Mating Disruption of Citrus Leafminer Mediated by a Noncompetitive Mechanism at a Remarkably Low Pheromone Release Rate

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1 J Chem Ecol (28) 34: DOI 1.17/s Mting Disruption of Citrus Lefminer Medited by Noncompetitive Mechnism t Remrkbly Low Pheromone Relese Rte L. L. Stelinski & J. R. Miller & M. E. Rogers Received: 7 Jnury 28 /Revised: 29 April 28 /Accepted: 9 My 28 /Published online: 26 June 28 # Springer Science+Business Medi, LLC 28 Abstrct The citrus lefminer, Phyllocnistis citrell Stinton (Lepidopter: Grcillriide), is worldwide pest of citrus. A seson-long investigtion ws conducted tht evluted mting disruption for this pest. Effective disruption of the mle P. citrell orienttion to pheromone trps (98%) nd reduced flush infesttion by lrve ws chieved for 221 d with two deployments of 3:1 blend of (Z,Z,E)- 7,11,13-hexdectrienl/(Z,Z)-7,11-hexdecdienl t remrkbly low rte of 1.5 g ctive ingredient (AI)/h per deployment. To gin insight into the mechnism tht medites the disruption of P. citrell, mle moth ctch ws quntified in replicted plots of citrus treted with vrying densities of pheromone dispensers. The densities of septum dispensers compred were: (/h,. g AI/h),.2 (one every fifth tree or 35/h,.5 g AI/h), 1 (215/h,.29 g AI/h), nd 5 per tree (1,1/h, 1.5 g AI/h). Profile nlysis by previously published mthemticl methods mtched predictions of noncompetitive mting disruption. Behviorl observtions of mle P. citrell in the field reveled tht mles did not pproch mting disruption dispensers in ny of the dispenser density tretments. The current report presents the first set of profile nlyses combined with direct behviorl observtions consistent with previously published theoreticl predictions for noncompetitive mechnism of mting disruption. The results suggest tht disruption of P. citrell L. L. Stelinski (*) : M. E. Rogers Entomology nd Nemtology Deprtment, Citrus Reserch nd Eduction Center, University of Florid, Lke Alfred, FL 3385, USA e-mil: stelinski@ufl.edu J. R. Miller Deprtment of Entomology, Michign Stte University, Est Lnsing, MI 48824, USA should be effective even t high popultion densities given the density-independent nture of disruption for this species nd the remrkbly low rte of pheromone per hectre required for efficcy. Keywords Phyllocnistis citrell. Mting disruption mechnisms. Desensitiztion. Cmouflge. Competitive ttrction. Citrus Introduction The citrus lefminer, Phyllocnistis citrell Stinton (Lepidopter: Grcillriide), originted from Indi (Stinton 1856) nd is mjor citrus pest throughout the world (Heppner 1993). It ws first recorded in Florid in 1993 (Heppner 1993) nd since hs spred throughout the US Gulf Cost s well s to Cliforni (Gill 1999) nd Hwii (Ngmine nd Heu 23). Although this species infests ll vrieties of citrus, s well s other Rutcee nd certin ornmentl plnts, grpefruit, tngerine, nd pumello re the preferred hosts (Legspi nd French 23). Mted femle P. citrell oviposit on host leves, nd emerging lrve tunnel within young leves to feed. Infesttions greter thn 16% lef re dmge reduce yield on Thiti lime (Peñ et l. 2). Control of the lefminer with chemicl sprys is often ineffective in Florid becuse of the prolonged nd spordic lef flush (immture leves s described by Hll nd Albrigo 27) influenced by frequent rin nd the fct tht lrve re conceled within feeding glleries. Consequently, to be effective, sprys need to be pplied biweekly (Peñ et l. 22; Rogers nd Stelinski, unpublished dt). The ssocition of P. citrell with citrus bcteril cnker, Xnthomons xonopodis pv. citri, mjor disese ffect-

2 118 J Chem Ecol (28) 34: ing citrus, is of greter importnce thn its impct s n herbivore. Infection by X. xonopodis results in defolition, premture fruit drop, nd generl decline in tree qulity (Grhm et l. 24). Although this disese is spred primrily by wind-driven rin, the serpentine-feeding glleries of P. citrell re esily colonized by the bcterium, nd the resulting cnker lesions generlly re lrger nd more infectious thn those formed without the benefit of P. citrell lef injury (Grhm et l. 24; Gottwld et l. 27). In Jpn, (Z,Z)-7,11-hexdecdienl (Z7Z11-16Ald) ws reported s the behviorlly ctive sex pheromone (Mfi et l. 25). Brzilin nd US popultions of P. citrell produce 3:1:1 mixture of (Z,Z,E)-7,11,13-hexdectrienl (Z7Z11E13-16Ald), Z7Z11-16Ald, nd (Z)-7-hexdecenl (Lel et l. 26; Moreir et l. 26). However, 3:1 blend of Z7Z11E13-16Ald/Z7Z11-16Ald is sufficient for eliciting the full complement of mle sexul behviors (Lel et l. 26; Moreir et l. 26) nd is now being exploited in mngement progrms for this pest (Lpointe et l. 26; Stelinski nd Rogers 28). Recently, two mthemticl trnsformtions of moth ctch versus dispenser density dt were developed to differentite between competitive nd noncompetitive mechnisms of mting disruption (Miller et l. 26,b). Competitive disruption occurs when mles re ttrcted to the source of synthetic pheromone, while noncompetitive mechnisms, such s cmouflge or sensory desensitiztion, by definition, do not require ttrction to the synthetic pheromone source (Miller et l. 26). If competitive ttrction occurs, then plotting 1 over mle visittion rte to given ttrctnt source ginst dispenser density (on the Y- nd X-xes, respectively, Miller Gut plot) yields stright line with positive slope, while plotting mle visittion rte to given ttrctnt source ginst dispenser density visittion rte (Miller de Lme plot) results in stright line with negtive slope (Miller et l. 26). In contrst, noncompetitive ttrction predicts chrcteristiclly concve Miller Gut plot, s well s recurved Miller de Lme plot (Miller et l. 26). Post hoc nlyses of 13 published mting disruption trils cross rnge of moth species were consistent with the hypothesis tht competitive ttrction is the mechnism tht explins the mjority of cses (Miller et l. 26b). The first objective of the current investigtion ws to evlute the potentil of using mting disruption s mngement tctic for P. citrell in Florid citrus. The second ws to gin insight into the behviorl mechnisms tht underlie disruption of this species, which my help fcilitte development of robust nd economicl mngement of P. citrell with pheromones. In ddition, the current study ws designed to test directly the predictions recently outlined by Miller et l. (26) by developing moth ctch versus dispenser density profiles while concurrently observing moth behvior in the field. Methods nd Mterils Field plots The experiment ws conducted in n 8-yr-old 1.2-h ornge grove (Citus sinensis [L.] vr. Vlenci ) in Clermont, FL, USA. Trees were plnted on 3 6-m spcing, nd the verge cnopy height ws 4 m. The grove ws mnged by the University of Florid ccording to commercil pruning, irrigtion, herbicide, nd fungicide mngement prctices but without the input of insecticides. Dispenser Density Tretments nd Experimentl Design Disruption trils were conducted by compring four ppliction densities of red rubber sept (The West Compny, Lionville, PA, USA): (/h,. g ctive ingredient [AI]/h),.2 (one every fifth tree or 35/h,.5 g AI/h), 1 (215/h,.29 g AI/h), nd 5 (1,1/h, 1.5 g AI/h) per tree loded with 1. mg of Z7Z11E13-16Ald nd.33 mg of Z7Z11-16Ald (ISCA Technologies, Riverside, CA, USA). Pheromone components were greter thn or equl to 98% pure by gs chromtogrphic nlysis. The experiment ws rrnged s rndomized complete block design with five replictes, ech consisted of 3-tree (.14 h) plot of five rows of six trees. Replicte plots were seprted by 4 m, nd blocks of tretments were seprted by 5 m. Rubber septum dispensers were ffixed to folige vi metl pper clips on the edge of tree cnopies pproximtely 2. m bove ground level, which is the loction of gretest mle P. citrell ctivity within trees pproximtely 4 m tll (Stelinski nd Rogers 28). Tretments were pplied on 4 April 27 nd renewed on 15 June 27 so tht the experiment could be conducted throughout the P. citrell sesonl flight. Orienttionl Disruption Mesurements Disruption of mle P. citrell orienttion ws quntified by using two pheromone trps (LPD Scenturion Gurdpost, Suterr, Bend, OR, USA) deployed within ech replicte plot. One trp ws plced in the centrl tree of ech plot nd the second on the inside border row two trees from the plot edge. All trps were bited with single red rubber septum lure loded with.1 mg of Z7Z11E13-16Ald nd.3 mg of Z7Z11-16Ald s this hs been shown to be highly effective for trpping mle P. citrell in Florid (Stelinski nd Rogers 28). Monitoring trps were hung t lest 1. m from the nerest mting disruption dispenser, t pproximtely m bove ground level in the midcnopy (Stelinski nd Rogers 28). Pheromone lures were replced totl of four times or pproximtely every 7.5 wk throughout the seson bsed on known longevity of ttrctiveness (Lpointe nd Lel 27). Moths cptured in trps were counted nd removed weekly. Flush Infesttion Dmge to newly flushed leves ws ssessed weekly 15 April through 28 October, 27, except during the weeks of 16 July, 6 nd 13 August, 1 nd 17

3 J Chem Ecol (28) 34: September, nd 15 October becuse of insufficient new flush on those dtes. Twenty shoots, ten from the midcnopy (2.5 m) nd ten from the lower cnopy (1. m), were inspected t rndom from 2 trees per replicte block (2, flush smples per tretment), nd the number of shoots per tree contining live mining P. citrell lrve ws recorded. Field Observtions Mle P. citrell behvior ws studied in the field to test the prediction tht mle moths pproch mting disruption dispensers in pheromone-treted plots, s other studies hve reported mle moths of vrious species orienting to, closely pproching, nd even touching pheromone dispensers of wide rnge of relese rtes in the field (Stelinski et l. 24; Epstein et l. 26). Observtions of dispensers in tree cnopies were conducted for pproximtely 2 hr ech night between 21: nd 23: hours, the period of gretest mle P. citrell response (Stelinski nd Rogers 28), on eight nights between 24 August nd 13 September nd on five subsequent nights between 27 September nd October 11. An observer rotted mong plots conducting 2 min observtionl bouts per tretment such tht multiple tretments were observed on given night. The order of observtions cross tretments ws rndomized nightly. In ddition, mle moth orienttion to pheromone trps (s described bove) ws observed for 2-hr periods on four seprte nights (14 22 September 27) in control plots to verify tht mle P. citrell could be observed orienting to n ttrctive point source in the field. The number of moths observed orienting to such trps, s well s the number cught in trps under observtion, ws ssessed. During the observtions of both dispensers nd trps, dt were dictted into hnd-held microcssette udio recorder by n investigtor stnding.75 m from the pheromone source under observtion. Observtions fter dusk employed nightvision goggles (Rigel, Model 325, DeWitt, IA, USA) s described by Stelinski et l. (24). Profile Anlyses Moth ctch vs. dispenser density dt were nlyzed ccording to the profile nlyses developed by Miller et l. (26,b). In ddition to exmining the untrnsformed dt, two types of trnsformtions were performed on mle ctch vs. dispenser density dt: (1) 1 over mle ctch per trp per night on the y-xis ws plotted ginst dispenser density on the x-xis (Miller Gut plot), nd (2) mle ctch per trp per night on the y-xis ws plotted ginst dispenser density visittion rte on the x-xis (Miller de Lme plot). Trpping Evlution of Pheromone Dispensers An experiment ws conducted to compre the lure dose used to monitor the effect of disruption tretments (.1 mg of Z7Z11E13-16Ald nd.3 mg of Z7Z11-16Ald) with the dose used to induce mting disruption (1. mg of Z7Z11E13-16Ald nd.33 mg of Z7Z11-16Ald). The objective ws to determine whether the relese rte of the pheromone from the mting disruption dispensers ws ttrctive to P. citrell in pheromone-free ir over the course of the mting disruption study. This test ws conducted on 13 April through 1 November, 27 in 4. h of untreted plots of Vlenci ornges. Fresh lures were instlled every 7.5 wk into plstic delt trps. Unbited delt trps were included s negtive control tretment. The experiment ws rrnged in rndomized complete block with five replictes. Trps, hung pproximtely m bove ground level in the upper third of the tree cnopy, were spced pproximtely 4 m prt within replictes, nd replicte blocks were spced by 6 7 m. Moths cptured in trps were counted nd removed weekly, t which time the position of trps ws rotted. Sttisticl Anlyses For orienttionl disruption nd trpping studies, dt were trnsformed to ln (x+1) (which normlized the distributions) nd then subjected to nlysis of vrince (ANOVA). Flush injury dt were rcsine trnsformed prior to ANOVA. When significnt ANOVAs were identified, differences mong mens were seprted by using the lest significnt difference (LSD) test (SAS Institute 2). In ll cses, the significnce level ws α<.5. Percent disruption ws clculted s 1 [(men moth ctch per trp in the pheromone-treted block/men moth ctch per trp in the control block)] 1. Results Moth Ctches nd Lef Infesttion Preliminry nlysis reveled no significnt difference in moth ctch between trps plced t the centers nd borders of plots. Thus, dt from the two trps per plot were combined for subsequent nlyses. Fewer (F=29.3, df=3, 16, P<.1) mle P. citrell were cptured in trps in plots treted with 1,1 dispensers per hectre (five dispensers per tree) thn in ny other tretment (Fig. 1). This highest dispenser density tretment resulted in 98% disruption of moth ctch in trps reltive to untreted control plots over the seson. There lso ws significnt reduction in mle ctch in trps plced in plots treted with 215 dispensers per hectre (69% disruption) compred with plots treted with 35 dispensers per hectre nd untreted control plots; however, there ws no difference in mle ctch between the ltter two tretments (Fig 1). There ws trend of declining infesttion with incresing dispenser density with significnt reduction (F=12.1, df=3, 16, P<.1) in infesttion of flush by both the 1,1- nd 215-dispensers-per-hectre tretments reltive to untreted plots (Fig. 1b), nd the lowest infesttion occurred

4 111 J Chem Ecol (28) 34: Men number of P. citrell mles per trp per seson b. Men percent sesonl flush infesttion by lrvl P. citrell / h 35 / h 215 / h 11 / h / h 35 / h 215 / h 11 / h Fig. 1 Men cptures of mle Phyllocnistis citrell in lure-bited delt trps in plots contining vrious densities of red septum dispensers of 3:1 blend of Z7Z11E13-16Ald nd Z7Z11-16Ald (), Men percent flush infesttion by P. citrell lrve (b). Mens followed by the sme letter re not significntly different (AVOVA followed by LSD test t α<.5) in plots treted with 1,1 dispensers per hectre. Flush infesttion in plots treted with 35 dispensers per hectre ws not significntly different from control plots. Field Observtions No mle P. citrell were observed orienting to rubber septum disruption dispensers in ny of the tretments during 26 hr of observtion. In contrst, in control plots, 17.±2.1 (men±se) mles per night (N=4 nights) were observed orienting to bited monitoring trps, nd 11.6±.9 mles were cptured. Profile Anlysis The untrnsformed plots of dispenser density (Fig. 2), s well s both secondry trnsformtion plots (Fig. 2b,c), were consistent with the predictions of mting disruption by noncompetitive mechnism. The untrnsformed plot ws initilly liner (Fig. 2), the Miller Gut plot ws concve (Fig. 2b), nd the Miller de Lme plot ws recurved (Fig. 2c). This set of trits is dignostic of noncompetitive mting disruption mechnism (Miller et l. 26). b b c c Trpping Evlution of Pheromone Dispensers In plots not under pheromone disruption, the number of mle P. citrell cptured per night in trps bited with the lower-loding monitoring lures (261.4±18.2, X±SEM) ws significntly greter (F=15.7, df=2, 8, P<.1) thn the number cptured with those bited with higher-dose mting disruption dispensers (179.3±16.9). Trps bited with both lure dosges cptured significntly more moths over the course of the seson thn blnk negtive control trps (.3±.1).. Ctch (mles/trp/night) b. 1/Ctch (mles/trp/night) c. Ctch (mles/trp/night) * ctch Fig. 2 Untrnsformed (), Miller Gut (b), nd Miller de Lme (c) plots of the disruption profile vrying pheromone dispenser density for disruption of P. citrell

5 J Chem Ecol (28) 34: Discussion Nerly complete disruption of P. citrell orienttion to femle-proxy-monitoring trps ws chieved for 221 d with only two deployments of just 1.5 g AI/h ech. This would be sufficient for the seson-long disruption of P. citrell mles in Florid. Furthermore, nerly 7% disruption ws chieved with only.25-g/h rte. The pheromone rte per hectre required for the disruption of P. citrell ws well below 75 3 g of pheromone per hectre required for effective disruption of other species such s the Orientl fruit moth, Grpholit molest (Rice nd Kirsch 199), the Europen grpe moth, Eupoecili mbiguell (Chrmillot et l. 1987), the grpe berry moth, Prlobesi viten (Trimble et l. 1991), nd the codling moth, Cydi pomonell (Howell et l. 1992). Ten grms of pheromone per hectre is one of the lowest effective rtes for disruption of pink bollworm, Pectinophor gossypiell, when pplied every 23 weeks s microencpsulted spryble formultion (Critchley et l. 1984). Short (2 3 wk) residul ctivity is chrcteristic of spryble formultions in generl (Gut et l. 24). Effective disruption t reltively low deployment rte (1 g of pheromone per hectre) ws lso chieved for different lefmining species, the tomto pinworm (Keiferi lycopersicell; Jenkins et l. 199). Thus, the low mount of pheromone required for effective seson-long disruption of P. citrell is unique mong moth species investigted to dte nd my be chrcteristic of Grcillriids nd Gelechiids. One of the objectives of this investigtion ws to test directly the predictions of Miller et l. (26,b) by conducting disruption experiment where mle moth ctch in pheromone monitoring trps ws quntified in plots with vrying dispenser densities to differentite between competitive nd noncompetitive ttrction. Furthermore, the outcomes of the theoreticl predictions were compred with behviorl dt collected directly in the field, thus providing evidence for noncompetitive mechnism of disruption for P. citrell (Fig. 2 c). As predicted, mles did not pproch mting disruption dispensers in ny of the dispenser density tretments. Furthermore, we confirmed tht mle P. citrell could be observed orienting to ttrctive pheromone dispensers in plots not treted with pheromone. In ddition, our trpping study confirmed tht the dosge of pheromone loded into the dispensers used s the mting disruption tretment ttrcts mle P. citrell in control plots. These findings present dilemm how does noncompetitive disruption profile rise from deployment of dispensers tht, in trpping study, were ttrctive? We speculte tht the relese rte of pheromone from the disruptive dispensers ws well bove norml but insufficient to preclude brief ttrction events when such dispensers were sprse nd hence rrely encountered. However, when these higher-dosge dispensers were pcked together promoting numerous plume encounters, mles enveloped in them for prolonged periods becme desensitized nd cesed plume following, or discrete plumes were enveloped within mism of bckground pheromone precluding orienttion to n individul point source. Cesstion of ttrction under high dispenser density ws supported both by the profile nlysis nd the filure to observe mles rriving t dispensers in the disruption trils. Hd ttrction been required first step mediting disruption of ll mles under these conditions, some mles should hve been observed pproching dispensers in pheromone-treted plots, nd the profiles should hve reflected competitive ttrction. It ppers tht the disruption in this study ws occurring minly t some distnce from the dispensers. This resoning rises the question of over wht re ech dispenser exerted given effect. An exmintion of Fig. 2 revels tht pproximtely 1 dispensers per hectre were required to reduce mle ctch by 5% (11.5 to 5.7 mles per trp per night). Since 1 h=1, m 2, ech dispenser cn be clculted to hve hlved ctch cross pproximtely 1 m 2 of citrus grove (1, m 2 per 1 dispensers). If ech dispenser hd relesed ll of its 1.33 mg of pheromone over the 14 weeks it ws deployed, the verge relese rte per dispenser per hour would be.6 μg/hr, nd the corresponding specific re for 1/2 trp suppression per microgrm pheromone per hour would be 167 m 2. We suspect tht this vlue underestimtes pheromone specific ctivity for this study, becuse it is likely tht pheromone lod ws not completely exhusted over the 14 wk of deployment, given tht ctch in trps ws still being suppressed when the dispensers were replced on 15 June. Nevertheless, this specific ctivity vlue for P. citrell pheromone is 4-fold higher thn the 4 m/ μg pheromone/hr clculted to hlve mle ctch of Orientl fruit moth bsed on the noncompetitive disruption profiles reported by Miller et l. (26b). Mting disruption could be n importnt contribution to P. citrell mngement progrms in the USA nd elsewhere. Spry progrms for lefminers in citrus re often ineffective, require biweekly ppliction given continul growth of new flush, nd re detrimentl to nturl enemy popultions of P. citrell nd other citrus pests (Peñ et l. 22). In the current study, new flush infesttion by lrvl P. citrell ws reduced by more thn hlf in the highest pheromone rte tretment, despite the smll size of study plots (.14 h). It is well known tht disruption outcomes re better in lrger plots (see reviews by Gut et l. 24; Witzgll et l. 28), nd thus, the current dt suggest tht the disruption of P. citrell should be effective on lrger scle. Furthermore, the control of this species by mting disruption should be density independent given the noncompetitive mechnism (Miller et l. 26,b). This bodes well for the development of commercil formultions tht re economiclly fesible in the fce of high P. citrell popultions in Florid (Lpointe et l. 26; Stelinski nd Rogers 28).

6 1112 J Chem Ecol (28) 34: The primry chllenge to developing commercilly vible mting disruption formultion for P. citrell is the complexity of the pheromone chemistry (Lel et l. 26; Moreir et l. 26), which currently renders the cost of synthesis economiclly prohibitive from mngement perspective. Fortuntely, little pheromone is required for effective disruption, nd even lower rtes of pheromone my prove effective for integrted progrms tht combine pheromone nd reduced insecticide input. However, opportunities lso exist to improve the economic fesibility of this pheromone technology if less expensive synthesis protocol could be developed. In ddition, even though it hs been proven tht 3:1 blend of Z7Z11E13-16Ald/Z7Z11-16Ald is required for the ttrction of P. citrell to trps (Lel et l. 26; Moreir et l. 26), the evidence for noncompetitive mechnism of disruption, such s desensitiztion or cmouflge, suggests tht the diene or triene components lone might yield effective disruption. Indeed, Z7Z11-16Ald lone hs been shown to effectively disrupt communiction of P. citrell in Jpn (Mfi et l. 25). Finlly, the lrge crege of citrus in Florid will demnd mechnicl ppliction for economic fesibility; therefore, long-lsting formultions mendble to mechnicl ppliction should be explored (Stelinski et l. 27). Acknowledgments In Jckson, Angel Hoyte, nd Wendy Meyer re grtefully cknowledged for ssistnce with trp deployment nd mintennce. We thnk ISCA Technologies for providing lures nd pheromone to conduct the studies herein. A previous version of the mnuscript ws improved by Pul Jenkins, Rufus Iscs, nd Steve Lpointe. We lso thnk two nonymous reviewers for helpful comments. References CHARMILLOT, P. -J., BLOESCH, B., SCHMID, A., nd NEUMANN, U Lutte contre cochylis de l vigne Eupoecili mbiguell Hb., pr l technique de confusion sexuelle. Rev. Suisse Vitic. Arboric. Hortic. 19: CRITCHLEY, B.R.,CAMPION, D.G.,MCVEIGH, E.M.,MCVEIGH, L.J., JUSTUM, A.R.,GORDON, R.F.,MARKS, G.J.,NASR EL-SAYED,A., nd HOSNY, M. M Microencpsulted pheromones in cotton pest mngement, pp , in Proceedings of British Crop Protection Conference: Pests nd Diseses. British Crop Protection Council, Croydon, Surrey, UK. EPSTEIN, D., STELINSKI, L. L., REED, T. R., MILLER, J. R., nd GUT, L. J. 26. Higher densities of distributed pheromone sources provide disruption of codling moth, (Lepidopter: Tortricide) superior to tht of lower densities of clumped sources. J. Econ. Entomol. 99: GILL, R. J Citrus lefminer found in Cliforni. Cl. Dept. Food nd Agric., Cl. Plnt Pest & Disese Rep. 18:79 8. GOTTWALD, T. R., BASSANEZI, R. B., AMORIM, L., nd BERGAMIN- FILHO, A. 27. Sptil pttern nlysis of citrus cnker-infected plntings in São Pulo, Brzil, nd ugmenttion of infection elicited by the Asin lefminer. Phytopthology 97: GRAHAM, J. H., GOTTWALD, T. R., CUBERO, J., nd ACHOR, D.S. 24. 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