BASE Biotechnol. Agron. Soc. Environ.201115(3),459-470 Focus on:

Theuseofsemiochemicalslow-releasedevicesinintegratedpestmanagementstrategiesStéphanieHeuskin(1,2),FrançoisJ.Verheggen(3),EricHaubruge(3),Jean-PaulWathelet(2),GeorgesLognay(1)(1)Univ.Liege-GemblouxAgro-BioTech.DepartmentofAnalyticalChemistry.PassagedesDéportés,2.B-5030Gembloux(Belgium).E-mail:stephanie.heuskin@ulg.ac.be(2)Univ.Liege-GemblouxAgro-BioTech.DepartmentofGeneralandOrganicChemistry.PassagedesDéportés,2.B-5030Gembloux(Belgium).(3)Univ.Liege-GemblouxAgro-BioTech.DepartmentofFunctionalandEvolutionaryEntomology.PassagedesDéportés,2.B-5030Gembloux(Belgium).

ReceivedonJuly30,2010;acceptedonJanuary11,2011.

Thedevelopmentofintegratedpestmanagement(IPM)strategiesisincreasingsincemanyproblemsappearedwiththeuseofsyntheticpesticides.Semiochemicals–informativemoleculesusedininsect-insectorplant-insectinteraction–aremoreandmoreconsideredwithinIPMstrategiesasalternativeorcomplementaryapproachtoinsecticidetreatments.Indeed,thesespecies-specificcompoundsdonotpresentanyrelatedadverselyaffectationofbeneficialorganismsanddonotgenerateanyriskofpestinsectresistanceasobservedwithinsecticides.Becauseoftheircomplexbiologicalactivity,theirdispersionintheenvironmenttobeprotectedormonitoredneedstheelaborationofslow-releasedevicesensuringacontrolledreleaseofthebiologicallyactivevolatilecompounds.ThesesensitivemoleculesalsoneedtobeprotectedfromdegradationbyUVlightandoxygen.Manystudieswereconductedonestimationofrelease-ratefromcommercializedorexperimentalslow-releasedevices.The influenceof climatic parameters anddispenser typewere estimatedbyprevious authors in order to provideindicationsabouttheon-fieldlongevityoflures.Thepresentreviewoutlinesalistofslow-releasestudiesconductedbymanyauthorsfollowedbyacriticalanalysisofthesestudies.Keywords.Integratedpestmanagement,pestinsects,pheromones,controlledrelease,chemicalecology.

L’utilisation de systèmes à libération lente de sémiochimiques dans les stratégies de lutte intégrée.Ledéveloppementdesstratégiesdelutteintégréeestencroissancedepuisquedenombreuxproblèmessontapparussuiteàl’utilisationabusiveetnonraisonnéedespesticidesdesynthèse.Lessémiochimiques(moléculesinformativesutiliséesdanslesinteractionsinsecte-insecteouplante-insecte)sontdeplusenplusconsidérés,auseindesstratégiesdelutteintégrée,commedesapprochesalternativesou complémentaires aux traitements insecticides.En effet, ces composés, spécifiques à chaque espèce, ne présentent pasd’effetsnégatifsrelatésdanslalittératureenverslesorganismesbénéfiquesetn’engendrentaucunrisquederésistancechezlesinsectesravageurscommeobservésaveclesinsecticides.Enraisondeleuractivitébiologiquecomplexemaisaussideleurrisquededégradationparlesrayonsultravioletsouàl’oxygènedel’air,leurdispersiondansl’environnementnécessitel’élaboration de systèmes garantissant une libération lente et contrôlée des composés volatils actifs. Plusieurs études ontétémenéesafind’estimerletauxdelibérationdesystèmescommercialisésoumisaupointenlaboratoire.L’influencedesparamètresclimatiquesetdutypedediffuseuraétéestiméeparplusieursautresauteursafindefournirdesindicationssurlalongévitédesdiffuseurssurterrain.Laprésenterevueanalyseetcritiqueunelisted’étudesdesystèmesàlibérationlente.Mots-clés.Gestionintégréedesravageurs,insectenuisible,phéromone,libérationcontrôlée,écologiechimique.

1. IntroductIon

During the seventies and the eighties, environmentaland social side effects of synthetic pesticides led tothedevelopmentofintegratedpestmanagement(IPM)

programsintheUSAandAsia.Sincethen,manyIPMstrategieshavebeensuccessfulworldwide.Indeed,theoveruseofinsecticidespresentsmanydrawbackslikethe appearance of insect resistances, environmentalconcerns, and risks for human health.Moreover, the

460 Biotechnol. Agron. Soc. Environ. 201115(3),459-470

action of pesticides is generally non species-specificwith the risk of disturbing the natural ecologicalequilibrium(Witzgall,2001).

IPMimpliesvariousstrategies,whichideallyhaveto be combined at different levels. In 1998, Kogandefined IPM as “a decision support system for theselectionandtheuseofpestcontroltactics,singlyorharmoniouslycoordinatedintoamanagementstrategy,based on cost/benefit analyses that take into accounttheinterestsofandtheimpactsonproducers,societyandtheenvironment”.

The efficiency of these approaches needs aninterdisciplinary collaboration between agronomists,entomologists, chemists having an experience inpest behaviors, technologists, and finally the cropproducers. It isparticularly truewhen the IPMtacticimplies theuseof insect semiochemical slow-releasedevicesastoolstomodifythebehaviorofinsectpests.Indeed, the release systems must be economical,effective, environmentally safe without harmfulside effects, and field-tested to prove the efficiencytowards targeted insects before legal authorizationand commercialization. The validation of all thesemanufacturing steps is not possible without theinteractionofmulti-disciplinaryfieldsofknowledge.

On anhistorical point of view, the role of sexualpheromonesininsectmatingwasdemonstratedinthelate19thcentury.Thecharacterizationofthefirstinsectsex pheromone was established in 1959 (Butenandtet al.,1959)andwasisolatedfromfemaleBombyx mori(Lepidoptera).Thistechnologicaloverhangled,inthemid-seventies,toanincreaseofcommercialactivitiesinsynthesisofsemiochemicalspreviouslyidentifiedaspotentialagentsforcontrollingpests.Thiswasthefirststeptoreplacesyntheticinsecticideswithpheromoneproducts(Cork,2004).Inthesametime,theresearchon insect chemical communication grew up and ledto the emergence of a new scientific discipline: thechemical ecology. In 1971, Edward Wilson gave adefinitionofthechemicalcommunication:“thisistheemission of a stimulus by one individual andwhichinduces a reaction in anotherone, the reactionbeingbeneficial to the emitter, to the receptor or both”. Inparallel,thegaschromatographyappearedinchemistryand brought simplicity in identification of volatilemolecules.Rapidly, theeconomical interestforusingpheromone compounds in pest controlswas updatedandincludedinintegratedpestmanagementprograms(Brossut,1997).

The present review deals with the developmentof the major approaches to control pests by usingsemiochemical (chemical communication signal)slow-release devices. Furthermore, the authors willfocuson the techniques implemented in the studyofreleaseratesandontheestimationofon-fieldlongevityofsemiochemicaldevices.

2. SeMIocheMIcaLS

2.1. definitions

Semiochemicals, from semeion (inGreek) or signal,canbedefinedaschemicalsemittedbylivingorganisms(plants, insects, etc.) that induce a behavioral or aphysiological response in other individuals. Thesecompoundscanbeclassifiedintwogroupsconsideringwhether they act as intraspecific (pheromones) orinterspecific(allelochemicals)mediators.Allelochemi-cals include allomones (emitting species benefits),kairomones(receptorspeciesbenefits)andsynomones(both species benefit) (Figure 1). However, a singlechemical signal may act as both as pheromone andallelochemical.

Therearedifferenttypesofpheromonesaccordingto the response they induce on the perceivingindividuals.Themostcommonarepresentedhereafter(Brossut,1997;Cork,2004):– Sexpheromonesaregenerallyproducedbyfemales of a species in order to attractmales of the same species for mating. Some exceptions exist where malebutterflies(e.g. Bicyclus anynana)producesex pheromonestoseducefemalesduringthecourtship (Nieberdingetal.,2008).Sexpheromonesconsistin individualmoleculesorspecificblendofcompounds inagivenratio.Themoststudied,andusedinIPM, sexpheromonesarethatemittedbyLepidoptera;– Aggregationpheromonesarereleasedbyonegender of a species to attract individuals (both sexes) of the same species in order to exploit a specific resource(food,appropriatematingsite,etc.).They aremainlyemittedbyColeopterousspecies;– Alarm pheromones alert conspecifics in case of threats. Generally the response behavior results in dispersion of congeners. These pheromones, characteristicofsocialorgregariousinsects,occur insomeimportantinsectpestsincludingAphididae

Figure 1.Semiochemicals–Les sémiochimiques.

Semiochemicals

Pheromones Allelochemicals

Intraspecifi

c interactio

ns Interspecific interactions

– Sex pheromones– Aggregation pheromones– Alarm pheromones– Trail pheromones– Host marking pheromones

– Allomones (+ emitter)– Kairomones (+ receptor)– Synomones (+ emitter AND receptor)

461

and Thripidae. This class of pheromones has potentialinIPM(Verheggenetal.,2010);– Trail pheromones are present in social colonies toindicatethetrailtobefollowedwhensomescout insects locate food resource.Walking insects, like ants,typicallyproducethesepheromones;– Hostmarking pheromones reduce the competition between members of the same species, like it is observed in parasitoids thatmark a host inwhich theyhavelaidanegg.

2.2. chemistry and properties of semiochemicals

Pheromones and semiochemicals in general, consistinawiderangeoforganicmoleculeswhichcouldbevolatileornon-volatile.Non-volatile semiochemicalsinclude cuticular hydrocarbons, acting in materecognition or in cannibalism regulation of severalinsect species. Wilson et al. (1963) suggested thatthe volatile pheromones naturally exploited in insectcommunication have between 5 and 20atoms ofcarbon with molecular weights ranging from 80 to300.Thosehavingamolecularweightabove300arenot sufficiently volatile to allow a communication atlongdistance.Cork(2004),inhisPheromone manual,cites the major pheromones identified in moths andbutterfliesaccordingtotheirchemicalclasses.

Thebiosynthesisofsuchsemiochemicalmoleculesissupposedtocomefromthefood.Theyaregenerallysynthesizedde novobyexcretingcells.Thebiosynthesisof sexual pheromones iswell known in LepidopteraandDiptera.Inbothcases,thepheromonesconsistinlong carbon chains (alcohols, aldehydes and acetatesforLepidoptera;hydrocarbonshavinghighmolecularweight for Diptera) derived from themetabolism offattyacids(Brossut,1997).

The efficiency of semiochemical substances inchemicalcommunicationdependsonvariousphysicalproperties including chemical nature, volatility,solubility and lifetime of the molecules in theenvironment.An important abiotic factor controllingtheeffectivenessofthepheromonesisthetemperaturewhich increases thediffusionof themolecules in theair. The stability of these volatile compounds alsoaffectstheefficiencyinIPM.

3. IPM StrategIeS uSIng SeMIocheMIcaLS

There aremanybenefits to formulate semiochemicalsubstances in integrated pest management outline.These molecules are naturally occurring and aregenerally environmentally friendly. Additionally, inIPM strategies the compounds are generally used atconcentrationsclosetothosefoundinnatureand,due

to theirhighvolatility, theycanactat longdistancesand dissipate rapidly. The risk to human health andenvironment is also reduced compared to pesticides.Forallthesereasons,semiochemicalsarecompoundsofpotentiallyhighinterestinIPM.

3.1. IPM strategies

Various strategies exist depending on the goalsand scopes to achieve. Some of them are describedhereafter.

Monitoring. Monitoring of insect populations hasgenerally three purposes: to detect the presence ofinvasive pests; to estimate the relative density of apestpopulationat a specific site; to indicate thefirstemergence or peak flight activity of a pest speciesinagivenarea.Theappropriate control actions (e.g.local insecticide treatment) can then be carried out(Weinzierletal.,2005).

trapping. Trapping with pheromone lures is amechanical control action that consists in removinglargenumberofpestsinanareaaftermonitoringstep.The traps can be used simultaneouslywith a killingsubstance (“lure and kill” strategy) which has thebenefitofnotbeingindirectcontactwiththecrop.Thistechniqueisalsousefulinstored-productpestcontrol(Phillips,1997).

Mating disruption. The technique of matingdisruption by using species-specific sex pheromonesinlargequantityisprincipallyappliedtocontrolmothpopulations in orchards. In moth, females generallyreleasesexpheromones toattractmales,at relativelylongdistances (several kilometers), for reproduction.Thefemaleslaytheireggsonorchardtreesandlarvaedevelopinsidefruitswhicharethennomoreeatable.

Matingdisruptionconsistsinaffectingthebehaviorof males in their search of a female for matingby releasing high quantities of synthetic femalepheromones in the atmosphere. The disruption ofmalescanbeachievedbyaffectingdifferentbiologicalmechanismswhichwereoriginallydefinedbyBartell(1982).ThesemechanismshavebeenrecentlyrevisedbyMilleretal.(2006a,2006b)andweresynthesizedin a review by Stelinski (2007). To be an efficienttechnique to control pests, surrounding orchards orfieldsmustideallyalsobepartofIPMprograms.Whenthepopulationofmothistoolarge,matingdisruptioncanbeassociatedwithtargetedpesticidesatlocalandpunctualapplications.

Push-pull strategy. Also called stimulo-deterrentdiversion, push-pull strategy is a more recentapproach than the other described IPM practices. It

462 Biotechnol. Agron. Soc. Environ. 201115(3),459-470

consists in a combination of repellent and attractivestimulimodifying the behavior of insect pests and/orof their natural enemies. The insects are deterred orrepelledawayfromthecrops(pushstrategy).Theyaresimultaneously attracted by lures (pull strategy) andconcentrated inotherareaswhere theyare trappedorkilled in a controlled manner. This strategy requiresa clear understanding of the pest biology, chemicalecology,andoftheinteractionswithhosts,conspecificsandnaturalenemies(Cooketal.,2007).

Biological control. Biological control of the insectpestsisdefinedbyStoner(2004)as“theuseoflivingorganisms (insects or pathogens) to suppress pestpopulations, making them less damaging than theywouldotherwisebe”.Insectnaturalenemies,alsocalledbeneficial insects, can be classified in two classes:predatorsandparasitoids.Beneficialinsects,sometimesexotic,canbeartificiallyintroducedininfestedfields.This practice must be cautiously managed in orderto verify that no-indigenous specieswill not have anadverseenvironmentalandeconomicimpact,likeitwasthecasewith the introductionof theAsian ladybeetle Harmoniaaxyridis Pallas (Coleoptera:Coccinellidae)(Huelsmanetal.,2002;Royetal.,2006;Brownetal.,2008).

Anewconceptconsistsinattractinglocalbeneficialinsects on crops bymeans of kairomonal substancesasexplainedinHeuskinetal.(2009)forthebiologicalcontrolofaphidswiththeirparasitoidwasps(Aphidius ervi Haliday (Hymenoptera: Braconidae)) (Du et al.,1998;Powelletal.,2003)andtheirhoverfliespredators(Episyrphus balteatus De Geer (Diptera: Syrphidae))(Francisetal.,2005;Verheggenetal.,2008;Verheggenetal.,2009).

4. SLow reLeaSe oF SeMIocheMIcaLS

4.1. Slow release dispensers

Majorvolatilesemiochemicalsbeingextremelyunstableduetotheirchemicalstructure,itisnecessarytoformulatethem so that they are protected from degradation byUVlightandoxygen.Moreover,theformulationmustensure a controlled release of semiochemicals.To beefficientinIPMstrategies,semiochemicalslow-releasedevicesmusthaveparticular specifications: the aerialconcentrationafterreleasemustbesufficientlyhightobedetectedbyinsects;thereleaseofsemiochemicalsmustbeeffectiveduringalltheperiodofinsectoccurrence;theproductionofdispensermustbereproducible.Theapplicationofdispensersmustberealizedearlyintheseasonwhenthepestdensityisnottoohigh,giventhattheirreleaserates,forthemajorityofdevices,decreasewithtime(Witzgall,2001).

Several formulations and dispensers have beendeveloped and commercialized with various slow-release capacities. Some examples of dispensersare described hereafter. The majority of theminvolve mating disruption of moth. Three groupscan be distinguished: solid matrix dispensers, liquidformulations to sprayand reservoirsof formulations.On an historical point of view, the first related andthemostcommonlyusedpheromonedispenseris thenaturalrubberseptum(Roelofsetal.,1972).

Solidmatrixdispensersarehand-appliedoncropsor in orchards.The semiochemicals are incorporatedinasolidmatrix.Becauseofthevariousmaterialsthatcanbeusedtoconstituteamatrix,thereleaseratesforasinglemoleculecandiffersignificantlyfromonedevicetoanother,asdemonstratedbyGolubetal.(1983)forthemeasurementofreleaserateofgossyplure((Z,Z)-and (E,Z)-7,11-hexadecadien-1-yl acetate), the sexpheromoneblendofthepinkbollworm(PectinophoragossypiellaSaunders,Lepidoptera:Gelechiidae)fromdifferentformulations.

Themostcommonsolidmatrixusedindispensersare polyethylene tubes (twist tie dispensers likeIsomate®), polyethylene sachets (Torr et al., 1997),polyethylene vials (Johansson et al., 2001; Zhanget al., 2008), membrane dispensers (CheckMateCM-XL®),spiralpolymerdispensers(NoMateCM®)(Tomaszewska et al., 2005), polymer films, rubbersepta(McDonough,1991;Möttusetal.,1997),rubberwicks,polyvinylchloride(PVC),hollowfibers(Golubet al., 1983), impregnated ropes, wax formulations,gel-likedispensersmatrices(Atterholtetal.,1999).

Drawbacks encountered with solid matrixdispensers include the difficulty to maintain a zero-order release kinetic (constant release rate) duringa long period of time, and the decreasing of aerialsemiochemical concentration with the distance fromthedispenser.Consequently,thesedispensersareonlyefficient to attract and trap insects at short distance.A way to by-pass this problem is to apply devicesin sufficient sites in the crop or in the orchard. Theresulting disadvantage is the highmanpower neededfor application of dispensers in the fields. Anothershortcoming is the non biodegradability of theformulatedpolymers(Stipanovicetal.,2004).

The effective lifetime of the biggest solidmatrixdispenserscanrangefrom60to140days.

Sprayableslow-releaseformulationsaregenerallycomposedofabiodegradableliquidmatrixcompoundin which the semiochemical is dissolved. Regularly,other components can be added to protect thesemiochemicals, likeUV-stabilizers,antioxidantsandsurfactants. Frequently, the sprayable formulationconsists in a micro-emulsion, resulting in polymericmicro-beads containing the semiochemicals (micro-encapsulatedpheromones)dispersedinaliquidmatrix

463

(deVlieger,2001).In1999,Atterholtetal.studiedthereleaseratesoforientalfruitmothsexualpheromonesformulated in aqueous paraffin emulsions as carriermaterial.

Thetimeofefficiencyofsuchformulationsrangesfrom days to weeks depending on environmentalfactors, microbeads size, release capacities, and thepheromoneschemicalproperties(Welteretal.,2005).

The major advantage of sprayable formulationscomparedtosolidmatrixdispensersis that theentirecropcanbetreated.

Reservoirdispensersgenerallyconsistintwoparts,areservoirandadiffusionarea.Hofmeyretal.(1995)described a dispenser consisting in glass tube actingas a pheromone-impermeable reservoir attached to ashortpolyethylenetubethroughwhichthepheromonecan diffuse. Another reservoir was tested by Shemetal.(2009)asrepellentallomonedeviceagainsttsetseflies.Theupperpart(reservoir)wasmadeofaluminumandthediffusionareawasmadefromTygon®silicontubing.

Aerosolemitters(e.g.Suttera®puffer),consistinginelectronicallyprogrammedreservoirsofformulation,release large amounts of pheromone by means of apressurizedaerosol.Puffscanbeemittedatfixedtimeintervals.The advantage of this system is the use offewerdispenserspersurfacetotreat.

Reservoirsystemsarethemostsuitabletoapproachzero-orderreleasekineticofsemiochemicals(Atterholtetal.,1999).

4.2. Slow release rate studies

Release rate study does not specify the biologicalefficiencyofasemiochemicaldeliverydispenser,butgivesanideaofthereleasekineticovertimeaccordingtoclimaticconditions.Manydispensersdonotguaranteeareleaseatasteadyrate,inducingadecreaseofreleaserate during the season.However, themost importantis toknowatwhichmoment thequantityofreleasedsemiochemicalisnomoresufficienttoinfluenceinsectbehaviour,andtochangethedispenser.

techniques to estimate release rates.Giventhatitisnoteasyandreliabletomeasurereleaseratesdirectlyinthefield,estimationsofsemiochemicalreleaseratesfrom formulations were performed in laboratory orsemi-controlledconditions.Threedifferenttechniqueswere improved over time: the gravimetric method,the total organic solvent extraction, and thedynamiccollectionofvolatiles.Thefirstprocedure,lessandlessused,consistsinweighingdispensersatdailyintervalsover the season and to determine the percentage ofmass loss with time. The major weakness of thistechniqueisthelackofprecisionandaccuracytosetupreleaserates.Sometimes,themassincreasesinstead

ofdecreasingduetothepresenceofhumidityanddustdepositedonthedispensers.

The second technique implies the total organicsolventextractionofsemiochemicalsfromdispenserstodetermine the residualconcentrationofcompoundinfield-ageddevices.Theconditiontohaveanoptimalpheromoneextractionimpliesthecompletedissolutionofcompoundcontainedinthedispenser(Lopezetal.,1991; Möttus et al., 1997). This technique has thebenefittopermittoqualifyandquantifythepheromoneand itspotentialvolatiledegradationproductsbygaschromatography (GC) analysis. However, it presentsa risk of not permitting detection of non-volatiledegradation products by GC (Tomaszewska et al.,2005).

Thethirdmethodtodeterminereleaserateconsistsin a dynamic sampling and an adsorbent trapping ofvolatile compounds from field-aged dispensers. Theevolutionofreleaserateisestimatedaccordingtofield-ageofdevices.Itisessentialtomeasuretherateeverytime in the sameconditionsofatmosphericpressure,temperature, relative humidity and airflow to obtainanalogousanalysesover time.Thevolatilecollectionsystemisgenerallycomposedofachamberinwhichair flows through the dispenser. The carried volatilesemiochemicalsaretrappedonanadsorbentcartridge,followedbysolventextractionorthermaldesorption,andGCanalysis.VariousadsorbentshavebeentestedlikeSuperQ(Mayeretal.,1998;Atterholtetal.,1999;Meagher,2002), silicagel (McDonoughetal.,1992;Pop et al., 1993), Tenax (Cross, 1980), Carbograph,PorapakQ (Cross et al., 1980), activated charcoal,polyurethanefoam(PUF)(VanderKraanetal.,1990;Tomaszewskaetal.,2005).Thechoiceoftheadsorbentdependsonthesemiochemicalproperties,andonthemaximum airflow to apply on the cartridge withoutbreakthroughofthecompounds.

Considering the advantages and shortcomingsof the three techniques, the last one is the mostappropriate and accurate in order to estimate releaserateofsemiochemicalsfromdispensers.

release rate studies. The release of volatilesemiochemicals in the atmosphere is reliant on twomajor factors: the diffusion speed of the compoundthrough the dispenser matrix and the evaporationspeedofthemoleculeintheair(Krügeretal.,2002).The first factor depends on the characteristics of thedispenser (type of matrix [Golub et al., 1983], size[Hofmeyr at al., 1995], shape, thickness, distributionofthesemiochemicalinthematrix[Stipanovicetal.,2004])whilethesecondfactor(speedofevaporation)mainly relies on environmental parameters like airtemperature, wind speed, relative humidity, and thephysical properties of the compound itself (Alfaro-Cid et al., 2009; CBC, n.d.). In the case where the

464 Biotechnol. Agron. Soc. Environ. 201115(3),459-470

evaporationprocessofpheromonefromthesurfaceofdispenser isslower than thediffusionstep, thespeedofevaporationisthelimitingfactor,andthefirst-orderreleasekineticequationisconsidered:

C0=Cte-kt,

whereC0istheamountofcompoundinthedispenserat the beginning of evaporation,Ct is the amount ofcompound at time t, and k is the evaporation rateconstant.Incaseofafirst-orderkinetic,ahalfof theamountofthepheromonecompoundwillbeevaporatedafter a time t½, called half-life of the compound(McDonoughetal.,1989;Möttusetal.,2001).

Manystudieswereconductedtogiveanestimationof the release rate of pheromone over time fromdispensers in definite experimental conditions.However,very fewstudiesdealtwith theconceptionof ratekineticpredictivemodelsaccording toabioticparameters(temperature,relativehumidity,windspeed,etc.).Moreover,theseexperimentscheckedparametersonebyoneratherthanconsideringtheircombinationregarding an experimental design to finally obtain arealistic ratemodeling, close to the kinetic expectedonthefield.

table 1 summarizes studies considering the typeof dispenser, the semiochemicals and insects of theresearch,thetargetedcropandthemainconclusionsofthereleaserateevaluation.

Most studies concluded to first-order releasekinetics, semiochemical rates decreasing with timeand release being dependent on the amount ofcompound present in the dispenser.Already in 1979and1981,Butleretal.showedthatalcoholandacetatemolecules (sex pheromones of many moth species)were released from rubber septa following a first-orderkinetic.Indeed,theyconcludedthatpheromonemolecular sizes, double bond positions and isomersconditioned the evaporation rates and the half-lifetimes of the molecules. McDounough et al. (1992)describedamodelingofpheromone(codlingmothsexpheromones)releaseratebydeterminingthehalf-lifetimesofcompoundsdeliveredfromfield-agedhollowplastictubedispensers.In1994,Kehatetal.alsofoundthatthesecodlingmothsexpheromonesweredesorbedfrom field-aged rubber septa dispensers followinga first-order kinetic. Zhang et al. (2008) measuredrelease rate of female sex pheromones of cocoa podborer,Conopomorpha cramerella, frompolyethylenevials placed in a fume hood (20-25°C; 129ft.min-1face velocity). They obtained the same kinetic ofpheromone delivery. PVC-resin controlled releaseformulationsdevelopedbyCorketal. (2008) for thedeliveryofyellowricestemborersexpheromonesweretested at various temperatures (from 22°C to 34°C).Releasesfollowedafirst-orderkinetic.Moreover,the

temperaturehighly influencedpheromone rates,half-livesdecreasingwithanincreaseofthetemperature.

Considering several other studies, temperatureis one of themost important climatic parameter thataffectsvolatile release rates. In1990,VanderKraanand Ebbers determined the influence of temperatureandairvelocityonavarietyofdispensersdeliveringmoth sex pheromones (tetradecen-1-ol acetate). Theauthorsconcludedthattheimpactoftemperaturewasmore important than wind speed on the kinetic ofrelease.Bradley et al. (1995) proposed a linear rate-temperature relationship model to predict release oflight brown apple moth pheromones (E11-14:OAc;E9,E11-14: OAc; Z11-14: OAc) from polyethylenetubingdispensers.Twoyears later,Torr et al. (1997)studiedthereleaseoftsetseflieskairomonalsubstancesfrompolyethylenesachets.Eventhoughreleaserateswere independent of the semiochemical amountpresentinthedispenser,theyincreasedexponentiallywith temperature.Atterholt et al. (1999) investigatedthe release of oriental fruit moth pheromone fromparaffin emulsions at three temperatures from 27°Cto 49°C.At the lowest temperature, the release ratewasconstantovertime(during100days).Thereleaseratewashigherat38°Cand49°C.However, theratedecreasedwithtimeatthesehighesttemperaturesduetopheromoneoxidationanddegradationphenomena.Once again, in 2001, Johansson et al. illustrated theincreaseof sawflies sexpheromone release ratewithtemperature frompolyethylenevialdispensers.Morerecently, Shem et al. (2009) studied the influenceof temperature on the release rate of a blend ofallomones derived from waterbuck odor (carboxylicacids, ketones, 2-methoxyphenol, δ-octalactone), ina reservoir type dispenser, to control tsetse flies.Asexpected, the release rate increased according to thetemperature.

It is not easy to develop and formulatesemiochemicaldeliverysystems,whichguaranteethediffusionofeffectiveamountofcompoundalongtheseason.Withfirst-orderreleasekinetics,semiochemicalratesdecreasequicklyand,asaconsequencedispenserfield-lifeisoftentooshorttocovertheperiodofpestoccurrence.

465

tabl

e 1.Developmentofsem

iochem

icaldispensersandformulationsandreleaseratestudies—

Dév

elop

pem

ent d

es d

iffus

eurs

et f

orm

ulat

ions

et

étu

des d

u ta

ux d

e lib

érat

ion

de sé

mio

chim

ique

s.ty

pe o

f disp

ense

r or

fo

rmul

atio

nSe

mio

chem

ical

s and

targ

et in

sect

Prot

ecte

d cr

opr

elea

se r

ate

stud

ies (

met

hod

of m

easu

rem

ent a

nd

obse

rvat

ions

)r

efer

ence

a. S

olid

disp

ense

rsPolyethylenesachets

Tsetseflies(Diptera:G

lossinidae:

Glossinasp.)kairomones:

1-Octen-3-ol,4-methylphenol

and3-n-propylphenol

Nocrop

(trapping)

Gravimetricandvolatilecollectionmethods.

Releaseratesareindependentoftheamountpresentin

dispenser(zero-orderreleasekinetic),arerelated

directlytosu

rfacearea,inverselyrelatedtowall

thicknessandincreaseexponentiallywithtemperature

Torretal.,1997

Maleaggregationpherom

oneof

Dynastbeetle,S

capa

nes a

ustr

alis

Bsdv.(C

oleoptera:Scarabaeidae):

2-butanol,3-hydroxy-2-

butanone,2,3-butanediol

Coconut

Noratestudy

Rochatetal.,2002

Polyethylenevials

andtubes

(e.

g.Shin-Etsu®)

Lepidopteransexpherom

onesfor

matingdisruption:tetradecen-1-

olacetates(Z9-14:AcandZ11-

14:A

c)

Orchards

Com

parisonofpolyethylenetubesw

ithother

dispensermaterials.

VolatilecollectiononPolyurethanefoam

(PUF)

cartridges+so

lventelution.

Releaseratedependson:typeofdispenser,

tem

perature,w

indvelocity

VanderK

raanetal.,

1990

Codlingmoth,C

ydia

pom

onel

laL.

(Lepidoptera:Olethreutidae),

matingdisruptantblend:(E,E)-

8,10-dodecadien-1-ol/dodecan-

1-ol/tetradecan-1-ol

Orchards

Volatilecollectiononsilicagelcartridges+so

lvent

elution.

Releaserateisfunctionofthechangeof

pheromonecontentw

ithtime(first-orderrelease

kinetic)

McD

onoughetal.,

1992

Sexpherom

onesoflightbrown

applemoth,E

piph

yas

pos

tvitt

ana(W

alker)

(Lepidoptera:Tortricidae):E

11-

14:OAc/E

9,E11-14:OAc/Z

11-

14:OAc

Orchards

Volatilecollection+measureofliquidpherom

one

lengthovertime.

Com

parisonofm

easuredandmodelledpredicted

releaserateconsideringrealon-fieldmeasured

tem

perature(linearreleaserate–temperature

relationship)

Bradleyetal.,1995

Sexpherom

onesofsaw

flies:

Neo

dipr

ion

sert

iferG

eoffr.and

Dip

rionp

iniL

.(Hym

enoptera:

Diprionidae).A

cetateso

fpentadecanol/(2S,3S,7S)-3,7-

dimethyl-2-tridecanol/(2S,3R,

7R)-3,7-dimethyl-2-tridecanol

Pinetrees

Gravimetricmethod.

Releaseratesincreasewithtemperature

Johanssonetal.,2001

466 Biotechnol. Agron. Soc. Environ. 201115(3),459-470 ta

ble

1 (c

ontin

ued

1).D

evelopmentofsem

iochem

icaldispensersandformulationsandreleaseratestudies—

Dév

elop

pem

ent d

es d

iffus

eurs

et

form

ulat

ions

et é

tude

s du

taux

de

libér

atio

n de

sém

ioch

imiq

ues.

type

of d

ispen

ser

or

form

ulat

ion

Sem

ioch

emic

als a

nd ta

rget

inse

ctPr

otec

ted

crop

rel

ease

rat

e st

udie

s (m

etho

d of

mea

sure

men

t and

ob

serv

atio

ns)

ref

eren

ces

a. S

olid

disp

ense

rsPolyethylenevials

andtubes

(e.

g.Shin-Etsu®)

Femalesexpherom

onesofcocoa

podborer,C

onop

omor

pha

cra

mer

ella

(Snellen)

(Lepidoptera:Gracillariidae):

(E,Z,Z)-and(E

,E,Z)-4,6,10-

hexadecatrienylacetatesand

correspondingalcohols

Cacao,

Theo

brom

a ca

caoL.

Totalsolventextractionmethod.

First-orderreleaserate

Zhangetal.(2008)

Rubbersepta

Alcoholandacetatemolecules

foundassexpheromonesof

variousmothspecies

Orchards

Totalsolventextractionmethod.

Pherom

onemolecularsizeisoneofthemajorfeatures

determiningevaporationratesinrubbersepta.

Doublebondpositionsandisom

ersconditionthehalf-

lives

Butleretal.,1979;

Butleretal.,1981

Sexpherom

onesofcodlingmoth,

Cyd

ia p

omon

ellaL.(Lepidoptera:

Olethreutidae):(E,E)-8,10-

dodecadien-1-ol

Appleandpear

orchards

VolatilecollectiononPorapakQcartridges+so

lvent

elution.

Releaseratesd

ecreasewithfieldagingofdispensers

Kehatetal.,1994

Hollowfibers

Sexpherom

oneblendofthepink

bollworm(P

ectin

opho

ra

gos

sypi

ellaSaunders

(Lepidoptera:Gelechiidae):

(Z,Z)-and(E

,Z)-7,11-

hexadecadien-1-ylacetate

Orchards

Totalsolventextraction.

Com

parisonofreleaserateforvariousdevices:hollow

fibers,redrubbersepta,redrubberwick.Rateis

differentaccordingtothetypeofm

atrix.

Golubetal.,1983

Plasticdispensers

(PV

C,PVC-resin,

etc.)

Sexpherom

onesofH

elic

over

pa z

ea(B

oddie)(L

epidoptera:

Noctuidae):(Z)-11-hexadecenal/

(Z)-9-hexadecenal/(Z)-7-

hexadecenal

Cornandcottonfields.

VolatilecollectiononTenaxcartridges+so

lvent

elution.

Lineardecreaseofreleaseratewithtime.

Lopezetal.,1991

Sexpherom

onesofyellowrice

stemborerS

cirp

opha

ga i

ncer

tula

s(Walker)(L

epidoptera:

Pyralidae):(Z)-9-hexadecenal/

(Z)-11-hexadecenal

Ricecrops

Totalsolventextractio

Halflivesofp

heromonedecreasewithanincreaseof

temperature.

First-orderreleaseratekinetic

Corketal.,2008

467

tabl

e 1

(con

tinue

d 2)

.Developmentofsem

iochem

icaldispensersandformulationsandreleaseratestudies—

Dév

elop

pem

ent d

es d

iffus

eurs

et

form

ulat

ions

et é

tude

s du

taux

de

libér

atio

n de

sém

ioch

imiq

ues.

type

of d

ispen

ser

or

form

ulat

ion

Sem

ioch

emic

als a

nd ta

rget

in

sect

Prot

ecte

d cr

opr

elea

se r

ate

stud

ies (

met

hod

of m

easu

rem

ent a

nd

obse

rvat

ions

)r

efer

ence

B. S

pray

able

form

ulat

ions

Paraffinem

ulsions

Orientalfruitm

oth

Gra

phol

ita

mol

esta(B

usck)(Lepidoptera:

Tortricidae)matingdisruptant

blend:(Z)-8-dodecen-1-yl-

acetate/(E)-8-dodecen-1-yl-

acetate/(Z)-8-dodecen-1-ol

Orchards

VolatilecollectiononSuperQcartridges+solventelution.

Releaserate:

-isd

ependentoftheformulationandtheevaporative

surfacearea;

-increaseswithtemperature

Atterholtetal.,1999

Microcapsules:

pheromone

immobilizedona

poroussubstrate

coatedwithapolym

er

filmmem

brane

Sexpherom

onesofcodlingmoth,

Cyd

ia p

omon

ellaL.(Lepidoptera;

Olethreutidae)(codlem

one:

(E,E)-8,10-dodecadien-1-ol)and

gypsymoth,L

yman

tria

dis

parL

.(Lepidoptera:Lym

antriidae)

(disparlure:(Z)-7,8-epoxy-2-

methyloctadecane)

Orchards

Gravimetricmethod.

Releaseratedependsoncoatingofthemicrocapsule,

surfacearea,microporevolum

e

Stipanovicetal.,

2004

Hom

e-madereservoir

dispensers:glassand

polyethylenetubing

Pherom

onetrapblendagainst

falsecodlingmoth,C

rypt

ophl

ebia

l

euco

treta(M

eyr.)(L

epidoptera:

Tortricidae):(E)-7-dodecenyl

acetate/(E)-8-dodecenylacetate/

(Z)-8-dodecenylacetate

Orchards

Gravimetricmethod.

Releaserateisfunctionofthesizeofpolyethylenetubing

Hofmeyretal.,1995

Reservoirwithsilicon

diffusionarea

Blendofallomones(w

aterbuck

odour)(carboxylicacids,

ketones,δ-octalactone,

2-methoxy-4-methylphenol)

againsttsetsefly(Diptera:

Glossinidae:G

loss

inasp.)

Nocrop

Gravimetricmethod.

Releaserateisdependentofthetemperature.The

com

poundsintheblendinteractwitheachother.The

ratekineticisdifferentforonecom

pound(zero-order)

andfortheblend(fi

rst-order)

Shem

etal.,2009

468 Biotechnol. Agron. Soc. Environ. 201115(3),459-470

5. concLuSIon

Attheendofthisreview,twoquestionsremain:whatkindofdispenseristhebestinIPMprograms?Whatisthelifetimeofdispenserintermsofsemiochemicaldiffusionefficiency?

Toanswerthefirstquestion,thechoiceofdispenser(solid matrix, formulation, reservoir, puffer) willmainlydependontheneedsofthecropfarmers,takinginto account the labor and the manpower costs toimplementIPMstrategies.Otherimportantdecisionalcriteriaarethetargetedpest,theseasonofoccurrenceoftheinsects(withtheknowledgeofthemeanclimaticconditions) and the IPM tactic itself. Moreover,environment protection can also be determinativein the dispenser selection. Biodegradable matrix,environmentally safe, could be preferred as slow-release device material for semiochemical delivery.Alfaro-Cidetal.(2009)recentlyattemptedtodevelopan eco-friendly biodegradable dispenser for codlingmothmatingdisruption.Additionallythisexperimentalsystem seemed to have small sensitivity to climaticconditions.

The secondquestion implies theknowledgeof thesemiochemical release rate kinetic. As demonstratedall along the review, this kinetic relies on the type ofmolecule,thedispenser,andtheclimaticconditions.Theperspective to develop case by case (semiochemical-dispenser) predictive slow-release models taking intoaccounttheclimaticparametersisanidealbutdifficultapproach. Experiments conducted to reproduce theenvironmental conditions faced the constraint that thefluctuationsobservedinfieldaretoounpredictableandrandom to be duplicated in laboratory.The laboratorystudies can only predict limitations of use in fixedconditionsandgivetheoreticalinformationondispenserlifetime. Furthermore, such studies are generally timeandmoneyconsuming.Forthesereasons,thebestwayto estimate diffusion efficiency consists in regularlymeasuring the residual semiochemical quantity and/ordeterminingreleaseratefromfield-ageddispensers.Thisapproach,generallylesstimeconsuming,givesadirectindicationofthedispenserreleaseeffectivenessandthemomenttoreplacepheromonedeliverysystemonfield.

Inconclusion,theperspectivesofsemiochemicalsuse in IPMprograms seem tobepromisingwith theincreasing worldwide biological agriculture. Slow-release dispenser and formulation improvement willcontinue with the contribution of multiple scientificfields of research (entomology, chemistry, ecology,etc.)andthecropfarmerskills.

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