Community composition and structure had no effect on forest susceptibility to invasion by the emerald ash borer (Coleoptera: Buprestidae)

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1 1 Community composition nd structure hd no effect on forest susceptibility to invsion by the emerld sh borer (Coleopter: Buprestide) Annemrie Smith, Dniel A. Herms, Robert P. Long, Kml J.K. Gndhi 1 Abstrct Emerld sh borer (EAB), Agrilus plnipennis Firmire (Coleopter: Buprestide), is non-ntive, wood-boring beetle tht hs cused widespred mortlity of sh (Frxinus Linneus (Olecee)) in estern North Americ. During , we determined whether forest community composition nd structure of blck (F. nigr Mrshll), green (F. pennsylvnic Mrshll), nd white (F. mericn Linneus) sh stnds influenced their susceptibility to EAB invsion in southest Michign, United Sttes of Americ. There ws no reltionship between EAB-induced sh decline or percentge mortlity nd ny mesure of community composition (tree species diversity, stnd/sh density, totl bsl re, or reltive dominnce of sh). There ws lso no reltionship between mesures of EAB impct (density of EAB signs, sh decline rting, percentge sh mortlity, or percentge infested sh) nd forest ttributes (sh/totl stnd density, bsl re, sh importnce, or stnd diversity). Decline nd mortlity of blck sh dvnced more rpidly thn tht of white nd green sh. Percentge mortlity of sh incresed from 51% to 93% during Distnce from the epicentre of the invsion ws negtively correlted with sh mortlity, but this reltionship dissipted over time. Stnd composition dt suggests tht sh will be replced by Quercus Linneus (Fgcee), Acer Linneus (Spindcee), nd Tili Linneus (Mlvcee); such vegettion chnges will irreversibly lter the structure nd function of these forests. Introduction Forest composition nd structure cn influence susceptibility of plnt communities to invsion by non-ntive herbivores (Mck et l. 2000; Von Holle et l. 2003; Ytes et l. 2004; Jctel et l. 2005). For exmple, the presence of high density nd diversity of host plnt species cn result in higher popultions of insect herbivores if host qulity is mintined. Niemelä nd Mttson (1996) suggested tht diverse North Americn forest communities fcilitte the estblishment of Europen phytophgous insects by providing more potentil hosts for invders. Jctel et l. (2002) indicted tht higher plnt diversity my lso impede invsion by non-ntive insects if it enhnces mortlity from nturl enemies, observing tht the percentge mritime pine (Pinus pinster Aiton (Pincee)) colonised by pine stem borer (Dioryctri sylvestrell (Rtzeburg)) (Lepidopter: Pyrlide) decresed s plnt diversity incresed becuse of higher prsitism rtes. Also, high diversity of non-host plnts my interfere with host loction by insects, for exmple by Received 22 September Accepted 7 November A. Smith, United Sttes Green Building Council, Centrl Ohio Chpter, P.O. Box 14105, Columbus, Ohio 43214, United Sttes of Americ; nd Deprtment of Entomology, The Ohio Stte University, Ohio Agriculturl Reserch nd Development Center, 1680 Mdison Avenue, Wooster, Ohio 44691, United Sttes of Americ D.A. Herms, Deprtment of Entomology, The Ohio Stte University, Ohio Agriculturl Reserch nd Development Center, 1680 Mdison Avenue, Wooster, Ohio 44691, United Sttes of Americ R.P. Long, United Sttes Deprtment of Agriculture Forest Service, Northern Reserch Sttion, 335 Ntionl Forge Rod, Irvine, Pennsylvni 16329, United Sttes of Americ K.J.K. Gndhi, 1 Deprtment of Entomology, The Ohio Stte University, Ohio Agriculturl Reserch nd Development Center, 1680 Mdison Avenue, Wooster, Ohio 44691, United Sttes of Americ; nd Dniel B. Wrnell School of Forestry nd Nturl Resources, The University of Georgi, Athens, Georgi 30602, United Sttes of Americ 1 Corresponding uthor (e-mil: kjgndhi@ug.edu). Subject editor: Krist Ryll doi: /tce Cn. Entomol. 00: 1 11 (2015)

2 2 Cn. Entomol. Vol. 00, 2015 msking host voltiles, nd reducing host qulity through interspecific resource competition (Zhng nd Schlyter 2004; Jctel et l. 2011). Conversely, impct of herbivory my be higher on low-density species, if the specilised herbivores re ble to locte nd concentrte on rre, isolted hosts. North Americn forests hve long history of disturbnce by non-ntive, invsive insects, nd pthogens such s gypsy moth (Lymntri dispr (Linneus)) (Lepidopter: Lymntride), hemlock woolly delgid (Adelges tsuge (Annnd)) (Hemipter: Adelgide), nd the cusl pthogens of Dutch elm disese (Ophiostom ulmi (Buismn) Melin nd Nnnfeldt; Fungi: Ophiostomtcee) nd chestnut blight (Cryphonectri prsitic (Murrill) Brr; Fungi: Cryphonectricee) (Lovett et l. 2006; Gndhi nd Herms 2010). These non-ntive orgnisms hve cused widespred mortlity of dominnt cnopy trees resulting in significnt ecologicl nd economic consequences in their introduced rnge (Liebhold et l. 1995). More recently, the non-ntive wood-boring insect emerld sh borer (EAB), Agrilus plnipennis Firmire (Coleopter: Buprestide), hs cused widespred mortlity of sh (Frxinus Linneus (Olecee)) where it hs estblished in North Americ (Cppert et l. 2005; Herms nd McCullough 2014; Klooster et l. 2014). Emerld sh borer lrve feed on the phloem nd outer spwood creting serpentine glleries tht girdle nd kill trees generlly within two to four yers of ppernce of symptoms (Herms nd McCullough 2014). Unlike ntive wood-boring buprestid beetles such s bronze birch borer (A. nxius Gory) (Coleopter: Buprestide) nd two-lined chestnut borer (A. bilinetus (Weber)) (Coleopter: Buprestide), which preferentilly colonise stressed trees (Dunn et l. 1990; Muilenburg nd Herms 2012), EAB lso colonises nd ultimtely kills helthy North Americn sh trees (Cppert et l. 2005; Knight et l. 2013). These dynmics re due to wekly defended sh trees presumbly becuse of their lck of coevolutionry history with EAB (Liu et l. 2003; Rebek et l. 2008). Emerld sh borer thretens the existence of North Americn sh trees s it continues to spred cross the continent. While substntil work hs been conducted on the nturl history, ecology, nd mngement of EAB (Herms nd McCullough 2014), little work hs been conducted on the effects of forest structure nd composition on the invsion dynmics of EAB. We therefore, investigted the susceptibility of forests to invsion by EAB in reltion to forest community structure, including species diversity, totl stnd density nd bsl re, s well s density, bsl re, nd reltive importnce of sh in southestern Michign, United Sttes of Americ. Mterils nd methods Study re The study ws conducted in the Huron River Wtershed in southestern Michign. All stnds were within Michign Stte Recretion Ares or Huron-Clinton Metroprks (see Smith 2006 for stnd descriptions), nd locted km from the epicentre of EAB infesttion in Cnton Township, Michign (42 19'N, 83 29'W) (Siegert et l. 2014). The Huron River Wtershed extends cross western Oklnd County, southestern Livingston County, nd north centrl Wshtenw County. The study sites re dominted by extensive res of cly lke plins, ground morine, end morine, nd outwsh plins (Albert et l. 1986). There is little vrition in elevtion with most ridges m in height nd the tllest reching mximum of 60 m. Soil texture is minly lom to cly, with snd found on outwsh plins nd chnnels. Thirty-one stnds were smpled cross rnge of forest hbitts tht vried in soil moisture, dominnt overstorey species, topogrphy, sh density, sh frequency, community composition, totl bsl re, nd tree density (Tble 1). Stnds were further selected to generte grdient rnging from hydric (intermittent stnding wter or submerged flood plin with mostly blck sh (Frxinus nigr Mrshll) nd some green sh (F. pennsylvnic Mrshll) to mesic (moist generlly riprin sites with mostly green sh), nd xeric (drier uplnd sites with mostly white sh (F. mericn Linneus). Three replicte rdil plots (18 m rdius), ech 0.1 h in re, were locted within ech stnd. Upon entering stnd, trnsect ws estblished long rndomly selected compss heding between 0 nd 90. The centre of the first plot ws chosen s point 18 m from the first sh tree encountered long the trnsect. Ech plot contined t lest two mture sh trees.

3 Smith et l. 3 Tble 1. Minimum, mximum, nd men vlues of stnd (n = 31) structurl vribles in in the Huron River Wtershed of southest Michign. Stnd vrible Minimum Mximum Men ± SD Stnd BA (m 2 /h) Stnd density (stems/h) Ash BA (m 2 /h) Ash density (stems/h) Reltive density of sh (%) Reltive dominnce of sh (% BA) Ash importnce vlue Shnnon diversity index (H') Notes: Overll mens were clculted from the individul stnd mens, which were the men of three replicted 0.1 h plots within ech stnd. BA, bsl re. Fig. 1. Rting scle used to quntify degree of sh (Frxinus species) cnopy decline, with 1 indicting helthy sh tree, 2, 3, nd 4 successive degrees of decline, nd 5 ded tree (from Smith 2006; Flower et l. 2013; Klooster et l. 2014) Ash cnopy decline rting Within ech 18 m rdius min plot, ll overstorey trees (dimeter t brest (DBH) > 12.5 cm) were identified to species nd their DBH recorded. Centred within ech min plot ws subplot with rdius of 8 m (0.02 h) where ll understorey tree species (DBH cm) were identified nd their DBH recorded. Eleven stnds (33 plots) were surveyed in the summer of 2004 nd 20 dditionl stnds (60 plots) were estblished nd surveyed in the summer of These stnds were resurveyed for specific forest ttributes including sh tree (DBH 2.5 cm) decline, density, nd bsl re in Emerld sh borer colonistion nd sh cnopy rtings To quntify the impct of EAB t the individul tree nd stnd level, sh cnopy decline of ech tree ws rted on scle from 1 to 5, with 1 indicting helthy tree with no symptoms of decline; 2, 3, nd 4 indicting successive degrees of cnopy thinning; nd 5 indicting ded tree (Fig. 1) (Smith 2006; Flower et l. 2013; Klooster et l. 2014). This rting protocol hs been shown to correlte well with EAB lrvl density (Flower et l. 2013). A plotlevel cnopy rting ws obtined by verging the vlue for ech tree within plot, nd stnd-level cnopy rting ws obtined by verging the mens of the three replicte plots. Percentge sh mortlity ws determined bsed on the number of trees with cnopy rting 5. To confirm the role of EAB s the cusl gent for observed ptterns of cnopy decline, EAB colonistion density (combined number of emergence holes nd woodpecker predtion ttcks/m 2 of brk surfce re) ws recorded on the min trunk between 1.25 nd 1.75 m from the bse of the tree. This ttribute is herefter referred to s density of EAB signs.

4 4 Cn. Entomol. Vol. 00, 2015 Community composition nd structure Men bsl re (m 2 /h) nd density (stems/h) for ll overstorey nd understorey tree species were clculted for ech stnd by verging those vlues for the three replicte plots within ech stnd. Reltive dominnce of sh (% sh bsl re) ws clculted for ech replicte plot s sh bsl re divided by totl bsl re. Reltive density of sh (% sh stems) ws clculted for ech plot by dividing the number of sh stems by totl number of stems of ll species. Reltive dominnce nd density of sh for ech stnd were clculted s the verge of ech of the three replicted plots within ech stnd. Shnnon- Wiener Diversity Index (H') ws clculted for ech plot (Stiling 1999). The three vlues of H' (one for ech replicte plot) were verged to clculte men diversity for ech stnd. Ash importnce vlues were lso clculted for ech stnd by summing the reltive dominnce, reltive density, nd reltive frequency (McCormick nd Pltt 1980). Reltive frequency of the three sh species combined ws determined first by clculting their bsolute frequency nd tht of ll other overstorey gener in ech stnd. Absolute frequency is defined s the percentge of plots within ech stnd where given genus cn be found. Reltive frequency of sh is the bsolute frequency of Frxinus species divided by the sum of bsolute frequencies for ll overstorey gener found on the stnd. Sttisticl nlyses Person correltion nlysis ws used to quntify reltionships between density of EAB signs, percentge sh mortlity, nd sh cnopy rting nd community composition vribles including totl nd sh bsl re, totl nd sh density, diversity, nd stnd distnce from the epicentre (Minitb Inc. 2005). The reltionship between density of EAB signs nd sh cnopy rting ws lso exmined using correltion nlysis. The curviliner reltionship between these vribles ws trnsformed to liner by log-trnsformtion of density of EAB signs. Dt were bck-trnsformed for presenttion. Correltion nlyses were used to quntify the reltionships between sh tree density (stems/h) nd percentge sh mortlity in nd 2007 (SAS Institute 2013). Since these dt were non-norml nd could not be rectified by trnsformtions, Spermn s Rnk Correltions were used for these nlyses. Anlysis of vrince (ANOVA) nd Tukey s pirwise comprisons were used to test for differences in density of EAB signs mong white, green, nd blck sh species, EAB-infested stems, percentge sh mortlity, nd sh cnopy rting (Minitb Inc. 2005). Dt were first ssessed for normlity nd homogeneity of vrince. Dt for percentge sh mortlity nd infested stems met both ssumptions, while density of EAB signs were squre-root trnsformed to meet these ssumptions. The ordinl-scled sh cnopy decline rtings did not conform to these ssumptions nd trnsformtion did not improve the distribution or homogeneity of vrince. Hence, for sh cnopy rtings, we used the non-prmetric nlysis of ordinl dt in two-wy fctoril design with three sh species nd smpling yer ( , 2006, nd 2007) s min fctors (Shh nd Mdden 2004; SAS Institute 2013). The reltionship between sh tree mortlity nd men distnce from the presumed centre of infesttion in Cnton Township ws chrcterised by regression nlysis for ech smpling yer ( , 2006, nd 2007) nd for ech species (blck, green, nd white sh for ). Blck, white, nd green sh were sorted into the following six dimeter clsses to determine if the pttern of EAB-induced cnopy decline ws consistent cross stem dimeter size clsses: , , , , , nd 22.5 cm DBH. Dt were not normlly distributed nd vrinces were not homogeneous. Trnsformtion of cnopy rtings did not improve the distributions to meet the ssumptions of ANOVA. Hence, we used the non-prmetric nlysis of ordinl dt in twowy fctoril design with three sh species nd six dimeter clsses s min fctors (Shh nd Mdden 2004; SAS Institute 2013). Results Overll stnd ttributes Stnd structure nd composition were vrible mong stnds when first mesured in , s indicted by the minimum nd mximum stnd bsl re, stnd density, sh density, sh bsl re, reltive density of sh, reltive dominnce of sh, sh importnce vlue, nd the Shnnon Diversity Index (Tble 1). A totl of 1611 sh

5 Smith et l. 5 trees were present in the 31 stnds. The composition of sh species vried mong smpled stnds. White sh trees were present in ll 31 stnds, with four contining only white sh. Eleven stnds contined mixture of white nd green sh. The remining 16 stnds contined mixture of ll three species. Green sh outnumbered the other two species with totl 697 stems in smpled plots. White nd blck sh numbered 478 nd 436 stems, respectively. Men (± SD) stnd nd sh bsl res were 26 ± 6 nd 6 ± 3m 2, respectively. Men tree density ws 735 ± 193 per h, nd sh density verged 171 ± 112 per h. Percentge sh density nd dominnce of sh were 22 ± 12 nd 25 ± 12, respectively with men sh importnce vlue being 62 ± 23 (Tble 1). Forest understorey ws primrily dominted by the gener Acer Linneus (Acercee), Frxinus, Tili Linneus (Tilicee), nd Ulmus Linneus (Ulmee), while Quercus Linneus (Fgcee), Frxinus, nd Acer were most common in the overstorey (Fig. 2). The bsl re of these species vried depending on whether they were present in hydric, mesic, nd xeric stnd-types (Fig. 2). Emerld sh borer colonistion nd impct Men density of EAB signs on brk surfce t brest height rnged from 0.3 to 70.3 per m 2 cross ll stnds in The overll men (± SE) ws 16.6 ( ± 3) ttcks per m 2 of sh brk surfce. When verged t the stnd level, men sh cnopy decline rting incresed non-linerly s function of density of EAB signs t brest height (r = 0.72, P < 0.001). EAB sign density did not rech high levels t brest height until cnopy decline ws well dvnced (Fig. 3). EAB sign density ws highest on blck sh followed by Fig. 2. Bsl re of 10 most common overstorey (A) nd understorey (B) tree gener in in hydric (n = 9), mesic (n = 11), nd xeric (n = 11) stnds in which the most common sh species were Frxinus nigr (blck), F. pennsylvnic (green), nd F. mericn (white) sh, respectively. Overstorey 16 Hydric stnds Mesic stnds Xeric stnds Frxinus Quercus Acer Tili Prunus Ulmus Understorey Lrix Cry Juglns Populus Frxinus Quercus Acer Tili Prunus Ulmus Lrix Cry Bsl re (m 2 /h) Juglns Populus

6 6 Cn. Entomol. Vol. 00, 2015 green nd white sh, lthough these differences were not sttisticlly significnt (P = 0.25) (Tble 2). Men percentge EAB-infesttion (percentge infested stems) ws highest for blck sh, intermedite for green sh, nd lowest for white sh (F = 4.58, df = 2, 73, P = 0.014) (Tble 2). In , the percentge of sh trees infested with EAB rnged from 9% to 86%, with the men (± SE) of 51% ( ± 4%) cross ll stnds (Tble 2). The verge sh cnopy decline rting rnged from cross ll 31 stnds, with men of 3.5 (± 0.10). Percentge sh mortlity rnged from 5% to 78% in smpled stnds, with men of 42% (± 4%) cross ll stnds (Tble 2). Fig. 3. Reltionship between sh cnopy decline rting [stnd specific mens of Frxinus nigr (blck), F. pennsylvnic (green), nd F. mericn (white) sh], nd density of EAB signs (sum of dult emergence holes nd woodpecker predtion ttcks) in on 1 m trunk section centred t brest height. Ash cnopy rting EAB signs/m 2 of brk surfce Percentge sh mortlity ws highest for blck sh, followed by green nd white sh, which did not differ (F = 9.66, df = 2, 73, P < 0.001). Cnopy decline rting of blck sh ws significntly greter thn those of white nd green sh, these ltter two species did not differ (F = 4.39, df = 2, 73, P = 0.003) (Tble 2, Fig. 4). There were significnt differences in cnopy decline rting mong sh dimeter clsses, with decline generlly more dvnced in lrger size clsses (F = 6.03, df = 3.81, 163, P < 0.001), nd with blck sh showing more dvnced decline in most dimeter clsses thn green or white sh (F = 9.91, df = 1.93, 163, P < 0.001), but the interction between these vribles ws not significnt (P = 0.219) (Fig. 5). Cnopy decline rting of blck sh ws highest in ll but the two smllest dimeter clsses ( nd cm), which did not differ mong the three species. Cnopy decline rting did not differ between white nd green sh for ny size clss (Fig. 5). The non-prmetric fctoril test for ordinl dt indicted tht smpling yer (F = 77.95, df = 1.66, 116, P < 0.001), sh species (F = 8.47, df = 1.97, 116, P = 0.004), nd their interction (F = 4.18, df = 3.2, 116, P = 0.005) hd significnt effects on cnopy decline. Men sh cnopy rting hd incresed to 4.8 in 2007 from 3.5 in (Fig. 4). Blck sh trees expressed bout 20% greter decline thn the other two sh species in , but differences between the three sh species were bsent by s mortlity of ll three species reched high levels (P > 0.05) (Fig. 4). Percentge sh mortlity rnged from 36% to 100% nd the men hd incresed to 84% (± 7%) cross ll stnds by (Fig. 4). Tble 2. Impct of emerld sh borer (EAB) on blck, green, nd white sh, nd ll three species verged cross ll stnds nd in in forests of the Huron River Wtershed of southest Michign. Ash species EAB sign density (m 2 brk surfce) Infested sh stems (%) Ash mortlity (%) Cnopy decline rting Blck sh (F. nigr) 22± 9 64 ± 6 64 ± ± 0.2 Green sh (F. 18 ± 4 34 ± 5b 34 ± 5b 3.3 ± 0.2b pennsylvnic) White sh (F. mericn) 12± 3 32 ± 5b 32 ± 5b 3.4 ± 0.2b All Frxinus species combined 17 ± 3 42± 4 42± ± 0.1 Vlues within column followed by the sme letter re not significntly different.

7 Smith et l. 7 Fig. 4. Men cnopy decline rting from for Frxinus nigr (blck), F. pennsylvnic (green), nd F. mericn (white) sh cross ll stnds (1 = helthy, 2, 3, 4 = successive degrees of decline, 5 = ded). Comprisons re cross yers for ech sh species. Fig. 6. Reltionship between percentge sh (Frxinus species) mortlity nd sh density (stnd specific mens) for ll sh species combined in nd Ash cnopy rting b Frxinus mericn Frxinus nigr Frxinus pennsylvnic Percentge tree mortlity Fig. 5. Men cnopy decline rting in by dimeter clss t brest height for Frxinus nigr (blck), F. pennsylvnic (green), nd F. mericn (white) sh cross ll stnds (1 = helthy, 2, 3, 4 = successive degrees of decline, 5 = ded). Ash cnopy rting b b b b b Frxinus mericn Frxinus nigr Frxinus pennsylvnic Stnd structure, diversity, nd the impct of emerld sh borer None of the mesures of EAB impct, including stnd mortlity, were correlted with stnd diversity (Shnnon Diversity Index) or stnd density, whether erly in the infesttion when mortlity ws < 50% ( ) or lter when mortlity ws pproching 90% ( ). In , there were lso no reltionships between stnd bsl re nd percentge infested sh (P = 0.72), sh cnopy rting (P = 0.25), percentge sh mortlity (P = 0.11) or density of EAB signs (P = 0.86), nor ws sh bsl re correlted with cnopy decline rting (P = 0.35), percentge infested sh (P = 0.29), percentge Ash dimeter clss (cm) b Ash density (stems/ h) sh mortlity (P = 0.13), or EAB sign density (P = 0.92). Ash density, reltive density of sh, reltive dominnce of sh nd sh importnce vlue were lso not correlted with ny mesure of EAB impct (percentge infested stems, percentge sh mortlity, cnopy rting, nd EAB signs) (Fig. 6). Impct of emerld sh borer in reltion to distnce from the epicentre of invsion Distnce of the smpled stnds from the presumed epicentre of the EAB infesttion in Cnton Township, Michign (Siegert et l. 2014) rnged from 25 to 50 km, nd ws negtively correlted with ll four mesures of EAB impct (percentge sh mortlity, cnopy decline rting, percentge infested stems, nd density of EAB signs) when verged cross ll sh species. Regression nlyses of percentge sh mortlity nd distnce from Cnton Township indicted significnt negtive reltionship in (percentge sh mortlity = *Distnce, F = 15.2, df = 1, 30, P < 0.001, R 2 = 0.34), 2006 (percentge sh mortlity = *Distnce, F = 14.81, df = 1, 30, P < 0.001, R 2 = 0.32), nd 2007 (percentge sh mortlity = *Distnce, F = 5.43, df = 1, 30, P = 0.03, R 2 = 0.16) (Fig. 7). The negtive slope of the line remined lrgely unchnged between nd 2006 ( decrese in percentge sh tree mortlity of 2% per km from the epicentre), but declined

8 8 Cn. Entomol. Vol. 00, 2015 Fig. 7. Reltionship between percentge sh tree mortlity (stnd specific mens) for ll sh (Frxinus) species nd distnce from the epicentre of the invsion in Cnton Township, Michign from 2004 to Percentge sh mortlity Men distnce from the epicenter of infesttion (km) nd levelled out by 2007 s percentge mortlity incresed in ll stnds. The y-intercept of the lines incresed drmticlly over time s percentge mortlity incresed (Fig. 7). When percentge sh mortlity versus distnce to the epicentre ws nlysed individully for ech sh species in , the pttern ws strongest for blck sh (percentge sh mortlity = *Distnce, F = 7.64, df = 1, 15, P = 0.02, R 2 = 0.35). White sh displyed similr pttern, but the reltionship ws mrginlly significnt (P = 0.08). The slope of the regression line ws not s steep ( 1.4), with lower y-intercept (81.1). The sme trend ws evident for green sh but the regression ws not significnt (P = 0.21). The slope ws shllower ( 1.1), nd the y-intercept ws lower still (71.9). A similr pttern ws evident for the correltions between cnopy rting of white, green, nd blck sh nd distnce from the epicentre, with the pttern strongest for blck sh (r = 0.76, P = 0.004), while correltions for white sh (P = 0.45) nd green sh (P = 0.21) were not significnt. When verged cross ll sh species in , the percentge of sh trees infested by EAB lso decresed with incresing distnce from Cnton (r = 0.53, P = 0.002), s did sh cnopy decline rting (r = 0.40, P = 0.03), indicting tht crown vigour improved with distnce from Cnton. Density of EAB signs on ll sh species lso decresed with incresing distnce from the epicentre but the reltionship ws only mrginlly significnt (r = 0.36, P = 0.07). There were no significnt correltions between distnce from epicentre nd density of EAB signs or percentge infested trees when exmined seprtely for ech sh species. Discussion This four-yer study ( ) reveled the following mjor ptterns s the EAB invsion of the Huron Wtershed region in southest Michign progressed: (1) density of EAB signs ws ssocited with incresing decline nd mortlity of sh trees; (2) sh cnopy decline rting nd mortlity incresed rpidly over time with little effect of tree size (lthough decline of the smller size clsses ppered to lg slightly behind other size clsses); (3) blck sh initilly declined fster thn white nd green sh, which lgged by one to two yers; (4) there ws no reltionship between density of EAB signs, sh cnopy decline rting, or percentge sh mortlity nd ttributes of forest structure nd composition including sh density, bsl re, nd importnce; nd (5) percentge sh mortlity initilly declined with distnce from the epicentre of the invsion, lthough this trend leveled off by 2007 s sh mortlity incresed rpidly in ll stnds. Emerld sh borer cused significnt decline nd mortlity of sh in the study re, hving visibly infested 51% nd killed 42% of ll sh trees, respectively, in The men cnopy rting cross ll species ws 3.6 (on scle from 1 to 5, where 1 is helthy nd 5 is ded tree) in nd 4.8 in 2007, indicting tht the sh decline progressed rpidly to severe levels during the study. By 2010, sh mortlity exceeded 99% in these stnds (Klooster et l. 2014). The strong correltion between density of EAB signs nd sh cnopy rting (Fig. 3) provides evidence tht EAB ws indeed the cusl gent of decline nd mortlity. This reltionship ws non-liner with shrp increse in cnopy decline t low ttck density tht plteued s density of ttcks incresed suggesting tht by the time EAB ttcks re pprent t brest height, colonistion nd decline of the tree is in n dvnced stge. This pttern is consistent with previous observtions tht initil ttcks of EAB occur high in the cnopy, with lter colonistion occurring progressively lower on the stem (Cppert et l. 2005; Tluczek et l. 2011).

9 Smith et l. 9 EAB sign density, cnopy decline rting, percentge infested stems, nd percentge mortlity were ll higher for blck sh in thn for green nd white sh. By 2006, there were no differences between the species in cnopy decline rting nd percentge mortlity, which hd incresed to high levels for ll three species. Blck sh my hve initilly declined more rpidly becuse it is preferred s n oviposition host over green nd white sh (Rigsby et l. 2014), perhps becuse txonomiclly it is much more closely relted to Mnchurin sh (F. mndshuric Ruprecht) (Jendroz et l. 1997; Wllnder 2001), which shres coevolutionry reltionship with EAB in Asi (Liu et l. 2003; Rebek et l. 2008). Jendroz et l. (1997) suggested tht Mnchurin sh diverged from blck sh evolutionrily fter blck sh dispersed to Asi during period of connection between these continents in the Middle nd Lte Tertiry periods nd then ws subsequently isolted by rise in se level s glciers retreted. Blck sh obviously possesses cues tht llows it to be recognised s preferred host by ovipositing femles, but lcks defences of Mnchurin sh tht hve been selected for by EAB (Whitehill et l. 2012). Green nd white sh decline nd mortlity incresed to the high levels of blck sh following one to two-yer time lg, suggesting tht vrition in susceptibility of the three species to EAB my ultimtely hve miniml ecologicl relevnce for the structure nd function of these forests. In , there were lso no differences in cnopy decline rting mong tree dimeter clsses, except possibly for the smllest ctegories. This indictes tht once mortlity ws modertely high (42%), trunk dimeter hd little effect on probbility of being colonised nd killed; similr pttern hs been observed by Mrshll et l. (2013) nd Jennings et l. (2014). Although the community structure nd sh density of smpled stnds were quite vrible, there ws no reltionship between ny mesure of stnd structure, composition, or species diversity nd EAB colonistion or impct, s indicted by degree of sh cnopy decline, percentge sh mortlity, nd percentge of infested stems. Low-density sh stnds were just s susceptible to EAB colonistion nd sh mortlity s highdensity sh stnds, s lso observed by Knight et l. (2013). This suggests tht non-host trees do not hinder host loction efforts by EAB, s observed for some other forest insects (Jctel et l. 2002), possibly becuse EAB is highly specilised on sh with well-developed chemosensory cues for locting hosts (Crook nd Mstro 2010), even t low densities. The only vrible tht ws relted with ny mesure of EAB impct ws distnce from the epicentre of the invsion in Cnton Township, even though ll stnds were locted within nrrow rnge of 24 nd 48 km from the epicentre. All mesures of EAB impct (cnopy rting nd mortlity, percentge infested sh, nd density of EAB signs) were significntly nd negtively correlted with distnce from epicentre, with the reltionship strongest for percentge sh mortlity, which ws significntly negtively correlted when mesured in , 2006, nd The slope of the line describing the decrese in sh mortlity with distnce from the epicentre remined unchnged from t 2%, indicting tht sh mortlity continued to increse t rte of 2%/km s overll percentge sh morlity incresed by 30% during tht time period. By 2007, the slope flttened considerbly s sh mortlity climbed to high levels in ll stnds. All three species of sh demonstrted similr pttern of decresing decline nd mortlity with incresing distnce from the epicentre with the pttern being strongest for blck sh. Decresing sh decline nd mortlity s distnce from the epicentre incresed hs lso been reported in southestern Michign studies conducted t different sptil scles thn exmined in this study (Smitley et l. 2008; Kshin nd Witter 2011). The lmost totl extirption of sh in these forests (Klooster et l. 2014) will hve substntil impct on the future structure nd function of these forests (Gndhi nd Herms 2010b; Gndhi et l. 2014). Aside from sh, the most common gener in the overstorey were (Quercus) ndmple(acer), which seem poised, t lest in the short-term, to increse their dominnce in these stnds. Reltive to their bundnce in the overstorey, oks were underrepresented in the understorey, perhps due to limited recruitment nd/or deer browsing (e.g., Rooney nd Wller 2003). Thus, in the longerterm, mple nd bsswood (Tili) species, which were the most common tx in the understorey (other thn sh), could become the most dominnt

10 10 Cn. Entomol. Vol. 00, 2015 overstorey species. Elm (Ulmus) species were lso common in the understorey, but virtully lcking in the overstorey, presumbly due to mortlity from Dutch elm disese (Brnes 1976). Brnes (1976) documented the impct of the Dutch elm disese invsion on the community structure of these sme forests nd predicted presciently tht green sh would replce Americn elm (Ulmus mericn Linneus, Ulmcee) s dominnt species, unless nd until mjor disturbnce impcts sh. Our results clerly show tht ll stnds in our study re were highly vulnerble to invsion by EAB regrdless of their structure, species composition, nd sh density nd importnce (which rnged from low to very high). This suggests tht silviculturl prctices such s thinning hve little potentil to prevent invsion of forest stnds by EAB nd subsequent sh mortlity. The decimtion of sh is once gin ltering the structure nd function of the forests of the Huron River Wtershed of southest Michign, s predicted by Brnes (1976), nd potentilly mrks the beginning of the functionl end of these sh species throughout North Americ. Acknowledgements This reserch ws funded by the United Sttes Deprtment of Agriculture Forest Service Northestern Reserch Sttion s progrmme Reserch on Biologicl Invsions of Northestern Forests, United Sttes Deprtment of Agriculture Forest Service Northern Reserch Sttion, the D.B. Wrnell School of Forestry nd Nturl Resources, University of Georgi, nd by stte nd federl funds pproprited to the Ohio Agriculturl Reserch nd Development Center nd The Ohio Stte University. We pprecite the hrd work of Dine Hrtzler, Brynt Chmbers, Dn Rice, Rodrigo Chorbdjin, nd Alejndro Chiribog (The Ohio Stte University), ll of whom ssisted with fieldwork. Brittny Brnes (University of Georgi) formtted the pper. References Albert, D.A., Denton, S.R., nd Brnes, B.V Regionl lndscpe Ecosystems of Michign. School of Nturl Resources, University of Michign, Ann Arbor, Michign, United Sttes of Americ. Brnes, B.V Succession in deciduous swmp communities of southern Michign formerly dominted by Americn elm. Cndin Journl of Botny, 54: Cppert, D., McCullough, D.G., Polnd, T.M., nd Siegert, N.W Emerld sh borer in North Americ: reserch nd regultory chllenge. Americn Entomology, 51: Crook, D.J. nd Mstro, V.C Chemicl ecology of the emerld sh borer, Agrilus plnipennis. Journl of Chemicl Ecology, 36: Dunn, J.P., Potter, D.A., nd Kimmerer, T.W Crbohydrte reserves, rdil growth, nd mechnisms of resistnce of ok trees to phloem-boring insects. Oecologi, 83: Flower, C.E., Knight, K.S., Rebbeck, J., nd Gonzlez- Meler, M.A The reltionship between the emerld sh borer (Agrilus plnipennis) nd sh (Frxinus spp.) tree decline: using visul cnopy condition ssessments nd lef isotope mesurements to ssess pest dmge. Forest Ecology Mngement, 303: Gndhi, K.J.K. nd Herms, D.A Direct nd indirect effects of lien insect herbivores on ecologicl processes nd interctions in forests of estern North Americ. Biologicl Invsions, 12: Gndhi, K.J.K. nd Herms, D.A. 2010b. Potentil biodiversity loss due to impending devsttion of the North Americn genus Frxinus by the exotic emerld sh borer. Biologicl Invsions, 12: Gndhi, K.J.K., Smith, A., Hrtzler, D.M., nd Herms, D.A Indirect effects of emerld sh borer-induced sh mortlity nd gp formtion on epigeic beetles. Environmentl Entomology, 43: Herms, D.A. nd McCullough, D.G Emerld sh borer invsion of North Americ: history, biology, ecology, impcts, nd mngement. Annul Review of Entomology, 59: Jctel, H., Biefweon, G., Andersson, S., nd Schlyter, F Non-host voltiles medite ssocitionl resistnce to the pine processionry moth. Oecologi, 166: Jctel, H., Brockerhoff, E., nd Duelli, P A test of the biodiversity-stbility theory: met-nlysis of tree species diversity effects on insect pest infesttions nd re-exmintion of responsible fctors. In Forest diversity nd function: temperte nd borel systems. Edited by M. Schere-Lorenzen, C. Körner, nd E.D. Schulze. Springer-Verlg, Berlin, Germny. Pp Jctel, H., Goulrd, M., Menssieu, P., nd Goujon, G Hbitt diversity in forest plnttions reduces infesttions of the pine stem borer Dioryctri sylvestrell. Journl of Applied Ecology, 39: Jendroz, S., Roy, A., nd Bousquet, J Phylogeny nd phylogeogrphy of the circumpolr genus Frxinus (Olecee) bsed on internl trnscribed spcer sequences of nucler ribosoml DNA. Moleculr Phylogenetics nd Evolution, 7:

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