim Haye (CABI) and used with permission.

Fig. 2. Map showing distribution of Halyomorpha halys pheromone traps during the 2020 surveillance

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programme. Key: 1 trap at 17 sites (from West to East: Cardiff; Ashton Keynes, Wiltshire; Leighton, Shropshire; Leicester; Gosport, Hampshire; Alton, Hampshire; Arborfield, Berkshire; Fulham, London; South Kensington, London; Cambridge; East Malling, Kent; Robertsbridge, East Sussex; East Farleigh, Kent; Chatham, Kent; Barrow, Suffolk; Ashford, Kent; Ash, Kent). 2 traps at 1 site (RSPB Rainham Marshes, Purfleet, Essex). 3 traps at 1 site (Alice Holt / Birdworld area, Hampshire).

Fig. 3. Halyomorpha halys pheromone trap in situ with black pheromone lures visible, fixed next to the double-sided sticky trap (located at a pear orchard site in Suffolk, image courtesy of D. Evans).

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Fig. 4. Adult male Halyomorpha halys captured using pheromone traps located in Essex and London. a) ventral view of Rainham Marshes insect; b) dorsal view of Rainham Marshes insect; c) dorsal view of South Kensington insect (pinned).

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Fig. 5. Potential number of Halyomorpha halys generations per year under a) historical 30-year (1961- 1990) average climate and b) projected climate for 2050.

a)

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b)

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References to published material 9. This section should be used to record links (hypertext links where possible) or references to other published material generated by, or relating to, this project. Couch, Y. & Powell, G. 2020. First report of the brown marmorated stink bug Halyomorpha halys in Essex. Essex Naturalist (New Series) 37: 147-150.

Powell, G. AHDB Webinar “Brown marmorated stink bug information and question session”, 20th November 2020. https://www.youtube.com/watch?v=waSj5ERPVlA&t=1814s

Powell, G., Barclay, M.V.L., Couch, Y. & Evans, K.A. 2021. Current invasion status and potential for UK establishment of the brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae). British Journal of Entomology and Natural History (in press).

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