Separating the Attractant from the Toxicant Improves Attractand-Kill of Codling Moth (Lepidoptera: Tortricidae)
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1 Separating the Attractant from the Toxicant Improves Attractand-Kill of Codling Moth (Lepidoptera: Tortricidae) Author(s): Juan Huang, Larry J. Gut, and James R. Miller Source: Journal of Economic Entomology, 106(5): Published By: Entomological Society of America URL: BioOne ( is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne s Terms of Use, available at Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
2 HORTICULTURAL ENTOMOLOGY Separating the Attractant From the Toxicant Improves Attract-and-Kill of Codling Moth (Lepidoptera: Tortricidae) JUAN HUANG, 1,2 LARRY J. GUT, 1 AND JAMES R. MILLER 1 J. Econ. Entomol. 106(5): 2144Ð2150 (2013); DOI: ABSTRACT The behavior of codling moth, Cydia pomonella (L.), responding to three attract-andkill devices was compared in ßight tunnel experiments measuring attraction and duration of target contact. Placing a 7.6 by 12.6 cm card immediately upwind of a rubber septum releasing pheromone, dramatically increased the duration on the target to 60 s. In this setting, nearly all the males ßew upwind, landed on the card Þrst, and spent the majority of time searching the card. In contrast, male codling moths spent 15 s at the source if given the lure only. In a forced contact bioassay, knockdown rate or mortality of male codling moths increased in direct proportion to duration of contact on a -cyhalothrin-loaded Þlter paper. When this insecticide-treated paper was placed immediately upwind of the lure in the ßight tunnel, 90% of males contacting the paper were knocked down 2 h after voluntary exposure. These Þndings suggest that past attempts to combine insecticide directly with sex pheromones into a small paste, gel, or other forms of dollops are ill-advised because moths are likely over-exposed to pheromone and vacate the target before obtaining a lethal dose of insecticide. It is better to minimize direct contact with the concentrated pheromone while enticing males to extensively search insecticide-treated surface nearby the lure. KEY WORDS ßight tunnel, sex pheromone, -cyhalothrin, insect behavior, lethal effect The identiþcation and synthesis of codling moth, Cydia pomonella (L.), sex pheromone (Roelofs et al. 1971) revolutionized the management of this major pest of apples. Mating disruption by broadcasting synthetic sex pheromone into an orchard has been adopted as an integral part of codling moth management for 160,000 ha worldwide (Witzgall et al. 2008). However, the effectiveness of mating disruption for codling moth varies with pest density and the shape, size, and isolation of the treated area (Gut et al. 2004, Witzgall et al. 2008). New approaches may lead to enhanced consistency and efþcacy of pheromonebased controls for codling moth. Attract-and-kill uses semiochemicals as attractants in combination with insecticides, sterilants, or insect pathogen to provide pest control (El-Sayed et al. 2009). Most attract-and-kill formulations use sex pheromone to lure the pest to sources of a contact insecticide (Haynes et al. 1996). This approach attempts to achieve levels of control superior to mating disruption alone, while offering high selectivity, low rates of active ingredients, reduced selection pressure, and no insecticide residues on the fruit. Optimization of this tactic requires excellent attraction of the target insect to the toxicant, and delivery of a lethal or sub-lethal dose before leaving the pheromone source (El-Sayed et al. 2009). 1 Department of Entomology, Michigan State University, 578 Wilson Road, East Lansing, MI Corresponding author, huangju@msu.edu. Attract-and-kill has been evaluated for control of several lepidopteran pests with various degrees of success. Use of sex pheromone along with an insecticide provided better control than the pheromone alone against the pink bollworm moth, Pectinophora gossypiella (Saunders) (Floyd and Crowder 1981, Haynes and Baker 1985). The combination of sex pheromone and an insecticide enhanced levels of population suppression of the light brown apple moth, Epiphyas postvittana (Walker) (Suckling and Brockerhoff 1999). Various attract-and-kill formulations have been tested under Þeld conditions and reported to be effective for codling moth control (Hofer and Brassel 1992, Charmillot et al. 2000, Lösel et al. 2000, Reinke et al. 2012). However, most Þeld studies drew this conclusion by comparing moth captures and fruit injury in attract-and-killðtreated plots with those in untreated control plots (Lösel et al. 2000, Ebbinghaus et al. 2001, Claudio and Angeli 2002, Krupke et al. 2002, Lösel et al. 2002, Pluciennik and Olszak 2006, des Apfelwicklers 2008, Mansour 2010, Somsai et al. 2010). In the absence of a pheromone-only treatment, it is impossible to partition the effect of the formulation to insecticide poisoning of the males through contact with the insecticide versus mating disruption because of the presence of thousands of pheromone-laden dollops per hectare. By including a pheromone-only treatment, Evenden and McLaughlin (2004) determined that formulations with or without insecticides provided equivalent levels of disruption of oriental fruit moth, Grapholita molesta (Busck). Exclusion ex /13/2144Ð2150$04.00/ Entomological Society of America
3 October 2013 HUANG ET AL.: ATTRACT-AND-KILL OF CODLING MOTH 2145 periments revealed that mating disruption alone accounted for 50% of the activity of an attract-and-kill formulation against light brown apple moth (Suckling and Brockerhoff 1999). To date, attract-and-kill formations for tortricid pests have been applied as dollops of paste or gel containing a mixture of sex pheromone and an insecticide. Sirene CM (Charmillot et al. 2000), Last Call CM (Krupke et al. 2002), and Appeal (Lösel et al. 2002) are examples of current or former commercial formulations. Presented in this manner, optimal effectiveness of attract-and-kill depends on target insects contacting the pheromone source to pick up a lethal dose of insecticides (Suckling and Brockerhoff 1999). Longer retention on the formulation or direct transfer of the formulation to the insect increases the likelihood of delivering a lethal dose. However, exposure to high concentrations of pheromone near the source can desensitize males to pheromone through adaptation or habituation and abbreviate the response to pheromone (Stelinski et al. 2005). Therefore, a key hurdle in the implementation of attract-and-kill technology is development of a delivery system that is highly attractive, yet does not limit male contact with the insecticide-loaded pheromone source because of desensitization. Another major problem with current formulations is that moths are only presented with a very small surface ( 1 cm in diameter) to land on and expose themselves to an insecticide. Retention time on the source has generally been neglected in developing commercial formulations. Less than optimal contact with the formulation is likely a major reason why the toxicant has not been a more signiþcant contributor to the efþcacy of attract-and-kill formulations for tortricid pests. The aim of this study was to demonstrate how ef- Þcacy of the attract-and-kill tactic might be improved by manipulations of the spatial arrangement of pheromone and toxicant. Three spatial arrangements of pheromone lures were offered to codling moth males in a ßight tunnel measuring their attraction and duration of source contact. In addition, -cyhalothrin was used as a model toxicant to examine the contact time required to deliver a lethal dose against codling moth males. Its sublethal activity on subsequent moth behaviors was also examined. Materials and Methods Insects. Codling moths were supplied as late instar larvae in strips of double-sided corrugated cardboard (2 by 40 cm) by the U.S. Department of AgricultureÐ Agricultural Research Service (USDAÐARS) Yakima Agricultural Research Laboratory (Wapato, WA). Larvae were maintained at 24 C during the day and 18 C at night, 60% relative humidity (RH), and a photoperiod of 16:8 (L:D) h in a growth chamber until they pupated. Pupae were sorted by sex and placed in petri dishes in a Bugdorm-1 cage (30 by 30 by 30 cm, Megaview Science Education Services Co., Taiwan) with 5% sucrose solution through cotton dental wicks as food. All experiments used 1- to 2-d-old males. Flight Tunnel Assay Procedures. Detailed descriptions of a ßight tunnel (1.3 by 0.8 m in cross-section and 2.4 m in length) with a laminar air ßow and assay procedures were described in Huang et al. (2010). Brießy, 1- to 2-d-old male moths were placed in cylindrical release cages (two per cage) 30 min before the onset of scotophase, then immediately transferred into a walk-in environmental chamber (21Ð22 C) containing the ßight tunnel, for 1 h ofacclimation before assays. A pheromone target was placed at the upwind end of the tunnel, and moths were released from the cages at the downwind end of the tunnel. Moths were allowed 3 min to respond to the target, and then removed by a portable vacuum. The following behaviors were recorded: wing fanning; nonanemotactic ßight from the release cage (ßying out only); positive, plume-following anemotactic ßight toward but without touching the target (either pheromone lure or its surroundings) (ßying upwind); plume-following ßight followed by landing on the target (contacting the lure or its surroundings). No detectable behavioral response was also noted. Proportions of moths exhibiting these behaviors were calculated as numbers of moths with a particular behavior divided by total moths tested. Treatment order was randomized daily unless otherwise indicated to minimize possible effect of time after the onset of scotophase. After daily use, the interior of the ßight tunnel was wiped with a paper towel wetted with acetone and rinsed with water immediately to avoid damaging the Plexiglas. Release cages, the ring stand, and the glass rod used to deploy the targets were also washed with acetone, and baked at 120 C for 2 h after each use. Experimental Design and Statistical Analysis. All experiments used a randomized complete block design. Blocks were accumulated over different days and used different batches of 1- to 2-d-old moths. The proportions of moths exhibiting a designated behavior, and durations of contact times, were analyzed by analysis of variance (ANOVA) (SAS Institute 2010). Mean separations were performed using TukeyÕs signiþcant difference (honestly signiþcant difference [HSD]) tests. Data for knockdown rate and mortality were subjected to probit analysis (SAS Institute 2010) to calculate the LT 50 and LT 90 values (time taken to achieve 50 and 90% knockdown or mortality). Experiment 1: Target Configuration. The pheromone source was a female-like red rubber septa loaded with 0.1 mg codlemone ( 98% isomeric and chemical purity, Suterra, Bend, OR) (henceforth referred to as lure). This lure consistently provides high levels of attraction and upwind ßight in wind tunnel assays (Stelinski et al. 2005, Huang et al. 2010). The lure was presented in three different conþgurations at the upwind end of wind tunnel: a lure secured by a string to a metal rod attached to a steel ring-stand (lure only), a lure pinned 1 cm above a horizontal yellow card (7.6 by 12.6 cm) held by a 9-cm glass rod attached to the steel ring-stand (lure with a card beneath), and a lure pinned 1 cm away from the index card that was hung vertically upwind of the lure by a twist tie onto the metal rod attached to the ring-stand (lure with a
4 2146 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 106, no. 5 Fig. 1. Proportion of male codling moths exhibiting behavioral responses to a 0.1 mg lure only, a 0.1 mg lure with a card beneath, and a 0.1 mg lure with a card upwind in a ßight tunnel. Bars labeled with different letters within groups differed signiþcantly at 0.05 (TukeyÕs test). card upwind) (Fig. 1). In addition to recording the behaviors as described above, observers recorded duration of time on the cards and the lures. This experiment contained three replicates using different batches of 16Ð20 moths based on moth availability. To visualize the odor plumes generated by the three different conþgurations, smoke plumes were generated by small cotton wicks, size similar to the lure and soaked with titanium tetrachloride. Experiment 2: Forced Contact Bioassay in Petri Dish. Warrior containing 11.4% -cyhalothrin active ingredient (Syngenta Crop Protection, Inc., Greensboro, NC) in a capsule suspension was diluted in distilled water to a Þnal concentration of 9.8 g/ l. This solution (900 l) was evenly loaded onto a Whiteman Þlter paper (9 cm in diameter) at 139 g/cm 2 and air dried for 1 h before the bioassay. The treated Þlter paper lined the bottom of a petri dish (9 cm in diameter). Ten male codling moths, 1Ð2 d old, were individually held on treated Þlter paper for 0, 5, 10, 30, and 60 s. If moths moved off of Þlter paper, a slight tap outside the petri dish jarred them back onto the Þlter paper. After exposure, moths were transferred into diet cups (118 ml) with a cotton ball soaked with 10% sugar solution. Numbers of males knocked down (leg twitching, leg autotomy, or inability to ßy) or dead were recorded 2 and 24 h after initial contact. The entire experiment had three replicates using different batches of moths. Experiment 3: Contact Bioassay in Flight Tunnel. A Whiteman Þlter paper (5.5 cm in diameter) was loaded with 400 l ofa9.8 g/ l warrior solution to yield a Þnal concentration of 165 g/cm 2. The paper was air dried for 1 h before use. Based on results from experiment 1, the optimal arrangement of the card vertical and upwind from the lure was used in this ßight tunnel contact bioassay; however, the card was replaced with a treated Þlter paper to deliver the insecticide. A control treatment was similarly designed but received water only. Groups of 16Ð20 males were ßown to control or treated papers. All moths touching the papers were captured, and their survival was assessed after 1 h. Differences in behavior between control and treated Þlter paper were scrutinized for evidence of possible repellency by -cyhalothrin. This experiment included three replicates. Experiment 4: Sublethal Effect of -Cyhalothrin. This experiment documented whether pre-exposure to -cyhalothrin impacted subsequent behavioral response by male moths to a synthetic pheromone in the ßight tunnel. Two hours before the test, groups of 20Ð30 males were exposed to Warrior-treated Þlter paper for 1 min as described in experiment 1, but at a 10 times lower dose (15 g/cm 2 ). A pilot test showed that this low dose caused 25% knockdown at 2 h postexposure. Control moths were exposed to watertreated Þlter paper. After treatment, all moths were kept in a walk-in growth chamber as described above. Before the ßight tunnel assay, moths unable to ßy were discarded, and 16Ð20 ßight-capable moths were used in each treatment. Their behavioral response to the 0.1-mg lure with a card beneath was compared in a ßight tunnel. This experiment contained three replicates. Results Experiment 1: Target Configuration. Target con- Þguration signiþcantly affected the proportion of moths exhibiting fanning and contacting the lure (fanning: F 256, df 2, 8, P ; lure contact: F 34.06, df 2, 8, P ) (Fig. 1). Addition of the card upwind or below the lure signiþcantly increased the numbers of moths wing fanning compared with the lure alone. Placing a card upwind of the lure signiþcantly decreased the number of moths contacting the lure; however, card position did not affect the number of moths orienting to or contacting the card (F 6.49; df 1, 5; P 0.12). The numbers of males ßying out of the release cage and upwind were similar across the treatments (upwind: F 0.79, df 2, 8, P 0.5; ßight out: F 0.25, df 2, 8, P 0.8). In addition, target conþguration signiþcantly affected duration of contact (Fig. 2). Placing a card upwind of the lure signiþcantly increased the total contact time on the target compared with the other two arrangements (F 49.6; df 2, 101; P ). Also in this setting, all the moths landed on the card Þrst, and spent the majority of time searching the card. In contrast, males spent equal time either on the lure or on the card when the lure was presented horizontally above the card. Moths spent signiþcantly more time on the card and less time on the lure when the card was presented upwind compared with beneath the lure (time on the card: F 78.5, df 1, 87, P ; time on the lure: F 8.2, df 2, 101, P ). No difference was found in total contact time and time on the lure between lure alone and lure with the card beneath. Experiment 2: Forced Contact Bioassay in Petri Dish. As expected, the number of moths knocked down, dead, or both, increased with duration of exposure to -cyhalothrin-treated Þlter paper (Fig. 3).
5 October 2013 HUANG ET AL.: ATTRACT-AND-KILL OF CODLING MOTH 2147 Fig. 2. Duration of elapsed time, total contact time, time on the card and lure by male codling moths given lure, lure with a card beneath, or lure with card upwind in a ßight tunnel. Bars labeled with different letters within groups differed signiþcantly at 0.05 (TukeyÕs test). Thirty seconds of exposure or more resulted in 100% knockdown 2 h later. However, many moths recovered normal ßight capability 24 h after 30 s of exposure to the toxicant. Mean lethal times for 50 and 90% knockdown (LT 50 and LT 90 ) were 7 and 13 s within 2 h after exposure (intercept 4.0, , P ; slope 4.8, , P ), whereas 24 h after exposure, the LT 50 and LT 90 increased to 18 and 159 s, respectively (intercept 1.7, 2 4.6, P 0.03; slope 1.3, 2 8.1, P 0.004). Experiment 3: Contact Bioassay in Flight Tunnel. -Cyhalothrin-treated Þlter paper slightly, but significantly, increased the proportion of moths ßying upwind (F ; df 1, 5; P ), and contacting either the card (F 72.05; df 1, 5; P ) or the lure (F 81; df 1, 5; P ). The insecticide decreased proportions of moths exhibiting nonanemotactic ßight from the release cage (F 61.71; df 1, 5; P ) compared with controls (Fig. 4). However, there was no signiþcant difference in the proportion of moths exhibiting fanning behavior (F 1.0; df 1, 5; P ). Fig. 4. Proportion of male codling moths exhibiting behavioral responses to control versus -cyhalothrin-treated Þlter paper at 165 g/cm 2 with 0.1 mg lure in a ßight tunnel. Bars labeled with different letters within groups differed signiþcantly at 0.05 (TukeyÕs test). Knockdown was signiþcantly higher for moths contacting the treated Þlter paper than the untreated control (2 h: F ; df 1, 5; P ; 24 h: F 86.1; df 1,5; P ). Over % (mean SEM) of the moths contacting the Þlter paper were knocked down 2 h afterwards, and % were dead after 24 h. Experiment 4: Sublethal Effect of -Cyhalothrin. Sublethal exposure to the pesticide 2 h before the ßight tunnel assay resulted in signiþcantly lower proportions of males responding to the pheromone afterwards (Fig. 5). Many pre-exposed moths were still able to fan their wings, but the number was signiþcantly lower than controls (F 39.9; df 1, 5; P 0.02). Only a small proportion of pre-exposed males could orient to (F 187.4; df 1, 5; P 0.005) or contact the source (F 254.3; df 1, 5; P ). Most of them remained inside the release cages with Fig. 3. The relationship between duration of contact on a -cyhalothrin-treated Þlter paper at 139 g/cm 2 with numbers of moths knocked down 2 and 24 h after forced contact. Fig. 5. Proportion of male codling moths exhibiting behavioral responses to a 0.1 mg lure after forced exposure to -cyhalothrin-treated Þlter paper at15 g/cm 2 in a ßight tunnel. Bars labeled with different letters within groups differed signiþcantly at 0.05 (TukeyÕs test).
6 2148 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 106, no. 5 no detectable behavioral response during the 3-min observational period (F 39.5; df 1, 5; P 0.02). All the moths contacting the card also contacted the lure; therefore, the data for proportion of moths contacting the lure were not shown. Discussion Effects of Configuration on Plume Structure. The manner in which the attractant, in this case a pheromone lure, was presented to male codling moths, C. pomonella, signiþcantly affected their searching time near and at the source (Fig. 2). Odor-plume structure and its concentration are known to affect pheromonemediated ßight of moths (Murlis et al. 1992, Willis et al. 1994, MafraÐNeto and Cardé 1995). In a ßight tunnel and under natural Þeld conditions, odor molecules dissipate from their source mainly by turbulent ßow when a point source is attached to solid objects (Murlis et al. 1992). However, under a laminar air ßow, a small point source detached from large solid objects generates a ribbon-like plume (MafraÐNeto and Cardé 1995). Placing a solid object immediately upwind of the rubber septum lure generated air turbulence resulting in wider plumes consisting of packets of pheromone intercalating with clean air (MafraÐ Neto and Cardé 1994, 1995). Male moths such as Cadra cautella (Walker) and Lymantria dispar (L.) ßew faster and found sources more frequently when responding to wider and turbulent plumes than continuous narrow plumes (MafraÐNeto and Cardé 1994, 1995; Willis et al. 1994). Similarly in this study, the lure with a card immediately upwind generated a wider and more turbulent plume compared with the other two conþgurations as judged by smoke release. Such a plume likely made a mothõs task of Þnding the septum lure more difþcult than when it was presented alone. However, in the ßight tunnel where all plumes were carefully directed over the release cages, plume structure did not signiþcantly affect the proportion of male codling moths ßying upwind and contacting either the card or lure (Fig. 1). We suggest that main reason why male codling moths were more prone to remain on the cards than on the lure was likely because of difference in pheromone concentration. Exposure to pheromone can cause adaptation of olfactory receptors, habituation of the central nervous system, or both, of male codling moths (Judd et al. 2005; Stelinski et al. 2005, 2006), resulting in their either leaving or not being able to locate the source after high exposure. Adaptation, habituation, or both, may occur more quickly after exposure to pheromone through direct contact than airborne exposure because sex pheromones are readily transferred to and retained by the insectõs waxy cuticle. For codling moth, Stelinski et al. (2006) found that touching a septum lure loaded with 0.1 mg codlemone produced adaptation in male codling moths more long-lasting than did a close visit to an Isomate-C Plus dispenser containing 108 mg codlemone but with no touch. Furthermore, increase in plume size is often associated with reduction of pheromone concentration (MafraÐNeto and Cardé 1995). Thus, we suggest that moths on the card upwind of the lure received less pheromone than those touching the lure directly. Visits only to the card likely delayed adaptation, habituation, or both, allowing moths to search longer around the lure not yet found. Effects of -Cyhalothrin on Behaviors. Sublethal exposure to a low dose of -cyhalothrin signiþcantly impaired subsequent orientational behaviors of male codling moths (Fig. 5). Substantial numbers of preexposed moths did not respond to the pheromone source, indicating sublethal doses of the pesticide completely abolished their ability to sense or respond to the pheromone. Still appreciable numbers of insecticide-exposed moths were able to initiate wing fanning after detecting the pheromone plume, suggesting that their sensory system was still functioning at some level. However, transitions from wing fanning to upwind ßight were dramatically inhibited, 45% of those with wing fanning were able to orient and initiate upwind ßight to the source. This reduction suggests that either integration of sensory stimuli at central nervous system or regulatory of motor pathways was affected. However, nearly all responding males were capable of counterturning across the wind and progressing toward the source once ßight was initiated. Furthermore, all sublethal exposed males had an ability to sustain their ßight when tossed into the air. In these aspects, the sublethal effects of -cyhalothrin on codling moths were strikingly similar to the effects of permethrin on oriental fruit moths, G. molesta (Linn and Roelofs 1984) and pink bollworm, P. gossypiella (Haynes and Baker 1985). -Cyhalothrin is a type II pyrethroid with an -cyano group, acting not only on nervous transmissions through sodium channels leading to repetitive nerve discharges, but also on Gaba receptors affecting postsynaptic response to acetylcholine (Delpuech et al. 1999). Therefore, -cyhalothrin would be expected to impact mating behavior of codling moth males through both peripheral and central nervous systems. Haynes and Baker (1985) postulated that pyrethroid insecticides may interfere with pheromone perception not only by blocking the receptor at the peripheral nervous system level, resulting in no response by some males, but also by changing quantity or quality of signals at the central nervous system, causing males incapable of completing various phases of mating behavior. Potential Improvement of Attract-and-Kill. From a practical standpoint, an effective attract-and-kill device should keep target insects from contacting the source directly to avoid desensitization of the olfactory apparatus, while providing a surface that allows them sufþcient time to contact the toxicant and acquire a lethal dosage. Duration of contact with the insecticide signiþcantly affected the knockdown rate for codling moth males (Fig. 3). As the majority of insecticides are lipophilic, the degree of absorption heavily depends on the contact time with the insect cuticle. However, conventional attract-and-kill formulations in which sex pheromones are directly mixed with an insecticide would discourage moths contact-
7 October 2013 HUANG ET AL.: ATTRACT-AND-KILL OF CODLING MOTH 2149 ing the insecticide surface for prolonged times. Based on the current study, the better approach would be to separate the sex pheromone or other desensitizing attractant from the toxicant. In the ßight tunnel, male codling moths spent 15 s at the source if given the lure only; however, the addition of a 7.6 by 12.6 cm card, immediately upwind of the lure, increased the search time by more than fourfold (Fig. 2). This spatial orientation allowed male moths to obtain a lethal dose, resulting in 90% knockdown rate at 2 h postexposure. Moths that were not knocked down after exposure would be unlikely to Þnd pheromone source thereafter. We suggest that the attract-and-kill tactic is indeed a worthy approach, but it must be informed by knowledge of the behavioral details. Acknowledgments We thank Douglas B. Aho for rearing codling moths and Peter McGhee for helping obtain research materials. 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Haynes, K. F., W. G. Li, and T. C. Baker Control of pink bollworm moth (Lepicoptera: Gelechiidae) with insecticides and pheromones (attracticide): lethal and sublethal effects. J. Econ. Entomol. 79: 1466Ð1471. Hofer, D., and J. Brassel Attract and kill to control Cydia pomonella and Pectinophora gossypiella. IOBC/ WPRS Bull. 15: 36Ð39. Huang, J., L. L. Stelinski, and L. J. Gut Mating behaviors of Cydia pomonella (Lepidoptera: Tortricidae) as inßuenced by sex pheromone in electrostatic powder. J. Econ. Entomol. 103: 2106Ð2010. Judd, G.J.R., M.G.T. Cardiner, N. C. DeLury, and G. Karg Reduced antennal sensitivity, behavioural response, and attraction of male codling moths, Cydia pomonella, to their pheromone (E, E)-8,10-dodecadien- 1-ol following various pre-exposure regimes. Entomol. Exp. Appl. 114: 65Ð78. Krupke, C. H., B. D. Roitberg, and G.J.R. Judd Field and laboratory responses of male codling moth (Lepidoptera: Tortricidae) to a pheromone-based attract-andkill strategy. Environ. Entomol. 31: 189Ð197. Linn, C. E. Jr., and W. L. Roelofs Sublethal effects of neuroactive compounds on pheromone response thresholds in male oriental fruit moths. Arch. Insect Biochem. Physiol. 1: 331Ð344. Lösel, P. M., G. Penners, R.P.J. Potting, D. Ebbinghaus, A. Elbert, and J. Scherkenbeck Laboratory and Þeld experiments towards the development of an attract and kill strategy for the control of the codling moth, Cydia momonella. Entomol. Exp. Appl. 95: 39Ð46. Lösel, P. M., R.P.J. Potting, D. Ebbinghaus, and J. Scherkenbeck Factors affecting the Þeld performance of an attracticide against the codling moth Cydia pomonella. Pest Manag. Sci. 58: 1029Ð1037. Mafra Neto, A., and R. T. Cardé Find-scale structure of pheromone plumes modulates upwind orientation of ßying moths. Nature 369: 142Ð144. Mafra Neto, A., and R. T. Cardé Inßuence of plume structure and pheromone concentration on upwind ßight of Cadra cautela males. Physiol. Entomol. 20: 117Ð133. Mansour, M Attract and kill for codling moth Cydia pomonella (Linnaeus) (Lepidoptera: Tortricidae) control in Syria. J. Appl. Entomol. 134: 234Ð242. Murlis, J., J. S. Elkinton, and R. T. Cardé Odor plumes and how insects use them. Annu. Rev. Entomol. 37: 505Ð 532. Pluciennik, Z., and R. W. Olszak Controlling the codling moth (Cydia pomonella L.) with the attract and kill agent appeal 04 PA. J. Fruit Ornam. Plant Res. 14: 197Ð201. Reinke, M. D., J. R. Miller, and L. J. Gut Potential of high-density pheromone-releasing microtraps for control of codling moth Cydia pomonella and obliquebanded leafroller Choristoneura rosaceana. Physiol. Entomol. 37: 53Ð 59. Roelofs, W. L., A. Comeau, A. Hill, and G. Milicevic Sex attractant of the codling moth: characterization with electroantennogram technique. Science 174: 297Ð299. SAS Institute SAS/STAT userõs guide, version 6, 4th 383 ed., vol. 1. SAS Institute, Cary, NC. Stelinski, L. L., L. J. Gut, and J. R. Miller Occurrence and duration of long-lasting peripheral adaptation among males of three species of economically important tortricid moths. Ann. Entomol. Soc. Am. 98: 580Ð586. Stelinski, L. L., L. J. Gut, and J. R. Miller Orientational behaviors and EAG responses of male codling moth after exposure to synthetic sex pheromone from various dispensers. J. Chem. Ecol. 32: 1527Ð1538. Somsai, A. P., I. Oltean, L. Gansca, I. Oprean, P. Raica, and E. Harsan Control of two sympatric tortricids, Cydia pomonella and Adoxophyes reticulana (Lepidop-
8 2150 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 106, no. 5 tera: Tortricidae) by an experimental attract and kill formulation. Bull UASVM Hortic. 67: 453Ð457. Suckling, D. M., and E. G. Brockerhoff Control of light brown apple moth (Lepidoptera: Tortricidae) using an attracticide. J. Econ. Entomol. 92: 367Ð372. Willis, M. A., C. T. David, J. Murlis, and R. T. Cardé Effects of pheromone plume structure and visual stimuli on the pheromone-modulated upwind ßight of male gypsy moths (Lymantria dispar) in a forest (Lepidoptera: Lymantriidae). J. Insect Behav. 7: 385Ð409. Witzgall, P., L. Stelinski, L. Gut, and D. Thomson Codling moth management and chemical ecology. Annu. Rev. Entomol. 53: 503Ð522. Received 29 March 2013; accepted 11 July 2013.
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