Predicting the potential for spread of emerald ash borer ( Agrilus planipennis ) in Great Britain: What can we learn from other affected areas?

Emerald ash borer (EAB) is thought to have arrived in North America and European Russia at least 10 years prior detection. Despite heightened awareness that EAB could invade Great Britain (GB), detection the early stages of establishment difficult, initial symptoms might be mistaken for Chalara dieback. Our results suggest if partial resistance Fraxinus excelsior does not significantly dampen population dynamics, then establish spread across large parts southern England within a relatively short time period; however, further northern may limited by cool climate. (EAB; Agrilus planipennis) member family Buprestidae, jewel beetles. The genus notable having largest number species, more than 3,000 (Bellamy, 2008), any single animal kingdom. Only few species are considered pests, which both A. anxius (bronze birch borer) currently form potential threat forests. Within there only known endemic Agrilus, most notably biguttatus which, until recently, was treated as vulnerable but now pest relation Acute Oak Decline (Brown et al., 2015). beetle native north-eastern Asia where it an manageable controlled several natural enemies (Wang 2010). first identified 2002 assigned common name Entomological Society aid communication (Cappaert 2005; Haack 2002). Between 2003 2006, specimens were also collected entomologists different Moscow, Russia; they officially confirmed 2007 (Baranchikov 2008; Valenta 2017). Dendrochronological analysis outbreak south-eastern Michigan suggests introduced somewhere between late 1980s 1990s (Siegert 2014) possible this case (Musolin Current surveillance data indicate majority Western Europe free pest; widespread increasing risk imminent (Orlova-Bienkowskaja 2020). Larval feeding creates distinctive serpentine galleries under bark inhibit flow water nutrients canopy, trunk roots, leading canopy dieback eventually tree death 2005). Hundreds millions trees been killed directly indirectly 35 states United States (United Department Agriculture, Animal Plant Health Inspection Service [USDA APHIS]), five Canadian provinces (Canadian Food Agency [CFIA]) 16 regions 2020) immense economic (Kovacs 2010) social cost (Donovan 2013; Kondo Billions dollars spent on control EAB, dealing with infested replacement non-host (Poland & McCullough, 2006), literature has built up around research driven questions life cycle behaviour strategies disease control. destructive forest ever recorded eradication from affected region no longer viable option (Aukema 2011; Herms 2014). Three factors make so difficult manage are: Once becomes established, ceases or practical option. However, developing slow rate spread, such biological targeted chemical protection host trees, enables removal managed efficiently (McCullough, Ash forests already suffering due rapid fungal pathogen Hymenoscyphus fraxineus, causes referred (ADB). A recent meta-analysis mortality (Coker 2019) highlighted lack systematic assess impact ADB. Coker al. (2019) concluded whilst some plantations reporting 85% ADB, woodlands showing lower levels mortality. This enable recover, seedlings resistant help re-establish woodland populations. can survive combined attack ADB? key question how much countries should invest pre-emptive strategies, attaining approval agents, mitigate against arrival EAB. answer depends complex interaction climatic suitability, genetic profile ash, health, density, influence human predators parasites dynamics. second abundant GB, feature hedgerows (Maskell 2013) presenting highly connected landscape through disperse. potentially important difference America, GB distribution particular species. predominant (European Ash), rarely planted and, F. Russia, non-native pennsylvanica, many cities along highways 2014; Musolin Evidence relative versus pennsylvanica interpret reported longitudinal studies. Whilst evidence appears damage 2020; Straw another American nigra (Showalter 2020), clear all studies partial. Examination main botanical garden Russian Academy Sciences Moscow found 70% (45 out 64) dead dying had infestation compared 89% (48 54) factor duration varies 1 2 (Herms precise mechanisms driving unclear climate, larval subspecies, health apparent contributing Jones 2019; Orlova-Bienkowskaja Bieńkowski, 2016; Siegert 2010; Tluczek 2011). general, warm climates, univoltine cooler climates 2-year predominates. two extremes, less predictable vary cohorts annual temperature fluctuations (Jones 2016). In New York, mixture cycles observed, peaks third/fourth instar larvae peak attributed overwintered arising eggs laid season 2019). peak, adequate degree day accumulation same season, neither pupae nor pharate adults detected after July supporting hypothesis needs overwinter prepupal stage complete It likely compulsory overwintering prepupae leads observed synchronisation adult emergence, emergence local populations occurring 4- 6-week period (Duart, range mathematical models spatial regional scales developed investigate dynamics inform policy Early role anthropogenic need effective firewood quarantines (BenDor 2006; Muirhead Iverson Prasad Economic analyses, using exponential dispersion kernel simulate long-distance pest, demonstrated importance investing measures identifications new incursions slow, eradicate, As become available landscape, used explore options slowing down given feasible (McCullough Mercader, 2012; Mercader 2011, Kovacs Lyttek Refined predictions direction outbreaks remain uncertainties over drivers flight, variation human-mediated management event identification established urgent would “How far we eradicate pest?” Uncertainties other variables typical setting mean that, absence area estimate parameters, adapting existing obtain challenging. We therefore adopted simpler approach estimating extent infestation, encompassing multiple satellite outbreaks, GB. paper, consider simple metrics gauge part our analysis, compare States, Canada national level records. part, environmental suitability comparing predicted dates areas, based review days ask whether climate provides suitable environment expect semivoltine. Finally, combine these analyses scale accidentally imported into either central Southeast (i) soon became established; (ii) 5–10 before its presence detected, analogous delays America. purpose implementing highlight investment strategies. take global overview rate, focussing dispersal areas speed National year obtained (Figure 1). dataset compiled USDA APHIS, consists county records positive (Ward Canada, CFIA supplied Open Government Licence—Canada (later manually extracted individual reports; Agency, georeferenced point locations identification. Geolocated (2020). These comprise ad hoc reports epidemiological surveys. survey conducted 2009 covering radius approximately 150 km 2008). years. Borer 2002. During six counties (Macomb, Livingston, Monroe, Oakland, Washtenaw Wayne) Essex County, Ontario (Haack Subsequent dendrochronological reconstruction points towards originating suburb Canton north west Wayne County (estimated 42.31°N, 83.49°W) 1997 assume site forms epicentre Canada. dominant well city 2008) 55.81°N, 37.64°E). For each dataset, Euclidean distance centroid location, applicable, country specific calculated converted kilometres. estimated fitting linear functions intercept fixed maximum cases identified. appropriate function describe selected minimum r2 value, measure explained regression. Direct comparison values datasets because differences observation numbers protocols collection (all occurrences vs. surveys Russia). accumulated degrees Reported relationship days, vary. can, (average value formula sine wave methods, base 13.5°C 10°C); measured (direct observation, indirect via recording exit holes, capture flying traps); frequency observations (see, example, Brown-Rytlewski Wilson, 2004; Cappaert Duart, Lyons Jones, Poland 2011) factors. purposes exploratory threshold aim literature: 230°C DD10, consistent (and often quoted basis study 2004) 500°C consistently thresholds met year, lifecycle predominantly univoltine. regions, later Regions calendar unlikely provide establish. Accumulated 1st January modified sine-wave method (Baskerville Emin, 1969) assuming 10°C, below development occurs (Brown-Rytlewski 2004). start date commonly calculation phenological insect Northern Hemisphere convenient insects state quiescence. Weather 2007–2018 ERA5-Land (Copernicus Climate Change (C3S; 2019): C3S reanalysis. Copernicus Service, access: 14 February ). reanalysis combining weather model data. land decades improved resolution ERA5 (0.1° × 0.1° 0.25° 0.25°). temporal output hourly, fields masked oceans. Two hypothetical epicentres introduction contextualise invasion rates equivalent those conditioned upon availability sufficient permit development. starting points: Dover, South East coast and; Birmingham, England; represent entry shipping direct transport. illustration define zero. Following Ward (2020) marks end phase during minimal spread. induced occurred 2014), 5 commencement recording. 2002, 102 (2014). implies average allowing jumps, 20 km/year 5-year period. Thereafter, use (see results: 47 km/year). extents radial cumulative expansion plotted overlaid map 2018. illustrative reach DD10 DD10. cut-off September able cut-off, area. on: feed leaves 5–7 mating oviposition 2005); flight May June elsewhere; staggered beetles 2010); cessation August latitudes location when wavefront reaches it, onward occur future even All plotting MATLAB® 2020b in-built functions, user contributed Violinplot (Bechtold, 2016) ColorBrewer (Cobeldick, Data Toolbox (Greene continued host. addition active extreme jump Maryland 2003; Colorado 2013 600 miles (equivalent entire length GB) nearest (Alexander 2019), saplings despite restrict regions. infestations better captured (linear: = .48 exponential: .27; Figure 2a); little distinguish .70 .73). visual fit 2b) particularly years—the slower barrier provided Lakes. cause decline America; extended 80 assumed 100 Fitting set gives edge 48 (95% CI: 47–49) per 50.2 48.5–51.8) Combining sets slightly 47.1 46.3–47.9) since furthest distances (102 km; cf 2a,b,d). infer Section 3.3). tended south 1b). Recent close border Ukraine Belarus 900 best .31 .48; 2c); wide low confidence result. Reanalysing 2009, 107 km, 2012–14 2018–19 40.4 30–50.7, .42) note missing sets. Based averaging (2008–2018), see northerly commence earlier elsewhere 3c). Similarly, 3a), published weeks 3a). mild winters, southeast expected accumulate earliest Wales Note, 10-year hides reached larger (Figures 4 5). Scotland, summer autumn, conducive unless adapt 2c). Accumulation (cf 3b,d) leaf-fall Wales, never high lying Scotland. Extending exploration Europe, although 3c), 3d), similar phenology unaffected 1- move 1-year Europe. do hypothesised If intercepted breeding, chance increased will missed phase. Assuming phase, 1,000 km2 search 4, Year 1) delay 4). onwards initially 2a,b). Whether efficacy quarantine reducing probability mediated unclear. 1a highlighting small size encompassing, expand (47 km/year), Dispersal very resulting food emerging beetles; 2017 2018 (Years 11, 5), enabled present. Long pests pathogens international trade travel devastating effect delayed recognition thread subsequent enquiries. increases their range, hosts coevolution, evolutionary naïve (Gandhi Herms, Hence, about invasion. present being reared point, extensive efforts identify researchers papers China insight Since billions poured >800 published. still uncertainty including controlling pest. Efforts quarantine, failed stop spreading continue An issue long cryptic whereby colonisation deep crevices holes easily 2002) replicate disperse wider three generations without result, apparently isolated too costly stamp out. Much but, witnessed devastation countries, concerned accidental import lead destruction infection fugal H. causal organism paper focused exploring precursor concern landscape. find unsuitable low-temperature result all. rapidly causing colonies ease dispersed routes means true larger. gravid females seeking hosts, suggested hitchhiking clothing, vehicles (Buck Marshall, and/or train carriages (Short bulk transport contaminated wood saplings. Teasing mechanism complicated occur: disturbances, activity pruning storage; movement vehicles, saplings, timber firewood. insects, complication choice intraspecific competition, preference availability. By mill measurements speeds, Taylor (2010) capable >20 km/day enabling flight. Overlaying highlights silent valid criticism imposing Russia. transportation recreational camping trips. bundles purchased retailers selling public Rocky Mountains, USA 50% contained one taking 18 months emerge (Jacobi 2012). Bieńkowski (2018) argue mainly processes 2018; Short 2013). Hitchhiking harder control; current seems Kingdom, campsites allow open fires, supply campers; source heating fuel. domestic Kingdom 7.5% households fuel (Waters, Comparison struggle synchronise survive, semivoltine cycle. There biophysical affect conclusion. winters completion autumn; restricted photoperiod timing winter dormancy (Saunders, 2020); weakened ADB unknown (Dearborn Showalter distribution, mix planting density distances; parasitoids (Bauer addition, activity, link appear strong rest offers growth (Mercader conversely newly undetected focus ongoing dominance Experimental laboratory conditions field, growth, thereby providing window outbreaks. 500 forest, situated 25 apart signs stands detailed surveys, traps, required opportunity invade, intend pursue proactive intensive implementation limit arrive. Passive trapping miss significant occur, investigation assumption UK examples show once inevitable biocontrol ash. contains information licensed Licence—Canada. authors grateful Dr Chris MacQuarrie, Natural Resources Andrew Liebhold, Forest sourcing Daniel Bonnéry, University Cambridge discussion statistical work funded Environment, Rural Affairs QMSC modelling programme. CRW planned carried project advice CAG. CAG wrote manuscript. TM sourced