1971 ry 2019 , unpublised). et al. 1,7 * insecticide, bare row and bare + The seasonality of adult borer flights and egg depo- 5 making it difficult to predict the optimal timing of trunk Olivier) (FHAB) is a native pest of fruit, shade and 1,4,7,10 Correspondence to:Tennessee KM State University, Addesso, 472 OtisE-mail: Cadillac [email protected] L. Lane, McMinnville, Floyd TN Nursery 37110, Research USA. Agricultural Center, and Environmental Sciences, Otis L. Floyd Nursery ResearchCollege Center, of Agriculture, Tennessee State University, McMinnville, TN, USA The most effective treatment for FHAB is a systemic drench Previous research has demonstrated that nursery tree rows ∗ sprays. Generally, the FHAB lifeeggs deposited cycle in late is spring completed or early in summer,take but 1 some 2 larvae year years can to with complete theirdifferences development, in which the also timing can of cause adult emergence. In this two-year trial,resulted half in 100% the control labeledbut in high had the rate a non-herbicide-weedy of 15% treatment, loss imidacloprid in the herbicide treatment during that same application of imidacloprid, although dinotefuranchlorpyrifos, bifenthrin drenches, and permethrin and trunk sprays alsomonly are used. com- treated with pre-emergent herbicide have more FHAB attacks than trees with standing weeds at the base (Oliver JB sition vary by regionyears, and environmental conditions in different 5,9 2,3 Tilia spp.), (Olivier) The wide 4,5 Malus femorata This borer can Although trees 6 Acer saccharinum Prunus americana 5,9 A single larva can 8 L.), apple ( The most common hosts 1,10 spp.). 7 spp.), American basswood ( L.) grown under four treatment regimes (cover crop, cover crop Cornus L.), silver maple ( L.), common apricot ( Quercus Prunus domestica : 1971–1978 www.soci.org © 2019 Society of Chemical Industry 75 Acer rubrum Acer rubrum Individual trees may be repeatedly attacked over 5 2019; The borer’s distribution is ubiquitous, covering the crimson clover; annual ryegrass; winter wheat; imidacloprid; barrier; red maple L.), and dogwood ( Prunus persica 1

insecticide) were evaluated for damage by FHAB and impact on tree growth parameters. +

entire continental United States and extending into Canada. multiple years, which usually kills them. Pest Manag Sci In general, newly transplantedof maples have attack, slightly but highertransplanting. rates maples may continue to be attacked well after It has been reportedtrees as in problematic Oklahoma, Kentucky, for Georgia, damage and Tennessee. on ornamental The flatheaded appletree borer, 1 INTRODUCTION (Coleoptera: ) (FHAB),the is United a States and serious isnut pest reported trees. as throughout injurious to fruit, shade and BACKGROUND: The flatheaded appletree borer ( cover crop Abstract ornamental nursery production with a winter Sujan Dawadi, Jason B Oliver, Paul O’Neal and Karla M Addesso (Chrysobothris femorata Olivier) in woody (wileyonlinelibrary.com) DOI 10.1002/ps.5310 Management of flatheaded appletree borer Research Article Received: 10 September 2018 Revised: 17 December 2018 Accepted article published: 4 January 2019 Published online in Wiley Online Library: 10 Februa attack more than 30 species of trees. completely girdle a tree within a single year. are red maple ( attacked by FHAB do not alwayslarval die, tunneling the trunk ruins damage the caused economic by quality of the nursery tree. host range ofto FHAB exclude, despite has continuous made research it efforts. difficult for orchard owners nut trees throughout the Unitedvegetable States. and Use cereal production of systems, coverThe but crops goal its is of impact an this in study effective woody wasRed pest ornamental to maple management production evaluate trees the tool systems ( effectiveness has for of not somerow a been key winter investigated. cover crop pests for in management of FHAB in nursery production. Marsh), garden plum ( americana L.), peach ( different species of oak ( Keywords: Supporting information may be found in the online version of this article. RESULTS: The cover crop reducedin FHAB FHAB damage, attacks in with cover results cropor equivalent treatments may interference to be standard with due imidacloprid to accessfor microclimate treatments. resources. to changes The at oviposition reduction preferred oviposition sites. sites, Tree trunk camouflage growth wasCONCLUSION: reduced Physical in blockage the of oviposition coverFHAB sites damage. crop Therefore, by cover treatments crops cover can due crops be© and to an 2019 alternative Society subsequent competition to of microclimate chemical Chemical changes insecticides. Industry protected against , 1 of N, − ∘ 1 et al. − )and 1 − insecticide, insecticide) : 1971–1978 insecticide), + + 75 + L.) were sown 0.01 cm at 15 cm ± 2019; 0.80 cm were planted 2 factorial design. The ± × 24.4 m field site). Tree rows × Pest Manag Sci Lolium multiflorum )( 1 − 11 m plot with 25 randomly assigned trees standard nursery herbicides), and (iv) bare × . Seeds were lightly disked into the field following via , and again in 2017 with a total of 31 g N tree 1 using a Herd GT77 Spreader (Herd Seeder Co., Inc., 1 − − 22 A single tree space was skipped after the fifth tree in W) (Warren Co.) was the field site for this study. ∘ 21 insecticide (Fig. S1). Treatment combinations were selected + For the second-year of the experiment, clover (16.8 kg ha based on current recommended practices (bare row our practice of interest (cover cropboth in cover tree crop rows), a and treatment chemicaland with controls a (cover negative crop control(bare row). to Each provide treatment aconsistedofan11 block baseline was for replicated FHAB four(i.e., 100 activity times trees per and treatment; 97.5were m spaced 2.1 m aparttrees with 1.8 following m within-row current spacingplanting. between recommendations for a short duration row (iii) bare row ( Logansport, IN, USA). Half thebecause two high cover rate crops were of combined cover andexisted no crops on prior was how knowledge well used theyRTV1140 would work (Tractor for and FHAB Equipment, control. TennesseeTN, A Valley, USA) Kubota McMinnville, with the spreader attachedspeed was of 1 operated m with s a ground each row as a buffer zone between treatment plots. 2.1.2 Plant material Red maple ‘Franksred’ liners werein propagated June as 2014 rooted and cuttings transplantedHummert into International, #3 Earth containers City, (C1200,tainers MO, 10.9 were USA) top L, dressed in with April slow-release(Harrell’s fertilizer 2015. (12N–6P–6K) Inc., Con- Lakeland, FL,gation USA) until transplant and the heldtrees following under fall. with overhead Four an hundred irri- average dormant trunk diameter of 1.13 above the soil linein and ten a rows height on(model of 13 TR-8, 154 November Rigsby 2015 Manufacturing Co.,by using Walling, a a TN, John nursery USA) Deere drawn treewere 640 top-dressed planter with tractor fertilizer in (John March and Deere, June 2016of Moline, with a 22 IL, total g N USA). tree Trees broadcast. Cover crops were allowed to senescethe naturally summer through months and row middles11 were disked August into 2016 the soil with on aa John 1.2 m Deere (4 Model ft) 770 wideufacturing tractor model Co.). fitted disc Cover with crops with were scallopedorder allowed edges to to (Rigsby evaluate senesce Man- the naturally maximum in growth. impact of the cover crop on tree 22.1 MATERIALS AND METHODS Experimental design 2.1.1 Field plots Moore Nursery in Irving College, TN, USA (35.583889 85.713056 Four treatments were assignedtreatments included: in (i) a cover 2 crop, (ii) cover crop agricultural grade fertilizer (15N–15P–15K)tively, (Harrell’s Inc.), and respec- pruned toremove suckers. develop The or amount of maintain fertilizerond was a increased year central in of the leader the sec- experimenttree and growth. to meet additional requirements for 2.1.3 Cover cropCrimson application clover and winter wheatson,GA,USA)weresownbeforetreetransplanton15October (Adams-Briscoe Seed Co., Jack- 2015 at half the recommended high rate (16.8 and 84.2 kg ha respectively) annual ryegrass (34 kg ha 18 In no L.), and 13 16,17 www.soci.org S Dawadi 19,20 Astudy 12 the authors 11 © 2019 Society of Chemical Industry 20 cm above the soil Triticum aestivum if it is allowed to reach < and may be planted in 1 − 16 spp.) and other crops. L.), wheat ( The approximate date of maturity Therefore, any cover crop used for 5 15 Vicia , unpublished). Based on the FHAB prefer- L.). Crimson clover is often used as a winter Secale cereale The height of winter wheat varies with variety, et al. spp.), vetch ( 14 Therefore, clover supplies sufficient nitrogen to the 15 Trifolium Although cover crop incorporation for insect pest management Based on our knowledge of FHAB behavior and the limita- If a weedy barrier is sufficient to prevent or reduce FHAB attacks Trifolium incarnatum FHAB management must reach a sufficient heightfrom to accessing block that portion of the treeWinter at wheat the serves time as of a female winter flight. crop or cover crop for weed for winter wheat inplant Tennessee is will the reach first itscover week crop full of used June, height in but by( the the southern early United May. States Another is common crimson clover cover crop in vegetable or field crops wileyonlinelibrary.com/journal/ps so the maximum heightcoincides with of the likely wheat oviposition period and of FHAB.predicted clover Therefore, that it that in is crimson clover the and wheat late wouldheight be at spring to the interfere ideal with FHABthe movement tree and trunk. oviposition around has been performed in vegetable and cereal production, period (Oliver JB ence for depositing eggs near the base of the tree, research on the usetion of for cover insect pest crops management exists. in Following the redples same as princi- maple in vegetable nursery and produc- cereal farming,was the to minimize objective FHAB of damage this in study field-grown redthere maple. However, are unique challenges intems that woody are perennial not present production in seasonal sys- tion. vegetable Normally, and a grain cover produc- crop iscrop applied to seasons. a In fallow a field in mapletransplanted between while production dormant system, in late tree fall linersspring or planting must early may spring. be necessitate Fall or planting early treesviously directly planted winter into cover a crop and pre- overseeding the fielding follow- transplant. In subsequent years, the coverbroadcast crop at the will base need of to the be trees, butin can the only row be disked middles or to drilled cover prevent damage crop to is the also tree likely roots.early spring to A growth. winter compete with the maple trees during tions of current conventional managementthis practices, study the goal was of tofor develop FHAB an in alternativewere management nursery two-fold: method (i) production. to evaluatecrop The the to objectives effectiveness protect of maple of atify trees this winter from the cover FHAB study impacts attacks, ofgrowth. and a (ii) cover to iden- crop management strategy on tree but ranges from 78 to 102 cm. field without the need toAdult FHAB add are predominantly more active fertilizer from mid-May to to early the July, wheat cover. mixes with grains toclover grows provided to supplemental between 30 nitrogen. andmanure Crimson that 90 cm, can add and 76.6–170.5 is an kg N excellent ha green the late bloom stage before being killed or turned under. erosion control. hypothesized that the weeds provided protection from egg-laying by FHAB. on trees, then aCommonly cover used crop winter could cover beStates crops used include in rye in ( the the southeasternclover same ( United fashion. Tennessee, growers generally apply 20–40wheat field. kg N to a production of FHAB damage inthat the red height maple of borer trees damageline, averaged in but ranged weedy up to plots 100 cm. suggested

1972 1973 ) ∘ width 0.001; 5,11 16.02 + < ± P ∘ 5 0.0019; Fig. S2). 26.60, 0.001). There was = = < P P (1) 2 𝜒 0.0001; Fig. S3). 0.001). There was no dif- 14.89, 26.60, < < = P = P (3) (1) canopy height)/3. 2 2 𝜒 wileyonlinelibrary.com/journal/ps + 33.04, 𝜒 2.61 cm above the soil line, respec- 22.17, = ± = (canopy width at widest point (3) (1) 2 = 2.3 cm, and the first week of April 2017 was 𝜒 2 ± 𝜒 2.41 and 19.62 ± insecticide: 2.5 and 27.25 insecticide treatment (current recommended practice). One × ± + The average lowest and highest average height of FHAB damage tree from theThe bare cover row crop treatments treatment reducedinsecticide was FHAB was applied attacks attacked (cover: whether in or not both years. perpendicular to widest point Attacks were initiatedupward. from No larval ground damage level wasthe trees. observed and On above average, larvae damage 39 faced cm southwest tunneled on (189.09 any of to July 2016 and monthlyture/external in soil temperature 2017 meter with (Spectrum Technologies, an Inc., infraredEast crop Plainfield, tempera- IL, USA). Temperatureto measurement was monthly changed in 2017in upon the prior evaluation year. The height of of temperature biweekly measurementsen was measurements cho- as 20 cm because most attacks occur at or below 20 cm. cover a significant interaction of coveron crop FHAB and attacks, insecticide with a treatments strongerthe effect bare ground of treatments insecticide (insecticide: observed in 3RESULTS 3.1 Flatheaded appletreeOf borer damage 26 FHAB damagedtreatment trees, (Fig. two 1). werebare Twenty-three found row in treatment damaged the (negativerow cover trees control) crop and were one was in in the the bare 2.3 Tree growth Tree height and trunk diameterand were repeated recorded in before September transplant measured 2016 using and digital calipers 2017. (Mitutoyo Corp., Kanagawa, Trunk Japan) diameterat was 15 cm (6used in) to create above a groundmeasurements mark at on level. the the A same tree location.recorded permanent trunk Canopy for to size marker all facilitate index was treatments (CSI) subsequent following was in September formula: 2016 and CSI 2017 by the 2.4 Statistical analyses Flatheaded appletree borer attackgeneralized counts linear were interactive analyzed model withnegative (PROC binomial a GENMOD) distribution fitted and to treatment LSmeans a arated were by sep- Tukey’s Multipletute, Comparison Inc., Test (SAS Cary, 9.3,tion NC, and SAS USA). height Insti- on Thetest the proportion tree of trunk of proportions were attacksand analyzed (PROC by by weeds FREQ). chi-squared direc- samples, Biomassand of trunk canopy dried temperature, size index cover treelyzed measurements crop by height, of a diameter maple generalized linear treesGENMOD) interactive fitted were to model ana- a procedure normal (PROC distributionby with Tukey’s multiple LSmeans comparison separated test. 3.1.1 Cover cropThe height and height biomass of the24.8 cover crop in the first week of April 2016 was with 77.27% of all damage recorded ontion the of southern-facing the direc- tree trunk ( ference in FHAB attackswithout detected insecticide (Fig. between 1). cover crop with and was 7.84 tively. Most of the observedbelow damage 20 (88.46%) cm was on concentrated the trunk ( , ® et al. 0.70% + ,flumiox- ® cover crop samples Original (glyphosate 2 of trunk diameter in ® 1 − in November 2015, March 2016, August 1 5 − : 1971–1978 © 2019 Society of Chemical Industry N/G insecticide (imidacloprid 2.94% 75 C and dry weight was recorded. Final height of ® ∘ 2019; 6-month intervals or whenever vegetation began to break ∼ Trees in the insecticide treatments were treated with a basal Pest Manag Sci 2.2.1 Cover cropFor height and both biomass cover evaluation crop treatmentsmeasurement (i.e., of with cover crop or height without wasMarch insecticide), performed to July biweekly 2016 and from monthly in 2017proved when biweekly unnecessary. recordings On 27 July 2016, 30 cm 2.1.4 Herbicide andTree insecticide rows application in plots with no coverprogram crop were of maintained bare pre- with and a and post-emergent broadleaf herbicides weeds. to The control pre-emergent grass (SureGuard Cover crop for flatheaded appletree borer managementin September 2016 usingScotts a Co. Scott’s LLC, Edge Marysville,annual rye Guard™ grass OH, in spreader the second USA). year (The because, unlike Wheatwill wheat, ryegrass germinate was on replaced contact with with disking the in the ground tree and rows. does not require www.soci.org azin 51%, Valent U.S.A. Corp., Walnutat Creek, CA, USA) was applied through the herbicide barrier.of SureGuard 708.8 g was product applied ha at a rate 2016, and April 2017. The post-emergent herbicides Finale (glufosinate-ammonium 11.33%, BayerResearch Triangle Environmental Park, NC, USA) Science, or Gly41%, Star Albaugh, LLC, Ankeny, IA, USA) with(Ragan 80–20 and (0.5%) surfactant Massey,as Inc., spot Ponchatoula, treatments LA,pre-emergent barrier. to USA) control were weeds applied that brokedrench through of Discus the cyfluthrin; OHP, Inc., Bluffton,the SC, USA) labeled On rate 11 (11 mL April 2016 product at 2.5 cm half were removed from each treatment plot atlocations five within randomly the tree selected rows by cutting atcrops ground and level. The weeds cover were separated. Separatedin materials an were oven dried at 40 2.2.2 Trunk temperature evaluation Trunk temperature on theheight southwest side from of the each tree soil at line 20 cm was recorded biweekly from March the cover crop was measured justinto before the the soil cover on crop 27 was July tilled 2016 and 2017. 60 mL water) based on previous efficacy data (Oliver JB 2.2 Flatheaded appletreeAll borer damage trees evaluation were evaluatedand for spring characteristic of year FHABtwo one damage (October (October in 2016 2017 fall andtrunks and April above April 2017) and 2018). thelength year Height soil of larval of surface surface attacks damagemissing, was (i.e., or on sunken). bark recorded If tree that trees was using werecontinuous cracked, attacked the twice split, boring or a visible tunnels, treelength had average two were lower calculated. height Directionacteristics of and D-shaped initial average damage holes orof were four any quadrants: recorded northeast, char- southeast, and southwest and assignedAlthough northwest. the to adult borers oviposit one on treessummer, in the late spring new and larval early damage isfall apparent or spring only after in the the larva following To has make grown it and useful the for damage data increased. reported analysis borer and damage interpretation in purpose, the we fall andfromthesameseason. following spring as damage unpublished). 2 2 𝜒 𝜒 et al. 9.46, 0.045, 0.001; 0.036). 0.001). 0.001). = 278.75, 241.27, = < = < < = = P P (1) P P P insecticide: insecticide: : 1971–1978 2 (1) (1) × × 𝜒 0.534) and no 75 2 2 0.511), nor was interaction: = 4.01, 𝜒 47.49, 4.40, 𝜒 × = 47.57, P = = = P 493.05, = 2019; = (1) (1) (1) (1) 0.39, 0.95) was observed in 2 2 2 (1) 0.43, 2 = 0.001) with the insecti- = 𝜒 𝜒 𝜒 𝜒 0.131, cover = 2 0.001), where insecticide P 0.345) (Fig. 2B). However, < 𝜒 = (1) < 0.592). P = The FHAB height preference (1) 2 P 0.001; Table 1), as did trees P P 2 = 𝜒 < 𝜒 P 0.00, 5,11 P Pest Manag Sci = 2.28, 24.64, 0.89, (1) = 32.52, 0.29, = 2 = = = (1) 𝜒 70.17, (1) 2 (1) (1) (1) = 𝜒 2 2 2 2 𝜒 𝜒 0.001, insecticide: 𝜒 (1) 𝜒 0.001). In September 2017, similar results < 0.001). However, no effect of insecticide was = 2 0.951). Overall, the effect of temperature reduc- 0.001; Table 2). The application of insecticide P P 𝜒 < = < P 0.252). P insecticide: P = × P 25.48, 10.64, 5.32, insecticide: interaction: 0.00, insecticide: insecticide: = = = × × = × × 1.31, 536.62, (1) (1) 0.002), but there was no interaction (cover 0.001). Insecticide application did not affect diameter growth 0.001) and insecticide application (insecticide: (1) (1) = = = 2 2 2 2 < < tion was similar𝜒 in 2017 during the cover crop period (cover: observed in year two (insecticide: there a significant interaction of cover(cover and insecticide treatments However, no interaction betweencide cover (cover treatments and insecti- There was also an interaction(cover of cover and insecticide treatments 𝜒 interaction of row treatment and insecticide (cover on trunk temperature (insecticide: in cover crop treatments, but did increase diametertreatment in (insecticide: the bare row were observed where treesgrowth in (cover: bare rows had greater diameter application in treatments withplant bare height. rows In September was 2017, found treatments withhad to bare enhance rows a again better𝜒 height growth than cover-cropped trees (cover: (1) 4Flatheaded DISCUSSION appletree boreron the has lower trunk a of host preference trees. for ovipositing (1) also increased canopy size (insecticide: with insecticide applied (insecticide: there was upward trend ofin temperature cover during crop last applied treatments week as of thequickly June cover in crop senesced 2017 more (Fig. 2B).first sampling Trunk date temperatures of were each year lowestout and the at gradually late the increased spring through- and early summer to a peak in June (Fig.3.2 2B). Tree growth 3.2.1 Height At transplant, average heights ofacross experimental trees all were treatments similar (Tabletransplant 1). (2016), In treatments Octoberthan 2016, without cover at cover crop 1 crops year treatments post grew (cover: more P There was a significant interaction between coverand crop treatments insecticide treatments (insecticide: 3.2.2 Trunk diameter There was no difference inplanted average trees diameter for in all2016, October newly trunk 2015 trans- diameter (Table growth 1).compared was However, with greater by in October cover-cropped trees in trees bare rows (cover: cide effect stronger inwere the similar bare to 2016 row for treatments. cover In treatments (cover: 2017, results P P year two. 3.2.3 Canopy sizeIn index fall 2016, tree canopy size wascrops smaller in trees compared grown with cover with trees grown in bare rows (cover: 𝜒 cover cover 2 2 𝜒 𝜒 3.16, 0.05, 0.734, 88.80, 59.72, = = www.soci.org S Dawadi 6.3 and 4.8 and = = = rows were ± P ± (1) (1) 1.8 g) and insecticide (1) (1) = 2 2 ± 2 15.22 g) and + 𝜒 𝜒 2 𝜒 ± © 2019 Society of Chemical Industry 𝜒 0.12, = 1.68 g; dry weight: (1) ± 0.344). However, the 3.57 cm, and in 2017 insecticide and cover 14.55 g; dry weight: 2 = ± + 𝜒 ± P 0.90, insecticide (34.77 = + labeled rate of Discus N/G (imidaclo- insecticide (181.62 × 1.94 cm for the cover (1) + ± 2 3.6 and 70.92 𝜒 insecticide and cover crop only treat- ± + 0.94). However, the average final height of 2.4 cm in the cover = 13.87 g) treatments (dry weight: 1.6 g) treatments (dry weight: 8.19 g, cover crop: 32.65 ± P ± ± ± 0.044). The heights of cover crop in first week 0.306). Similarly, there was no difference in cover 14.97 g, cover crop: 188.0 = 0.001). Similarly, there was no difference in cover = 0.01, 0.463, 2017; P ± 2.24 and 71.69 < P = = P ± P Total number of trees attacked by flatheaded appletree (1) 4.05, 1.05, 2 cover crops in tree rows were crimson clover and winter wheat 2.4 cm, and in5.0 last week for of the June cover 2017 was 70.3 2.0 and 33.2 = = 𝜒 trees were drenched with 0.5 cyfluthrin) in April 2016. = 85.30, 0.54, ± ± ± = + 0.076) in 2017. In 2017, however, fewer weeds were observed 0.818). 0.001) (Fig. 2A). There was no effect of insecticide application 0.001). (1) (1) = = In 2016, weeds broke through the cover-cropped tree rows 2 2 = = < < ments, respectively. No differences were observed betweenof either the treatments in both years (2016: 89.3 72.0 were 72.67 and cover cropof only the treatments, cover crop respectively. the The last week final of height June 2016 was 92.6 of May 2016 were 65.22 𝜒 crop dry weights between cover cover only (30.53 wileyonlinelibrary.com/journal/ps (1) cover only (186.36 prid (1) 29.3 (2016), and crimson clover andmaintained annual weed-free rye with grass (2017). pre-cide Bare and post-emergent herbicides. Insecti- crop treatments, respectively. Therein was initial height no of difference cover crops detected in either of the treatments (2016; Figure 1. borer (FHAB).Cover Values with different letters are statistically different. P in the cover-croppedperiod, tree and the rows dry weight at(weeds: 43.88 of the cover crop end outweighed the of weeds the evaluation P 3.1.2 Trunk temperature Trunk temperatures at 20 cmments were compared lower with in bare the roweffective cover treatments crop throughout treat- the cover 2016 crop standing period (cover: 2017; P P as the coverweight of senesced cover andples crop (weeds: there 26.7 and was weeds no in difference the harvested in row dry sam- cover crops was lower in 2017 than in 2016 (height: crop weights between cover average initial height of𝜒 cover crop was higher in 2017 (height:

1974 1975 b a b a The 03 03 11 04 . . . . 0 0 0 0 11,23 C higher ± ± ± ± ∘ 30 cm start- 86 38 73 25 . . . . C higher on 0 1 0 1 > ∘ 5 SEM) at 20 cm above c a c b ± C 01 03 10 03 cm at the end of June. . . . . ∘ labeled rate of Discus N/G 0 0 0 0 trees were drenched with + × ± ± ± ± = Sunny locations might be 31 44 41 17 . . . . 0 1 0 1 5,11 wileyonlinelibrary.com/journal/ps a a a a 02 01 02 02 . . . . 0 0 0 0 ± ± ± ± 14 12 13 13 . . . . 1 1 1 1 trees were drenched with 0.5 = b a b a 46 45 94 37 . . . . There are at least three possible mechanisms by which the In addition to lower light penetration, the cover crop could have 2 2 2 4 and treated with basal drenchestwo of imidacloprid. management Although methods these providedcontrol, significant 23% levels of of unprotectedtrial FHAB period. trees The 23% were level lost ofnursery loss production over is areas typical the where for FHAB susceptible two-year is trees present. in ing in May and gradually increased to 70 cover crops protectedtles the are trees reported frommostly to on FHAB the be sunny attack. side heliophilic,southwestern of the The targeting sides tree in their (i.e., bee- our primarily oviposition the locality) south and preferred for oviposition byadded wood-boring heat females will because accelerate the development of the larvae. growth of the cover cropthe around entry the of base sunlight ofThe the throughout lower tree the decreased light female penetration ovipositiontemperatures. period. resulted Trunk in measurably temperaturesin lower were trunk the routinely bare 2 row treatments, and as much as 4 extremely hot daysences in were 2016. less Although dramatictreatments in the the remained temperature 2017 differ- consistently coversample date. crop higher mix, in bare row all butprovided the a simple final physicaldeterred attacks. barrier The height to of both FHAB cover crops was that also may have ± ± ± ± 47 68 09 91 . . . . 56 83 56 79 a b c c 02 85 66 59 . . . . c a c b 1 1 1 1 cover crops in tree rows were crimson clover and winter wheat (2016), and crimson clover 45 92 18 84 ) ± ± ± ± . . . . 3 = 1 2 1 1 7 4 8 9 . . . . cover crops ± ± ± ± 79 76 = 117 108 26 59 28 60 . . . . rows were main- 8 Growth 2016 Growth 2017 Initial diameter 2015 Growth 2016 Growth 2017 10 65 40 = Height (cm) Diameter (cm) cyfluthrin) in April 2016. SEM) at 20 cm above the soil surface in 2016. (B) Monthly trunk temperature ( + a ± a b c c C a a a a ∘ labeled rate of Discus N/G 80 33 21 03 . . . . 18 18 06 71 . . . . × 1 1 1 1 3 2 3 2 Canopy size index (cm ± ± ± ± ± ± ± ± rows were maintained weed- free with pre- and post-emergent herbicides. Insecticide 2016 2017 = 29 42 35 30 . . . . 03 23 74 72 . . . . cover crops in tree rows were crimson clover and winter wheat (2016), and crimson clover and annual rye grass (2017). = : 1971–1978 © 2019 Society of Chemical Industry 75 cyfluthrin) in April 2016. + cyfluthrin) in April 2016. 2019; + a Insecticide 157 Increase in height and trunk diameter of ‘Franksred’ red maple trees grown under four management regimes 1 and 2 years post transplant Mean canopy size index of ‘Franksred’ red maple trees 1 and Insecticide 155 + Insecticide 54 (A) Biweekly trunk temperature ( + Insecticide 113 trees were drenched with 0.5 + labeled rate of Discus N/G (imidacloprid + rows were maintained weed-free with pre- and post-emergent herbicides. Insecticide = × = Bare 153 Cover Bare Cover 153 Values with different letters are statistically. Cover Values with different letters are statistically different. Cover Bare Bare 90 Cover a Treatments Cover 52 Table 2. 2 years post transplant a Table 1. Treatments Initial height 2015 and annual rye grass (2017). Bare in tree rowscrimson clover were and crimson annual rye clover grass (2017). and Bare winter wheat (2016), and 0.5 tained weed-free withcide pre- and post-emergent herbicides. Insecti- (imidacloprid Pest Manag Sci observation led to the proposal thatbarrier incorporating to a plant-related FHAB access aroundtect the nursery base trees of from tree attack. trunksconfirmed could The that pro- results attacks of on thisgrowing red a two-year maple winter study cover trees crop at can thewas be base observed of in prevented trees. the by Only cover 2% crop treewhereas plots loss over 1% the course tree of the lossrecommended study, best was practice, where observed trees were grown in in bare plots rows with the currently Bare the soil surface in 2017. Cover Figure 2. Cover crop for flatheaded appletree borer management www.soci.org (imidacloprid 52 L.), et al. many 5 The effect In addition : 1971–1978 Rhizoctonia Bactris gasi- 53 In that study, 51 75 55 Secale cereale (Breda de Haan). 2019; 1,10 An additional alternative to imi- Pest Manag Sci 7 insecticide-treated trees. Although the Horn. + Phytophthora nicotianae The same principle of cover cropping also was insecticide treatment in year one. In the second 54 + (J.G. Kühn) and Kunth) orchard system showed that ground covers impeded To the best of our knowledge, this is the first study to explore the The major negative impact of the cover crop management Although the difference in maple tree growth between cumulative differences in growth are substantial, it iscompetitive clear advantage that of the the bare row treatmentthe decreased trees once were established. Although FHABtrees can continue during to the attack entire production cycle of a nursery tree, could provide improved summer weed suppression. year, however, cover-croppedgained trees by added the bare 67% row of the height investigated for vine growth in first-year vineyards. effect of cover cropping onduction borer system. Flatheaded management appletree in borer, a a major nurserydeciduous insect pest nursery pro- of trees in thetrolled United using a States, winter was cover crop. efficiently This research con- providestive an to alterna- imidacloprid treatment for managing FHABother and species potentially with similar life habitsborer, such as the Pacific flatheaded otherwintercovercrops,suchascerealrye( Trees in cover crop plotstemperature-related also trunk had stress cooler may trunks, bethe so broader reduced. sunscald positive In and impacts of addition cover cropping,practice to this also management may benefit nurserypesticide producers exposure by and reducing eliminating worker and the cost it considerable takes to labor treat time trees with insecticide drenches. method was the reduction inwas tree not growth. Tree an growth unexpected reduction outcome,growth as of cover trees crops due can to competition impede for the soil resources. of competition has been shownThe study in of several ground covers woody on a plantpaes Pejibaye systems. peach palm ( growth, lowered yield and delayed the harvestand during the half first one years. cover crops reduced the vine dry mass weightters by up compared to with three- quar- cover-free systems, butweed were able biomass to suppress by upcover to crop and 95%. weeds in The theweeds similar first also year dry of contribute biomass replication to suggests between thewhen that reduction cover crop in biomass tree outweighed growth.ond weed Similarly, year biomass of in replication, the thereparameters sec- was between cover less crop difference and in bare treatments. plantis Therefore, also growth it important to keep weedsfield. under control in a cover-cropped cover-cropped andthe bare first row year postond treatments transplant, year the (Tables was 1 differencetreatment and decreased substantial added 2). the only in For sec- 12% example,thebarerow of trees the in height the gained cover by crop the trees in to weed suppression, greenhouse bioassays conducted using soils from this field study suggest that cover-cropped soilspathogens can suppress of concern to maple productionsolani including dacloprid for FHAB management couldevent be of very regulatory important loss in oflinator the imidacloprid concerns registrations or due the to developmenttance. Future pol- of avenues of FHAB research imidacloprid must address resis- coverselection crop and species early senescence of the cover cropminimize with herbicides the to impact of the cover cropa on significant tree growth. factor In addition, totree explore is growth the losses use from of irrigation competing to vegetation, mitigate by eliminating authors report this pestduring to the be initial transplant the years. most significant to tree crops like Nec- They 32 www.soci.org S Dawadi 24 Ragweed 50 Cover crops Alternatively, provide weed © 2019 Society of Chemical Industry 25 45 43,44 However, this sys- The ability of FHAB 24 as well as create alter- Similarly, in our study 33,34 41,42 28–32 and was sufficient to block FHAB oviposi- 18 Summer weeds, including ragweed, are diffi- 49 and reduce the attack of non-targeted increase soil organic matter, 46–48 In many cropping systems, the use of imidacloprid is 5 In addition to non-target impacts, the use of a sole active 38–40 25–27 35–37 canker in the rigid tree guard treatments. Basal drenches of imidacloprid provided 99–100% control of Based on our results, cover crops that stand at least 30 cm before positively correlated with plant growth. FHAB in this study.include Current a basal recommendations drench of for afuran). neonicotinoid FHAB (imidacloprid Imidacloprid, control or in dinote- particular, isdamage an and effective the control insecticide ofmore can years, FHAB allowing persist growers to in treat once thetion for a plants cycle. multiyear produc- for two or wileyonlinelibrary.com/journal/ps The May to Juneperiod of period May coincided to July with the active FHAB flight native hosts and habitat for beneficial . suppression during the first year wesize found increased that due to height, the diameterthe application and bare of canopy rows. insecticides, The especially effect in ofeters imidacloprid were on reported plant as growth a param- phytotonic effect. tion based on our results. Athis study one conducted attempted simultaneously to with use tree wraps to block FHAB attack. tria evaluated several types of tree guardsto protect commonly the used trunks of in newly forestry transplanted trees. Noneucts of the protected prod- trees from FHAB over thewere three-year study. able Females to enter the smallrigid amount tree of wraps airspace and left the betweenment, trunk. the females In were the able biodegradable to paperwraps. reach Trunk treat- wraps the likely tree increased the by temperature crawlingof and humidity under the the tree trunks, as evidenced by the higher incidence of cult to manage in local nurserycompeting plantings. Weeds with are main all crops known for forprimary moisture crop and growth nutrients, in reducing a nursery production system. pests of red maple. the cover crop couldFHAB. have altered the predation risk of female ingredient for FHAB controltial to on result a in resistance regionalcover development level in crop FHAB has management populations. the method The and poten- provides an alternative flexibility to neonicotinoids, particularly to on growers floweringspecies. tree the female flight period are sufficient to protectwithout trees against the FHAB need for chemicaltion treatments. from In FHAB, addition cover to croppingkeybenefits.Covercropscanbeusedtomanagesoilandwater protec- can provide growers witherosion, other may reduce the incidence of soilborne pathogens, females to overcome physical barriersgests placed that on some host other trees characteristictrees sug- of from the FHAB cover females. croptree In trunk, protected the addition presence to of a physicallyist cover pests blocking crop like also the FHAB, may reducing confuse colonization special- success. okra and cotton. Similarly, the effectplant of imidacloprid growth on parameters red maple was inconsistentreplication over in the our research, two and yearsommended thus as of imidacloprid a plant cannot growth-enhancing be agentduction rec- in system. red Imidacloprid maple and other pro- neonicotinoids haveassociated been with potential negative effects on pollinators, especially bees. tem of phytotonic effects was mostly investigated field crops suppression was noted in theing second that year repeated of use this of study,of cover suggest- even crops recalcitrant can weeds. aid Although cover inselected crop specifically the species for management this were study not with weed suppression in mind,

1976 1977 Best Apis Field :5–8 , ; 1999 19 Pestology et al. :643–649 .Southern JPlantNutr 91 bug control in :11–28 (1994). Pestology :8–10 (1969). 50 Agron J 23 Environ Toxicol Chem Lygus Abelomoschus esculen- :188–204 (2017). Proceedings of National , National SARE Outreach . [Online], Handbook Series 109 :388–390 (2007). . [Online]. Xerces Society for Proc Southern Nutr Assoc Res Calif Agric 20 subspecies. control by strip cutting alfalfa. UC :2482–2486 (2001). :579–587 (2015). 20 98 Lygus wileyonlinelibrary.com/journal/ps Agric Ecosyst Environ :15–17 (1994). 18 :46–47 (1998). Soil Biol Biochem 22 Apis mellifera :2101–2108 (2013). Karnataka J Agric Sci Fla Entomol 106 . National Cotton Council of America, pp. 1098–1101 Pestology :145–159 (2016). 2 Pestology 196 Environ Toxicol Chem Managing Cover Crops Profitably . :18–24 (2018). Managing Cover Crops Profitably How Neonicotinoids Can Kill Bees 62 , , Seasonal flight activity and distribution of metallic wood [L] Moench). :1901–1905 (2000). :1234–1245 (2012). :5–9 (1993). 9, 3rd edn. Sustainable AgricultureCollege Research Park, MD, & USA Education (2012, Program, 2012).Learning-Center/Books/Managing-Cover-Crops-Profitably-3rd- Available: http://www.sare.org/ Edition [9 September 2018]. perature on egg and larval development ofborer the (Coleoptera: invasive emerald Buprestidae): ash implications for laboratoryJ rearing. Econ Entomol Crops Res main driver of soilvegetable production. microbial changes during six years ofManagement organic Practices: Guide for ProducingNursery Nursery Association, Crops Atlanta, GA (2007). chronic toxicity induced by imidacloprid and its metabolites in mellifera shelters on field grownConf maple liners. pests of orchards: a review. Houston CE and Garber MJ, Agricultural Extension Service Bull AXT–241 (1967). cotton through alfalfa interplanting. a seed dresser for the control of sucking pests of cotton. (1995). 5FS™ for early-seasonCotton Council: insect Proceedings of control, theJan Beltwide in 3–7, Cotton Conference Vol. 35 pests of chilli. seedlings. 19 27 treatment against initial sucking pests of cotton. on the plant growth attributes of cotton and okra. prid toxicity in two et al. Invertebrate Conservation, Portland,www.xerces.org/neonicotinoids-and-bees OR [17 (2016). July 2018]. Available: http:// under conservation tillage: residual soil nitrate. (1999). Agriculture Extension Service Ext Bull PB576 (2015). Handbook Series Book 9. National Agricultural Library,(2007). Beltsville, MD Clover Commission, Salem, OR (2000). et al. boring beetles (Coleoptera: Buprestidae) collected in Northand Carolina Tennessee. SV, Rye cover crop effects on maize: a system-level analysis. (1999). Available:1999/1999full.cfm. http://www.cotton.org/beltwide/proceedings/ ence of seed treatment and foliarproducts spray on with growth insecticides and and seed neem tus yield in okra ( 23 Duan JJ, Watt T, Taylor P, Larson K and Lelito JP, Effects of ambient tem- 20 Brennan EB and Acosta-Martinez V, Cover cropping frequency is21 the Yeager T, Bilderback T, Fare D, Gilliam C, Lea-Cox J, Niemiera A 22 Clark A ed, 36 Suchail S, Guez D and Belzunces LP, Discrepancy between acute and 24 Fare DC, Baysal-Gurel F, Addesso KA and Oliver JB, The effects of tree 25 Bugg RL and Waddington C, Using cover26 crops to Stern manage arthropod VM, van den Bosch R, Leigh TF,27 McCutcheon Stern OD, V, Sallee Mueller WR, A, Sevacherian28 V and Mote UN, Way Datkhile RV M, and Pawar SA, A new insecticide, Imidacloprid as 30 Van Tol NB, Lentz GL, Dugger P and Richter DA, Evaluation of Adage 33 Jarande NT and Dethe MD, Imidacloprid for effective control of sucking 34 Hule SM and Dethe MD, Imidacloprid seed treatment for healthy chilli 29 Mote UN, Datkile RV and Loage GR, Efficacy of imidacloprid as seed 32 Preetha G and Stanley J, Influence of neonicotinoid insecticides 35 Suchail S, Guez D and Belzunces LP, Characteristics of imidaclo- 37 Hopwood J, Code A, Vaughan M, Biddinger D, Shepherd M, Black SH 38 Kessavalou A and Walters DT, Winter rye cover crop following soybean 15 Shelby PP, Wheat production in Tennessee. The University of Tennessee 16 Clark A, 17 Ball, DM and Lacefield18 GD, Crimson Klingeman WE, clover. Hansen JA, Circular Basham JP, 00–1. Oliver JB, Oregon Youssef NN, Swink W 19 Martinez-Feria RA, Dietzel R, Liebman M, Helmers MJ and Archontoulis 31 Praveen KS, Sajjan AS, Patil RK, Dharmatti PR and Kurdikeri MB, Influ- . Weed Sci :112–119 :326–330 1 HortScience Great Lakes 69 :135–149 (2010). :1586–1595 (1993). 28 USDA Farmer’s Bull 57 Chrysobothris femorata Chrysobothris femorata :1–26 (2007). Pest Manag Sci J Econ Entomol 1652 J Environ Hort Horn). Soil Sci Soc Am J ) species, hybrids and cultivars to six Zootaxa Fab.) and the Pacific flatheaded apple Acer :B1–B4 (2013). 4 ) straw mulch level on weed-control. : 1971–1978 © 2019 Society of Chemical Industry :18–22 (1988). 75 6 Chrysobothris mali :8 (2011). 2019; 44 :1–15 (1919). , Evaluation of a single application of neonicotinoid and multi- Field Guide to the Jewel Beetles of Northeastern North America :600–603 (2000). :110–114 (1986). Chrysobothris femorata Triticum aestivum 1065 (Olivier, 1790) species group from(Coleoptera : North Buprestidae). America, north of Mexico tree borer ( (1919). SA, Canadian Food Inspection Agency, Ottawa (2012). management of maple tree pests in nurseries andJ urban Integr landscapes. Pest Manage (Olivier). Oklahoma AgriculturalStillwater, OK Experiment (1942). Station Bull B–259, susceptibility of maple ( records of NorthEntomol American Buprestidae (Coleoptera). (Coleoptera: Buprestidae) in nursery-grown redof maples: phenology emergence, treatmentJ timing, Environ Hort and response to stressed trees. et al. application contact insecticides forin flatheaded field borer grown red management maple cultivars. species of Buprestidaewood (Coleoptera) boring and insectUnited States. Sesiidae families PhD dissertation, occurring (Lepidoptera) (2010). University across of Tennessee, the Knoxville southeastern ( arthropod pests of production nurseries. (2012). use in vegetable production systems35 in North Carolina. ( 34 water infiltration and storage. 1 Brooks FE, The flat-headed apple-tree borer. 2 Wellso SG and Manley GV, A revision of the 8 Paiero SM, Jackson MD, Jewiss-Gaines A, Kimoto T, Gill BD and Marshall 9 Frank SD, Klingeman WE III, White SA and Fulcher A, Biology, injury, and 3 Hansen JA, Petrice TR and Haack RA, New state distribution and host 5 Oliver JB, Fare DC, Youssef N, Scholl SS,6 Reding ME, Hansen J, Ranger Identification CM and phylogenetic characterization of select 4 Potter DA, Timmons GM and Gordon FC, Flatheaded apple tree borer 7 Burke HE, Biological notes on the flatheaded apple tree borer Pest Manag Sci REFERENCES SUPPORTING INFORMATION Supporting information may be found inarticle. the online version of this ACKNOWLEDGEMENTS We thank Mrwith Benji us on Moore this at project.Matt We Moore thank Brown, Nadeer Nursery Josh Youssef, Manoj forand Basham, Pandey, Garrett collaborating Roper Debbie for Eskandarnia, assistance withwas Megan data collection. funded Patton This project inEvans-Allen (1007887). part by Southern SARE (OS14-084) and NIFA Cover crop for flatheaded appletree borer managementmoisture competition. Traditionally, field-grown nurserythe crops southeastern in United States are notwas grown the under irrigation, case as intransplanted trees this is known study. to have a However, positive effect regularcould on growth irrigation greatly and reduce of the newly study. impact The of knowledge cover gained crops fromevaluations observed this of study in cover will this crops support asornamental future production. a pest management www.soci.org tool in woody 11 Seagraves BL, Redmond CT and Potter DA, Relative resistance or 10 Fenton FA, The flatheaded apple tree borer ( 12 Creamer NG and Baldwin KR, An evaluation of summer cover crops for 13 Crutchfield DA, Wicks GA and Burnside OC,14 Effect of Dao winter-wheat TH, Tillage and winter-wheat residue management effects on Asp et al. Ann Rev HortScience : 1971–1978 Developments . 75 (in press). 2019; :1040–1043 (1997). 32 Fla Entomol HortScience Pest Manag Sci Triticale: Today and Tomorrow , ed. by Guedes-Pinto H, Darvey N and Carnide :9–14 (2003). :410–413 (1996). :57–64 (2015). 13 31 :545–570 (1997). 129 28 :814–815 (1998). Hort Technol cereal rye and wheat, in cropping on non-targetnursery production. arthropod Master’s thesis, pests of red maple trees in nisms of weed suppression in cover crop-basedHortScience production systems. by cover crops grown as livingAppl mulches Biol in perennial fruit crops. Ecol Syst establishment of heart-of-palm plantations33 in Hawaii. growth in first-year vineyards. in Plant Breeding: Vol. 5 VP. Springer, Dordrecht, pp. 749–750 (1996). tree production systems. Master thesis,Nashville, Tennessee TN State (2017). University, 50 Altland JE, Gilliam CH and Wehtje51 G, Weed Lemerle control D in and field Cooper nurseries. K, Comparative weed suppression by triticale, 49 Dawadi S, Oliver JB, O’Neal PA and Addesso KA, Impact of cover 47 Creamer NG, Bennett MA, Stinner BR, Cardina J and Regnier EE, Mecha- 48 Tzortzi M, Roberts H, Tatnell LV and Atwood J, The suppression of weeds 54 Clement CR and DeFrank J, The use55 of Bordelon ground BP and covers Weller SC, Pre-plant during cover crops the affect weed and vine 52 Dawadi S, Cover crop usage for53 pest Casper management BB in and Jackson red RB, maple Plant competition underground. , et al. Agron J www.soci.org S Dawadi :475–479 :264–270 9 231 © 2019 Society of Chemical Industry :42–48 (2001). 1 :952–960 (2000). JProdAgric 84 Commun Soil Sci Plant Anal Sci World J :322–332 (2005). Agric Ecosys Environ 97 Plant Dis Agron J :1221–1250 (2001). :594–602 (2002). cover crops togan recycle State nitrogen University and(2001). Extension protect Bulletin groundwater. E–2763, Michi- East Lansing, MI lessons from Malawi and Michigan. to improve soil32 and water quality. following tillage, cover cropping, and94 nitrogen fertilization. Evaluating cover crops forcropping benefits, system costs niches. and performance within (2016). ization and cover crops onpathogens populations in western of Oregon. selected soilborne plant foraging activity offacilitate weed omnivorous biological control. predators in seed patches and in sustainable agricultural systems. (1996). wileyonlinelibrary.com/journal/ps 39 Kinyangi JM, Smucker AJ, Mutch DR and Harwood RR,40 Managing Snapp S, Borden H and Rohrbach D, Improving nitrogen efficiency: 41 Dabney SM, Delgado JA and Reeves DW, Using winter cover crops 42 Sainju UM, Singh BP and Yaffa S, Soil organic matter and tomato43 yield Snapp SS, Swinton SM, Labarta R, Mutch D, Black JR, Leep R 45 Pinkerton JN, Ivors KL, Miller ML and Moore LW, Effect of soil solar- 44 Blubaugh CK, Hagler JR, Machtley SA and Kaplan I, Cover crops increase 46 Teasdale JR, Contribution of cover crops to weed management

1978