1023 Agrilus (McCullough 32 – 30 d Moreover, debarking or 27 – 24 minimizing applicator exposure, environmental 29 , 34 28 , , and Phillip A Lewis 33 16 , c 15 Correspondence to: Deborah G McCullough, 243 NaturalFarm Lane, Science East Building, Lansing, 288 MI 428824, USA. E-mail: [email protected] Department of Entomology, Michigan State University, East Lansing, MI, USA Department of , Michigan State University, East Lansing, MI, USA United States Department ofStation, East Agriculture, Lansing, MI, USA Service, Northern Research United States Department of Agriculture,Service, Animal Buzzards and Bay, Plant MA, USA Health Inspection Another management option for EAB involves the use of highly ∗ c a d b higher than on adjacent healthy ash. effective systemic insecticides. A productent with emamectin the benzoate, active sold ingredi- in(Arborjet, the Inc., United Woburn, States MA), provided as nearly TREE-äge™ for 100% control up of EAB to 3 years in large-scale field studies contamination and potentialThe effects insecticide affects on adult EAB non-target beetles, which throughout organisms. must their feed 3–6 on ash week lifespan, as well as neonate or DG, unpublished data).the This base systemic of productthe the is , tree injected and then into translocated in tissue to destroying girdled trees before larvae complete developmentreduce can growth of local EABmortality. populations and slow the rate of ash spp.) mortality resulting from emerald ash borer (EAB) ( 5 7 , 6 – 3 Fraxinus Female 23 Agrilus planipennis – as the most F. americana 21 Fairmaire), a could save or 18 , 16 Therese M Poland , 17 15 These estimates do 95% have been doc- 11 > a,b* ; girdled trees; emamectin benzoate; bait and kill A. planipennis Slowing EAB population growth Fraxinus Agrilus planipennis 14 Economic costs of replacing or treat- – Marshall) and white ash ( 10 12 : 1023–1030 www.soci.org © 2015 Society of Chemical Industry spp.) trees since it was first identified in North Ash mortality rates of Similarly, in North America, adult EAB beetles 72 2 , 20 1 , 19 2016; Fairmaire) invasion are severe in forested, residential and urban areas. Management options include girdling ash Fraxinus emerald ash borer; F. pennsylvanica are also commonly planted in landscapes within and 9

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A potential tactic to slow EAB population growth involves using 18 days earlier and could potentially be used in integrated management programs to slow EAB population growth. America in 2002. destructive and costly invasive forest insect in North America. -feeding insect nativelions of to ash ( Asia, has killed tens of mil- are attracted to volatiles emitted by stressed ash. girdled ash trees, whichsites effectively serve with as low ‘populationfunctions sinks’ EAB as in densities. a secondary In pest,dead its attacking ash stressed, native trees. dying or range newly in China, EAB Pest Manag Sci L.), the most widelyforests, distributed ash species in North American Recent economic analyses identified Green ash ( 1Emerald INTRODUCTION ash borer (EAB) ( Fairmaire) management Abstract BACKGROUND: Economic and ecological impacts of ash ( Deborah G McCullough, emerald ash borer ( (wileyonlinelibrary.com) DOI 10.1002/ps.4083 Lethal trap trees: a potential option for Research Article Received: 9 April 2015 Revised: 15 July 2015 Accepted article published: 21 July 2015 Published online in Wiley Online Library: 14 August 2015 and associated ash mortality in a given area beetles preferentially oviposit onand ash larval trees stressed density by on girdling, girdled ash can be at least 3–4 times beyond their natural range. not account for ecosystem servicesash lost trees when decline mature and landscape die. delay expenditures of billions ofincurred US to dollars treat that or will remove landscape otherwise ash be trees. umented in forested areas with a substantial ash component. ing landscape ash trees in urbanprojected areas and to adjacent exceed suburbs $US were 20 billion by 2019. Keywords: planipennis trees to attract ovipositinghighly adult effective, systemic beetles emamectin benzoate and insecticide. Injecting then thislater insecticide destroying and could then infested girdling effectively injected trees trees create atranslocation. before few lethal We weeks compared larvae EAB trap develop larval trees, densities or oninjected similar girdled protecting with trees, to the ash trees insecticide injected a with with and bait-and-kill the then a emamectin girdled tactic, benzoate 18–21 insecticide, if trees days later girdlingRESULTS: and Pretreatment does untreated larval controls not at densities multiple interfere did sites. and not with control differ trees insecticide among than treatments. on Current-year anythat larval trees girdling treated trees densities after with were insecticide insecticide higher injections at on did all not girdled sites. reduce Foliar insecticide residue translocation. analysisCONCLUSIONS: Girdling and ash adult trees EAB to bioassays showed attract≥ adult EAB did not© reduce 2015 efficacy Society of of emamectin Chemical benzoate Industry trunk injections applied DW). = Girdled). + : 1023–1030 72 of phloem area Girdled) and one 2 + 2016; 12mhigh.Shootsfromeach 5 cm in diameter were bucked > > Pest Manag Sci On 25 June and 23 July 2009, we used pole pruners to collect From October to November 2009, all trees were felled, and We wrapped a 30 cm wide band of plastic wrap tightly around On 7 July, -bearing shoots were collected from 2–4 aspects of As in the previous year, trees were randomly assigned to one of and phloem arounddrawknife, the 1 m circumference aboveground, on of 22 the June,injection. 21 trunk days after with the EmBen a leaf-bearing shoots from 2–4trees aspects at the of CLF the and WW canopy sites. In ofonthepolepruners,wewereunabletoreachshootsontreesat spite of the using study up to five extensions the LB site, manytree of were bagged, which placed were in coolers andState returned University to (MSU) the Forest Michigan Entomology laboratory.stripped Foliage was from shootsovernight and mail to the frozen, USDA APHIS then laboratoryresidue in analysis shipped Massachusetts (see for below). in coolers via the trunk and primary branches into 1 m long sections.number Each log of was old carefullythe debarked, galleries and number the representing of pretreatment newrecorded separately. galleries larvae The made average and diameter by of2.5 each current-year cm log, larvae measured from were bothexposed ends, on was each section. used Thecurrent-year to total larvae calculate number of the were pretreatment surface and standardized area per m Two trees per block wereusing injected the same with methods the as low inzoate, the rate 4%, previous of 0.1 year g TREE-äge (emamectin AI ben- device per 2.5 on cm 20 DBH) May. usingnon-injected One the tree (Girdled) ArborJet injected in QuickJet™ each tree block were (EmBen girdled onusing 8–9 the same June, methods as in 2009. the trunk of allthen covered study the plastic trees, wrap approximately withInsect a 1.3–1.5 thick Barrier m coat (Contech of high, Inc., Tree Tanglefoot The and Grand sticky Rapids, bands were Michigan) checked onbeetles. at 4 2 Beetles week June. were intervals returned to(MSU) collect to Forest EAB the Entomology laboratory, Michigan soakedremove State in the University Tanglefoot ethanol and then (75%) examined to underconfirm a species. microscope to the canopy of the study trees using polewere pruners, as bagged, in 2009. placed Leaves inEntomology coolers laboratory. We and were unable returned to reach to shoots onvery the several tall MSU trees, particularly Forest at the LB site. We collected foliage from exposedoneachtree. 2.2 2010 study We selected aash total trees of of 16 similar2010. blocks, size Trees within each and blocks condition were of spaced (64of 8–12 which trees green m included ash in apart. Eight trees, four total) blocks withselected in DBH May in ranging from wooded 12.4River and to State Wildlife 21.8 partially cm, area in were wooded Clintonof Co., Michigan areas (MR). white Four in blocks ash theselected trees, at Maple ranging Lincolnstand Brick from used (LB) 12.7 in park the toash previous in trees year. 20.1 averaging the cm Four 12.7–18.3 additional Eaton DBH, cmlot blocks Co. DBH of on were were white white private selected ash in land a in - Clinton Co., Michigan (D-Woodlot All study trees hadof EAB healthy infestation, canopies although andeach we no noted site a obvious had few evidence woodpeckergalleries. of holes the other or ash bark at cracks over oldthe larval four treatments (Control, Girdled, EmBen, EmBen © 2015 Society of Chemical Industry WW). Trees were including several www.soci.org DG McCullough, TM Poland, P Lewis = 29 , 35 28 , 16 , 15 by increasing the number of Girdled) (e.g. lethal trap tree) 41 + Treating all trees or even a portion of ash 32 , Adult EAB beetles attracted to volatiles emit- 31 40 Girdled), we removed a 20 cm wide band of outer – + 36 We hypothesized that injecting ash trees with emamectin ben- One tree in each block was randomly assigned to be (1) treated zoate and then girdling the trees a few weekscreate later lethal could effectively trap trees for EAB iftranslocation the of the girdling insecticide. did Lethal trap not trees, interfere which with employattract-annihilate the strategy of behavioral pestbeen management, used have for a wide range of insect pests, ted by girdled ash trees wouldof be treated trees, controlled reducing if oviposition they on fedhaps the on nearby treated trees. leaves tree The and insecticide per- woulddeveloping also on prevent larvae the from treatedductive trees, adults reducing emerging the the following number year. Therefore,the of combining repro- emamectin benzoate andtially girdling produce a treatments synergistic could effect poten- wileyonlinelibrary.com/journal/ps growing along the edgewooded of areas wooded areas and or exposedat scattered to breast between full height or (DBH)selected nearly at (measured the full 1.3 m WW sun.trees site aboveground) Diameter ranged in of from the trees 12.2 area toleft had 21.6 by evidence cm. woodpeckers of Numerous preying EAB onlarval infestation, EAB galleries such in larvae, the as bark upper cracks holes canopybranches. over or Study epicormic old sprouts trees on had large three trees relatively had woodpecker healthy holes in canopies, the upper although leader. portion Six of the blocks main of white ashDBH, were trees, selected ranging in a from well-stocked, even-aged 10.7 stand to ofin white 17.3 Lincoln ash cm Brick Park, Eaton Co., Michiganbetween (LB). a Trees prairie were and growing a denselyexposed forested area, to and full canopies were orash partial trees, with DBH sun. ranging from Two 13.2 blocks toin 23.9 a of cm, were right-of-way open-grown established cloverleaf white atMichigan a (CLF). highway Although intersection EAB was in present Ioniathe at Co., the study LB trees and had CLF healthy sites, canopiesinfestation. and no external evidence of with a trunk injectiondled of (Girdled), emamectin (3) benzoate injectedgirdled (EmBen), with 3 (2) emamectin gir- weeks benzoate and later then (EmBen 2METHODS 2.1 2009 study We selected a total ofof 12 blocks, similar each size consisting of andtotal) four condition, ash in at trees May three 2009. differentfrom Spacing sites 6 between (48 to trees trees 20 within m. in the blocks Four west ranged blocks side of of greenarea an ash in unmanaged Genesee trees Co., portion were Michigan (Wolverine of selected West Wolverine on recreation or (4) left as(TREE-äge™, 4%; untreated Arborjet, controls Inc.) was (Control).on injected Emamectin into 2 the benzoate June base of usinglowest trees the label ArborJet rate QUIK-Jet™ (0.1dled; g delivery EmBen AI system per at 2.5 the cm DBH). To girdle trees (Gir- early-instar larvae. adult EAB affected by the insecticide.tive, For this however, strategy the to insecticide be effec- tree must before girdling. be We compared larval translocated densities on through ashwere trees girdled, the injected that with emamectin benzoate, girdled following emamectin benzoate injection or left as untreatedwith controls varying at sites levels of EAB infestation. bark beetles. trees in a given area with emamectinoption, benzoate is not a only highly effective for protectingfor valuable slowing local landscape EAB trees population but growth. also

1024 1025 3, 2, = = 1.54 2.46 0.71; ± ± 0.602). 0.251). = respec- 1.09 cm 3.00 cm F = = 1 ± ± − P P 3.07; df 0.0007), but respectively 0.55; df 0.60 ppm in 0.05), Tukey’s = = Girdled trees = ± 1 1, 9; 3.87, 9.8 1, 0; F − P F < + = ± = P Girdled trees aver- 2.54 and 5.5 1.58 mg kg 2, 36; Girdled trees in June + ± ± 0.75). Diameter of trees = + 0.77 and 18.0 1.51; df 0.29; df = ± 0.75 mg kg = P = 0.53 ppm in July at the CLF F ± F Girdled). 43 ± 0.56). The pretreatment den- + 8.87; df 2.08, 6.7 = and 3.91 6, 36; = ± P 0.43 ppm and 2.21 1 SE) 17.8 F = − 0.63 cm DBH. The average DBH of wileyonlinelibrary.com/journal/ps ± All analyses were conducted using ± ± and 2.35 42 6, 36; 1 − = 0.57; df 0.508) or July ( 3.02, 6.15 0.602) and July ( 0.05). = = 1) transformed to normalize data for analyses. F 0.26 mg kg ± = < P 1.12 cm (EmBen P + P ± 2.36 ppm and 1.50 ± x 0.82; df ± 0.55) in 2009. The interaction of site and treatment 1, 9; 1, 9; = 0.41 mg kg = = = F ± P 0.67 at the CLF, WW and LB sites respectively, and differ- Girdled) at the CLF and WW sites were also similar in June ± 0.059). The density of pretreatment larvae did not differ + 0.65), nor was the interaction between site and treatment = = 3, 36; 0.48; df 0.29; df P P = = = Our primary interest was in the density of larvae that hatched F F Foliar residues fromaged EmBen 1.73 and EmBen respectively. and began feeding intions summer 2009, with following theinsecticide emamectin spring injec- application benzoate and significantly girdling. affected Girdling density and of the on the Control, Girdled, EmBen and EmBen 36; significant ( sity averaged 10.0 (Girdled) to 16.5 3.1.1 Foliar residues Girdling trees 18 daysdid after not injecting appear thecide. to emamectin Residues interfere benzoate ofleaves with emamectin collected benzoate translocation from EmBen did of and( not EmBen the differ insecti- between among trees assigned to different treatments ( was similar atsites, the where DBH Wolverine averaged West ( (WW) and Cloverleaf (CLF) respectively. Trees at the Lincoln Brick (LB) site werein tall but diameter, smaller averaging 14.1 trees assigned to different treatments ranged from 15.0 36; ences among sites were marginally insignificant ( and 3.7 was not significant ( and WW sites respectively. Aswas expected, no detected emamectin in benzoate foliagenot from injected. Control or Girdled trees that were 3.1.2 Larval densities The density of pretreatment larval galleries onber trees felled 2009 in Octo- was generallyhealthy low, appearance which of the was study not trees. Theleries surprising average from density given larvae of that the gal- fed prior to 2009 was 11.5 was similar among trees assigned to different treatments ( df Differences in adult EAB mortality onbioassay day were not 1 normalized and by day transformations. 3 Thesewere of variables tested the with foliar Friedmann’s non-parametric ANOVA followed by non-parametric multiple comparison testswere when significant ANOVA ( results and density of pretreatment and2010. current-year larvae When in ANOVA 2009least-squares and results multiple comparison test were was applied. Larval significantvalues density were ( log( Residue levels averaged 1.70 June and 4.28 SAS statistical analysis software v.9.2. 3RESULTS 3.1 2009 study Tree DBH differed among sites ( in June, and 0.94 tively in July. ResidueEmBen levels in leaves( of injected trees (EmBen, of exposed 2 Girdled tree. At + Girdled trees). A leaf from + : 1023–1030 © 2015 Society of Chemical Industry 72 Girdled) at the CLF and WW sites in 2009 and at to avoid matrix effects from the kit on account of + × 2016; Trees were felled, sectioned and debarked from October through Pest Manag Sci Lethal trap trees for emerald ash boreronly two trees at LB (one control,we one were girdled able tree). to At collect the foliage DW fromcollect site, 13 leaves of from the two 16 girdled trees, but and did one not EmBen www.soci.org the MR site, we could not reachgirdled, leaves two on EmBen nine of and the two 32 EmBen trees (five each of two shoots collectedset from aside opposite for sides bioassays of with the adultof beetles. tree a We was leaf inserted into the a petiole waterleaf into pic a petri to dish (15 slow cm desiccation, diameter). Three andinfested EAB ash adults then logs reared placed were from placed the in each dishallowed (six to beetles per feed. tree) Beetles and were 3–4dishes, days and old equal when numbers placed of into males petri andeach females tree. were assigned Beetles to were observedrecorded 24 periodically, h and (day mortality 1) and was used 72 in h bioassays were (day stripped from 3) the woody later. shoots, Remainingthen frozen and leaves shipped not via overnight mailMA to for the residue USDA analysis APHIS (see laboratory below). in December 2010 to assess larvalas density, in using 2009. Density the of pretreatment same larval methods galleries andlarvae current-year were again recorded and standardized per m 2.4 Statistical analyses Variables were tested forand normality using residual the plots. Shapiro–Wilk Two-wayences ANOVA test among was treatments, usedfactors sites to and on assess the tree differ- interaction DBH, of emamectin the benzoate two residues in foliage the MR and DW sites intrees 2010. Foliage per from site 3–6 was Controluntil or also Girdled ready analyzed. for Leafand samples analysis, petioles remained and and frozen stored thenseveral in days were paper until separated bags dry atand from and broken room brittle. by stems temperature Dried hand, for then leaves placedatop were into a compressed a two-speed 1.9 commercial L blender. stainless Leaf steelat material vessel was high blended speed for approximatelyand 30 s break to up homogenizethoroughly the the cleaned sample leaf after each tissuebetween use into to samples. a avoid To cross-contamination fine extractthe powder. ground the Vessels leaf insecticide, were material atrifuge was tube 0.5 weighed g and into sample then a3 of h 50 extracted mL on in plastic a 10 cen- table-top mLan Eppendorf shaker. of 5810 Samples pure high-speed in methanol centrifugeNY) tubes (Eppendorf, for New were at York, spun 6000 rpm downminimum for in of 20 10 min, andthe the methanol. supernatant Samples were was then run dilutedto on the a the manufacturer’s assay specifications. kits Individual according in samples were duplicate, run and samplesexceeded were the reassessed standard if curve themore resulting or than value 15% if between individual the duplicateaveraged samples wells. for varied Sample each values by were treeper and million. adjusted to achieve a value in parts 2.3 Foliar residues Foliar residues of emamectin benzoate incollected the in composite samples June andfied July using 2009 commercially andimmunosorbent available in 96-well July assay 2010 plateHoriba, (ELISA) were Ltd, enzyme-linked Kyoto, quanti- Japan). kits Because wetrees could (kit at not the reach LB number foliage site, on residues(EmBen, were EmBen 3100176052; quantified for the injected trees surface as before. 90% of Girdled Girdled in 2010 in > + + 2 : 1023–1030 72 0.45) or day 3 Girdled). Letters + = P 2016; adults caged in 2010 16 trees per treatment). larvae per m = n Girdled trees. In nearly all + Girdled) at the D-Woodlot (DW), + Pest Manag Sci A. planipennis A. planipennis 0.009). 0.0001) and in trees at the LB and MR sites < < P P spp. trees left as untreated controls (Control), 80% of beetles caged with leaves from EmBen ≥ Fraxinus 0.0001). < Girdled trees were dead within 24 h, and Girdled trees ( P + + Percentage mortality of Number of current-year spp. trees left as untreated controls (Control), girdled (Girdled), 0.0001) of the July bioassay (Fig. 2). Very few of the adult < 0.97). P = In contrast, leaves from the EmBen and the EmBen P ( Fraxinus injected with emamectin benzoatebenzoate (EmBen) or and injected then with emamectin girdled (EmBen with leaves from Figure 3. 28; EAB beetles caged with leaves from Controlduring and Girdled the trees bioassay. died On dayfrom 1, a a girdled single tree at beetle the caged LBwith with site foliage was foliage dead; from all other Controlless beetles or caged than Girdled 5% trees ofGirdled were trees the had alive. died beetles (Fig. By 2). Beetles caged day onfed Control 3, with and actively, Girdled leaves trees consuming from muchproducing Control abundant of frass. or the leaf in the petritrees dish were highly and toxic to beetlesthat (Fig. 2). beetles There was were nothe indication repelled insecticide, by noramong leaves did beetles we from caged observe trees withsites. any On treated leaves average, behavioral with from differences differentor treatments EmBen or beetles had died bycaged day with 3 leaves of from thepetri the bioassay, dishes EmBen including with all leavestrees, beetles from beetles died either after EmBen onlydid or one not EmBen or differ a few between bites. sites Beetle on mortality either day 1 ( Figure 2. Lincoln Brick (LB) and MapleLarval River densities (MR) were sites higher ( and in EmBen Control and Girdled trees than in EmBen girdled (Girdled), injected with emamectinwith benzoate emamectin (EmBen) or benzoate injected and then girdled (EmBen than in trees at the DW site ( indicate significant differences amongthe treatments bioassay on ( day 1 and day 3 of 7, = 0.58, 2, 58; 0.007) ± Girdled = = in 2009 in + P 2 92.37; df = © 2015 Society of Chemical Industry 0.0001) (Fig. 1). F 1.73; df 2, 36; 0.47). Trees aver- www.soci.org DG McCullough, TM Poland, P Lewis 0.80), nor was the < = = 0.38 cm DBH at the = P = F ± P 12 trees per treatment). P larvae per m = n 5.73; df 3, 36; 3, 52; 6, 52; = = = = Girdled trees (Fig. 1), which did F 0.54 cm respectively. Girdled) at the Wolverine West (WW), + ± + A. planipennis 0.53 and 17.0 0.0001) and day 3 ( 0.002). ± < 0.0001) and in trees at the WW site than in 0.33; df 0.95; df = P < = 16.67; df P = P F F = 0.0438). These results reflect the dramatic F = 7, 28; P = 0.54, 16.8 1.22 and 16.4 ± ± 3, 36; Girdled trees ( = + 68.04; df Girdled treatments had an average DBH of 16.8 Number of current-year SE) 15.8 = spp. trees left as untreated controls (Control), girdled (Girdled), + 0.49, 17.0 F ± ± 2.44; df 0.18) or treatments ( = The density of current-year larvae also differed significantly = F 3.2.1 Adult EABThe bioassays mortality of adult EABday beetles 1 differed ( among treatments on interaction significant ( aged ( D-Woodlot (DW), Lincoln Brickrespectively. Trees (LB) assigned and to MapleEmBen the River Control, Girdled, (MR) EmBen sites 16.4 and 3.2 2010 Study Tree diameter did not vary among sites ( increase in EAB density acrossand the 2009. Virtually entire all WW phloem siteWW on between girdled site 2008 and was control consumed treeslike at by most the EAB of larvae the other inor ash 2009, dying in by and the the these vicinity, endincreased trees, were of from severely the declining 2008 summer. to While 2009densities EAB at at population the levels these CLF sites andWW remained LB site considerably (Fig. sites, 1). lower At 2009 the than larval CLFlarvae at and LB the on sites, the density Control of and current-year 2 Girdled and trees 4 inrespectively. 2009 The times high EAB was larval as densities approximately at high thedifferences WW between site as obscured Control the andsites. Girdled density On trees of average, at the the pretreatmenthigher larval other on larvae densities two Girdled in trees 2009sites than respectively. were on 67 Control and trees at 53% the CLF and LB P (Fig. 1), and the interaction( of site and treatment was significant trees had no live larvae,infested. while every Control and Girdled tree was among the three sites in 2009 ( not differ from each other. Seven of the EmBen or EmBen The average densities ofControl trees larvae were on 4–10 Girdled timesthe higher trees EmBen than trees and the and larval untreated the densities EmBen on Fraxinus injected with emamectin benzoatebenzoate (EmBen) and then or girdled injected (EmBen withCloverleaf emamectin (CLF) and Lincoln Brick (LB) sites ( Larval densities were higherand in EmBen Control and Girdled trees than in EmBen trees at the LB and CLF sites ( wileyonlinelibrary.com/journal/ps current-year larvae ( Figure 1.

1026 1027 31 1.5 m high. In ≤ Leaves from trees 1 Minimally, a multifaceted 45 , 44 , 41 wileyonlinelibrary.com/journal/ps Girdled trees (25% of the total) as on the EmBen + If girdling does not impede conduction within xylem Recent studies indicate systemic insecticides applied 46 , 25 34 , , 24 33 Overall, the sticky bands wrapped around the trunk of our 2010 Our hypothesis was based on adult EAB feeding behavior and Girdling trees 18–20 days after injecting the emamectin ben- and 30% higher on Girdled trees than on(Fig. Control 3). trees Even respectively at the DWon site, the a four total Girdled of trees, 38four compared EAB Control with trees. larvae only were nine feeding larvae on the via trunk injectionxylem. are transported to the canopy primarily in study trees captured relativelythe few low beetles, EAB densities whichin and reflects the the both well-stocked, height even-aged sites. oflikely Activity the of concentrated bands adult in beetles on the was thefoliage-bearing upper shoots trees were portion present, minimizing opportunities of for thebeetles to canopies encounter the where sticky bands which were 4Integrating DISCUSSION two or more tacticslation to can manage result an in outcomes insectadditive that pest or yield popu- antagonistic, synergistic redundant, effects. treated with emamectin benzoate,girdling, were with highly or toxic to without beetles24 subsequent h, in at the least 2010 80% bioassay. of Within thetree beetles had caged died, with and a after leaf 3 frombeetle an days caged injected the with mortality a averaged leaf 90%.quently from Every a girdled tree was that dead was withinone injected 24 and h. or subse- Beetles two typically bites tookrates from only and leaves rapid mortality before of succumbing.trees adult Similarly treated EAB with high provided TREE-äge with were reported foliage in from previous studies. strategy should yield additive effects ongeting the two pest life population. stages Tar- oftactics, a for pest example, would with produce insecticides antic or additive effect. other effect A control synergis- occurs whencome the greater combination than the of combined tacticsWe individual yields effects hypothesized of an that the out- lethal tactics. with trap the trees, highly created effective bythe TREE-äge injecting trees insecticide, could ash and result then in aulation girdling synergistic if effect the on insecticide the was localthetreepriortogirdling. EAB effectively pop- translocated throughout the response of beetles to girdled trees.for Beetles at feed least on ash a leaves week before1–2 mating begins, females weeks feed for before another to oviposition feed begins throughout and their both 3–6 sexes week continue lifespan. tissue, it seems likely thatthe trees same could be day. girdled Futurepotential and injected effects studies on of to injection assesstions timing, on translocation local treatment weather efficacy rates or would and ticide be site residues helpful. condi- in For example, 2010 insec- ingenerally the higher green than ash trees in at the the white MR ash site trees were at the DW site. This addition, beetles that fed onhave foliage died, on probably within the a injectedof day, capture trees on further the would sticky reducing bands. the Nevertheless, girdling likelihood didattract appear adult to EAB. More than twiceon as many the beetles EmBen were captured trees (10%), while 40% of the beetles weretrees captured and on 20% the Girdled on the Control trees. zoate had no detectablefoliage compared effect with on trees insecticideWhen that we residue were girdled injected levels the but in outer bark not trees and girdled. in phloem, but 2009 werexylem. careful and to minimize 2010, injury we to the removed the 1.5, 1.98 6.43 5.16; 6, 52; 3, 52; 0.84). 6, 52; ± 2, 52; ± ± = = = = = 0.61) or = F P = at the DW, 0.03 larvae 5.61 larvae P 2 Girdled trees Girdled trees ± ± − Girdled trees, 2.26; df + + 1.69; df 0.48; df + 0.77, 15.0 = = 52.76; df = 2, 52; F F ± F = 2.15 and 5.9 = F ± Girdled trees at the DW + 0.12 and 0.03 3.39 and 23.9 2.22 larvae m 0.49; df respectively. Larval densities 2 ± ± ± = − 3.55, 5.3 F ± 1.13 ppm) than at the DW site 1.23 ppm respectively ( ± ± Girdled trees were similar, averag- at the DW, LB and MR sites respec- + 2 Girdled trees. Sticky bands captured at 0.0194) and were consistently higher − + = 3.30 and 9.0 3.45, 10.3 2.86 larvae m P : 1023–1030 © 2015 Society of Chemical Industry ± ± ± 72 0.0091) (Fig. 3), averaging 2.4 2, 15; 2016; Girdled trees but only one of the EmBen trees. = = 1.58, 9.7 P 2.31 larvae m + for Control, Girdled, EmBen and EmBen 1.40 ppm and 5.65 ± 2 Girdled trees, had any live larvae, and none had more ± ± − + 1.02 ppm). 10.3 and 20.6 ± respectively. Larval densities were higher on Control and respectively,thanontheEmBenandEmBen ± 2, 52; 5.19; df 0.82). Pretreatment larval densities were low at all sites, aver- 0.18), nor was the interaction significant ( 0.0001) (Fig. 3). Only four of the 32 trees injected with the 0.515). When only Control and Girdled trees were considered, 2 2 = = − − The density of current-year larvae that began feeding in The density of 2010 larvae also differed among sites ( = = < = F aging 4.8 P P among trees assigned to different treatments ( 3.2.4 Larval densities The density of pretreatment EAB larvaenot that differ fed among prior the to 2010 three did sites ( m 3.2.3 Beetle captures The sticky bands,ground which on were the approximately trunksbeetles. 1.3–1.4 of m This the above- was trees,had not captured virtually relatively unexpected, no few givenof foliage-bearing EAB the that branches trunk. our Beetle on activitycanopy study the was where lower likely trees leaves concentrated 6–8 were inthe m available the lower upper for portion feeding, rather ofto than the encounter on the trunk sticky wherebeetles: bands. beetles 18 We were on captured more controltrees a likely trees, and total 38 22 of on on EmBen 88 girdled adult trees, ten on EmBen least one beetle on eight ofthe the EmBen control and girdled trees, seven of than four live larvaevae on did the not entirewhich differ tree. had between The an EmBen density average and of of only EmBen live 0.30 lar- emamectin benzoateEmBen insecticide, including the EmBen and in trees at(3.02 the MR site (7.07 P the larval densities at the DW, LB and MR sites averaged 5.3 31.8 Residue levels differed( between treated trees at the two sites m larvae m respectively. 2010 was strongly affected by treatment ( P (Fig. 3). df and 10.4 Pest Manag Sci and MR sites indicatedcation that of the the girdling insecticide didfrom to not EmBen the reduce translo- canopy. and Residue levels EmBen in leaves ing 5.78 Lethal trap trees for emerald ash borer3.2.2 Foliar residues Analysis of emamectin benzoateJuly residues 2010 in from foliage the collected EmBen and in EmBen www.soci.org were notably low on all trees at theand DW LB site, sites, compared where with larval the densities MR did notferences differ (Fig. in 3). Overall EAB dif- density betweennot Girdled significant, and presumably Control reflecting trees theDW were low site. EAB At the density LB at and the MR sites, however, larval densities were 52 Girdled trees, which averaged 15.0 LB and MR sitessities respectively. averaged Similarly, 11.1 pretreatment larval den- tively, while the interaction was not significant ( Am Agrilus :859–873 16 : 1023–1030 but whether 72 32 Fraxinus pennsyl- , 31 2016; :768–776 (2014). Biol Invasions . Funding for this work ). ® 44 Pest Manag Sci :371–383 (2013). 15 Can J For Res spp.) mortality, regeneration, and seed . [Online]. Available: www.emeraldashborer. Agrilus planipennis Fraxinus spp.) trees infested by emerald ash borer ( :152–165 (2005). 51 ,Ash( ) overstory and regeneration at three stages of the emerald insecticide was provided courtesy of Joseph Doccola, Fraxinus ® et al. (2014). ash ( planipennis). Biol Invasions vanica ash borer invasion wave. A bank dynamics in mixedemerald hardwood ash borer following ( invasion by info [16 January 2015]. borer in North America: a research and regulatory challenge. Entomol Emerald Ash Borer Website While TREE-äge or other highly effective, systemic insecticides 5 Knight KS, Brown JP and Long RP, Factors affecting the survival of 4 Klooster WS, Herms DA, Knight KS, Herms CP, McCullough DG, Smith 3 Burr SJ and McCullough DG, Condition of green ash ( 1 Cappaert D, McCullough DG, Poland TM and Siegert NW, Emerald ash 2 was provided by the USDA Forest Service, Northeasternand Area, State Private Forestry. are most likely to beash, used lethal for long-term trap protection trees ofagement high-value could programs. Ash play have a been roledecades, popular and in ornamental are trees operational often for EAB abundantroads in man- or landscapes, highways. parks and Inat along most least urban some or of the residentialhave landscape areas, other ash however, problems have and outgrown their needities space to have or be developed replaced. plans Manyspecies, municipal- gradually as resources to permit. replaceremoval Minimally, ash could ash be with trees girdled designated other inEAB for spring and in removed the in area fall, andAnother to eliminate attract option the may larvae involve developinginjections, girdling on which trees the would a ensure tree. trees year contributed tofor after 2 EAB years. TREE-äge mortality Studies have consistently shown thathighly TREE-äge remains effective for at least 2 years post-injection, ACKNOWLEDGEMENTS We thank NicholasEmily Pastula, Gooch, Andrew Tluczek and Andrea James Wieferich, all of Anulewicz,State Michigan University, Jacob for Bournay, theirAccess to assistance study sites in was provided the by JackieRichard field Blanc, Eaton Bowles, and Co. Parks, DeWitt, laboratory. ClintonCo. Co., Parks, and Bryan the Michigan Van Department of Patton,TREE-äge Natural Genesee Resources. The ArborJet, Inc., and David Cox, Syngenta REFERENCES insecticide efficacy would be reduced if trees wereafter girdled the injection year is notnated for known. removal obviously Injecting adds further andgirdled cost. girdling On trees the trees other must hand, desig- bedestroyed to debarked, prevent larvae burned, from emerging as chipped adultsyear. the or If following otherwise lethal trapbreaks, trees woodlots were or established forests, in wherehazard, areas they dead such could trees be as left would wind- inand not place. pose remove Eliminating the a or need to destroygirdling return costs. girdled Whether trees such costs couldsite-specific are offset objectives acceptable will and injection depend circumstances. and Nevertheless, on clear it that seems lethal trap trees could potentiallyagement play a programs. role Understanding in more EAB about man- howsystemic girdling insecticides interact and to affect EAB population growth over time will be needed to optimizegression efforts of to ash slow mortality. the onset and pro- 38 35 40 , 37 and 36 Sim- 39 52 In other Kirby, Hopkins, 51 , 50 , © 2015 Society of Chemical Industry Hopkins, 29 Zimmerman. www.soci.org DG McCullough, TM Poland, P Lewis (Hendel)] infestations 32 Adult EAB attraction to gir- 48 , 47 , 27 Dendroctonusrufipennis spp.) by distributing a pelletized – 24 Dendroctonus ponderosae Dendroctonus frontalis Bactrocera dorsalis Study trees at the DW site were growing Dendroctonus pseudotsugae 31 Cochliomyia To ensure adequate insecticide translocation and Lethal trap trees may function similarly. Girdling 49 In forested settings, lethal trap trees consisting of pine 51 As EAB densities build and more trees are stressed by , Injected tree. 29 53 27 , + and is most pronounced in areas with fairly low densities 24 21 Recent evidence from two large-scale studies indicates that The attract-annihilate or bait-and-kill method is by far the most Numerous studies and operational projects have consistently formulation containing a chemical(dried blood), a attractant feeding stimulant (swormlure), () and an food insecticide. girdling ash treesspillover effect, in resulting low-densityof in infestations higher ungirdled than can trees expected produce growing colonization a near girdled trees. wileyonlinelibrary.com/journal/ps the mountain pine beetle, the Douglas-fir beetle, The underlying strategypests of to the a locationble method or can is device be simple: wherea removed as attract long-distance from many attractant the the of (olfacatorykill environment. them or It as or visual) possi- trap usually and thebait-and-kill involves a approach attracted include device strategies pests. to to protect Well-knownscrewworm livestock from applications flies of ( the likely reflects site conditions rather than speciesthat differences, in given a large-scale, 2foliar year residues study of with emamectin substantial benzoate replicationand the were white similar ash in trees. green ash larval feeding, beetles are exposed tomany stress-related volatiles competing from trees, obscuringoperational attraction projects, to establishing girdled lethalmost trees. trap effective In trees in is infestations likelyeffective that to insecticides are be are relatively being recent usedable to or ash protect where trees. other, Wounds more or valu- can injuries, disrupt including translocation and EAB within-tree larvalinsecticides. distribution galleries, of systemic widely used behavioral manipulation for pest management. trees injected with emamectinattraction benzoate to may the not treatedon only tree, it nearby increase may untreated also treesGirdled reduce by larval killing densities adult EAB that feed on the of EAB. dled trees likely reflects changes intrees volatile profiles of the stressed optimize efficacy, trees should behigh treated larval with densities insecticide disrupt vascular before tissue. in a well-stocked, even-agedonly woodlot, partially and exposed their toand canopies translocation sun, of were which the insecticide. may At thewere have MR either site, reduced superdominant the or study uptake trees growingto in full openings or and nearly exposed fullaccounting sun, for which the may higher have foliar residues. increased translocation, shown that adult EAB areash attracted trees to stressed by and girdling. preferentially colonize or spruce trees that were sprayedor with insecticide baited and then with felled were semiochemicals used in (e.g. management efforts aggregationtles, targeting including pheromones) aggressive the spruce , bee- were eradicated using anwith attractant insecticide-saturated (methyleugenol) squares combined ofairplanes. cane fiber dispensed from ilarly, oriental fly [ the southern pine beetle, words, beetles attracted to aportion girdled of tree may their stillIntermixing deposit eggs or some surrounding on girdledincrease trees adjacent the with or likelihood treated that trees nearbygirdled beetles may tree ungirdled attracted will encounter to a trees. treated the tree,mortality. vicinity thereby increasing of adult a

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