PHYSIOLOGY, BIOCHEMISTRY, AND TOXICOLOGY

Occurrence and Duration of Long-Lasting Peripheral AdaptationAmong Males of Three Species of Economically Important

Tortricid Moths

L. L. STELINSKI, L. J. GUT, AND J. R. MILLER

Department of Entomology, Michigan State University, East Lansing, MI 48824

Ann. Entomol. Soc. Am. 98(4): 580Ð586 (2005)

ABSTRACT Electroantennograms (EAGs) of Cydia pomonella (L.), Pandemis pyrusana Kearfott,and Grapholita molesta (Busck) documented the presence and duration of long-lasting peripheraladaptation after pheromone preexposure. Moths of each species were preexposed for 1 h to varyingdosages (100 ngÐ100 mg) of the major components of their respective pheromone blends in 1-literTeßon containers with constant throughput of air. EAGs were performed on all insects 1 min afterpreexposure and at several subsequent intervals up to 120 min after exposure. Long-lasting peripheraladaptation was recorded by EAG after pheromone preexposure over a range of pheromone dosagesin both C. pomonella (100 �gÐ10 mg) and P. pyrusana (100 ngÐ100 mg). This reduction in EAGresponsiveness lasted �60 and 10 min, respectively, for these two species. ForG.molesta, a reductionin EAG responsiveness occurred only after 1 h of exposure to the highest dosage of pheromone tested(100 mg). Recovery from adaptation was also rapid in this species: EAGs were signiÞcantly reducedto all applied stimulus dosages only at 1-min postexposure. There was substantial variation in theprevalence and duration of decreased EAG responsiveness across the species investigated. However,where long-lasting adaptation was described, the phenomenon lasted �60 min. In addition, long-lasting adaptation was induced after prolonged exposures at estimated airborne concentrations ofpheromone in the range of nanograms per milliliter, which are much higher than the pheromoneconcentrations in Þeld plots treated with synthetic pheromone dispensers. Long-lasting peripheraladaptation after pheromone preexposure does not seem to be an important contributor to matingdisruption.

KEY WORDS long-lasting adaptation, electroantennogram, Grapholita molesta, Cydia pomonella,Pandemis pyrusana

PHEROMONE-BASED MATING DISRUPTION IS an importantbiorational alternative to insecticides for controllinglepidopteran pests and has been under developmentfor more than three decades (Carde and Minks 1995,Gut et al. 2004). Mating disruption is achieved by therelease of synthetic pheromones into a crop canopy todisrupt pheromone-mediated mate-Þnding behaviors.Various mechanisms have been proposed to explainhow mating disruption works (Rothchild 1981, Bartell1982, Carde 1990). In no speciÞc order, syntheticpheromones are thought to camoußage natural, fe-male-released plumes; act as false trails for searchingmales; cause an imbalance of sensory input; or desen-sitize males to pheromone through peripheral sensoryadaptation or central nervous system habituation.These mechanisms are thought not to be mutuallyexclusive (Carde et al. 1998).

A plethora of studies have been conducted exam-ining the possible mechanisms of mating disruption(Sanders 1982, 1985, 1996, 1998; Valeur and Lofstedt1996; Mafra-Neto and Baker 1996; Carde et al. 1998;Evenden et al. 1999a, b, c, 2000; Stelinski et al. 2004,

2005). However, progress has been modest in distin-guishing whether a certain mechanism is of greaterimportance than others. Furthermore, it has provendifÞcult to falsify the importance of any of the mech-anisms mentioned above. Delineating the primary ver-sus secondary mechanism(s) will aid in the develop-ment of pheromone technologies for practical use.The likelihood of effectiveness for a pheromone prod-uct is enhanced by knowing how it achieves matingdisruption in the Þeld.

Continuous and pulsed exposure to pheromone de-creases behavior and electrophysiological responsive-ness in many moth species (Bartell and Roelofs 1973;Bartell and Lawrence 1976a, b, c; Linn and Roelofs1981; Kuenen and Baker 1981; Sanders 1985; Rumboand Vickers 1997; Schmitz et al. 1997; Daly andFigueredo 2000). Typically, this effect, termed adap-tation, is dosage-dependent and reversible. In addi-tion, a form of “long-lasting” peripheral adaptation hasbeen described for Choristoneura rosaceana (Harris)(Stelinski et al. 2003a, b) that is similar in duration tothe adaptation described for Antheraea polyphemus

0013-8746/05/0580Ð0586$04.00/0 � 2005 Entomological Society of America

(Cramer) by Kaissling (1986). SpeciÞcally, preexpo-sure of male C. rosaceana to the major component ofits pheromone blend at concentrations ranging from 1to 56 ng/ml for durations of 15 or 60 min reducedsubsequent EAG responses for up to 11 min postex-posure. Most recently, evidence for an even longerlasting variant of this adaptation has been documentedfor Cydia pomonella (L.) (Judd et al. 2005). Ten- and30-min preexposures ofC. pomonella to its major pher-omone component at �35 ng/ml reduced EAG re-sponses for �1 h. However, not all tortricid mothspecies exhibit long-lasting adaptation (LLA). Argy-rotaenia velutinana (Walker) retains normal EAG re-sponses after pheromone preexposures that inducelong-lasting adaptation in C. rosaceana (Stelinski et al.2003a).Thus, signiÞcantvariationexists across species.

With respect to mating disruption, the questionbecomes, is long-lasting adaptation an important con-tributing factor? If so, mating disruption technologiescould be tailored to exploit this phenomenon by max-imizing the pheromone exposure dosage male mothsreceive in the Þeld. However, falsifying the role oflong-lasting adaptation in mating disruption wouldhelp researchers and engineers focus on mechanismsof greater signiÞcance. To investigate whether long-lasting adaptation is an important contributing factorto mating disruption, we sought to determine whetherit is prevalent among multiple pest moth species andwhether it can be induced at pheromone concentra-tions achieved in the Þeld. The objective of this studywas to document the presence and duration of long-lasting peripheral adaptation after pheromone preex-posure of varying intensity in three tortricid pests ofeconomic importance: C. pomonella, Pandemis pyru-sana Kearfott, and Grapholita molesta (Busck).

Materials and Methods

Insect Colonies. C. pomonella and G. molesta wereobtained from 1- and 2-yr-old laboratory colonies,respectively, originally collected as larvae from appleorchards in southwestern Michigan. P. pyrusanawereobtained from a colony established in 1990 from acommercial apple orchard in Yakima, WA (J. Brunner,Washington State University). P. pyrusana collectedfrom an untreated apple orchard in Wenatchee, WA,were added to this colony in 2000 and 2003. Eachspecies was reared at 24�C on pinto bean diet (Shoreyand Hale 1965) under a photoperiod of 16:8 (L:D) h.Male pupae of each species were segregated in 1-literplastic cages and provided with 5% sucrose solution.Electroantennograms (EAGs). The EAG system

and test protocols were identical to those described inStelinski et al. (2003a, b). Brießy, our EAG systemconsisted of a data acquisition interface board (TypeIDAC-02) and universal single ended probe (TypePRS-1) from Syntech (Hilversum, The Netherlands).The recording and indifferent electrodes consisted ofsilver-coated wire in glass micropipettes (10-�l micro-hematocrit capillary tubes) containing 0.5 M KCl.

Male insects of each species were 2Ð4 d old when usedfor electroantennograms. EAGs measured the maxi-mum amplitude of depolarization elicited by the ap-plied stimulus cartridge and were conducted on intactantennae of live insect preparations.Chemicals and Stimulus Delivery. The major

pheromone components of each species were usedas EAG stimuli and as preexposure treatments inadaptation experiments. For experiments withC. pomonella, (E,E)-8,10-dodecadien-1-ol (99% iso-meric and chemical purity) was obtained from Be-doukian Co. (Danbury, CT). For experiments withP. pyrusana and G. molesta, (Z)-11-tetradecenyl ace-tate [96.1% (Z)-11-tetradecenyl acetate and 3.9%(E)-11-tetradecenyl acetate] and (Z)-8-dodecen-1-yl-acetate (99% isomeric and chemical purity), re-spectively, were obtained from Shin Etsu (Tokyo,Japan). Chemical purities were conÞrmed with gaschromatography. Stimulus cartridges used to deliverpheromone to insect antennae for EAG recordingswere prepared according to the protocol detailed inStelinski et al. (2003a, b). Brießy, various concentra-tions (Figs. 1 and 2) of each pheromone in hexane(20-�l total solution) were pipetted onto 1.4 by 0.5-cmstrips of Whatman No. 1 Þlter paper. After 5 min in afume hood for solvent evaporation, treated strips wereinserted into disposable glass Pasteur pipettes. Stim-ulus puffs (1 ml) were generated through the car-tridges with a clean hand-held 20-ml glass syringeconnected to the pipettes with a 1-cm piece of Tygontubing.Effect of Pheromone Preexposure Dosage on EAGResponses. Moths of each species were preexposedto pheromone by using adaptation chambers (Stelin-ski et al. 2003a, b). Brießy, these chambers were cylin-drical, 1-liter Teßon containers (Jensen, Coral Springs,FL) equipped with two 64-mm ports in their lids. Glassinlets and outlets were afÞxed to the lids allowingpressurized air that had been Þltered through carbonto pass through the chambers at 30 ml/min. Chamberswere divided with wire mesh such that insects wereconÞned in upper halves, whereas one 2-cm-diameterby 0.5-cm-deep stainless steel planchette loadedwith a given dosage of pheromone was placed in thelower half. The highest dosage of pheromone testedfor each species was 100 �l of neat pheromone in theplanchette. Successively lower dosages were achievedby serial dilutions in mineral oil (Aldrich, Milwaukee,WI); pheromone loadings ranged in decade stepsfrom 100 ng to 100 mg. Chambers always equilibratedfor 60 min before insertion of insects. Thirteen malesof each species were assayed 1 min after 60 min ofpreexposure to each pheromone concentration. Thecontrol treatment consisted of moths (n � 13) pre-exposed in chambers to mineral oil only. Moths werepreexposed individually and treatments were alter-nated at random.Recovery from Long-Lasting Adaptation. EAGs

were performed on 10Ð13 males of each species be-fore conÞnement in adaptation chambers for 60 minof continuous pheromone exposure at the 100-mg

July 2005 STELINSKI ET AL.: LONG-LASTING PERIPHERAL ADAPTATION AMONG TORTRICIDS 581

pheromone dosage. After exposure, moths were re-moved from adaptation chambers and placed intopheromone-free air within 1-liter plastic containers.EAGs were performed on all insects 1 min after pre-exposure and at several subsequent intervals up to120 min (Fig. 2).Statistical Analysis. Data collected when testing

the effect of preexposure dosage were subjected to

analysis of variance (ANOVA), and differences inpairs of means were separated using TukeyÕs multiplecomparisons test (SAS Institute 2000). Data collectedwhen testing the effect of recovery interval weresubjected to repeated measures ANOVA, and differ-ences in pairs of means over time were separated byTukeyÕs test. In all cases, the signiÞcance level was � �0.05.

Fig. 1. Effect of 60 min of conÞnement of (A) C. pomonella, (B) P. pyrusana, and (C) G. molesta (n � 13 moths pertreatment) in adaptation chambers with various pheromone-loading dosages. Bars with * indicate signiÞcant (P � 0.05)decrease relative to the control response. 1Average standard error of the mean for EAG amplitude across all treatments.

582 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 98, no. 4

Results

Effect of Pheromone Preexposure Dosage on EAGResponses. The EAG responses of male C. pomonellato each stimulus cartridge loading tested were sig-niÞcantly (F � 11.7; df � 7, 96; P � 0.05) reducedafter preexposure dosages ranging from 1 to 100 mg(Fig. 1A). At the 100-�g preexposure dosage, EAGresponsesofC.pomonellawere signiÞcantly(P�0.05)

reduced only to the 200-�g and 2- and 20-mg stimuluscartridge loadings (Fig. 1A).

The EAG responses of male P. pyrusana were sig-niÞcantly (F � 17.1; df � 7, 96; P � 0.05) reduced inresponse to the majority of stimulus cartridge loadingsat preexposure dosages ranging from 100 �g to 100 mg(Fig. 1B). In addition, EAG responses to the 2- and20-�g stimulus cartridge loadings were signiÞcantly

Fig. 2. Recovery from long-lasting adaptation in (A)C. pomonella, (B) P. pyrusana, and (C)G.molesta (n� 10Ð13 mothsper time interval) after 60 min of conÞnement in adaptation chambers with the 100-mg preexposure dosage of pheromone.Bars with * indicate signiÞcant (P � 0.05) decrease relative to the control response. 1Average standard error of the meanfor EAG amplitude across all treatments.

July 2005 STELINSKI ET AL.: LONG-LASTING PERIPHERAL ADAPTATION AMONG TORTRICIDS 583

(P� 0.05) reduced after preexposure to dosages rang-ing from 10 ng to 100 �g (Fig. 1B).

For male G. molesta, EAG responses to all stimuluscartridge loadings were signiÞcantly (F� 9.8; df � 7,96; P � 0.05) reduced only after preexposure to the100-mg dosage. There was a signiÞcant (P � 0.05)reduction of EAG response to the 2- and 20-�g stim-ulus cartridge loadings after preexposure to the 10-mgdosage (Fig. 1C).Recovery from Long-Lasting Adaptation.One hour

of exposure signiÞcantly (F� 15.5; df � 5, 60;P� 0.05)reduced EAG amplitudes for C. pomonella at moststimulus cartridge loadings for up to 60 min (Fig. 2A).By 2-h postexposure, EAG responses of C. pomonellawere virtually indistinguishable from responses re-corded before exposing moths (Fig. 2A).

EAG responses to most stimulus cartridge loadingswere signiÞcantly (F � 8.9; df � 5, 60; P � 0.05)reduced for male P. pyrusana up to 10-min postexpo-sure (Fig. 2B). In addition, EAG responses to the20-�g stimulus cartridge loading were signiÞcantly(P� 0.05) reduced at 15-min postexposure (Fig. 2B).By60-minpostexposure,EAGresponsesofP.pyrusanawere virtually indistinguishable from responses re-corded before exposing moths (Fig. 2B).

For male G. molesta, EAG responses to all stimuluscartridge loadings were signiÞcantly (F� 16.8; df � 4,48; P � 0.05) reduced only at 1-min postexposure(Fig. 2C). In addition, EAG responses were signiÞ-cantly (P � 0.05) reduced to stimulus cartridge load-ings ranging from 2 to 200 �g at 5-min postexposure(Fig. 2C). By 10-min postexposure, EAG responses ofG. molesta were equal to responses recorded beforeexposure treatment (Fig. 2C).

Discussion

LLA was documented by EAG after pheromonepreexposure in two of the three species investigated.Where present, LLA was dosage-dependent and de-cayed over time. For C. pomonella, EAG responseswere reduced to all of the stimulus cartridge loadingsafter preexposure in chambers with dosages rangingfrom 1 to 100 mg of (E,E)-8,10-dodecadien-1-ol. How-ever, after preexposure at lower pheromone dosages(100 and 10 �g), LLA was recorded only with thehigher stimulus cartridge loadings (200 �gÐ20 mg).Decreased EAG responsiveness was recorded up to60 min after pheromone exposure and was completelyreversed by 120 min. These results corroborate therecent Þndings that C. pomonella exposed in staticchambers to 500 �g of pheromone for 10Ð30-min in-tervals also reduced EAG responsiveness for �1 h(Judd et al. 2005). The estimated airborne pheromoneconcentration that induced this decreased response(�35 �g/liter) (Judd et al. 2005) is in the range re-quired to induce LLA in C. rosaceana (Stelinski et al.2003b).P. pyrusana also exhibited LLA with similar char-

acteristics to that described previously for anotherleafroller species, C. rosaceana (Stelinski et al. 2003a,

b). LLA was recorded with all of the cartridge load-ings after preexposure in chambers with pheromonedosages ranging from 100 �g to 100 mg. These expo-sure dosages correspond to airborne pheromone con-centrations ranging from 19 to 56 ng of (Z)-11-tetra-decenyl acetate per ml (Stelinski et al. 2003b). LLAwas also recorded for P. pyrusana to the 2- and 200-�gcartridge loadings after preexposure dosages in cham-bers ranging from 10 �g to 100 ng. The 100-ng pre-exposure dosage yields an airborne pheromone con-centration of �0.5 ng/ml in adaptation chambers andis the lowest concentration at which LLA is inducedfor C. rosaceana (Stelinski et al. 2003b). The LLAobserved for P. pyrusana (Fig. 2B) was also similarto that of C. rosaceana in recovery time, which lasted�12 min (Stelinski et al. 2003a).

For G. molesta, reduced EAG responsiveness toall of the cartridge loadings occurred only after mothswere preexposed for 1 h in chambers containing100 mg of neat pheromone. Furthermore, recoveryfrom adaptation was much more rapid than in theabove two species. Full recovery was observed withthe 2- and 20-mg stimulus cartridge loadings after5 min and by 10 min, adaptation could no longer bedetected. These results are similar to those obtainedwithA. velutinana,where LLA could not be measuredbyEAG1minafter1-hpreexposureswith100mgofneat(Z)-11-tetradecenyl acetate (Stelinski et al. 2003b).However, normal behavioral responsiveness to pher-omone in bothG.molesta (Figueredo and Baker 1992,Rumbo and Vickers 1997) and A. velutinana (Bartelland Roelofs 1973) is reduced for prolonged periodsafter pheromone exposures similar to the ones per-formed in our EAG studies, suggesting that habitua-tion of the central nervous system occurs. Similarresults have recently been obtained withC. pomonellain which behavioral responsiveness to pheromonewas reduced 4 times longer than electrophysiologicalresponsiveness (Judd et al. 2005).

There is considerable variation in the prevalenceand duration of LLA among tortricid species. How-ever, does this phenomenon have any bearing onpheromone-based mating disruption? Current datasuggest that LLA is probably not an important con-tributing factor to mating disruption. First, the rate ofrecovery from adaptation in G. molesta and A. veluti-nana, species for which mating disruption hasproven highly effective (Gut et al. 2004), is very rapid(Table 1). Stelinski et al. (2003a, b) postulated thatlack of LLA may be related to higher propensity forhabituation; however, this has yet to be proven. Fur-thermore, LLA lasts only 10Ð12 min in the leafrollersC. rosaceana and P. pyrusana. Only for C. pomonelladoes this effect last for upwards of 1 h. The second andmore important factor suggesting that LLA is not animportant contributor to mating disruption is that thephysiological effect is induced at airborne concentra-tions of pheromone that are much higher than the 1 to2 ng/m3 achieved with synthetic pheromone dis-pensers in the Þeld (Koch et al. 1997, 2002). However,the presence of LLA in each species does seem to be

584 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 98, no. 4

inversely related to their known susceptibility tomating disruption (Table 1).

It has been suggested that minutes- to hours-longexposure of male moths in the Þeld to pheromonedispensers such as polyethylene tubes (Stelinski et al.2003b) or repeated visits to such dispensers (Stel-inski et al. 2003b, Judd et al. 2005) might causeLLA. However, Stelinski et al. (2004, 2005) foundthat feral C. rosaceana, A. velutinana, G. molesta, andC. pomonella approach and remain near such phero-mone dispensers for very brief periods (�30 s) inorchard plots and do not receive the required pher-omone exposure to induce LLA. It is yet to be deter-mined whether repeated visits to dispensers of syn-thetic pheromone induce LLA.

Peripheral adaptation occurs when olfactory recep-tor neurons are being directly challenged by small andlargeamountsofpheromone(KuenenandBaker1981;Baker et al. 1988, 1989), but the effect is often rapidlyreversible in clean air. Reductions of behavioral re-sponsiveness seem to last much longer than peripheraladaptation in pheromone preexposed moths, suggest-ing that habituation is involved (Bartell and Roelofs1973; Figueredo and Baker 1992; Rumbo and Vickers1997; Stelinski et al. 2003a, b; Judd et al. 2005). How-ever, given that effective mating disruption occurs inthe Þeld at pheromone concentrations that are muchlower than those required to desensitize moths byadaptation or habituation (Schmitz et al. 1997, Rumboand Vickers 1997, Judd et al. 2005), the relevance ofthese mechanisms as important contributing factors tomating disruption should be questioned. Tortricidmoth species are known to closely (�0Ð100 cm) andbrießy (�2Ð30 s) approach polyethylene tube pher-omone dispensers (Stelinski et al. 2004, 2005). Deter-mining the fate of attracted moths leaving these syn-thetic dispensers of pheromone should help elucidatewhether effects of preexposure during these visitscontribute to mating disruption or whether compet-itive attraction between dispensers and feral femalesis the primary disruptive mechanism.

Acknowledgments

We thank Kevin Vogel, Meghan McAdam, Danny Bang-hart, and Noah Ressa for diligent maintenance of insectcolonies. We gratefully acknowledge two anonymous re-viewers for improving an earlier version of the manuscript.This research was funded by USDA Grant 34325Ð10585.

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Table 1. Prevalence of long-lasting adaptation among tortricid species versus level of difficulty for meeting requirements for successfulmating disruption as defined by Gut et al. (2004)

SpeciesPresence (and approximate duration)

of long-lasting adaptation

Level of difÞculty in meetingrequirements for successful

mating disruption

C. rosaceana (obliquebanded leafroller)a Present (12 min) DifÞcultP. pyrusana Present (15 min) DifÞcultC. pomonella (codling moth)b Present (60Ð75 min) Moderate to difÞcultArgyrotaenia velutinana (redbanded leafroller)a Absent EasyGrapholita molesta (oriental fruit moth) Absent Easy

a Source data found in Stelinski et al. (2003a, b).b Additional data found in Judd et al. 2005.

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Received 1 February 2005; accepted 13 April 2005.

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