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1 Biologil Control 56 (211) Contents lists ville t SieneDiret Biologil Control journl homepge: Evlution of herivore-indued plnt voltiles for monitoring green lewings in Wshington pple orhrds Vinent P. Jones,, Shwn A. Steffn, Nik G. Wimn, Dvid R. Horton, Eugene Milizky, Qing-He Zhng, Cllie C. Bker Deprtment of Entomology, Tree Fruit Reserh nd Extension Center, Wshington Stte University, 11 N. Western Ave., Wenthee, WA 9881, United Sttes USDA-ARS, Ykim Agriulturl Reserh Lortory, 523 Konnow Pss Rod, Wpto, WA 98951, United Sttes Sterling Interntionl In., 388 N. Sullivn Rd., Bldg 16BV, Spokne, WA , United Sttes rtile info strt Artile history: Reeived 17 June 21 Aepted 6 Otoer 21 Aville online 14 Otoer 21 Keywords: HIPV Squlene Methyl sliylte Iridodil Chrysop nigriornis Chrysop oult Chrysoperl plorund We evluted five herivore-indued plnt voltiles plus mle-produed pheromone s ttrtnts for dult green lewings in Wshington pple orhrds in 28. We found t lest five ttrtnts or omintions of ttrtnts were ttrtive to the three most undnt green lewing speies in our trils. Chrysop nigriornis nd Chrysop oult were ttrted to the omintion of methyl sliylte nd iridodil with iridodil lone eing the seond est ttrtnt. Chrysoperl plorund ws found in lower numers thn C. nigriornis nd C. oult, ut did exhiit signifint ttrtion to enzldehyde. In mid-summer, we dded the herivore-indued plnt voltile squlene to the study nd found it to e exeedingly ttrtive, ut only to mle C. nigriornis. Whether lone or in omintion, squlene ttrted 4 5-fold more C. nigriornis thn ny other ompound tested. Our dt hve reveled C. nigriornis to e n undnt orhrd predtor tht n e redily monitored with squlene-ited trps. Despite the ovious promise of HIPVs in iologil ontrol progrms, we urge ution in their deployment s lrge-sle ttrtnts, t lest until further studies hve investigted potentil disruption of nturl enemy popultion dynmis. Ó 21 Elsevier In. All rights reserved. 1. Introdution While sex pheromone sed monitoring progrms for key pests in griulture or forest environments hs een ommon for dedes, the disovery nd use of prtil ttrtnts for monitoring nturl enemies hs een slower proess tht hs foused on plnt voltiles indued y herivore feeding (known s herivore-indued plnt voltiles or HIPVs). Most of these ompounds were disovered y hemil eologists who ompred voltile profiles relesed y herivore-dmged plnts to those of undmged ontrol plnts; speifi omintions of voltiles were then ssyed in ehviorl studies to determine tivity (Dike et l., 23; Turlings et l., 1998). The literture on HIPVs shows tht the eologil roles nd ehviorl intertions medited y them is onsiderly roder nd more omplex thn those medited y sex pheromones lone (see reviews y Pré nd Tumlinson (1999) nd Vet nd Dike (1992)). Studies of HIPVs in griulturl systems hve reently inresed in numer, with the gol of using them s tools to indue host plnt resistne nd/or to onentrte nturl enemies in res for purposes of iologil ontrol (Gurr nd Kvedrs, 21; Khn et l., Corresponding uthor. Fx: E-mil ddress: vpjones@wsu.edu (V.P. Jones). 28). Most studies hve een preliminry steps towrds field pplition, either y piring prtiulr voltile (or mixture of them) with trp to determine the types of nturl enemies ttrted, or y testing individul HIPVs in smll plots to evlute effets on nturl enemy diversity nd undne (Jmes, 25; Lee, 21). These pprohes hve een used to evlute HIPVs s ttrtnts in hops (Jmes, 23,, 25; Jmes nd Prie, 24), grpes (Jmes nd Prie, 24), otton (Willims et l., 28; Yu et l., 28), per (Sutrenu et l., 1997), herry (Toth et l., 29), orn nd sorghum (Khn et l., 28), nd strwerry (Lee, 21). From these studies nd others, it is pprent tht green lewings (Neuropter: Chrysopide) s group respond to lrge numer of HIPVs, ut two ttrtnts generlly stnd out in the reent literture. The first is the HIPV methyl sliylte (MS), whih is onsidered to e ttrtive to wide rnge of other nturl enemies (Jmes, 23, 25, 26). The seond ompound is iridodil, whih is mle-produed mle ggregtion pheromone for ertin lewing speies. Iridodil hs een reported to ttrt (t vrious levels) severl lewing speies inluding Chrysop oult Sy, Chrysop nigriornis Burmeister, Chrysop olordensis Bnks, Chrysop qundripuntnt Burmeister, nd Chrysop septempuntt Wesmel (Chuhn et l., 27, 24; Zhng et l., 24, 26,). Another powerful lewing ttrtnt ws identlly disovered in erly summer 27 when one of us (NGW) evluted /$ - see front mtter Ó 21 Elsevier In. All rights reserved. doi:1.116/j.ioontrol
2 V.P. Jones et l. / Biologil Control 56 (211) severl HIPVs s possile ttrtnts for dult thinid prsitoids of oliquended lefroller, Choristoneur rosen (Hrris) (Lepidopter: Tortriide). In those evlutions, squlene-ited trps were found to e highly ttrtive to the lewing C. nigriornis (NGW, unpulished). The hoie of squlene in this initil sreening ws prompted y the work of Dutton et l. (22, 2), who showed tht the hemil ws relesed from golden deliious pples s the fruit ws fed upon y the lefminer, Phyllonoryter pomonell Zeller (Lepidopter: Grillriide), nd showed lso tht the hemil ttrted the lefminer prsitoid Pholetesor iolor Ness (Hymenopter: Bronide). Squlene ws provided to Curtiss (28) (y NGW), who further evluted it s n ttrtnt in eologil studies of the movement of nturl enemies into pple nd per orhrds. Curtiss s studies showed the potentil of the ttrtnt s monitoring tool nd ompred squlene to MS nd omintion of MS + squlene. His results lerly showed tht MS y itself hd limited ttrtion for C. nigriornis ompred to either squlene y itself or the omintion of MS + squlene. Our studies were designed to evlute severl promising HIPVs, the lewing pheromone iridodil, nd squlene s tools for monitoring undne, diversity, nd phenology of lewings in tree fruits. This fous ws hosen s wy to expnd our understnding of the eologil role of the different nturl enemy speies nd to enhne iologil ontrol through onservtion nd potentilly sptil mnipultion of nturl enemy popultions. 2. Mterils nd methods 2.1. Lure onstrution We exmined effiy nd relese rtes for six hemils (Tle 1). The produts were seleted on the sis of literture ounts suggesting tht eh might hve some ttrtive properties to some nturl enemies. Lures were onstruted using 5 m wide polyethylene tuing (PE) tht were either.16 or.152 mm thik (Assoited Bg Compny, Milwukee, WI). We exmined two types of wiking mteril, either 4 4 m piee of polyester felt (Kunin Group, Hmpton, NH), or single 3.8 m long dentl wik (lrge size 12.5 mm di.; Ptterson Dentl, St. Pul, MN). Wik hoie ws sed on the totl volume of ttrtnt needed for lure longevity; dentl wiks provided greter pity to sor ttrtnts thn the felt mteril, ut the felt provided greter surfe re for relese of voltiles t low volumes. Tuing length ws 5 m in length for lures ontining the felt wiks nd 7.5 m in length for lures ontining dentl wiks. To onstrut the lures, we first het-seled one setion of tuing t one end to rete smll g. We dded wik to the g, then dispensed single ttrtnt on eh wik t these rtes:.5 ml per dispenser for enzldehyde; 4 mg for iridodil; nd 2 ml for ll other mterils. After the ttrtnt ws dispensed, the g ws het-seled t the open end. If omintions of ttrtnts were to e used, the individul ttrtnts were eh pled in its own lure, nd multiple lures were pled in eh trp. We used white plsti delt trps (Tréé, In.; Adir, OK) to pture lewings tht pprohed the lures. The finl size of the ttrtnt-ontining setion of the lure lures; the 1.5 m exess (i.e., unseled) portion of the tuing ws used to tth the lure to the delt trp. One onstruted, lures were stored in impermele het seled metlized rrier pouhes (Assoited Bg Compny, Milwukee, WI) nd frozen t 2 C until use. Control lures were onstruted the sme wy, ut inluded distilled wter in ple of ttrtnt Evlution of lure relese rtes Relese rtes for lures dispensing enzldehyde, is-3-hexene- 1-ol, is-3-hexenyl ette, MS, squlene, nd iridodil were determined for 3 4 weeks under field onditions. Lures were pled inside delt trps, nd trps were pled in the nopy of lrge ( m tll) pple trees in n orhrd t the Wshington Stte University Tree Fruit Reserh nd Extension Center in Wenthee, WA. Lures were periodilly rought into the lortory, weighed with n Ohus Pioneer nlytil lne (.1 mg ury) (Pine Brooke, NJ) nd returned to the field. Tests were run during the erly spring (16 My to 13 June), summer (3 July to 27 August) nd fll (3 Otoer to 17 Otoer) of 28. We used four pkets per lure/ttrtnt omintion nd lulted verge weight loss per dy over period extending to 28 d. If umultive weight loss of lure leveled out efore the full 28 d hd elpsed, we onsidered the lure to e depleted t the time the hnge ourred. We used liner regression to determine the reltionship etween umultive weight loss nd time; the slope of the regression provides n estimte the men dily relese rte. The longevity of the lure ws lulted y dividing the totl ttrtnt weight y the verge weight loss per dy Long-term omprison of different ttrtnts The 28 field studies were onduted using rndomized lok design with the lures tested, orhrd lotions, test durtions, nd lure replement intervls shown in Tle 1. We hd four loks per orhrd. Within eh lok, trps were seprted y minimum of 2 m; djent loks were seprted y t lest 4 m. Tretments were rndomly lloted mong trp lotions within loks. Trps were pled m high in the tree nopy Tle 1 Lures evluted for lewing ttrtion during summer 28 in Centrl Wshington pple orhrds. Attrtnts Soure Replement intervl (weeks) Quiny WSU-Sunrise Moxee Wenthee Vlley College is-3 Hexenyl ette Sigm Aldrih W My 9 Otoer 8 My 7 Otoer 28 My 1 Otoer 9 My 7 Otoer Benzldehyde Sigm Aldrih My 9 Otoer 8 My 7 Otoer 28 My 1 Otoer 9 My 7 Otoer is-3-hexen1-ol Sigm Aldrih W My 9 Otoer 8 My 7 Otoer 28 My 1 Otoer 9 My 7 Otoer Iridodil (IR) Sterling Interntionl 4 8 My 9 Otoer 8 My 7 Otoer 28 My 1 Otoer 9 My 7 Otoer Methyl sliylte (MS) Sterling Interntionl 4 8 My 9 Otoer 8 My 7 Otoer 28 My 1 Otoer 9 My 7 Otoer MS + IR Sterling Interntionl 8 My 9 Otoer 8 My 7 Otoer 28 My 1 Otoer 9 My 7 Otoer Squlene (SQ) Sigm Aldrih S July 9 Otoer SQ + MS 18 July 9 Otoer 17 July 7 Otoer SQ + IR 17 July 7 Otoer SQ + IR + MS 18 July 9 Otoer Control 8 My 9 Otoer 8 My 7 Otoer 28 My 1 Otoer 9 My 7 Otoer Orhrd size (h) Attrtnt omintions used seprte lures of the sme omposition nd soure s the single omponent lures. All lures were mde of.16 mm thik polyethylene tuing nd used felt wiks s desried in Setion 2.
3 1 V.P. Jones et l. / Biologil Control 56 (211) (generlly in the top third of the nopy). The trps were rotted weekly to redue lotion effets. During eh rottion of the trps, the trps were moved to trees offset from trees previously ontining lure. This rottion minimizes hnes tht ontmintion of tree (or indution of HIPVs) used y the presene of n erlier lure would ffet susequent lure performne. Eh experiment ws dismntled nd ompletely re-rndomized monthly. Trp liners were removed eh time the trps were heked, overed with srn wrp (S.C. Johnson & Son, In., Rine, WI), mrked with lotion, lok nd lure type, nd pled in freezer until lewings were identified nd ounted. Trils were done t four orhrds loted in entrl nd northentrl Wshington Stte: Moxee, Quiny, the Wshington Stte University Sunrise Orhrd (WSU- Sunrise) ner Rok Islnd, nd the Wenthee Vlley College (WVC) orhrd in Est Wenthee. All of the orhrds were used to evlute the sme seven lures or omintion of lures (Tle 1). Trps t the Moxee orhrd were heked weekly, nd trps t the other three lotions were heked twie weekly. Attrtnts tht ught <2 lewings t eh lotion over the entire tril durtion were exluded from sttistil nlysis. We lso eliminted ttrtnts tht hd trp th tht ws less thn one-hlf of the ontrol trps t prtiulr orhrd. We ensored the dt euse we were interested only in iologilly tive mterils. For exmple, t the Moxee orhrd (heked only one week), we monitored 76 trps (4 reps 19 weeks) over the seson. Thus, totl of 2 lewings olleted over the durtion of seson provided n verge of.26 lewings per week, well elow ounts tht would llow the ttrtnt to e used s monitoring tool. Even with this ensoring, some of the remining ttrtnts were only wekly ttrtive. To overome this prolem, we nlyzed lewing numers olleted per trp summed ross the entire trpping period, rther thn weekly ounts. Normlity nd homogeneity of vrine ws ssessed in eh nlysis. When deprtures from ssumptions ourred, we trnsformed the dt (typilly using log e(x +.5)); if trnsformtion filed to improve deprtures from normlity nd heterogeneity, we performed ANOVA on the rnks of the dt. All post ho tests used Tukey s HSD test to seprte tretment mens (Anonymous, 29). Mens were trnsformed k into the originl units for presenttion Mid-seson squlene omprisons The WSU-Sunrise nd the Quiny loks were lrge enough to test severl squlene-sed ttrtnts. These tests egn in mid- July (Tle 1), one trps egn to onsistently ollet lewings. Squlene-sed ttrtnts were ompred to the est performing mterils of the long-term study, evluted speifilly over the period tht the squlene-sed lures were present (i.e., 17 July to 7 Otoer t the WSU-Sunrise orhrd nd 18 July to 9 Otoer t the Quiny orhrd; Tle 1). Dt nlysis ws s desried ove (Setion 2.3) Effet of squlene lure ge nd wik type on trp ptures The longevity of the squlene lures ws tested y ging lures in n orhrd loted in Quiny, WA. Lures were ged 1, 8, 15, 22, nd 29 d efore testing them for ttrtiveness. We tested oth felt nd dentl wik dispensers (Setion 2.1). All wiks were pled in.16 mm thik PE tuing using the methods desried previously. Trps were heked every 3 4 d from 7 August to 19 August 29. Dt were nlyzed in two wys. First, we used two-wy AN- OVA to evlute the min effets of wik type, ge of lure, nd the intertion of lure ge wik type for the first smpling period nd the lst smple periods. For the seond nlysis, we oded eh lure y its reltive ge so tht 1 ws the youngest lure, 2 the next youngest, to the oldest lure. We then used three-wy ANOVA nd evluted the min effets of wik type, dte smpled, reltive lure ge nd ll the two nd three wy intertions Effet of squlene relese rte on trp ptures The relese rtes of the lures re generlly funtion of the PE tuing thikness nd the surfe re of the tuing tht houses the wik. To redue the relese rte elow tht otined with.152 mm PE tuing (the thikest ville), we onstruted pouh omposed of the.152 mm memrne het-seled long one side to n impermele metlized rrier mteril (desried in Setion 2.1). This onstrution resulted in relese re of 5% smller thn provided y n unltered pouh. To otin even lower relese rtes, we onstruted lures using the metlized rrier enompssing smll windows of PE tuing, het-seled together. We were unle to estimte relese rtes of the squlene lures grvimetrilly, s weight loss ws insignifint. Thus, to indiretly evlute relese rtes for squlene, we onduted field iossys using the different lure onstrutions. The first tril ws run from 29 June to 24 July 29 nd onsisted of five tretments: stndrd.16 mm thik PE lure with 1 ml of squlene,.152 mm thik PE tuing + foil lure, nd grey hlo utyl ruer sept (West Phrmeutil Servies, Lionville, PA) dosed with either 1, 1, or 1 ll of squlene diluted in n equl volume of hexne. The sept were pled in fume hood for 7 d to llow the squlene to e sored ompletely into the sept. The seond tril ws done from 24 July to 19 August 29 nd inluded the sme first two lure formultions, ut with the sept repled y foil lures hving.16 mm thik PE window tht ws.5, 1., or 1.5 m wide y 3.8 m long; ll lures hd 1 ml of squlene dded. The lures were pled in n orhrd in Quiny, WA using the field protools disussed Setion Seletivity of ttrtnts Seletivity of the ttrtnts ws evluted y determining the reltive undne of eh speies ssoited with eh ttrtnt, lulted s perentge of the totl lewing pture omposed of eh speies. The dt were olleted s prt of the experiments in Setions 2.3 nd 2.4. We did not test if there were differenes in the proportion of the three different lewing speies ptured etween ttrtnts euse we do not hve urte estimtes of the reltive undne of eh speies tht ws independent of the ttrtnt trps. Insted, we were interested in the reltive seletivity of the different ttrtnts t eh lotion Sex rtio of C. nigriornis ttrted to squlene-ited trps We lso exmined the sex rtio of C. nigriornis ught in the squlene trps in 28. We determined sex of 2119 lewings on totl of 2 trps olleted 13 June to 28 August t n orhrd in the Quiny re. Trpping protools (trp height, sping, serviing methods) were the sme s those desried for experiments in Setion 2.3. In 29, we expnded this study to evlute sex rtio of lewings ught on trps in whih squlene or the mixture of MS + squlene were used s ttrtnts. This tril ws done to ssess whether sex rtio hnged with ddition of MS to squlene. We smpled ommeril orhrd in the Quiny re from 31 July to 28 August nd determined the sex in 4195 speimens (1959 from the squlene trps, 2154 from the MS + squlene trps). Trpping protools were the sme s desried in Setion 2.3.
4 V.P. Jones et l. / Biologil Control 56 (211) Tle 2 Relese rtes of vrious ttrtnts determined y weight loss over time in the field t different times in 28. Attrtnt PE tuing thikness (mm) Lure lod (ml) Spring Summer Fll Relese rte (mg/dy ± SEM) Longevity (d) Relese rte (mg/dy ± SEM) Longevity (d) Relese rte (mg/dy ± SEM) Benzldehyde ± ± ± ± ± ± is-3-hexene-1-ol ±.2 >5 12. ±.4 >5 nt nt ±.1 >5 9.6 ±.3 >5 nt nt is-3-hexenyl ette ± < ± ± < ± Methyl sliylte ± ± ± nt nt ± ±.9 >5 Men temperture ( C ± SD) 17.6 ± ± ± 2.7 Period 16 My 13 June 3 July 27 August 3 Otoer 17 Otoer Amount of ttrtnt in lure/relese rte; longevities >5 d not reported. Not tested during this period. Lure ws ompletely depleted t first hek intervl. Longevity (d) 2.9. Lewing identifition Lewings were identified using the keys in Brooks (1994), Brooks nd Brnrd (199), nd Penny et l. (2). Representtive speimens hve een stored s vouhers in 7% ETOH t the WSU- Behvior nd Eology l in Wenthee, WA. 3. Results 3.1. Lure relese rtes Tests with the iridodil nd squlene lures did not show suffiient weight loss to lulte relese rtes. However, for the remining lures the relese rte of eh ttrtnt ws liner until depleted. The relese rtes were typilly highest in the summer, followed y the spring, nd then the fll, most likely euse of the different temperture profiles during those periods (Tle 2). The is-3-hexene-1-ol lures hd longevities >1 month t oth g thiknesses nd overll testing periods, so tht relese rtes ould e redily ontrolled. Benzldehyde is proly the most prolemtil of the lures, euse it underwent slow hnge from liquid to rystlline form strting 5 7 d fter plement of lures in the field; t tht point, the relese rtes lowered drmtilly. This hnge in stte used us to reple those lures t 1-week intervls throughout our experiments. Inresing the volume or lure thikness did not seem to ffet the rte of rystlliztion (dt not shown). The is-3 hexenyl ette lure relesed very quikly, espeilly during the summer when the lures were found to e depleted the first time they were heked (3 4 d old). During the fll nd spring,.152 mm thik lures of is-3-hexenyl ette hd longevities of 19 d (spring) nd 34.4 (fll). Relese rtes y the MS lures were fold higher in summer thn spring nd fll (Tle 2) Long-term omprison of different ttrtnts Speies omposition of lewings on trps vried mong orhrds. C. nigriornis ws esily the most undnt lewing speies Tle 3 Totl numer of green lewings ught t four orhrds with seven different ttrtnts during summer 28. Lotion C. oult C. nigriornis C. plorund Moxee Sunrise Quiny Wenthee Vlley College ptured t the three orhrds in north-entrl Wshington nd ounted for 85%, 72%, nd 87% of the totl lewings t the Sunrise, Quiny, nd WVC sites, respetively (Tle 3). At the Moxee site, C. oult omprised 56% nd C. nigriornis 4% of the ptures. At the other three orhrds, C. oult ws the seond most ommon speies t WVC nd Quiny nd roughly equl in numers to Chrysoperl plorund (Fith) t the WSU-Sunrise orhrd. C. plorund ws ught in numers only t the WSU- Sunrise nd Quiny orhrds (Tle 3). The ttrtnts is-3 hexenyl ette, enzldehyde, nd is-3- hexen-1-ol ught only 16 C. oult summed over ll sites, thus these ompounds were dropped from further nlysis for this speies. The lrgest numers of ptures ourred in the iridodil (619 lewings) nd MS + iridodil (1252 lewings) tretments. MS y itself ppered to e nerly intive with only 32 C. oult ught over the trpping periods in the four orhrds. We nlyzed sttistilly the iridodil, MS + iridodil, MS, nd wter tretments to evlute the effets of ll possile omintions of MS nd iridodil lures (Fig. 1A). The dt were highly nonnorml euse of the low trp thes in the wter nd MS tretments nd ould not e trnsformed, so tht we used the rnked ANOVA. In ll four orhrds, the ttrtnt effet ws highly signifint, with the numer ptured lwys MS + iridodil > iridodil > MS > wter. In three of the orhrds, ll mterils were sttistilly different from eh other. In the fourth orhrd (Quiny), the MS nd wter tretments were not signifintly different (Fig. 1A). Numers of C. nigriornis olleted in the is-3-hexen-1-ol or enzldehyde ited trps were very low, thus these ompounds were dropped from sttistil nlysis. The MS + iridodil tretment ws gin the est numerilly t ll lotions, ut ws sttistilly etter thn iridodil in only one orhrd nd etter thn MS in only three of the four orhrds (Fig. 1B). MS y itself nd is- 3 hexenyl ette were sttistilly etter thn the ontrol in one orhrd eh. The low numers of C. plorund on trps mde it diffiult to evlute the ttrtnts (Fig. 1C). We found enzldehyde hd the highest numer of ptures in ll four orhrds, with MS, MS + iridodil, nd the ontrols following (Fig. 1C). At the Sunrise orhrd the enzldehyde tretment ws sttistilly etter thn the MS nd MS + iridodil tretments. At the other lotions, MS ws generlly the seond est mteril nd ws not sttistilly different thn the enzldehyde tretment Mid-seson squlene omprisons Squlene + MS nd squlene + iridodil were dded to the Sunrise orhrd on 17 July 28 nd squlene, squlene + MS,
5 12 V.P. Jones et l. / Biologil Control 56 (211) Men No. C. oult per Trp Men No. C. nigriornis per Trp Men No. C. plorund per Trp A d B C d d d Control MS Iridodil MS+Iridodil d Control MS Iridodil MS+Iridodil 3-hexenyl ette Moxee Sunrise Quiny WVC Lotion Control MS MS+iridodil enzldehyde Men No. C. nigriornis per Trp Dy SQ + MS SQ + IR MS+IR SQ + MS Squlene SQ+MS+IR MS+IR Attrtnt Fig. 2. Men pture per trp dy of C. nigriornis from mid-july to erly Otoer 28 for the est non-squlene ttrtnt nd those ontining squlene t (A) WSU-Sunrise nd (B) Quiny. SQ, squlene; MS, methyl sliylte; nd IR, iridodil. Brs with the sme letters indite signifint differenes within lotion ording to ANOVA sed on rnks nd Tukey s HSD test A B A Fig. 1. Long-term ttrtnt evlutions t four different orhrds in Wshington during 28. (A) Chrysop oult, (B) Chrysop nigriornis, nd (C) Chrysoperl plorund. Numers re men ptures per trp over the entire trpping period. Letters indite signifint differenes within lotion ording to ANOVA sed on rnks nd Tukey s HSD test. nd squlene + iridodil + MS were dded to the Quiny orhrd on 18 July 28. Evlution of the men trp th from those periods to the end of the seson t eh orhrd lerly demonstrted tht squlene ws extremely ttrtive to C. nigriornis either lone or when found in omintion with MS or iridodil (Fig. 2A nd B). At the Sunrise orhrd, we ught n verge of 1.4 nd 23.5 C. nigriornis per trp dy, respetively, for squlene + iridodil nd squlene + MS over the 82 d the trps were in the field. At the Quiny orhrd, we ught n verge of 8., 7.6, nd 8.6 C. nigriornis per trp dy, respetively, for the squlene, squlene + MS, nd squlene + iridodil + MS lures over the 83 d trps were in the field. Men No. C. nigriornis per Trp Dy mm PE g.152 mm + foil lure sept 1 ul sept 1 ul sept 1 ul d B 3.4. Effet of squlene lure ge nd lure type The nlysis on the first smpling intervl showed no signifint differenes ourred y wik type (p =.9, df = 1, 3), lure ge (p =.11, df = 4, 3) or the intertion of wik type lure ge (p =.17, df = 4, 3). The lst smpling intervl showed similr trends with no signifint differenes found in ny of the three f-.16 mm PE g.152 mm + foil lure.5 m PE window Lure Evluted 1. m PE window 1.5 m PE window Fig. 3. Effet of different lure types on trp th of C. nigriornis during summer 29. (A) 1 July to 24 July. (B) 24 July to 19 August. Brs with the sme letters indite no signifint differenes ording to ANOVA nd Tukey s HSD test.
6 V.P. Jones et l. / Biologil Control 56 (211) tors tested. Anlysis on the entire dt set showed tht the only signifint effet ws the smpling dte (p <.1, df = 4, 15). Thus over the entire ourse of the experiment, lure ge out to 44 d did not ffet trp pture nd there were no signifint differenes relted to wik type Squlene dose effets The first tril showed n inresing dose response with inresing trp th s the sept lod vried from 1 to 1 ll (Fig. 3A). The 1-ll sept lod ws signifintly poorer thn the.16 mm thik PE tuing lure, ut not signifintly different thn the.152 mm PE tuing + foil lure. Although we were le to rete the 1-ll sept lures for this study, sorption required 1 week period, whih mkes this loding imprtil for nything ut experimentl purposes. The seond test showed tht trp th ould e lowered y use of foil pkets with smll windows of PE tuing dded (Fig. 3B). There were no signifint differenes etween ny of the foil g tretments, suggesting tht the esiest wy to redue lure effiieny is to use.152 mm PE tuing + foil lure, whih still ught signifint numers of C. nigriornis, ut is esier to mke thn the lures with the smller size windows Sex rtio of C. nigriornis olleted on trps ited with squlene Of the 2119 speimens of C. nigriornis olleted in 28, 237 were mle nd 82 were femle (3.3% femle). A 2 2 ontingeny tle nlysis showed tht femle nd mle distriutions were not independent (G = 1.96, df = 1, p =.1). Femles ourred only on trps tht hd lso ptured t lest four mles. In our omprisons of sex rtios on trps ited with squlene versus squlene + MS, we ptured 4 femles out of 1959 totl ptures of C. nigriornis on the squlene trps (.21%) nd 79 femles out of 2154 C. nigriornis (3.5%) on the squlene + MS ited trps. These two sex rtios were signifintly different (G =74.4, 1 df = 1, p<.1). Femles were ptured only on trps tht hd olleted minimum of 21 nd 28 mles for the squlene nd squlene + MS ited trps, respetively Seletivity of the lures for different lewings Reltive pture rtes of the three speies mong the different lures were tulted for eh lotion (Tle 4). It ws pprent tht lures ontining squlene ttrted primrily C. nigriornis (14,472 ught), with only 94 C. oult nd 18 C. plorund trpped. This result my in prt e due to the reltive size of the Tle 4 Seletivity of different ttrtnts to three lewing speies olleted in Wshington pple orhrds in summer 28. Lotion Attrtnt % C. oult % C. nigriornis % C. plorund N Moxee Quiny WSU-Sunrise Wenthee Vlley College is-3 Hexenyl ette Benzldehyde is-3-hexen-1-ol Iridodil (IR) Methyl sliylte (MS) MS + IR Control Totl 1594 is-3 Hexenyl ette Benzldehyde is-3-hexen-1-ol... IR MS MS + IR Squlene (SQ) SQ + MS SQ + MS + IR Control Totl 1,135 is-3 Hexenyl ette Benzldehyde is-3-hexen-1-ol IR MS MS + iridodil SQ + IR SQ + MS Control Totl 827 is-3 Hexenyl ette Benzldehyde is-3-hexen-1-ol IR MS MS + IR Control Totl 2476 Grnd totl 22,232 Only out from 18 July to end of test. Only out from 17 July to end of test.
7 14 V.P. Jones et l. / Biologil Control 56 (211) different lewing popultions in eh orhrd, however, reltively lrge numers of C. oult were found in oth the iridodil nd iridodil + MS lures in these orhrds. Thus, it ppers tht squlene hs limited ttrtion to C. oult unless it ws mixed with iridodil. Iridodil ttrted reltively high numers of C. nigriornis s well s C. oult, so tht use of iridodil long with squlene in monitoring progrm would require identifition of lewings to speies. C. plorund ws most ommonly found in the enzldehyde ontining lures. 4. Disussion Our dt show tht we n esily monitor popultions of ll three lewing speies ommon in Wshington pple orhrds. C. plorund ws ptured only in low numers in our studies, ut this my e due to numer of different ftors: the need for etter lure, different sesonl phenology (our reent tests show it emerges very erly in the seson ompred to the other two speies), differentil suseptiility to pestiides, or simply euse it is less undnt thn the other two speies. The relese rte nd longevity of the lures used for the vrious ttrtnts re key ftors tht need further reserh. It is ler tht the.16 mm thik PE tuing lure with 2 ml of is-3-hexenyl ette eme depleted during the summer well efore we hnged the lures. Thus, our lk of response to this lure should e viewed with ution. Reent studies (V.P.J. nd C.C.B., unpulished) show tht higher initil lod of the ttrtnt (3 ml) nd use of.152 mm PE tuing + foil lure ontrols relese rtes during the summer nd lsts >1 month. While we were le to regulte most of the other ompounds well, there is no gurntee tht the relese rtes we hieved were optiml for ttrting these lewing speies. Hving urte estimtes of relese rtes will e ruil for omprison of effets mong different studies nd lewing speies. Our results with MS, iridodil nd the other HIPVs mirror mny of the results reported y Zhng et l. (26). MS y itself ppered to hve no ttrtion for C. oult, nd ws only sttistilly etter thn the ontrol in one orhrd for C. nigriornis. Iridodil ws ttrtive to oth C. oult nd C. nigriornis, ut the omintion of MS + iridodil ws sttistilly more ttrtive thn either iridodil or MS lone. These results pper to onflit with other studies in Wshington Stte, where Jmes (23, 26) found MS ws ttrtive to oth C. nigriornis nd C. oult. We nnot explin the differenes other thn to note the likely differenes in relese rtes etween Jmes studies nd ours; our studies (nd those of Zhng et l. (26)) used the PE tuing lures, while Jmes studies used glss vils with otton loosely pked in the opening. Our studies showed tht squlene is highly ttrtive semiohemil tht provided nerly speies nd sex-speifi ttrtion of mle C. nigriornis. Femle C. nigriornis were never found on trps without >4 mles present, whih suggests tht the femles re eing ttrted (wekly) to the mles (either hemilly, visully, or oustilly). The use of the low femle pture my e similr to tht oserved with C. oult ttrtion to iridodil, where femles were found ttrted to the viinity of trps ut rrely entered them (Chuhn et l., 27); studies re ongoing to investigte whether femle C. nigriornis exhiits similr response to squlene-ited trps. The extreme ttrtiveness of squlene to C. nigriornis is lso notle when ompred to ny of the mterils reported for vriety of nturl enemies either in the literture or from the MS, iridodil or the omintion of MS nd iridodil in our trils. Men trp pture per trp dy esily exeeded 2 dult mle C. nigriornis over long periods of time. While the high trp pture is impressive nd provides us with n exellent tool with whih to trk C. nigriornis popultion density nd phenology, it is lso ler tht lower relese rte lures my e neessry to prevent removl of C. nigriornis in suh numers tht its popultion dynmis re ffeted. Our studies of relese rtes provide severl lure formultions tht n either redue or inrese the trp sensitivity; the longevity studies show tht ll of them were stle for t lest 44 d. Although some my see squlene s perfet ndidte for mnipulting sptil distriution of C. nigriornis in n ttempt to mximize predtion in the tree nopy, there re mny potentil pitflls with this pproh. First, if the ttrtnt is uniformly distriuted throughout the orhrd, it my redue predtor effiieny t low prey densities if C. nigriornis were no longer le to use herivore-indued squlene prodution to nrrow its serh re. This effet my tully inrese the overll prey density, resulting in greter eonomi dmge. Seondly, if femles re not ttrted t lest ner to the lotions where squlene lures re pled, then the lures my disrupt the mte finding proess, whih would redue numeril response in susequent genertions. Third, C. nigriornis ppers to e primrily found in the tree nopy (Horton et l., 29), so tht over rops re unlikely to e high-density soure tht n e used in push pull type strtegy. Thus, ssuming long-rnge ttrtion (of whih we hve no proof t this point), movement of C. nigriornis from djent loks will result in roing Peter to py Pul senrio. If the ttrtion is muh more lol, then mnipulting sptil distriution my hve prtil pplitions (if the other ojetions in this prgrph re stisfied). Our ojetions to use of squlene re primrily ginst its use s seson-long tool to onentrte C. nigriornis. We do see enefits to ggregting the popultion for shorter periods of time (e.g., 1 2 weeks) to ugment funtionl nd numeril responses to help suppress pest popultions in smll portion of the environment or to move popultions to res tht will not e sujet to pestiide tretments. Irrespetive of the use of squlene s tool to hnge sptil or temporl ggregtion in the orhrd, hving lure tht ttrts nturl enemies relily hs rod onsequenes for studies of popultion dynmis nd for implementing onservtion iologil ontrol ttis in griulturl nd forestry environments. In prtiulr, the implementtion of iologil ontrol is hindered y mny IPM onsultnts pereption tht it is ineffetive, t lest in prt euse of the ineffiieny of norml smpling methods (e.g., et trys). For exmple, we smpled five ommeril orhrds 2 3 times week using et trys from 1 Mrh to mid- Otoer 29 nd ptured only 12 dult C. nigriornis. In the sme orhrds during the sme time period, four squlene trps ptured totl of 25,64 dult C. nigriornis. The lrge numer of C. nigriornis ptured in the trps nd the ility to detet hnges in dult popultion levels efore nd fter tretment should provide powerful tool for tht will help IPM prtitioners to understnd the role of C. nigriornis in iologil ontrol nd its sensitivity to different mngement progrms. Aknowledgments The field ssistne of Teh Clement, Cmeron Aguilr, Kodi Jspers, Stey MDonld, nd Ivn Arroyo is grtefully knowledged. This reserh ws funded in prt y grnts to V.P.J. nd D.R.H. from the Wshington Stte Tree Fruit Reserh Commission nd USDA-NIFA SCRI Grnt No Referenes Anonymous, 29. JMP Sttistis nd Grphis Guide. Version 8.2. SAS Institute In., Cry, NC. Brooks, S.J., A txonomi review of the ommon green lewing genus Chrysoperl (Neuropter: Chrysopide). Bulletin British Museum (Nturl History) Entomology 63,
8 V.P. Jones et l. / Biologil Control 56 (211) Brooks, S.J., Brnrd, P.C., 199. The green lewings of the world: generi review (Neuropter: Chrysopide). Bulletin British Museum (Nturl History) Entomology 59, Chuhn, K.R., Levi, V., Zhng, Q.-H., Aldrih, J.R., 27. Femle goldeneyed lewings (Neuropter: Chrysopide) pproh ut seldom enter trps ited with the mle-produed ompound iridodil. Journl of Eonomi Entomology 1, Chuhn, K.R., Zhng, Q.-H., Aldrih, J.R., 24. Iridodils: enntiospeifi synthesis nd stereohemil ssignment of the pheromone for the golden-eyed lewing, Chrysop oult. Tetrhedron Letters 45, Curtiss III, R.T., 28. Attrtiveness of Semiohemils to Green Lewings for Biologil Control in Pome Fruit. MS Thesis. Wshington Stte University, Pullmn, 83pp. Dike, M., de Boer, J.G., Hofte, M., Roh-Grndos, M.C., 23. Mixed lends of herivore-indued plnt voltiles nd forging suess of rnivorous rthropods. Oikos 11, Dutton, A., Mttii, L., Amdo, R., Dorn, S., 22. A novel funtion of the triterpene squlene in tritrophi system. Journl of Chemil Eology 28, Dutton, A., Mttii, L., Dorn, S., 2. Plnt-derived semiohemils s ontt host lotion stimuli for prsitoid of lefminers. Journl of Chemil Eology 25, Gurr, G.M., Kvedrs, O.L., 21. Synergizing iologil ontrol: sope for sterile inset tehnique, indued plnt defenes nd ulturl tehniques to enhne nturl enemy impt. Biologil Control 52, Horton, D.R., Jones, V.P., Unruh, T.R., 29. Use of new immunomrking method to ssess movement y generlist predtors etween over rop nd tree nopy in per orhrd. Amerin Entomologist 55, Jmes, D.G., 23. Field evlution of herivore-indued plnt voltiles s ttrtnts for enefiil insets: methyl sliylte nd the green lewing, Chrysop nigriornis. Journl of Chemil Eology 29, Jmes, D.G., 23. Syntheti herivore-indued plnt voltiles s field ttrtnts for enefiil insets. Environmentl Entomology 32, Jmes, D.G., 25. Further field evlution of syntheti herivore-indued plnt voltiles s ttrtnts for enefiil insets. Journl of Chemil Eology 31, Jmes, D.G., 26. Methyl sliylte is field ttrtnt for the goldeneyed lewing, Chrysop oult. Bioontrol Siene nd Tehnology 16, Jmes, D.G., Prie, T.S., 24. Field-testing of methyl sliylte for reruitment nd retention of enefiil insets in grpes nd hops. Journl of Chemil Eology 3, Khn, Z.R., Jmes, D.G., Mideg, C.A.O., Pikett, J.A., 28. Chemil eology nd onservtion iologil ontrol. Biologil Control 45, Lee, J.C., 21. Effet of methyl sliylte-sed lures on enefiil nd pest rthropods in strwerry. Environmentl Entomology 39, Pré, P.W., Tumlinson, J.H., Plnt voltiles s defense ginst inset herivores. Plnt Physiology 121, Penny, N.D., Tuer, C.A., De Leon, T., 2. A new speies of Chrysop from Western North Ameri with key to North Amerin Speies (Neuropter: Chrysopide). Annls of the Entomologil Soiety of Ameri 93, Sutrenu, P., Drukker, B., Bruin, J., Posthumus, M.A., Selis, M.W., Voltiles from Psyll infested per trees nd their possile involvement in ttrtion of nthoorid predtors. Journl of Chemil Eology 23, Toth, M., Szentkirlyi, F., Vuts, J., Letrdi, A., Tilor, M.R., Jstd, G., Knudsen, G.K., 29. Optimiztion of phenyletldehyde sed ttrtnt for ommon green lewings (Chrysoperl rne s. l.). Journl of Chemil Eology 35, Turlings, T.C.G., Bernsoni, M.L., Bertoss, R., Bigler, F., Crloz, G., Dorn, S., The indution of voltile emissions in mize y three herivore speies with different feeding hits: possile onsequenes for their nturl enemies. Biologil Control 11, Vet, L.E.M., Dike, M., Eology of infohemil use y nturl enemies in tritrophi ontext. Annul Review of Entomology 37, Willims III, L., Rodriguez-Son, C., Cstle, S.C., Zhu, S., 28. EAG-tive herivoreindued plnt voltiles modify ehviorl responses nd host ttk y n egg prsitoid. Journl of Chemil Eology 34, Yu, H., Zhng, Y., Wu, K., Go, X.W., Guo, Y.Y., 28. Field-testing of syntheti herivore-indued plnt voltiles s ttrtnts for enefiil insets. Environmentl Entomology 37, Zhng, Q.-H., Chuhn, K.R., Ere, E.F., Vellore, A.R., Aldrih, J.R., 24. Semiohemistry of the goldeneyed lewing Chrysop oult: ttrtion of mles to mleprodued pheromone. Journl of Chemil Eology 3, Zhng, Q.-H., Shneidmiller, R.G., Hoover, D.R., Young, K., Welshons, D.O., Mrgryn, A., Aldrih, J.R., Chuhn, K.R., 26. Mle-produed pheromone of the green lewing, Chrysop nigriornis. Journl of Chemil Eology 32, Zhng, Q.-H., Sheng, M., Chen, G., Aldrih, J.R., Chuhn, K.R., 26. Iridodil: powerful ttrtnt for the green lewing Chrysop septempuntt (Neuropter: Chrysopide). Nturwissenshften 93,
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