Optimization of native biocontrol agents, with parasitoids ... · Optimization of native biocontrol agents, with parasitoids of the invasive pest Drosophila suzukii as an example

University of Groningen

Optimization of native biocontrol agents with parasitoids of the invasive pest Drosophilasuzukii as an exampleKruitwagen Astrid Beukeboom Leo W Wertheim Bregje

Published inEvolutionary Applications

DOI101111eva12648

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Citation for published version (APA)Kruitwagen A Beukeboom L W amp Wertheim B (2018) Optimization of native biocontrol agents withparasitoids of the invasive pest Drosophila suzukii as an example Evolutionary Applications 11(9) 1473-1497 httpsdoiorg101111eva12648

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Download date 02-06-2020

Evolutionary Applications 2018111473ndash1497 emsp|emsp1473wileyonlinelibrarycomjournaleva

Received30October2017emsp |emsp Revised3May2018emsp |emsp Accepted8May2018DOI 101111eva12648

R E V I E W S A N D S Y N T H E S E S

Optimization of native biocontrol agents with parasitoids of the invasive pest Drosophila suzukii as an example

Astrid Kruitwagen emsp|emspLeo W Beukeboomemsp|emspBregje Wertheim

ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicensewhichpermitsusedistributionandreproductioninanymediumprovidedtheoriginalworkisproperlycitedcopy2018TheAuthorsEvolutionary ApplicationspublishedbyJohnWileyampSonsLtd

GroningenInstituteforEvolutionaryLifeSciencesUniversityofGroningenGroningenTheNetherlands

CorrespondenceAstridKruitwagenGroningenInstituteforEvolutionaryLifeSciencesUniversityofGroningenGroningenTheNetherlandsEmailajkruitwagenrugnl

Funding informationNederlandseOrganisatievoorWetenschappelijkOnderzoekGrantAwardNumberALWGR20156

AbstractThedevelopmentofbiological controlmethods for exotic invasivepest specieshas becomemore challenging during the last decade Compared to indigenousnaturalenemiesspeciesfromthepestareaoforiginareoftenmoreefficientdueto their long coevolutionary history with the pest The import of these well-adaptedexoticspecieshoweverhasbecomerestrictedundertheNagoyaProtocolonAccessandBenefitSharingreducingthenumberofavailablebiocontrolcandi-datesFindingnewagentsandwaystoimproveimportanttraitsforcontrolagents(ldquobiocontroltraitsrdquo)isthereforeofcrucialimportanceHerewedemonstratethepotentialofasurprisinglyunder-ratedmethodforimprovementofbiocontroltheexploitationofintraspecificvariationinbiocontroltraitsforexamplebyselectivebreedingWe propose a four-step approach to investigate the potential of thismethodinvestigationoftheamountof(a)inter-and(b)intraspecificvariationforbiocontroltraits(c)determinationoftheenvironmentalandgeneticfactorsshap-ingthisvariationand(d)exploitationofthisvariationinbreedingprogramsWeillustrate this approachwith a case studyonparasitoids ofDrosophila suzukii ahighly invasivepestspecies inEuropeandNorthAmericaWereviewallknownparasitoidsofD suzukiiandfindlargevariationamongandwithinspeciesintheirabilitytokillthisflyWethenconsiderwhichgeneticandenvironmentalfactorsshapetheinteractionbetweenD suzukiianditsparasitoidstoexplainthisvaria-tion Insight into thecausesofvariation informsusonhowand towhatextentcandidateagentscanbe improvedMoreover itaids inpredictingtheeffective-nessoftheagentuponreleaseandprovidesinsightintotheselectiveforcesthatare limiting the adaptation of indigenous species to the new pestWe use thisknowledge to give future research directions for the development of selectivebreedingmethodsforbiocontrolagents

K E Y W O R D S

artificialselectionbiologicalcontrolagentcoevolutionexoticspecieshostndashparasiteinteractionspestmanagementphenomicsspottedwingDrosophila

1474emsp |emsp emspensp KRUITWAGEN ET Al

1emsp |emspINTRODUC TION

Invasivepestspeciesareaworldwideproblemandcancausehigheconomic losseswhentheyfeedoneconomically importantcrops(Aukema etal 2010 Oliveira Auad Mendes amp Frizzas 2013PimentelZunigaampMorrison2005Pimenteletal2001)Anexam-pleofsuchinvasivepestistheSpottedWingDrosophilaDrosophila suzukii (Speciesauthoritycanbefoundateolorg)ThisAsiaticfruitfly has invaded Europe and North America since 2008 (CalabriaMaacutecaBaumlchliSerraampPascual2012CiniIoriattiampAnfora2012Hauser2011)andcauses largeeconomicdamagetoawiderangeof softandstone fruits (BoldaGoodhueampZalom2010DeRosAnfora Grassi amp Ioriatti 2013 Goodhue Bolda FarnsworthWilliamsampZalom2011Walshetal2011)TosuppressexoticpestpopulationssuchasD suzukiithereisagrowinginteresttodevelopenvironmentalfriendlymanagingmethodstoreducetheapplicationofharmfulpesticidesAtraditionalnonchemicalmethodisbiologicalcontrolthereleaseofapestrsquosnaturalenemytosuppressitspopula-tionThismethodhasbeenproposedasthebestpestmanagementstrategy formaximizing environmental safety and economic prof-itability (Cocketal2010vanLenteren2012b)and isoftenusedincombinationwithotherstrategies(egmasstrappingsanitationcroprotation)aspartofan integratedpestmanagement (IPM)ap-proach(Cocketal2010)

To develop a biocontrol managing strategy a control agentshould be chosen that is highly efficient at suppressing the pestpopulationgrowthExoticpestspecieshoweverhave(initially)nooronlyalimitednumberofnaturalenemiesintheinvasiveareaastheseindigenousnaturalenemiespresentintheinvasiverangearenot(yet)adaptedtothepestThisalsoappliestoD suzukiiasithasonlyfewspeciesofnaturalenemiesintheinvasiveareacomparedtoitsareaoforigin(Asplenetal2015ChabertAllemandPoyetEslinampGibert2012Milleretal2015NomanoMitsuiampKimura2015)ThereforeitiscommonpracticetoimportandreleasenaturalenemiesfromthenativerangeofthepestastheyaremoreefficientduetotheirlongcoevolutionaryhistorywiththepestBiodiversityrisks(DeClercqMasonampBabendreier2011Hajeketal2016)andnewinternationalregulationsinparticulartheNagoyaProtocolonAccessandBenefitSharing(Cocketal2010Hajeketal2016vanLenteren2012b)howevercurrentlylimittheuseofexoticnaturalenemiesandchallengethedevelopmentofbiocontrolforalienpestspeciesAlthough these regulations arevital for theprotectionofnativespeciestheyalsorestrictthenumberofspeciesavailableforbiological control (vanLenteren2012bvanLenterenBolckmansKoumlhlRavensbergampUrbaneja2018)Thesefactorsoftenleadtotheuseoflessfitindigenousratherthanwell-adaptedexoticnaturalen-emiesfornewbiologicalpestmanagementstrategiesHencethereisastrongneedtodevelopmethodstoimproveindigenousnaturalenemiestoincreasetheirefficiencyandsafetyformanagingexoticpestspecies

Accordingtotraditionagentsarechosenbasedoninterspecificvariation(variationbetweenspecies)usingthosespeciesthatseembestatcontrollingthepestinthetargetarea(vanLenteren2012a

LommendeJongampPannebakker2017)Howeverthishasresultedinahighlyvariablesuccessrate(CollierampVanSteenwyk2004)andmaynotmeet thenumberof control agentsneeded in the future(Lommen etal 2017) A promising approach is to exploit naturalgenetic intraspecificvariation (variationwithinspecies) to improvecontrolagentsbyselectingandbreedingonlythoseindividualsofacandidatespecieswiththedesiredcharacteristics(Lommenetal2017)Intraspecificvariationcanbeusedintwoways(a)choosingthe most competent strain (ldquostrain selectionrdquo) for biocontrol and(b)selectingonlythose individualsfrompopulation(s)withdesiredtraitstoformtheparentsofthenextgeneration(ldquoselectivebreed-ingrdquo or ldquoartificial selectionrdquo) Surprisingly although this has beenproposed in the literature repeatedly (Hopper Roush amp Powell1993Hoy1986)andhasbeenwidelyappliedintraditionalagricul-ture (egplantandanimalbreeding)onlya limitednumberof re-searchershavetakenthisapproachtobiocontrolagents(Hoy1986Lommenetal2017)Novelgenetic techniquesarealsobeingde-velopedsuchasRNAinterferenceCRISPRCasgenomeeditingandReleaseofInsectswithDominantLethals(RIDL)(LeftwichBoltonampChapman2016)AlthoughthesetechniquesshowgreatpotentialtheycurrentlycannotbewidelyappliedduetoGMOregulationsandthe perceived high ecological risks (Kolseth etal 2015 Vagravezquez-SalatSalterSmetsampHoudebine2012WebberRaghuampEdwards2015)Selectivebreedingontheotherhandisanenvironmentallysafeandsociallyacceptedmethod

Optimization of traits important for biocontrol via selectivebreedingrequirespresenceofheritablegeneticvariationVariationandexpressionoftraitscanhoweveralsobeduetoenvironmentalvariation(phenotypicplasticity)andorvariationinhowgenotypesrespondtoenvironmentalchange (genotype [G]timesenvironment [E]interaction) (Figure1)Thisphenotypicplasticitymay impede traitoptimizationacrossdifferentenvironmentswhiletheextentofphe-notypicplasticitycanbeheritableInaninterestingmannerthisin-formationcanalsobeexploitedinselectivebreedingforaspecifictargetareaofreleaseincasethereisastrongGtimesEinteractionForexampleagentscanbeselectedforrobustness(highperformancein the range of relevant environmental conditions) or one can in-trogressallelesintheagentenablingadaptationtothetargetareaofrelease(HayesDaetwylerampGoddard2016)Moreoverthesuccessofacontrolagent isalso influencedbythephenotypeof thepest(Figure1)(eglarvalfeedingdepthandthusaccessibilitytoparasit-ization(MeijerSmitSchilthuizenampBeukeboom2016))Theinter-actionofthecontrolagentwiththepestcanhavevariableoutcomesdeathofthepestandortheagentwhichdependsonthegeneticandenvironmentalfactorstheybothencounterInotherwordsthesuccess of the agent depends on the genotype-by-genotype-by-environmental interaction (GhtimesGptimesE) (Agrawal2001ThomasampBlanford2003)Itisthereforeimportanttounderstandthegeneticaswellastheenvironmental factorsthat influencethephenotypeoftheagentforitssuccesstosuppressaspecificpestpopulationintheareaofreleaseOptimizationnotonly includestheuseofher-itablevariation(selectivebreeding)butcanalsoactonnonheritablevariationForexamplealteringspecificenvironmentalconditionsby

emspensp emsp | emsp1475KRUITWAGEN ET Al

additionalmanagementstrategiescanweakenthepestpopulationwhichmakes itmoresusceptible to thecontrolagentand this in-creasesthekillingefficiencyoftheagentMoreoverthekillingef-ficiency of the agent can also be influencedby experience of theagentwiththepestinparticularparasitoidsshowalearningabilitythatmayincreasetheirkillingefficiencyLearningabilitythereforecanalsobeusedtooptimizebiocontrolagents(Giuntietal2015)Henceoptimizationcanalsorelyonnonheritablesourcesofvaria-tion(eglearningofcertainstimuli)

InthisreviewweaddressthequestionHowcanevolutionarybiologyprinciplesbeusedto improvenativenaturalenemiesfortheiruseasbiocontrolagentbyexploitationoftheirintraspecifictrait variationWemainly focus on selective breeding but alsoindicateadditionalapproaches includingexploitationof learningabilityduringbreedingandmanipulationofenvironmentalcondi-tionsintheareaofreleasetoenhancetheimpactofthebiocon-trolagentTofullyappreciatethepotentialofselectivebreedingwefirstproposeafour-stepapproachinwhichweunderlinetheimportanceofanin-depthunderstandingofthosetraitsthatde-termine theperformanceof apotential agentboth its ability tosuppressthepestpopulationinthetargetareaanditsamenabil-itytomassrearingThisincludestheinvestigationofthegeneticvariationandheritabilityofthetraitofinterestandhowthiscanbe exploited as described by Lommen etal (2017) In additionwe show that besides genetic factors knowledge of biotic andabioticfactorsthataffecttheinteractionbetweenthebiocontrolagent and the pest is crucial for optimizationWe illustrate this

approachwithacasestudyonthenewinvasivepestD suzukii and its importantnaturalenemiesparasitoidsDevelopmentofenvi-ronmental friendlymanagementmethods is urgently needed forthismajorpestinEuropeandNorthAmericabecauseatthemo-mentthemaincontrolmethodislarge-scalepesticideuse(Asplenetal2015Brucketal2011Cinietal2012Hayeetal2016TimmerenampIsaacs2013)Basedonthefour-stepapproachandareviewofknowledgeaboutD suzukiindashparasitoid interactionsweshowhowtheperformanceofindigenousparasitoidsintheinva-siveareacanbeoptimizedforbiocontrolWewillnotreviewthedifferentmethodsofselectivebreedingasthishasbeenrecentlycoveredbyLommenetal(2017)Wealsosuggestfutureresearchdirectionsforimprovementofbiocontrolagents

2emsp |emspIMPROVEMENT OF NATUR AL ENEMIES BY E XPLOITING NATUR AL VARIATION A FOUR- STEP APPROACH

To improvetheperformanceofpotential indigenouscontrolagentsagainstaninvasivepestfirstthemostpromisingnaturalenemieshavetobechosenforoptimizationTheyshouldbeselectedbasedontraitsenablinghighbiocontrol performance that is efficient (large-scale)production and significant pest population reduction in the targetareaTheseldquobiocontroltraitsrdquo includehighkillingefficiencyrobust-nessunder(a)bioticconditionsintheareaofreleaseenvironmentalsafetyandabilitytobecost-effectively(mass)rearedinthelabora-tory (Table1) It should be recognized thatmany of the biocontroltraitsactuallycomprisemultipleaspectsofthebehaviorandphysiol-ogyoftheagentForexamplehighkillingefficiencyofaparasitoidmayrelyontheadequatelocalizationofhosthabitatshost-findinghostrecognitionandacceptancesufficientfecundityandhighpara-sitizationsuccessrate(FleuryGibertRisampAllemand2009)(Table1)

Followingthetraditionalmethodofbiocontroldevelopmentthe first step is to investigate the interspecific variation of natural enemies for relevant biocontrol traitstochoosethemostpromisingagentthatbestexpressesalltherequiredbiocontrolcharacteristics(Figure2Table1)Theuseofnativenaturalenemiesispreferredandexoticspeciesshouldonlybeusedassecondoptiontodecreasebiodiver-sityrisksandcircumventthelongprocessofobtainingimportationandreleasepermits Inthecaseofdrosophilidsparasitoidsareanimportant natural enemy that can cause highmortality in naturalpopulations (DriessenHemerikampVanAlphen1989Fleuryetal2004 JanssenDriessenDeHaanampRoodbol1987KeebaughampSchlenke2014) Inadditionparasitoidsareofteneffectivelyusedasbiocontrolagentduetotheirrelativeshortgenerationtimeeasetobreedinthe laboratoryandhighhostspecificityandefficiencyin killing the pest (MacQuarrie Lyons Seehausenamp Smith 2016StilingampCornelissen2005)Optimalbiocontroltraitvaluesforpar-asitoidsofD suzukiirelyforexampleonhostlocalizationinripeningfruitsratherthantherottingfruitsoftheindigenousfruit-breedingDrosophilaandhighvirulencetosuppressthehostsrsquoimmunesystem(Table1)

F IGURE 1emspSourcesofvariationthatdeterminetheoutcomeoftheagentndashpestinteractiondeathofthepesttheagentthepestandtheagentorthesurvivalofbothThefactorsleadingtothisvariationincludeheritableandnonheritablesourcesP=phenotypicvariationoftheagentandpestG=heritablevariationconsistingofgeneticandepigeneticvariationoftheagentandpestE=environmentalsourceofvariationaffectingtheagentandthepestSomeaspectsofthisenvironmentareperceivedbyboth(egtemperatureandpesticides)whileotheraspectsmayconcernonlythepestoragent(egabundanceofalternativehostspecies)Arrowsindicateinteractionbetweensourcesofvariationenvironmentaland(epi-)geneticsourcesaffectingthephenotypedirectlyorenvironmentalconditionsaffectingthegenotypicexpression(phenotypicplasticity)


TABLE 1emspListofbiocontroltraitsthatdeterminetheperformanceofa(potential)biocontrolagent

B iocontrol traits that determine performance

E xample of species trait values that determine performance

E xample of species trait values of parasitoids of Drosophila suzukii that determine performance

Highkillingefficiencyinareaofrelease

Hostlocalizationabilityfindinglargepartofthepestpopulation

LocalizeD suzukiiinripeningsoftfruitsontreesplantsand(in)fallen(fruits)onthegroundlongovipositortoreachlarvaeinsidefruits

Highattackrate(preferablyduringentirelifetime) Largenumberofmatureeggsavailable(eggload)highovipositionrate

Highkillingsuccessrateofindividualagentssuchthatalargepartofthepestpopulationiskilled

AbilitytosuppresshostimmuneresponsekillD suzukiilarvaepupae

Preferpestspeciesoveralternativepreyhost PreferenceforD suzukiioverotherhost(Drosophila)species

Lowdispersaltendencyfrompatchmicrohabitatofthepest(ifpestispatchilydistributed)

StayinfruitpatchuntilallD suzukiilarvaepupaehavebeenparasitized

Lowdispersalfromagriculturalhabitat(forlong-termcontrolpersistintheareaalsoatlowpestdensity)

Limitedlong-distancedispersal(eglt50ndash100m)and(forongoingcontrol)useofalternativehostspeciesatlowD suzukiidensity

Densityresponsiveness LocatelarvaepupaeatlowD suzukiidensityincreaseovipositionratewithincreasingD suzukiidensity

Recognizesuitablehostprey Abilitytorecognizealreadyparasitizedhosts(avoidancesuper-multiparasitism)inparticularwheneggsarelimitedandforlong-termcontrolwhensupernumeraryeggsresultindeathoftheagent

Abletoefficientlykillpestpopulationintargetarea(requiresinsightintopotentialintraspecificdifferencesbetweenpestpopulations)

AbletoovercomeimmuneresistanceofD suzukiipopulationintargetarea(requiresinsightintoamountofintraspecificvariationinimmunityofD suzukii)

Forongoingcontrolabletobuildupandmaintainapopulationovermultiplegenerations

CompleteentirelifecycleonD suzukii(surviveparasitizationofD suzukiilarvaeorpupae)findingofsuitablematesabilityofadultstofindfood

Robustnessunder(a)bioticconditionsinareaofrelease

Highfitnessatclimaticconditionsinareaofrelease(survivalhighkillingefficiency)Dependsonforexampletargetcropwhetheritisgrowingoutsideandvulnerabletoprecipita-tionandunpredictableweatherconditionsormorestableclimaticconditionsingreenhouse

Survivalandhighkillingefficiencyatrelativeloworhightemperature(eg15ndash20degCgt25degC)whenreleasedearlyorlateingrowingseasonandorathighlowhumidity

Highfitness(survivalhighkillingefficiencyactivity)attimingofrelease(earlymidlateingrowingseason)andduringaimeddurationofcontrol(1ormoregenerationsduringoneormultipleseasons)

Lowsensitivitytovariableclimaticconditionsthroughouttheyear(forlong-termcontrol)

Lowsensitivitytoagriculturalpracticesinareaofrelease

Toleranttocropmanipulationsappliedin(closesurroundingof)targetareasuchaspesticidesfungicidesfertilizationirrigationandpruning

Tolerancetohighpopulationdensity(egintraspecificinteractions)whenreleasedinhighnumbers

ToleranttoconspecificfemaleparasitoidsabilitytorecognizealreadyparasitizedD suzukiilarvaepupaelowmigrationrateinresponsetoincreasingparasitoiddensity

Abletokillthepestandreducepestpopulationdensitywithinspeciescommunitypresentinthetargetareaforexampleby1Avoidanceorbeastrongcompetitorofpredatorsandorotherspeciespresentintargetarea

2Beingcompatiblewithothernaturalenemiesofthepestinsuchawaythattheytogetherresultinhigherkillingefficiency

1NolimitedeffectofpresenceofpredatorsofparasitoidssuchashyperparasitoidP vindemmiaeorantsAvoidanceofmultiparasitismorsuperiorcompetitorduringmultiparasitism

2PreferenceforotherlifestagesofthepestormicroclimatethanothernaturalenemiesofD suzukiipresentintargetarea

(Continues)


Whentheselectedspecies showssuboptimalperformance forrelevantbiocontroltraitstheyshouldbesubjecttooptimizationSofar indigenousparasitoids thatoccur in the invadedareaofD su-zukiiandthathavebeenstudiedhavelowkillingefficiencyagainstD suzukii (Chabert etal 2012 Kacsoh amp Schlenke 2012) whichhinderstheiruseasbiocontrolagentHoweverindividualsofsomeparasitoidspeciesareabletoparasitizeD suzukiiandcauseflydeathandor can complete their development upon parasitizing the fly

indicatingthatthereispotentiallatentcompatibilitybetweentheseparasitoidspeciesandthe(new)hostTheirkillingefficiencyshouldthereforebeamaintargetforoptimization

Todeterminethepotentialforoptimizationoftraitsknowledgeoftheextentandmechanisticbasisofnaturalvariationinthetraitsis required Thus the second step is to investigate the intraspecific variationPhenotypicdifferencesamongstrainsofthesamenaturalenemyspeciesareafirstindicationthatgenetictraitvariationmay




Environmentalsafety

Noeffectonabundanceofotherorganismsintheecosystemofreleaseandnotablyinnontargetareaseitherdirectly(egkillingnontargetherbivoresorthroughintraguildpredation)orindirectly(egthroughcompetitionforresources)

Relativelyhostspecificnohyperparasitoidtolimitadverseeffectsonpopulationdensityofother(beneficial)parasitoidsandotherDrosophilaspeciespresent

Lowdispersalabilitytolimitnegativeeffectsinnontargetareas

Lowdispersaltendencytootherhabitats(egforests)lowflycapacitylowpassivedispersal(egbyairorhumantransport)

Novectorof(transferable)diseasesparasiteswhichmayaffectwildstrainsorotherspeciesincludinghumansnoeffectonpublichealth(egtoxicorallergicresponses)

NocarrierofWolbachiastrainsthatcausecytoplasmicincompatibility(CI)whenoutcrossingtowildstrains

Lowchanceofhybridizationwithcloselyrelatedspeciesintargetarea

Inabilitytomateandproduceviableoffspringwithotherparasitoidspeciespresentinareaofrelease

Inabilitytopermanentlyestablishoutsidereleaseareatoreducerisksinnontargetsystems

Highmortalityrateinwinterconditionsinnontargetareas

Cost-efficient(mass)rearingstoredtransportandrelease

Maintenanceoflargepopulationsizeforreleasewithoutinbreedingproblems

Highfemalefecundityhighsurvivalrateshortdevelopmentaltimefemale-biasedsexratiohighlongevity

Abletorearagentontargetpestorcloselyrelatedspeciesthatisrelativecheapinproductionwithoutlosingeffectivenessagainstthetargetpestinareaofrelease

CultureparasitoidsonD suzukii andor other DrosophilaspecieswithoutlosingeffectivenessagainstD suzukiipestIncaseculturedon D suzukiiabletoseparateparasitizedandnonparasitizedhostsbeforetransportandrelease

Abletorearagentthatisefficientagainstallvarietiesofthetargetpesttoaccountforpotentialintraspecificdifferencesbetweenpestpopulations

AbletocultureparasitoidthatisefficientagainstdifferentD suzukii populationsforexampleofdifferentresistancelevels

Abletorearagentinconditionsthatenableefficientproduction(egfastdevelopmenthighdensity)withoutlosingeffectivenessinthefield(egbychoosingconditionssimilarastargetareasuchastemperaturephotoperiodandpest-habitatstimuli)

Abilitytolearnhost-habitatcues(egfruitcolorandodor)toincreasepest-killingefficiencyabletorearatrelativehightemperatureenablingfastdevelopmenttimewithoutlossofeffectivenessuponrelease

Long-termstorage(gtweeks)withminimalfitnesseffectsoninparticularkillingefficiencyofthepest

Long-termsurvivalatforexamplelowtemperature(eg10degC)asadultorimmaturestageorbyinducingdiapausewithoutlossoffitness(egsurvivalfecunditypest-killingefficiency)

Abletotransportandreleasetheagenttointargetareawithoutnegativeeffectonfitness

Survivetransportationhazardssuchaschangesintemperatureandmechanicalimpactofboxesbeingshaken Possibilityofusingabankersystemforparasitoidreleaseforexampleartificialmediumcontainingalternativehosts(nonpest)aswellasparasitizedlarvaeandpupaofdifferentages

NotePerformanceisdefinedastheabilityofanagenttosuppressthepestpopulationinthetargetareaandtocostefficientlybe(mass)rearedandtransportedBiocontroltraitsthatdetermineperformancearecomposedoftraitvaluesacrossmultiplespeciestraitsExamplesofimportantspeciestraitvaluesarelistedforbiocontrolagentsingeneralaswellasforparasitoidsofD suzukiispecificallyAgentsshouldpreferablymeetallfourperfor-mancerequirementsNotethattraitvaluescandifferdependingonmanagementgoals(egdurationofeffectintermsofnumberofgenerationsorseasons)

TABLE 1emsp (Continued)


existwhichmaybeexploited fordevelopingofa (more)effectivebiocontrolagentassumingthatthevariationisheritableHoweverphenotypic variation might also be influenced by environmentalfactors (egduetodevelopmentalstochasticityorthephenotypeofthepest)Thiswouldlimittheresponsetoartificialselectionasphenotypicvariationcanonlybesubjecttoselectivebreedingwhenitis(partly)heritableInadditionthetargetareaforbiocontrolisanimportant aspect of the optimization as agentsmay perform bet-ter inaparticular climate (egMediterraneanvs tropical climate)andorexistinginsectcommunities(egEuropevsNorthAmerica)Thusweneedtocharacterizetheamountofphenotypicvariationinthebiocontroltraitsthatlimittheeffectivenessofthebiocontrolagent(Box1)

Inwhichwayandtowhatextentintraspecificvariationcanbeexploited for optimization depends on the genetic basis of and(stochastic)environmentaleffectsontheexpressionofthetraitofinterestHencethe third step is to determine environmental and genetic factors that shape the biocontrol trait variation Insightinto

theamountofgeneticvariationandgeneticarchitectureoftraitsmay aid the design of a breeding plan and prediction of the re-sponsetoselectionaswellasanticipatepotentialtrade-offsandgeneticcorrelatedresponses(Lommenetal2017)Selectiononatargettraitcanchangetheinvestmentin(trade-off)ortheexpres-sionofanothertrait(correlatedresponse)resultinginanuninten-tionalchangeinanontargettraitThisdoesnotalwayshavetobenegativetheeffectmightalsobeexploitedduringselectionNotethatbiocontroltraitsarecompositetraits(Table1)Trade-offsandcorrelated responses might therefore either (a) occur betweentraitsdeterminingthesamebiocontroltraitlikeldquokillingefficiencyrdquo(such as attack rate and host immune suppression ability) or (b)betweentraitsdeterminingtwodifferentbiocontroltraitssuchasldquokillingefficiencyrdquoandldquorobustnessunder(a)bioticconditionsrdquo(egbetweenkillingefficiencyandsurvivalrate)Inadditionenviron-mentalfactorscanalsoinfluencetraitvalueexpression(Figure1)Howeverthepestandnaturalenemymaybeaffecteddifferentlybythesameenvironmentalfactorswhichmayhaveanimpacton

F IGURE 2emspProposedfour-stepapproachtoexploitnaturalvariationtooptimizenaturalenemiesasbiologicalcontrolagentTheapproachinvolvesexploitationofheritableaswellasnonheritablevariationSeetextfordetailedexplanationofeachstepArrowsontheleftaftersteps2and4refertothecasewhenthecandidatecontrolagentdoesnotmeetallrequirementsIncasethemostpromisingspeciesdoesnotshowintraspecificvariationforthetraittobeoptimized(step2)anotherspecieshastobechosen(step1)Incasethepotentialagentdoesnotmeetallrequirementsforbiocontrolaftertestingtheirefficiency(step4)furtheroptimizationisneeded(step4)oranotherspeciesstrainshouldbechosenaspotentialbiocontrolagent(steps1and2)


theirinteractionThereforeidentificationofgeneticandenviron-mentalfactorsaffectingthetargettraitofthecandidateagentisrequiredtopredictitsfieldefficiencyandtosetoptimalbreedingconditionstosecureitssuccessinthefield

Measuringphenotypicvariation(ofthecontrolagent)inarele-vantrangeof(agriculturalandrearing)conditionscangiveinsight

into the extent of phenotypic plasticity (ie the different phe-notypesagenotypecanproduce indifferentenvironments)andwhich environmental factors influence expression of the trait(s)of interestThecollectionofallpossiblephenotypesacrosstime(eg developmental stages) and space (eg geographic regions)is called the ldquophenomerdquo (Houle Govindaraju amp Omholt 2010

Box 1enspPhenomics of biocontrol agents and pests

ComparedtothefieldofplantandlivestockbreedingselectivebreedingofbiologicalcontrolagentsisarelativelynewfieldofstudyPlantandanimalbreedinghasbeengreatlyadvancedbynewgenetechnologiesMosteconomicallyimportantplantsandlivestockhavebeensequenced(EdwardsampBatley2010JacksonIwataLeeSchmutzampShoemaker2011MichaelampJackson2013)andthisinforma-tioncanbeusedtoimproveandspeedupbreedingwithtechniquessuchasmarker-assistedselectionandgenomicselectionLinkingphenotypeandgenotypehoweverhasbecomeabottlenecktofurtherimprovebreedingsuccessasresearchonpreciseandefficientquantificationofphenotypeshasnotkeptpacewithgenomics(Furbank2009Houleetal2010Jacksonetal2011Whiteetal2012)ThisholdsinparticularforcomplextraitsthatarecontrolledbymultiplegenesandsubjecttoenvironmentalinfluenceInplantsandtoalimitedextentinlivestockthishasledtoanemergingnewfieldofinvestigationphenomicsthelarge-scaleandsystematicstudyofthephenome(allpossiblephenotypes)Inparticularplantphenotypescanbemeasuredatlargescalewithadvancednondestructivetech-nologies so-called high-throughput phenotyping (HTP) such as fluorescence imaging and near-infrared reflectance spectroscopy tomeasurephotosyntheticperformanceandcompositionofplanttissue(ArausampCairns2014)Accurateandefficientmeasuringofphe-notypesaidstheunderstandingofunderlying(genetic)mechanisms(reversephenomics)andthescreeningofphenotypestoforinstancechoosethebeststrainsforbreeding(forwardphenomics)(FurbankampTester2011)HistoryofanimalandplantbreedingunderlinestheimportancetohaveinsightintophenotypicvariationtoimprovetheirperformanceforagricultureItalsostimulates(re)thinkingabouthowbiocontrolagentsrsquophenotypescanbesystematicallyandaccuratelymeasuredacrosstimeandspaceforimprovementofbiocontrolstrategiesMeasuringandunderstandingphenotypicvariationisofgreatimportanceforthedevelopmentofbiocontrolagentsInlinewithplantandlivestockphenomicsbiocontrolphenomicswouldentailtheaccurateandsystematic(widescale)phenotypicdatacollectionofthecan-didateagent(speciesstrainsorgenotypes)andthetargetpestpopulation(s) inrelevantfieldandrearingconditionsacrosstime(egthroughlifetimeandseasonofagentandpest)andscale(allpossiblerelevanthabitatsandthusbioticandabioticconditions)Thiscanaidsolvingmajorchallengesinthedevelopmentofcontrolagents(a)findingsuitableagents(b)predictingtheirsuccessinaparticularagri-culturalenvironment(c)determiningconditionsforoptimalperformanceand(d)evaluatingwhethertheseconditionscanbealteredand(e) identifyingcharacteristicsof importantbiocontroltraitvalues Inaddition it isalsoof importanceforselectivebreedingto (f)setconditionsforselectivebreedingand(g)predictinwhichwayandtowhatextentagentscanbeimprovedbyartificialselectionThefeasibilityforlarge-scalephenotypingisstilllimitedespeciallyforarthropodsduetoeconomicalandpractical(egmobility)limitationsandtheirlowdetectabilityinthefield(smallsize)HowevertheirrelativeshortgenerationtimeandsmallsizecomparedtolivestockfacilitatephenotypinginlaboratorysettingsMicrobesarealreadybeingscreenedonlargescalefortheirapplicationascontrolagent(Figueroa-Lopez Cordero-Ramirez Quiroz-Figueroa amp Maldonado-Mendoza 2014 van Lenteren etal 2018 Stewart Ohkura ampMclean2010)TomeasurephenotypesofarthropodagentsandtheireffectonthetargetpestpopulationtoolssuchassensorsimagingandcamerascanbeusedtoincreaseaccuracyandscaletodetermineforinstancestressresponseofpestsinthepresenceofanagentandthepresencedistributionandmovementoftheagentsandthepestsinthefieldandorinthelaboratoryThesetoolsarealreadyusedinotherfieldsofstudy(NansenCoelhoVieiraampParra2014NansenRibeiroDadourampRoberts2015ReynoldsampRiley2002)althoughmostseemtobeespeciallyfeasibleatonlysmallscalesItwouldbeinterestingtomakethemapplicableinthefutureatlargerscalesMoreover imagingtechnologiesforplantphenomicssuchasthedetectionofplanthealthandplantresponsestopestsintheabsenceandpresenceofbiocontrolagents(Abdel-Rahmanetal2017ReynoldsampRiley2002WangNakanoOhashiTakizawaampHe2010ZhouZangYanampLuo2014)canalsobeusedtomeasuresuccessofbiocontrolThedifficultyisthatthesuccessofacontrolagentdoesnotonlydependongenotypetimesenvironmentinteractionsasmosttargettraitsinanimalandplantbreeding(exceptforpestresist-ance)butonanevenmorecomplextwo-speciestimesenvironmentinteraction(Figure1)Thefour-stepapproachproposedinthisreviewdisplayshowphenomicscanbeappliedtobiocontrolThefirstandsecondsteps(investigationofinter-andintraspecificvariation)areanalogoustoforwardphenomicsthatisscreenandchoosenaturalenemieswithdesiredphenotypesforbiocontroltraitsThethirdstep(investigationoffactorsthatshapethevariation)canbeseenasreversephenomicstodiscovermechanismsofvariationandwhichhelpstosettheconditionsforoptimaltraitexpression


Soule1967)(seealsoBox1)Thisknowledgecanbeusedtoiden-tifyenvironmentalfactorsthatmayconstraintheperformanceofanagentMoreover itcanyieldinsightsintotrade-offsthatmayhampertheadaptiveresponseandthusto(a)predictthesuccessofartificialselectionand(b)designabreedingprogram(Figure2step3)Inadditionagentswillencounterdifferentandagreaternumber of variable biotic and abiotic factors in the field thanunderlaboratoryconditionsThismayinfluencetheirkillingabilityof thepestForexample temperaturedifferencesand thepres-enceofcompetitorscanaltertheagentsrsquoperformanceinthefield(Andrade Pratissoli Dalvi Desneux and Santos Junior (2011)BoivinandBrodeur(2006)Henceknowledgeaboutenvironmen-tal effects is also required to (c)predict theperformanceof theagentinthefieldInaninterestingmannerinsightintosourcesofvariationcanalsobeusedto(d)identifyadditionalmethodstoop-timizeperformanceoftheagentbyexploitationofnonheritablevariationforexamplebylearningabilityoftheagentoralterationofenvironmentalconditionsinthegreenhousetoincreasekillingefficiencyofthepest

Atlastthe fourth step is to exploit the available variation and select (for) an agent with the most optimal combination of pheno-typic traits This can be either through (a) choosing the mostcompetent strain for the target area (ldquostrain selectionrdquo) (b)crossing populations present in the invaded area andor withones that are native of the pest (ldquocross-breedingrdquo) andor (c)optimization of a genetically variable strain through artificialselection(ldquoselectivebreedingrdquo)Theoptimizationapproachcanbeappliediterativelyeachtimeidentifyingthelimitingfactorsfortheeffectivenessofthebiocontrolagentandselectingon(trait valuesof the) differentbiocontrol traitsAt each roundthe selected agent should be tested for its ability to bemassreared and for its performance success in the target area toassess whether it can be implemented in pest managementwhether it needs further improvement or whether anothercandidateagenthastobeselectedincaseitshowsnopotential(Figure2)

BelowwereviewcurrentknowledgeofD suzukiindashparasitoidin-teractionsinmoredetailfollowingourproposedfour-stepapproachandpointatwaystooptimizeparasitoidsfromtheinvasiveareatodevelopefficientbiologicalcontrolagents

3emsp |emspSTEPS 1 AND 2 E XPLORING INTER- AND INTR A SPECIFIC VARIATION IN KILLING EFFICIENCY

31emsp|emspParasitoids in the invasive area Europe and North America

Several surveys performed in Europe (France Spain Italy andSwitzerland) and North America (Canada USA and Mexico) ex-plored the ability of native parasitoids to parasitize the invasiveD suzukiiAtotalof17parasitoidspecieshavebeeninvestigated

311emsp|emspInterspecific variation

In only 24 of the investigated species a population has beenfoundwithahighparasitizationsuccessrate (61ndash100Table2)Two pupal parasitoids Pachycrepoideus vindemmiae and Trichopria DrosophilaewererepeatedlyreportedtoparasitizeandemergefromD suzukii Two other pupal parasitoids Spalangia erythromera and Vrestovia fidenas andone larval parasitoidLeptopilina heterotomawere recorded once (Table2) Other species in particular thosethat parasitize the larval stage such asAsobara tabidaLeptopilina clavipes and Leptopilina boulardididnotsurviveinoremergefromD suzukii (Table2) Thus there is clear interspecific variation be-tweenparasitoidsintheirsuccesstoparasitizeD suzukiiandmostindigenousparasitoidspeciesthathavebeenstudiedareunabletocompletetheirdevelopmentonD suzukiihosts

312emsp|emspIntraspecific variation

Althoughmostparasitoid species couldnot successfullyparasitizeD suzukii intraspecific variation indicates potential future adapta-tiontothepestForexampleFrenchA tabidastrainscollectedfromIgeacuteandSablonsshowedlittletonoattempt(0ndash125)toovipositin D suzukii larvae(Chabertetal2012)whereasaSwedishstrainandanotherFrenchstraincollectedinSospelshowedaninfestationrateofabout50and80respectively(KacsohampSchlenke2012)Also whereas L boulardi was not able to emerge fromD suzukiiChabertetal(2012)reportedthattheydoovipositinD suzukii and inducehighhostmortalityBetween-populationdifferencesinpara-sitizationsuccesswerealsofoundamongthethreespeciescapableof successfully parasitizing D suzukii (Table2) Leptopilina hetero-tomafromOregonnorthwestItalyFranceCaliforniaSwedenandSwitzerlandwerenotable tocomplete their life cyclewhenpara-sitizingD suzukii in the laboratory (Chabertetal2012KacsohampSchlenke2012KnollEllenbroekRomeisampCollatz2017Mazzettoetal2016Poyetetal2013Stacconietal2015)butanItalianpopulation fromTrento could (Stacconi etal 2015) FurthermorewaspsfromaFrenchpopulationwerenotabletoovercomethefliesrsquoimmunedefensetoproduceviableoffspringalthoughsimilartoan-otherpopulation fromNorth Italy (LombardyandPiedmont) theydid oviposit and caused fly death (Chabert etal 2012Mazzettoetal2016) Inan interestingmannerwhenD suzukii larvae were parasitizedbyfourindividualsratherthanasinglewaspsomepara-sitoidsdevelopedandeclosed(Chabertetal2012)PopulationsofparasitoidT drosophilaealsodifferedintheirperformanceonD su-zukii Forexample the success ratedifferedbetween twopopula-tionswithinFrance(Chabertetal2012)andbetweenpopulationsfromSouthKoreaandCaliforniainwhichtheCalifornianpopulationunexpectedlyperformedsignificantlybetteronD suzukii than the Korean population (Wang Kacar Biondi ampDaane 2016b) Thesecasesprovideclearevidencefortheexistenceofintraspecificvari-ation inparasitizationabilitybetweenpopulationsofknownindig-enousD suzukiiparasitoids


TABLE 2emspOverviewofparasitoidsoccurringinthenewlyinvadedarea(mostlyEuropeandNorthAmerica)investigatedfortheirabilitytoparasitizeDrosophila suzukiiinthefieldandorthelaboratory

Natural enemy CountrystateD ocumented parasitoids of

D suzukii in the field

P arasitization success in the laboratory and encapsulation rate

F ly infestation rate (infestation) or coupled fly and parasitoid death (inadequacy) Reference

Pupalparasitoids

Pachycrepoideus vindemmiae

Mexico YesoninfestedD suzukii traps

Cancinoetal(2015)

France Serriegraverespopulationyesmediumsuccess

Highinfestation Chabertetal(2012)

MaisonNeuvepopulationmediumsuccess(populationsdonotdiffersig)

Mediuminfestation

Spain YesoninfestedD suzukii traps

Yeshighsuccess Highinfestation Gabarra et al (2015)

Switzerland Yeshighsuccess Knolletal(2017)

Italy YesoninfestedD suzukii traps

Yesmediumsuccess Noinadequacy Stacconietal(2013)

YesoninfestedD suzukii traps(mean035parasitoidtrap)

Milleretal(2015)

Yesmediumsuccess Mediuminfestation Stacconietal(2015)

California Yesonfield-collectedfruits(unpublisheddata)

Yessuccessful Fruitsmediumndashhighinfestationsoillowndashmediuminfestation(fruitvssoildiffersig)

Wangetal(2016b)

Oregon YesoninfestedD suzukii traps

Stacconietal(2013)

YesoninfestedD suzukii traps(mean193ndash606parasitoidstrap)

Milleretal(2015)

First-instarandsecond-instarlarvaenosuccess Third-instarpupaeyesmediumndashhighsuccess

First-instarandsecond-instarlarvae low infestationThird-instarpupaehighinfestation

Stacconietal(2015)

Pachycrepoideussp Georgia Yeslowsuccess Lowinadequacy KacsohandSchlenke(2012)

Trichopria cf Drosophilae Mexico YesoninfestedD suzukii traps

Cancinoetal(2015)

France SteFoypopulationyeslowsuccess

SFpopulationhighinfestation

Chabertetal(2012)

Sablonspopulationyeshighsuccess(populationsdiffersig)

SApopulationhighinfestation(SFandSApopulationsdiffersig)

Spain YesoninfestedD suzukii trapsandfield-collectedfruits(parasitizationratefruits38ndash107)

Yeshighsuccess Mediuminfestation Gabarra et al (2015)

(Continues)







Yessuccessful Mediumndashhighinfestation

Wangetal(2016b)

Switzerland Vaudstrainyeshighsuccess

Knolletal(2017)

Ticinostrainyesmediumsuccess(populationsdiffersig)

Italy Yeshighsuccess Noinadequacy Mazzettoetal(2016)

Yeshighsuccess Stacconietal(2015)

Trichopria sp California Yeshighsuccess Lowinadequacy KacsohandSchlenke(2012)

France Yeshighsuccess Noinadequacy KacsohandSchlenke(2012)

Spalangia simplex Mexico YesoninfestedD suzukii traps

Cancinoetal(2015)

Spalangia erythromera Switzerland Yeshighsuccess Knolletal(2017)

Vrestovia fidenas Switzerland Yeslowsuccess Knolletal(2017)

Larvalparasitoids

Asobara tabida France Igeacutepopulationnosuccess(ovipositin125larvae)

Chabertetal(2012)

Sablonspopulationnosuccess

Nosuccesshighencapsulationrate

Lowinadequacy KacsohandSchlenke(2012)

Sweden Nosuccessmediumencapsulationrate


Switzerland Nosuccess Noinadequacy Knolletal(2017)

Asoara citri IvoryCoast YesverylowsuccessLowencapsulationrate

Highinadequacy KacsohandSchlenke(2012)

Aphaereta sp Georgia Nosuccessmediumencapsulationrate

Verylowinadequacy

KacsohandSchlenke(2012)

Leptopilina clavipes Netherlands Nohighencapsula-tion rate

Mediuminadequacy


Leptopilina heterotoma France StEtienneChalaronnepopulationnosuccesshighencapsulationrate

Mediuminfestation Chabertetal(2012)

Antibespopulationverylowsuccesshighencapsulationrate

Highinfestation(STandANpopula-tionsdiffersignificantlyininfestation)


(Continues)






FrenchD suzukii strainnosuccesshighencapsulationrate

Lowinadequacy Poyetetal(2013)

JapaneseD suzukii strainnosuccessmediumndashhighencapsulationrate

Mediuminadequacy

Oregon YesoninfestedD suzukii traps(mean0ndash006parasitoidtrap)

Milleretal(2015)

Nosuccess Stacconietal(2015)

Italy YesoninfestedDsuzukii traps(mean101parasitoidtrap)

Milleretal(2015)

Nosuccess Mediumadequacy Mazzettoetal(2016)

Yeslowndashmediumencapsulationrate

Mediumndashhighinfestation

Stacconietal(2015)

California Nosuccesshighencapsulationrate

Mediuminadequacy



Sweden Nosuccesshighencapsulationrate


Switzerland Yesverylowsuccess Low(average)inadequacysignificantdifferencesbetweenstrains

Knolletal(2017)

Leptopilina victoriae Hawaii Nosuccesshighencapsulationrate

Mediuminadequacy


Leptopilina boulardi Mexico YesoninfestedD suzukii traps

Cancinoetal(2015)

France Sablonspopulationnosuccessmediumencapsulationrate


Eyguiegraverespopulationnosuccessmediumencapsulationrate(populationsdonotdiffersig)

Highinfestation



Italy Nosuccess Noinadequacy Mazzettoetal(2016)

Congo Nosuccesshighencapsulationrate

Mediuminadequacy



(Continues)


32emsp|emspParasitoids in the native area Asia

TheparasitoidspeciesthatattackD suzukiipopulationsintheareaof origin Asia have not been thoroughly investigated The firstpublicationsonnaturalenemiesofD suzukiionlyappearedin2007(MitsuivanAchterbergNordlanderampKimura2007)andresearchhasmainly focusedonparasitoidspecies inJapanandtoa limitedextent on species fromChina andKorea (Table3) A total of twopupal and 14 larval parasitoids have been identified that are ableto parasitizeD suzukii (Table3)Most of them belong toAsobara Ganaspis or Leptopilinabuttheseparasitoidsalsoshowdifferencesinparasitizationsuccess


Of the 16 investigated parasitoid species 88 are able to suc-cessfully parasitize D suzukii in the field andor in the labora-tory Only A pleuralis and L boulardiwerenotobservedtoemerge

fromD suzukiiatall(Daaneetal2016Nomanoetal2015)ThelargevariationinparasitizationbehaviorcanbeillustratedwiththeAsobara genusThereare largedifferencesamongspecieswithinthis genus in their ability to acceptD suzukii for oviposition andsuccessful development to adulthood While A pleuralis did not oviposit inD suzukii (Nomanoetal2015)A tabida A rufescens and A rossica did oviposit but all individuals died in the fly host(Nomano etal 2015) Only A sp TS1 A sp TK1 A japonica A leveri and A brevicaudawouldreadilyacceptD suzukii forovi-positon and were able to complete development (Daane etal2016GuerrieriGiorgini CasconeCarpenitoamp vanAchterberg2016 IdeoWatadaMitsuiampKimura2008KacsohampSchlenke2012Mitsui amp Kimura 2010 Nomano etal 2015) In an inter-esting manner while A tabida A rufescens and A rossica could notcompletetheirdevelopmentwhileparasitizingD suzukii in the laboratorytheyemergedfromfliescollectedinthefield indicat-ingthattheseparasitoidscansurviveonthishost(Nomanoetal2015)





Kenya Nosuccesshighencapsulationrate

Mediuminadequacy



Mediuminadequacy


Switzerland Nosuccess Lowinadequacy Knolletal(2017)

Leptopilina guineaensis Cameroon YeslowsuccessHighencapsulationrate

Mediuminadequacy


SouthAfrica Nosuccessmediumencapsulationrate

Mediuminadequacy


Ganaspis xanthopoda a Hawaii YesverylowsuccessHighencapsulationrate


Uganda Nosuccesshighencapsulationrate


Ganaspissp Florida YeslowsuccessHighencapsulationrate


Hawaii YesmediumsuccessHighencapsulationrate

Mediuminadequacy


NotesFieldsurveysincludetheplacementoftraps(D suzukii-infestedorD suzukii-uninfestedfruit-baitedtraps)andorthecollectionoffruitsfromnaturalhabitatsorcropsLaboratoryessayswereperformedtotesttheabilityofparasitoidstoparasitizeD suzukiibyexposureoflarvaepupaetotheparasitoid(s)inano-choicetestParasitizationsuccess(rate)isthepercentageofparasitoidsthateclosedfromD suzukiiDuetovariableexperimentalsetupandcalculationsparasitizationsuccessrateiscategorizedinldquonordquo(noparasitoidemergence)ldquoverylowrdquo(lt10successrate)ldquolowrdquo(10ndash29)ldquomediumrdquo(30ndash60)andldquohighrdquo(61ndash100)Whenexaminedflyinfestationrate(infestation)orcoupledflyandparasitoiddeath(inadequacy)arepresentedFlyinfestationrateincludesflydeathduetoparasitoidemergenceandorcoupledflyandparasitoiddeath(inadequacy)Notethatcompar-ingtheparasitizationresultsofthesestudiesinparticularquantitativeoutcomesiscomplicatedasdifferentcalculationsandexperimentalmethodswereusedInadditionhostgeneticbackgroundsmaydifferbetweenstudiesandinfluenceresultsThereforethereportedparasitizationratesshouldbeinterpretedcautiouslyfortheirextrapolationtoreal-worldapplicationsaReportedasG xanthopoda but would be G brasiliensasdescribedbyNomanoetal(2017)



TABLE 3emspOverviewofparasitoidsfromAsiainvestigatedfortheirabilitytoparasitizeD suzukiiinthefieldandorinthelaboratory

Natural enemy CountryD ocumented parasitoids of


P arasitization success in the laboratory (rate given when possible) Reference

Pupalparasitoids

Trichopria Drosophilae Korea Yesonuninfestedtraps Yes Daaneetal(2016)

China YesoninfestedD suzukiitraps ZhuLiWangZhangandHu(2017)

Pachycrepoideus vindemmiae Korea Noonlyonotherdrosophilids Yes Daaneetal(2016)

Larvalparasitoids

Asobara species(unidentified) Japan Yesonfield-collectedfruitslt1a Kasuyaetal(2013)

Asobara japonica Japan Yesonuninfestedtraps02parasitismrate

Mitsuietal(2007)

Yeshigh MitsuiandKimura(2010)

Noonlyfromotherdrosophilids Yesmedium Ideoetal(2008)

Yesonfield-collectedfruits02parasitismratea

Nomanoetal(2015)

Yeshigh KacsohandSchlenke(2012)

Yesmedium(21degC)tohigh(deg25C)

Chabertetal(2012)

Korea YesoninfestedD suzukiitraps Guerrierietal(2016)

Yesonuninfestedtrapsandfield-collectedfruits

Yes Daaneetal(2016)

Asobara leveri Korea YesoninfestedD suzukiitraps Guerrierietal(2016)

Korea Yesonuninfestedtrapsandfield-collectedfruits

Daaneetal(2016)

Asobara brevicauda Korea Yesonfield-collectedfruits Daaneetal(2016)

Asobara tabida Japan Yesonuninfestedtraps01parasitismrate

Mitsuietal(2007)

Yesonfield-collectedfruits02parasitismrate

Nobutovipositionobserved

Nomanoetal(2015)

Asobara rossica Japan Yesonfield-collectedfruitsAbout005aparasitismrate


Nomanoetal(2015)

Asobara rufescens Japan Yesonfield-collectedfruitsAbout005aparasitismrate


Nomanoetal(2015)

Asobara pleuralis Japan No Nomanoetal(2015)

Indonesia Nosuccesshighencapsulationrate


AsobaraspTS1b Japan Yesonfield-collectedfruits48a parasitismrate

Yeslow Nomanoetal(2015)

Ganaspis brasiliensis Japan Yesonuninfestedtraps39parasitismrate(ldquoD suzukii-typerdquo)c

Mitsuietal(2007)

Noverylowinfestationrate(33parasitized)(ldquoD lutescenestyperdquo)c

MitsuiandKimura(2010)

Yesonfield-collectedfruits4ndash7parasitismrate(ldquoD suzukii-typerdquo)c

Yeslow(onlyfromfruitsbutnotfromartificialdiet)(ldquoD suzukii-typerdquo)c

Kasuyaetal(2013)

Yesonfield-collectedfruits(ldquoD suzukii-typerdquo)c

Nomanoetal(2015)

Korea Yesonfield-collectedfruits Yes Daaneetal(2016)

(Continues)



ParasitizationsuccessvariesbetweenandwithinpopulationsofthesamespeciesTheAsobara spTS1populationofTsushima(Japan)forexampleisabletodevelopinD suzukiialthoughindividualsdif-feredinsuccess833diedinthelarvalstageandonly133oftheindividualswereabletocompletedevelopmentandeclose(Nomanoetal2015)Aninterestingexampleofbetween-populationdiffer-encesistheparasitoidGanaspis brasiliensisofwhichtherearediffer-entldquotypesrdquothatdifferinhostusemorphologynucleotidesequenceandgeographicdistribution(KasuyaMitsuiIdeoWatadaampKimura2013Nomanoetal2017)OnehasD lutescenesas itsmainhostandhaslimitedsuccesswhenparasitizingD suzukiitheotherisspe-cializedonD suzukiiandcansuccessfullyparasitizeD suzukii but not D lutescenes (Kasuyaetal2013) Inadditiondifferences inpara-sitization success betweenpopulationshavebeen found forA ja-ponicacollectedinthesurroundingsofTokyoOnestudyrecorded80eclosionoftheparasitoid(KacsohampSchlenke2012)anotherstudyaneclosionrateofonly44(Ideoetal2008)andMitsuiandKimura(2010)foundaneclosionsuccessof67suggestingthereissubstantialvariationbetweenparasitoidpopulations

4emsp |emspSTEP 3 UNDERSTANDING VARIATION IN D SUZUKIIndashPAR A SITOID INTER AC TION

The killing efficiency of parasitoids depends on a complex two-species interaction (Figure1)Belowwereviewwhathasbeen in-vestigatedascausalmechanismsforthephenotypicvariationandtheenvironmentalandgeneticfactorsthatcanshapetheinteraction

andcoevolutionofD suzukiiandtheirparasitoidsMoreoverwede-scribehowthesefactorscanaidthedevelopmentofbiologicalcon-trolagents

41emsp|emspSources of variation in D suzukii

411emsp|emspPhenotypic variation and its causal mechanisms

The resistance level of the host is an important trait determin-ingtheoutcomeofhostndashparasitoidinteractionsLikeseveralotherDrosophila speciesD suzukii canprotect itself fromparasitoidsbymelanotic encapsulation of the waspsrsquo egg (Chabert etal 2012KacsohampSchlenke2012)ItsimmuneresponsehoweverseemstobemuchstrongerthanD melanogasterandmostotherdrosophilidsThisisattributedtotherelativelyhighhemocytecountofD suzukii (KacsohampSchlenke2012Poyetetal2013)whichenables it tomountahighlysuccessfulimmuneresponsetowardawiderangeofparasitoidspecies(KacsohampSchlenke2012)

412emsp|emspGenetic effects

ThegeneticbasisandgeneticvariationofparasitoidresistanceinD suzukiihavenotyetbeen investigatedAsgeneticvariation inresistanceisreportedforotherDrosophilaspecies(egDubuffetetal2007GerritsmadeHaanvandeZandeampWertheim2013KraaijeveldampGodfray1997)itisalsolikelytoexistforD suzukii The amount of genetic variation in invasive species populationshoweverdependsonthesizeofthefounderpopulationandthenumberandsourcesofadditionalintroductionsWhenpreviously




Leptopilina japonica japonica Japan Yesonfield-collectedfruitslt1a parasitismrate

Kasuyaetal(2013)


Leptopilina japonica formosana Korea Yesonfield-collectedfruits Daaneetal(2016)

Leptopilina boulardi Korea Noonlyfromotherdrosophilids Daaneetal(2016)

Leptopilina japonica victoriae Philippines Nosuccessmedium50encapsulationrate


NotesFieldsurveysincludetheplacementoftraps(D suzukii-infestedorD suzukii-uninfestedfruit-baitedtraps)andorthecollectionoffruitsfromwildhabitatsorcropsLaboratoryessayswereperformedtotesttheabilityofparasitoidstoparasitizeD suzukiibyexposureoflarvaepupaetotheparasitoid(s)inano-choicetestParasitizationsuccess(rate)isthepercentageofparasitoidsthateclosedfromD suzukiiDuetovariableexperimentalsetupandcalculationsparasitizationsuccessrateiscategorizedinldquonordquo(noparasitoidemergence)ldquoverylowrdquo(lt10successrate)ldquolowrdquo(10ndash29)ldquomediumrdquo(30ndash60)andldquohighrdquo(61ndash100)WhenparasitismratewasnotcalculatedinthestudyestimationsweremadebydividingnumberofemergedparasitoidsbytotalnumberofpresentedcollectedflieswhenpossibleTheseestimationsareindicatedbythesymbolldquoardquoNotethatcompar-ingtheparasitizationresultsofthesestudiesinparticularquantitativeoutcomesiscomplicatedasdifferentcalculationsandexperimentalmethodswereusedInadditionhostgeneticbackgroundsmaydifferbetweenstudiesandinfluenceresultsThereforetheratesthathavebeenreportedhereshouldbeinterpretedcautiouslyfortheirextrapolationtoreal-worldapplicationsbUndescribedspeciesfromJapancPreviouslyassignedasG xanthopodabutlateridentifiedasG brasiliensbyNomanoetal(2017) Thereseemtobedifferent typesonespecializedonD suzukii (ldquoD suzukii-associated typerdquo)andoneunable toparasitizeD suzukii andmainlyparasitizeD lutescens (ldquoD lutescens-associatedtyperdquo)(Kasuyaetal2013Nomanoetal2017)



isolated populations start interbreeding (admixture events) therecombining of allelic variations can lead to increased geneticdiversityThroughout thecourseof the invasionofD suzukii itsgenetic diversity changed through bottlenecks and admixtureevents(Fraimoutetal2017)Acomparisonofthehostgenotypeacrossneutralmarkers(6ndash28microsatellites)andsixX-linkedlociin coding and noncoding sequences indicated relatively high in-traspecific genetic variation within and between populations intheinvadedregions(Adrionetal2014BahderBahderHambyWalshampZalom2015Fraimoutetal20152017)Itisthereforereasonabletoassumethatthereissubstantialintraspecificgeno-typicvariation in the invadedpopulations thatcancontribute tothe variable D suzukiindashparasitoidoutcome

413emsp|emspEnvironmental effects

Differencesinbioticandabioticenvironmentalconditionscaninflu-encehostresistance levelsBy layingeggs infruitsrich inatropineanentomotoxicalkaloidpresent inplantsof theSolanaceae family D suzukii can enhance resistance to parasitoids via transgenera-tionalmedication (Poyetetal 2017)Other abiotic factors that af-fecttheimmuneresponseindrosophilidsaretemperature(FellowesKraaijeveld amp Godfray 1999 Fleury etal 2004) and host diet(Anagnostou LeGrand amp Rohlfs 2010 Ayres amp Schneider 2009HowickampLazzaro2014MeshrifRohlfsampRoeder2016)InadditionanimportantbioticfactoraffectingtheimmuneresponseismicrobesIn Drosophila the microbiome can affect immunity by increasing(TeixeiraFerreiraampAshburner2008XieButlerSanchezampMateos2014) or decreasing resistance (Fytrou Schofield Kraaijeveld ampHubbard 2006) depending on microbial composition andor hostgenetic background (Chaplinska Gerritsma Dini-Andreote SallesampWertheim 2016) By experimental selection it is possible to in-creasetheabilityofparasitoidstoovercomethesymbiont-mediatedresistanceofthehost(RouchetampVorburger2014)InaninterestingmannerD suzukiipopulationsintheinvadedareaharbortheendos-ymbiont Wolbachia pipientis(ldquowSuzrdquostrain)(CattelMartinezJigginsMoutonampGibert2016CattelKauretal2016Hammetal2014MazzettoGonellaampAlma2015Sioziosetal2013Tochenetal2014)abacteriumpresentinawiderangeofarthropodsthatcanma-nipulatethehostrsquosbiologyindifferentways(seeegWerrenBaldoampClark2008)IncaseofD suzukiiitcanmediateresistancetowardRNAviruses(CattelMartinezetal2016)andcanincreasefemalefecundity(Mazzettoetal2015)HowevernotethatfitnesseffectsmightbedependedonthewSuzvariantduetointra-wSuzstrainvari-ation(KaurSioziosMillerampRota-Stabelli2017)Itwouldbeworth-whiletofurtherinvestigatetheroleofWolbachiaandothermicrobesin the D suzukiindashparasitoidinteraction

414emsp|emspImplications for selection or selective breeding of a biocontrol agent

Toassurehighparasitizationsuccessof thecontrolagentaD su-zukiipopulationhas tobechosen forselectivebreeding (and later

formassrearing)similartothoseinthetargetareaIt is importanttoprime theagent for anefficient attackbecause theremightbenatural intraspecificvariationinthelevelofresistanceinD suzukii intheinvasiveareasTheFrenchD suzukiistrainhasanhemocyteloadthatisabouttwiceashighastheJapanesestrainsandahigherencapsulationandparasitoid-killingability(Poyetetal2013)ThissuggeststhatthefoundingpopulationsinEuropehadahighimmuneresponsetowardparasitoidsandorunderwentafast-evolutionarychange in resistance ability Hence to select and breed a controlagentonaD suzukiipopulationitslevelofresistanceshouldbesim-ilartothepopulationinthetargetareaThereforemoreresearchisneededtoinvestigatetheamountofgeneticvariationinresistanceintheinvasiveareaMoreoverknowledgeofenvironmentalcondi-tionsthataredifficulttocontrolsuchaspresenceofatropinepro-ducingplantsmaybeofgreatimportancetopredictthesuccessofthecontrolagent

To increase the success of a control agent some factors thatweaken the pestmay bemanipulated for pestmanagement Themaintenance of the immune system in the absence of infectionand the investment in mounting a defense when infected bothhaveclearfitnesscostsasresourcesallocatedtowardtheimmunesystem cannot be invested in other life history traitsDrosophila melanogaster for instance had a lower reproductive success afteran immune challenge (Nystrand amp Dowling 2014) and lines se-lected for increased immunity had a lower larval competitiveability (Kraaijeveld amp Godfray 1997) Resource allocation can beinfluencedbyenvironmentalconditionsInstressfulconditionslikeinsecticideexposure(DelpuechFreyampCarton1996)orhighpop-ulationdensity(WajnbergPrevostampBouleacutetreau1985)resistanceofD melanogasterdecreasesIntraspecificvariationinD suzukii de-fensecanthereforeoccurduetodifferencesinresourceallocationTheenergybalanceofthepestcanbeexploitedduringpestman-agementbyforexamplestressingD suzukiibycombiningcontrolpractices (egasecondbiocontrolagent)orexposuretounfavor-ableclimaticconditionstomakethemmoresusceptibletoparasit-oidsTemperatureoutsidetheoptimumrange(plusmn22ndash26degC)andlowrelativehumidity (lt71RH)decrease the intrinsic rateofpopula-tion increaseofD suzukii (Tochenetal 20142016) Itwouldbeinterestingtoinvestigatewhetherthesefactorsalsoincreasetheirsusceptibilitytoparasitoids

42emsp|emspSources of variation in parasitoids of D suzukii


Naturalenemies requirevirulencestrategies toovercomehost re-sistance ofD suzukii Most parasitoids in the invasive area suchas larval parasitoids A tabida L boulardi L victoriae and G xan-thopoda do oviposit inD suzukii but their success rate is ratherlowastheirmortalityisnearly100(Table2)Themedium-to-high(30ndash100) ability of the generalist pupal parasitoids P vindem-miae and Tcf drosophilae to parasitizeD suzukii (Table2) suggests


adifferentparasitizationstrategyAsbothspeciesparalyzethehostbyinjectionofvenom(WangKacarBiondiampDaane2016aWangampMessing2004b)andpupaehavecomparedto larvaenolimitedresistanceagainstparasitoidsthesespecieshavedevelopedahighlyvirulent strategy that is nonspecies specific The larval parasitoidL heterotomaisalsoabletosome(low)extenttosuccessfullypara-sitizeD suzukii or it can inducehigh flymortality (Table2)AlongwiththeeggLeptopilinainjectsvirulenceparticlesthatmodifyhostphysiologyfacilitatingparasitization(Leeetal2009)Thecomposi-tionoftheseparticlesandtheireffectonthehostdifferbetweenspeciesandstrains(DupasBrehelinFreyampCarton1996Leeetal2009 Mortimer 2013 Poirieacute Carton amp Dubuffet 2009) whichthereforemightplayaroleintheobservedintraspecificvariationinD suzukiindashparasitoidoutcome

Parasitization ability is also influenced by the parasitoidrsquosabilitytofindthehostThisdependsontheirabilitytousehostcues (eg pheromones substrate odor and host tracks) (DickeLenterenBoskampampVoorst1985Perez-MalufRafalimananaCampanFleuryampKaiser2008WertheimVetampDicke2003)andtheirexperiencewiththehost(habitat)(associativelearning)(KaiserPerez-MalufSandozampPham-Delegue2003OliaiampKing2000PapajampVet1990SeguraViscarretPaladinoOvruskiampCladera 2007) In the case ofD suzukii host-finding may be achallengefortheparasitoidas(a) itsmainpatchlocation(ripen-ingfruits)isdistinctfrommostotherDrosophilaspecies(AtallahTeixeiraSalazarZaragozaampKopp2014AtkinsonampShorrocks1977MarkowampOrsquoGrady2008)Moreover(b)itseggsarehighlyscattered(MitsuiTakahashiampKimura2006Poyetetal20142015) whichmightmake alternative highly infested patches ofother drosophilids speciesmore attractive and time-efficient toexploit Furthermore due to its (c) recent invasion and (d) highimmuneresponseparasitoidsmaynotbeable(yet)torecognizeandsuccessfullyparasitizeD suzukiiThesefactorshighlightthedifferencebetweenlaboratoryandfieldexperimentsParasitoidsable to successfully parasitizeD suzukii in the laboratorymightnot be able to localize the pest in the field Parasitoids how-everhavebeenfoundemergingfromD suzukiibaitedfieldtrapsin Europe and North America (Table2) (Stacconi etal 2013GabarraRiudavetsRodriguezPujade-VillarampArno2015Milleretal2015AKruitwagenunpublishedresults)Howeverduetolimitations in experimental setups no clear conclusions can yetbe drawnon natural parasitization rates ofD suzukii relative to other drosophilids and on the parasitoidrsquos ability and efficiencyto localizeandexploitD suzukiihostpatchesFieldexperimentseither only included D suzukiibaitedtraps(Gabarraetal2015)soparasitizationcouldnotbecomparedwithotherfruitfliesorbaitswereplacedinsuchawaythatparasitoidsmaybeattractedto their co-occurring natural D melanogaster host (Miller etal2015)andortheunnaturallyhighnumberofimmaturefruitfliesinthebaits(Milleretal2015Stacconietal2013)HencemoreresearchisneededtoobtaininsightintoD suzukiindashparasitoidin-teraction in nature and to assesswhich factorsmight stimulatehost-findingability


Virulence the ability to infest or harm the host is determined atleastpartlybythegenotypeoftheparasitoid(CartonampNappi1989Dubuffetetal2007DupasampBoscaro1999DupasFreyampCarton1998 Goecks etal 2013 Kraaijeveld Hutcheson Limentani ampGodfray2001)Awell-studiedexampleistheparasitoidL boulardiwhichshowsintraspecificvariationinitsabilitytosuppressthehostimmuneresponseinD melanogaster and D yakuba(Dubuffetetal2007 Dupas etal 1998) Its virulence is determined by two im-munesuppressivegenesencodedatdifferentunlinkedloci(DupasampCarton1999)Twostrainshavebeendescribedwithdifferentgeno-typesonethatcansuccessfullyparasitizeD melanogasterbutnotD yakubaandishomozygousforallelesforvirulenceagainstD mel-anogaster but not against D yakuba (Dubuffet etal 2007) TheotherstrainishomozygousforallelesforvirulenceagainstD yakuba but not D melanogaster (Dubuffet etal 2007) In an interestingmannercontrarytowhatwouldbeexpectedbasedonitsgenotypethisstraincanalsoreproduceonD melanogaster ThissuggeststhatotherfactorsforexampleDrosophilahostgenotypealsodetermineparasitismsuccess(Dubuffetetal2007)


Different environmental conditions influence the performance ofparasitoidsTwoimportantstressfactorsaretemperature(DelavaFleury amp Gibert 2016 Ris Allemand Fouillet amp Fleury 2004)and insecticides (Cossentine amp Ayyanath 2017 Komeza FouilletBouletreauampDelpuech2001RafalimananaKaiserampDelpuech2002) Parasitism of P vindemmiae for example was significantlynegatively affected by Spinosad a commonly used insecticideagainst D suzukii (Cossentine amp Ayyanath 2017) Hence releas-ingP vindemmiae as biological control agent in insecticide-treatedfieldsmight reduce itsefficiencyTwobiotic factors thatcanalterparasitization success are heritable viruses that manipulate theparasitoidsrsquo biology (Martinez Lepetit Ravallec Fleury ampVaraldi2016Martinezetal2012)andcompetitorspeciesexploiting thesamehostresourceThelatterisespeciallyrelevantwhenapplyinganewbiologicalcontrolagentinanareawhereanotherparasitoidis alreadypresent as itmay reduce theoriginal agentsrsquo efficiencyIn contrast additive (Herrick Reitz Carpenter amp OrsquoBrien 2008Shapiro-Ilan Jackson Reilly amp Hotchkiss 2004 Snyder amp Ives2003)orevensynergisticinteractions(MesquitaampLacey2001)oftheagentwithotherspeciesarepossibleandmightenhancetheef-ficacyofthecontrolagent


Of the indigenousparasitoids thepupalparasitoidsofD suzukii appear to have the highest biocontrol potential as they seemnot to be affected by the high resistance level of the pest YetP vindemmiae and T drosophilaehavearelativelywidehostrange


This may cause high incidence of nontarget effects if releasedas control agentor lowbiocontrol efficiencyagainstD suzukii iftheyhavehigherpreferenceforotherhostspeciesForexamplethe pupal parasitoid P vindemmiae can parasitize more than 60fly speciesand isevenable tohyperparasitizeother (beneficial)parasitoids like A tabida and L heterotoma (Carton BouletreauvanAlphenampvanLenteren1986MarchioriampBarbaresco2007WangampMessing2004aZhaoZengXuLuampLiang2013)ThepupalparasitoidT drosophilaehasasmallerhostrangebutisstillable to develop on numerous Drosophila species (Carton etal1986Mazzettoetal2016)TheuseofthosespeciesascontrolagentsespeciallyP vindemmiaethereforerequiresextensiveas-sessment of ecological risks intraguild predation and potentialeffects on nontarget species (nontarget effects) Careful evalu-ation is needed to determinewhether these risks outweigh thebenefitsIncaseitisdeemedplausibletoimprovethesespeciestobecomesuitablebiocontrolagentsanobvioustraitthatthesespeciescouldbeoptimizedforistobecomemorehost-specific In factT DrosophilaeisalreadyonthemarketasbiocontrolagentinItalyalthoughitshostpreferenceandefficiencyincoldercondi-tions(eglt20deg)(Rossi-Stacconietal2017)mightneedtobeim-provedtoincreaseitssuccessrateandtobeeffectiveinnortherncountries(earlyintheseason)

The only indigenous larval parasitoidwith some parasitizationsuccessonD suzukii isL heterotoma The virulencemechanismofL heterotomaenablesittodeveloponarangeofspeciesofDrosophilaChymomyza and Scaptomyza(EijsEllersampVanDuinen1998Fleuryetal2009Janssen1989)includingD suzukiiWhethertheirgen-eralisticbehaviorisduetotheirvenomloadvenomcompositionorotherfactors ishowevernotclear IdentifyingthemechanismthatenablesatleastsomeL heterotomatoovercomehostresistanceofD suzukiicouldbebeneficialforthescreeningofindividualsforspe-cifictraitsforselectionAssayingproteinsorspecificallelesmaybeanefficientapproachtoselectspecificallyforatraitofrelevanceforkillingabilityoftheparasitoid

Inconclusion thesuccessofacontrolagentcanbe largelyinfluenced by both genetic and environmental factors For se-lective breeding it is important to be aware of factors deter-mining the agentsrsquo performance in the field and during (mass)rearingastheyareoftendifferentfromexperimentallaboratoryconditions Important factors to investigate include the host-finding ability of the agent in the field phenotypic expressionacrossabioticconditions(reactionnorm)andthenatureoftheirinteractionswithother species in the fieldKnowing these ef-fects is important to predict their efficiency in the field andunderlinestheimportanceofassessingfieldexperimentsinthetargetareaofreleaseInaninterestingmanneradditiveorsyn-ergisticinteractionsofthecontrolagentwithotherspeciescanbeexploitedforbiologicalcontrolHoweverthenatureoftheirinteraction(antagonisticoradditivesynergistic)dependsonforexampletiming(simultaneouslyorsequential)andrateofappli-cation(HusseinHabustovaPuzaampZemek2016Shapiro-Ilanetal2004)

5emsp |emspSTEP 4 IMPROVE AND DETERMINE THE SUCCESS OF THE PAR A SITOID

ThelargevariationinparasitizationsuccesswithinnaturalenemiesofD suzukiicanbeexploitedindifferentwaysThemoststraightfor-wardmethodisbycomparingstrainsandtochooseoneexpressingoptimalbiocontroltraitvalues(Lommenetal2017)Thishoweverwillnotalwaysyieldthedesiredtraitcombinationsandfurtheropti-mizationisthenrequiredThiscanbeachievedbyselectivebreedingorexperimentalevolutionofanpreferablynativeoutbredstrainormixture of strains (eg to increase genetic variation) Populationspresent in the invaded areamight also be crossedwith those co-evolvedwiththepesthowevertheir importandreleasemightbesloweddownbynationalandinternationalregulationsincludingthebefore-mentioned Nagoya Protocol (Hajek etal 2016) SelectivebreedingandexperimentalevolutioncanincreasethefrequencyofspecificallelestoexpressdesirabletraitvaluesinthepopulationofinvestigationThishasalreadybeendonesuccessfullyforcenturiesinlivestockandplantbreedingSelectivebreedingandexperimentalevolutionrequiresubstantialgeneticvariationofthetrait(s)ofinter-estanda largeeffectivepopulationsizeMethodsofselectionaredescribed in forexampleKaweckietal (2012)GarlandandRose(2009)andLommenetal(2017)Theyincludeexposingapopulationtoexperimentalconditionstoobtainastrainadaptedtothespecificenvironment (experimental evolution) and selecting and breedingonlythoseindividualsharboringthedesiredtrait(s)(artificialselec-tion)Agentscanbeselectedeitheronphenotypebreedingvalue(sumofeffectsofallallelesofanindividual)oronasinglealleleThechoicedependsontheabilitytomeasurephenotypicvaluegenomicknowledgeandmoneyavailableandonthegeneticarchitectureofthetrait(s)ofinterest(iewhetheronelocusoflargeeffectormanyloci of small effect are selected)When the candidate agentsrsquo ge-nome is sequenced geneticmarkersmay assist artificial selectionwhenvariable genomic region(s) are identified that are associatedwith the target trait(s) Using these markers to select individualsfortrait(s)ofinterest(marker-assistedselectiongenomicselection)cansave timeand increaseaccuracyof selection (Xuetal2012)InsteadorinadditionhybridizationofdifferentstrainscanincreasegeneticvariationoftheagenttobeimprovedandormaybeawaytogeneratenewgeneticcombinationstoaltertheperformanceofthecontrolagentAfewstudieshavedemonstratedthepotentialofse-lectivelybreedingbiocontrolagents(egHoy19851986Lommen2013) inparticularparasitoids (egKraaijeveldHutcheson etal2001 Rouchet amp Vorburger 2014 Weseloh 1986) The relativeshortgenerationtimeandsizemakes(selective)breedingofinsectsmorefeasiblecomparedtolivestockandcropsInadditionknowl-edgeaboutthegeneticbasisoftargettrait(s)couldmakeoptimiza-tionmore efficient usingmolecular tools (egmarkers) to rapidlyselectforcertaintrait(s)andpredicttheresponsetoselection

Twoimportantdrawbacksthatcanhinderthesuccessof(selec-tive)breedingarelowgeneticvariationandadaptationtolaboratoryconditions(Hopperetal1993Mackauer1976SoslashrensenAddisonampTerblanche2012)Theamountofgeneticvariationdependson


the startingpopulationand (selective)breedingmethodSelectivebreedingcausesadecreaseinvariationasonlyasubsetofthepop-ulationwiththedesiredcharacteristicsisselectedtocontributetothenextgenerationThisresultsinhigherchancesofinbreedingde-pressionand lossof (desirable) allelesand fixationof (deleterious)allelesduetogeneticdriftInparticularwhenisaimedforongoinglong-termcontrolofanagent (oneorseveralyears)adecrease ingeneticvariationmightlimittheirabilitytorespondtoenvironmen-talchangeswithinandbetweenyearsTo limit inbreedingeffectsthesource(s)andsizeof thestartingpopulationshouldbechosencarefullytokeepalargeeffectivepopulationsizeandthuslargege-neticvariation(Lommenetal2017Mackauer1976MeuwissenampWoolliams1994)Toretaingeneticvariationbreedingschedulesareavailablethatmaintainlargeeffectivepopulationsize(egLommenetal2017vandeZandeetal2014)Inadditiontheselectionre-gimeandthe intensityofselection influencegeneticvariationandshould therefore be chosen carefully tomaintain a fit populationInan interestingmanner inhaplodiploidsystems (includingallhy-menopteransparasitoids)inwhichmalesdevelopfromunfertilizedeggsandfemalesfromfertilizedeggsinbreedingdepressionislessprevalentDeleteriousrecessiveallelesthatareexpressedinmalesarerapidlypurgedbyselectionthusreducingdeleteriousallelefre-quencies(HenterampFenster2003)

Breeding and experimental conditions should preferably sim-ulatenatural conditionsof the target area to enhance the agentrsquossuccess rate and to prevent adaptation to laboratory conditionsMassrearingcanresult inunintentionalbehavioralchangesduetogenotypicchanges (selection)orenvironmentally inducedchanges(phenotypicplasticitysuchaslearning)(Chambers1977Mackauer1976)Parasitoidsrearedonartificialdietcanforexampledeveloppreferenceforanatypicalartificialdietoveritsnaturalone(BautistaampHarris1997)Inadditiondetrimentalbehavioralalterationofbio-control agents hasbeen shown in dispersal ability host searchingandmatingbehavior(Boller1972Chambers1977)Aparasitoidsrsquohost-searchingbehaviorisalsoinfluencedbylearningofhost(egpheromones)andhost-habitatcues(egshapesandsubstrateodor)Incorporationofstimuliduringmassrearingmaypreventbehavioralchangestounnaturalsituationsandincreaseitseffectivenessinthefield to localize and parasitize the pest (Boller 1972Giunti etal2015)Thusalsononheritablevariationcanbeexploitedintheop-timizationprocessofstrains takingadvantageof insights into thedifferent factors that contribute to the phenotypic variation Thiscanbeachievedby(a)massrearingtheagentonthepestandor(b)exposingthemtopest-relatedcuesofthehabitattobereleasedin(Giuntietal2015)Thereforealthoughmaybepracticallyandeco-nomicallychallengingcontrolagentsofD suzukiishouldpreferablyberearedonthepestitselfandpossiblyoneconomicallyimportantfruitstoincreaseandmaintaintheiradaptationtothepestandpesthabitatChallengesincludedietaryrestrictionsrelative lowfecun-dityandrelativehighsensitivitytoclimaticconditions(EmiljanowiczRyanLangilleampNewman2014Hambyetal2016Iacovoneetal2015)Thisresults inslowerestablishmentandbuild-upof labora-torypopulationandmoretimeandcaretorearthem(Iacovoneetal

2015personalobservations)Howeverwithincreasingknowledgeontheflyrsquosbiology(egHambyetal2016)andculturingmethods(egSampsonetal2016YoungBuckiewiczampLong2018)(mass)rearingisbecomingmorefeasibleOncealargepopulationhasbeenestablisheditcanbekeptundertherightlaboratoryconditionsInparticulartheinnateabilitytofindhoststheabilitytolearntolocal-izehostsandmemoryretentiondifferbetweenparasitoidspeciesandpopulations(vandenBergetal2011GeervlietVreugdenhilDickeampVet1998KoppikHoffmeisterBrunkhorstKiessampThiel2015 Perez-Maluf etal 2008 Smid etal 2007) This should betakenintoaccountbychoosingcandidateagentswithhighsearchingabilityortargetingthesetraitsforartificialselectionasforexam-pledonebyvandenBergetal(2011)

Qualitycontrolofaselectedcontrolagentisrequiredtoverifyitsimprovedperformanceformassrearingandorinthefield(Lommenetal 2017) In particular the effect of phenotypic plasticity andcorrelatedresponsesontheperformanceoftheagentshouldbein-vestigatedTodeterminethesuccessofacontrolagent(semi-)fieldexperiments should be performed with preferably the same pestpopulationandunderenvironmentalconditionssimilarasinthetar-getarea(s)forrelease(egcroptypeclimaticconditionspresenceofalternativepreyhosts) Important factors to investigatearethecontrolagentsrsquoabilitytokillthepestandreducecropdamagethedurationoftheagentrsquoseffect(oneormultiplegenerations)andthereleasemethodoftheagentInotherwordsitsefficiencyshouldbecharacterizedinavarietyofrelevantconditionsintimeandspacepreferably on large scale (phenomics see Box1) to determine inwhich conditions the agent can be used The second factor influ-encing its success is correlated responsesmeaning that selectionononetraitmightchangetheexpressionofothertraits(KraaijeveldLimentani ampGodfray 2001UenoDe JongampBrakefield 2004)Trade-offs abeneficial change inone trait that is linked toadet-rimental change in another may be caused by genetic correla-tions (pleiotropic effects genetic linkage) or resource allocation(Brakefield2003) andmaydecrease the fitnessandefficiencyofthecontrolagentParasitoidsselectedforhighcounterdefensesforexampleshowedasloweregg-hatchingratewhichmightgivethemafitnessdisadvantageduringsuper-ormultiparasitism(KraaijeveldHutchesonetal2001)Potential trade-offsand itseffecton theagentsrsquoefficiencyshould thereforebe investigateduponselectiontosecuretheefficiencyofthecontrolagent

6emsp |emspCONCLUSION AND FUTURE RESE ARCH DIREC TIONS

Findingandoptimizingpotentialagentsrequiresinsightintonaturalvariationof traits important forbiologicalcontrolandfactors thatdetermine this variation To what extent native natural enemiescanbeoptimizedbyselectivebreedingdependsonthegeneticar-chitectureof thetarget trait theamountofgeneticvariationandenvironmentalconstraintsThesefactorsvaryandshouldbedeter-minedforeachindividualcaseThereforetosystematicallydevelop


successfulcontrolagentsweproposea four-stepapproachtoex-ploitintraspecificvariationefficiently(Figure2)Wehaveillustratedthis optimization strategywith an example of killing efficiency ofparasitoids of the new invasive pestD suzukiiWe conclude thatthere is large variation in killing efficiency and field performancewithinandbetweenparasitoidspeciesAsthistraitseemsatleastinparttobedeterminedbygeneticfactorsandpreviousresearchhasshownfeasibilitytoincreasethekillingabilityofparasitoidsthroughselectivebreeding(KraaijeveldHutchesonetal2001)indigenousparasitoids ofD suzukii might be optimized for biological controlIn particular the pupal parasitoid T drosophilae and larval parasi-toid L heterotomamightbesubjectto improvement inEuropeandNorthAmericaBefore settingup efficient breedingprograms forthesecandidatespeciesadditionalfieldexplorationsareneededforexploring amounts of intraspecific variation to choose andor usethemostcompetentstrain(s)Besideskillingefficiencyothertraitscanbetargetedforoptimizationsuchashostrange(inparticularforpupal parasitoids) to increase environmental safety and fecunditytoincreasemassrearingefficiencyInaninterestingmannertraitsimportantforbiocontrol(Table1)couldalsobeofinterestforbreed-inginsectsforuseinsterileinsecttechnique(SIT)andforfeedandfoodproduction

MorepotentialagentsmightbefoundwithincreasingresidencetimeofthepestintheinvadedareaThenumberofindigenousspe-ciesabletokillD suzukiiisalmost70lowerthaninthepestrsquosnativerangeHoweverthereareatleastsomeparasitoidspeciesthatseemtobeable tocope to someextentwith the invasivepest suchasL heterotoma and T drosophilae inEuropeandNorthAmericaThepotential of these parasitoids to naturally adapt to the high resis-tanceofD suzukiiismorelikelywhentheyencounterthishostfre-quentlyAdaptationtoD suzukiimightgivecertainspeciesafitnessadvantageasitisanunderexploitedecologicalnichewithinthelocalecosystemHoweveritisdifficulttopredictthetimeframeinwhichthiswouldoccur

Optimizing control agents requires thorough understanding ofwhich traits significantly enhance their performance The assess-mentofbiocontroltraitsandpredictingoptimalexpressionvalueshoweverarecomplicatedaslaboratoryresultsdonotalwaysholdinnatureInadditionnolistofoptimaltraitvaluesexistsbecausethesemaydifferwithpestspeciesthecroptoprotectclimaticconditionsof target area release method (long-term vs short-term control)andtargetarea(greenhousesmallorlargeorchard)(Lommenetal2017Wajnberg2004)Identificationofimportantbiocontroltraitsforspecificpestsandtargetareasorfindingagenericapproachfortheir identification could be highly beneficial for the efficiency ofbiocontrol (ldquopersonalizedbiocontrolrdquo)Large-scalephenotypicdatacollection (phenomicsseeBox1)couldbeaneffectivemethodtoaccomplishthisInadditionbiologicalcontrolcouldgreatlybenefitfromgenomicresearchasitcanspeedupandincreasethesuccessofselectivebreedingofnaturalenemiesWholegenomesequenc-ingcanaidtheidentificationofgeneticmarkersformarker-assistedselection(DekkersampHospital2002)ortogeneratehigh-resolutionSNPmapstoinvestigatethegeneticarchitectureofrelevanttraits

Todategeneticdataonbiocontrolagentsareoftenlimitedasge-notyping costs are often too high for companies that are mass-producingbiocontrolagents(Lommenetal2017)Withdecreasingcostsitmaybecomemorefeasibleinthefuture

ACKNOWLEDG EMENTS

WethankBartPannebakkerandTomGrootforvaluablediscussionand twoanonymous reviewers for constructivecommentson thismanuscriptThiswork ispartof theresearchprogramGreenwithproject number ALWGR20156 which is partly financed by theNetherlandsOrganisationforScientificResearch(NWO)andpartlybyKoppertBiologicalSystems

CONFLIC T OF INTERE S T

Nonedeclared

DATA ARCHIVING

Nodataareassociatedwiththismanuscript

ORCID

Astrid Kruitwagen httporcidorg0000-0001-5952-1589

R E FE R E N C E S

Abdel-Rahman E M Landmann T Kyalo R Ongrsquoamo GMwalusepoSSuliemanSampLeRuB(2017)Predictingstemborerdensity inmaizeusingRapidEyedataandgeneralized lin-ear models International Journal of Applied Earth Observation and Geoinformation 57 61ndash74 httpsdoiorg101016jjag201612008-ampgt

Adrion J R Kousathanas A PascualM BurrackH JHaddadNMBerglandAOampSinghhellipND(2014)Drosophila suzukii The geneticfootprintofarecentworldwideinvasionMolecular Biology and Evolution31(12)3148ndash3163httpsdoiorg101093molbevmsu246

AgrawalAA(2001)Phenotypicplasticityintheinteractionsandevo-lution of species Science 294 321ndash326 httpsdoiorg101126science1060701

AnagnostouC LeGrandEAampRohlfsM (2010)Friendly food forfitterfliesndashInfluenceofdietarymicrobialspeciesonfoodchoiceandparasitoidresistance inDrosophila Oikos119(3)533ndash541httpsdoiorg101111j1600-0706200918001x

Andrade G S Pratissoli D Dalvi L P Desneux N amp SantosJunior H J G (2011) Performance of four Trichogramma spe-cies (Hymenoptera Trichogrammatidae) as biocontrol agents ofHeliothis virescens(LepidopteraNoctuidae)undervarioustempera-ture regimes Journal of Pest Science 84(3) 313ndash320 httpsdoiorg101007s10340-011-0364-3

Araus J LampCairns JE (2014)Fieldhigh-throughputphenotypingThenewcropbreedingfrontierTrends in Plant Science19(1)52ndash61httpsdoiorgdoi101016jtplants201309008

Asplen M K Anfora G Biondi A Choi D S Chu D DaaneK M hellip Desneux N (2015) Invasion biology of spottedwing Drosophila (Drosophila suzukii) A global perspective and


future priorities Journal of Pest Science 88 469ndash494 httpsdoiorg101007s10340-015-0681-z

AtallahJTeixeiraLSalazarRZaragozaGampKoppA(2014)ThemakingofapestTheevolutionofafruit-penetratingovipositor inDrosophila suzukiiandrelatedspeciesProceedings of the Royal Society of London B Biological Sciences 281(1781) 20132840 httpsdoiorg101098rspb20132840

AtkinsonWampShorrocksB(1977)Breedingsitespecificityinthedo-mesticspeciesofDrosophila Oecologia29(3)223ndash232httpsdoiorg101007BF00345697

AukemaJEMcCulloughDGVonHolleBLiebholdAMBrittonKampFrankelSJ(2010)Historicalaccumulationofnonindigenousforest pests in the continental United States BioScience 60(11)886ndash897httpsdoiorg101525bio201060115

Ayres J S amp Schneider D S (2009) The role of anorexia in resis-tance and tolerance to infections inDrosophila PLoS Biology7(7)e1000150httpsdoiorg101371journalpbio1000150

BahderBWBahderLDHambyKAWalshDBampZalomFG(2015)Microsatellite variation of two pacific coastDrosophila su-zukii(dipteraDrosophilidae)populationsEnvironmental Entomology44(5)1449ndash1453httpsdoiorg101093eenvv117

Bautista R ampHarris E (1997) Effect of insectary rearing on hostpreference and oviposition behavior of the fruit fly parasit-oid Diachasmimorpha longicaudata Entomologia Experimentalis Et Applicata 83(2) 213ndash218 httpsdoiorg101046j1570- 7458199700174x

vandenBergMDuivenvoordeLWangGTribuhlSBukovinszkyTVetLEhellipSmidHM(2011)Naturalvariationinlearningandmemory dynamics studied by artificial selection on learning ratein parasitic wasps Animal Behaviour 81(1) 325ndash333 httpsdoiorg101016janbehav201011002

Boivin G amp Brodeur J (2006) Intra-and interspecific interactionsamongparasitoidsMechanismsoutcomesandbiologicalcontrolInGBoivinampJBrodeur(Eds)Trophic and guild in biological interactions control(pp123ndash144)DordrechtTheNetherlandsSpringerhttpsdoiorg1010071-4020-4767-3

Bolda M P Goodhue R E amp Zalom F G (2010) Spotted wingDrosophilaPotentialeconomic impactofanewlyestablishedpestAgricultural and Resource Economics Update13(3)5ndash8

BollerE(1972)Behavioralaspectsofmass-rearingofinsectsBioControl17(1)9ndash25

BrakefieldPM(2003)Artificialselectionandthedevelopmentofeco-logicallyrelevantphenotypesEcology84(7)1661ndash1671httpsdoiorg1018900012-9658(2003)084[1661ASATDO]20CO2

BruckDJBoldaMTanigoshiLKlickJKleiber JDeFrancescoJhellipSpitlerH(2011)Laboratoryandfieldcomparisonsofinsecti-cidestoreduceinfestationofDrosophila suzukiiinberrycropsPest Management Science 67(11) 1375ndash1385 httpsdoiorg101002ps2242

Calabria GMaacuteca J Baumlchli G Serra L amp PascualM (2012) Firstrecords of the potential pest species Drosophila suzukii (dip-tera Drosophilidae) in Europe Journal of Applied Entomology136(1ndash2) 139ndash147 httpsdoiorg101111j1439-041820100 1583x

Cancino M D G Hernandez A G Cabrera J G Carrillo GM Gonzalez J A S amp Bernal H C A (2015) Parasitoids ofDrosophila suzukii (matsumura) (diptera Drosophilidae) in ColimaMexico Southwestern Entomologist 40 855ndash858 httpsdoiorg1039580590400418

Carton Y BouletreauM vanAlphen J JM amp van Lenteren J V(1986)TheDrosophilaparasiticwaspsInMAshburnerHLCarsonampJNThompson (Eds)The genetics and biology of Drosophila (pp348ndash394)LondonUKAcademicPress

CartonYampNappiCA(1989)Geneticvariabilityofhost-parasitere-lationshiptraitsUtilizationofisofemalelinesinaDrosophila simulans

parasiticwaspGenetics Selection Evolution21437ndash446httpsdoiorg1011861297-9686-21-4-437

CattelJKaurRGibertPMartinezJFraimoutAJigginsFhellipMillerW (2016)Wolbachia inEuropeanpopulationsof the invasivepestDrosophila suzukiiRegionalvariation in infection frequenciesPLoS ONE11e0147766httpsdoiorg101371journalpone0147766

Cattel J Martinez J Jiggins F Mouton L amp Gibert P (2016)Wolbachia-mediatedprotectionagainstviruses in the invasivepestDrosophila suzukii Insect Molecular Biology25(5)595ndash603httpsdoiorg101111imb12245

ChabertSAllemandRPoyetMEslinPampGibertP(2012)Abilityof European parasitoids (Hymenoptera) to control a new invasiveAsiaticpestDrosophila suzukii BioControl6340ndash47

ChambersDL (1977)Qualitycontrol inmass rearingAnnual Review of Entomology 22(1) 289ndash308 httpsdoiorg101146annureven22010177001445

ChaplinskaMGerritsmaSDini-AndreoteFSallesJFampWertheimB (2016) Bacterial communities differ amongDrosophila melano-gaster populations and affect host resistance against parasitoidsPLoS ONE 11(12) e0167726 httpsdoiorg101371journalpone0167726

Cini A Ioriatti C amp Anfora G (2012) A review of the invasion ofDrosophila suzukii in Europe and a draft research agenda for inte-gratedpestmanagementBulletin of Insectology65(1)149ndash160

CockM JWvanLenteren JCBrodeur JBarrattB IPBiglerFBolckmansKhellipParraJRP(2010)Donewaccessandbene-fitsharingproceduresundertheconventiononbiologicaldiversitythreaten the future of biological controlBioControl55 199ndash218httpsdoiorg101007s10526-009-9234-9

CollierTampVanSteenwykR(2004)Acriticalevaluationofaugmenta-tivebiologicalcontrolBiological Control31(2)245ndash256httpsdoiorg101016jbiocontrol200405001

Cossentine J E amp Ayyanath M (2017) Limited protection of theparasitoid Pachycrepoideus vindemiae fromDrosophila suzukii host-directed spinosad suppression Entomologia Experimentalis Et Applicata164(1)78ndash86httpsdoiorg101111eea12592

DaaneKMWangXGBiondiAMillerBMillerJCRiedlHhellipWaltonVM (2016)FirstexplorationofparasitoidsofDrosophila suzukii in South Korea as potential classical biological agentsJournal of Pest Science 89 823ndash835 httpsdoiorg101007s10340-016-0740-0

DeClercqPMasonPGampBabendreierD(2011)BenefitsandrisksofexoticbiologicalcontrolagentsBioControl56(4)681ndash698httpsdoiorg101007s10526-011-9372-8

DeRosGAnforaGGrassiAampIoriattiC(2013)Thepotentialeco-nomicimpactofDrosophila suzukiionsmallfruitsproductionintren-tino(Italy)IOBC- WPRS Bulletin91317ndash321

DekkersJCampHospitalF(2002)Theuseofmoleculargeneticsintheimprovement of agricultural populationsNature Reviews Genetics3(1)22ndash32httpsdoiorg101038nrg701

Delava E Fleury F amp Gibert P (2016) Effects of daily fluctuat-ing temperatures on the Drosophila- Leptopilina boulardi parasit-oid association Journal of Thermal Biology60 95ndash102 httpsdoiorg101016jjtherbio201606012

DelpuechJFreyFampCartonY(1996)ActionofinsecticidesonthecellularimmunereactionofDrosophila melanogasteragainstthepar-asitoid Leptopilina boulardi Environmental Toxicology and Chemistry15(12)2267ndash2271httpsdoiorg101002etc5620151221

Dicke M Lenteren J V Boskamp G amp Voorst R V (1985)IntensificationandprolongationofhostsearchinginLeptopilina het-erotoma(Thomson)(HymenopteraEucoilidae)throughakairomoneproduced by Drosophila melanogaster Journal of Chemical Ecology11(1)125ndash136httpsdoiorg101007BF00987611

DriessenGHemerikLampVanAlphenJJ(1989)Drosophilaspeciesbreeding in the stinkhorn (Phallus impudicus pers) and their larval


parasitoidsNetherlands Journal of Zoology40(3)409ndash427httpsdoiorg101163156854290X00019

Dubuffet A Dupas S Frey F Drezen J Poirie M amp Carton Y(2007)GeneticinteractionsbetweentheparasitoidwaspLeptopilina boulardianditsDrosophilahostsHeredity98(1)21ndash27httpsdoiorg101038sjhdy6800893

DupasSampBoscaroM(1999)GeographicvariationandevolutionofimmunosuppressivegenesinaDrosophilaparasitoidEcography22(3)284ndash291httpsdoiorg101111j1600-05871999tb00504x

DupasSBrehelinMFreyFampCartonY(1996)Immunesuppressivevirus-like particles in aDrosophila parasitoid Significance of theirintraspecific morphological variations Parasitology 113 207ndash212httpsdoiorg101017S0031182000081981

Dupas S amp Carton Y (1999) Two non-linked genes for specific vir-ulence of Leptopilina boulardi against Drosophila melanogaster and D yakuba Evolutionary Ecology 13(2) 211ndash220 httpsdoiorg101023A1006691431658

DupasSFreyFampCartonY (1998)A singleparasitoid segregatingfactor controls immune suppression in Drosophila The Journal of Heredity89(4)306ndash311httpsdoiorg101093jhered894306

EdwardsDampBatleyJ(2010)PlantgenomesequencingApplicationsforcropimprovementPlant Biotechnology Journal8(1)2ndash9httpsdoiorg101111j1467-7652200900459x

EijsIEMEllersJampVanDuinenGJ(1998)Feedingstrategiesindrosophilid parasitoids The impact of natural food resources onenergy reserves in femalesEcological Entomology23(2) 133ndash138httpsdoiorg101046j1365-2311199800117x

Emiljanowicz L M Ryan G D Langille A amp Newman J (2014)Development reproductive output and population growth of thefruitflypestDrosophila suzukii (DipteraDrosophilidae)onartificialdiet Journal of economic entomology107(4)1392ndash1398httpsdoiorg101603EC13504

FellowesMDEKraaijeveldARampGodfrayHCJ(1999)Cross-resistancefollowingartificialselectionforincreaseddefenseagainstparasitoids in Drosophila melanogaster Evolution 53 966ndash972httpsdoiorg101111j1558-56461999tb05391x

Figueroa-Lopez AM Cordero-Ramirez JDQuiroz-Figueroa F Ramp Maldonado-Mendoza I E (2014) A high-throughput screen-ing assay to identify bacterial antagonists against Fusarium verti-cillioides Journal of Basic Microbiology 54 S125ndashS133 httpsdoiorg101002jobm201200594

Fleury F Gibert P Ris N amp Allemand R (2009) Ecology andlife history evolution of frugivorous Drosophila parasitoidsAdvances in Parasitology 70 3ndash44 httpsdoiorg101016S0065-308X(09)70001-6

Fleury F Ris N Allemand R Fouillet P Carton Y amp BouletreauM (2004) Ecological and genetic interactions in Drosophila-parasitoids communities A case study with D melanogas-ter D simulans and their common Leptopilina parasitoids insouth-eastern France Genetica 120(1ndash3) 181ndash194 httpsdoiorg101023BGENE0000017640780879e

FraimoutADebatVFellousSHufbauerRAFoucaudJPudloPhellipChenX(2017)DecipheringtheroutesofinvasionofDrosophila suzukii by means of ABC random forest Molecular Biology and Evolution34(4)980ndash996

FraimoutALoiseauAPriceDKXuerebAMartinJVitalisRhellipEstoupA(2015)Newsetofmicrosatellitemarkersforthespotted-wingDrosophila suzukii(dipteraDrosophilidae)Apromisingmolec-ulartoolforinferringtheinvasionhistoryofthismajorinsectpestEuropean Journal of Entomology112(4)855ndash859

FurbankRT(2009)PlantphenomicsFromgenetoformandfunctionFunctional Plant Biology36(10)5ndash6

FurbankRTampTesterM (2011)Phenomicsndashtechnologies to relievethe phenotyping bottleneck Trends in Plant Science 16(12) 635ndash644httpsdoiorg101016jtplants201109005

FytrouASchofieldPGKraaijeveldARampHubbardSF (2006)Wolbachia infection suppresses both host defence and parasitoidcounter-defence Proceedings Biological Sciences 273(1588) 791ndash796httpsdoiorgF762H368T31L6455

Gabarra R Riudavets J Rodriguez G A Pujade-Villar J amp ArnoJ (2015) Prospects for the biological control of Drosophila suzukii BioControl 60 331ndash339 httpsdoiorg101007s10526-014-9646-z

GarlandTampRoseMR(2009)Experimental evolution Concepts meth-ods and applications of selection experimentsBerkeleyCAUniversityofCaliforniaPress

GeervlietJBVreugdenhilAIDickeMampVetLE(1998)Learningto discriminate between infochemicals from different plant-hostcomplexes by the parasitoids Cotesia glomerata and C rubecula Entomologia Experimentalis Et Applicata86(3)241ndash252httpsdoiorg101046j1570-7458199800286x

Gerritsma S de Haan A van de Zande L ampWertheim B (2013)Naturalvariationindifferentiatedhemocytesisrelatedtoparasitoidresistance inDrosophilamelanogaster Journal of Insect Physiology59(2)148ndash158httpsdoiorg101016jjinsphys201209017

GiuntiGCanaleAMessingRHDonatiEStefaniniCMichaudJPampBenelliG(2015)ParasitoidlearningCurrentknowledgeandimplications for biological control Biological Control 90 208ndash219httpsdoiorgdoi101016jbiocontrol201506007

GoecksJMortimerNTMobleyJABowersockGJTaylorJampSchlenkeTA (2013) Integrativeapproachrevealscompositionofendoparasitoidwasp venomsPLoS ONE8(5) e64125 httpsdoiorg101371journalpone0064125

GoodhueREBoldaMFarnsworthDWilliamsJCampZalomFG(2011) SpottedwingDrosophila infestationofCalifornia strawber-riesandraspberriesEconomicanalysisofpotential revenue lossesand control costs Pest Management Science 67(11) 1396ndash1402httpsdoiorg101002ps2259

GuerrieriEGiorginiMCasconePCarpenitoSampvanAchterbergC(2016)SpeciesdiversityintheparasitoidgenusAsobara(hymenop-teraBraconidae)fromthenativeareaofthefruitflypestDrosophila suzukii(dipteraDrosophilidae)PLoS ONE11(2)e0147382httpsdoiorg101371journalpone0147382

HajekAEHurleyBPKenisMGarnasJRBushSJWingfieldM JhellipCockM JW (2016) Exotic biological control agents AsolutionorcontributiontoarthropodinvasionsBiological Invasions18953ndash969httpsdoiorg101007s10530-016-1075-8

HambyKABellamyDEChiuJCLeeJCWaltonVMWimanNGhellipBiondiA (2016)Bioticandabiotic factors impactingde-velopment behavior phenology and reproductive biology ofDrosophila suzukii Journal of pest science89(3)605ndash619httpsdoiorg101007s10340-016-0756-5

HammCABegunDJVoASmithCCSaelaoPShaverAOhellipTurelliM(2014)WolbachiadonotlivebyreproductivemanipulationaloneInfectionpolymorphisminDrosophila suzukii and D subpulchrella Molecular Ecology234871ndash4885httpsdoiorg101111mec12901

HauserM (2011)Ahistoric accountof the invasionofDrosophila su-zukii(Matsumura)(DipteraDrosophilidae)inthecontinentalunitedstateswithremarksontheiridentificationPest Management Science67(11)1352ndash1357httpsdoiorg101002ps2265

Haye T Girod P Cuthbertson A G SWang X G Daane KMHoelmerKAhellipDesneuxN(2016)CurrentSWDIPMtacticsandtheirpracticalimplementationinfruitcropsacrossdifferentregionsaround the world Journal of Pest Science89643ndash651httpsdoiorg101007s10340-016-0737-8

HayesBJDaetwylerHDampGoddardME(2016)Modelsforge-nometimesenvironmentinteractionExamplesinlivestockCrop Science56(5)2251ndash2259httpsdoiorg102135cropsci2015070451

HenterHJampFensterC(2003)Inbreedingdepressionandhaplodip-loidyExperimentalmeasuresinaparasitoidandcomparisonsacross


diploid and haplodiploid insect taxa Evolution 57(8) 1793ndash1803httpsdoiorg101111j0014-38202003tb00587x

Herrick N J Reitz S R Carpenter J E amp OrsquoBrien C W (2008)Predation by Podisus maculiventris (Hemiptera Pentatomidae) onPlutella xylostella (Lepidoptera Plutellidae) larvae parasitized byCotesia plutellae (HymenopteraBraconidae)and its impactoncab-bage Biological Control 45(3) 386ndash395 httpsdoiorg101016jbiocontrol200802008

HopperKRoushRampPowellW(1993)Managementofgeneticsofbiological-controlintroductionsAnnual Review of Entomology38(1)27ndash51httpsdoiorg101146annureven38010193000331

HouleDGovindarajuDRampOmholtS(2010)PhenomicsThenextchallenge Nature Reviews Genetics 11(12) 855ndash866 httpsdoiorg101038nrg2897

Howick V M amp Lazzaro B P (2014) Genotype and diet shaperesistance and tolerance across distinct phases of bacte-rial infection Bmc Evolutionary Biology 14 56 httpsdoiorg1011861471-2148-14-56

HoyMA(1985)Recentadvancesingeneticsandgeneticimprovementof the PhytoseiidaeAnnual Review of Entomology30(1) 345ndash370httpsdoiorg101146annureven30010185002021

Hoy M A (1986) Use of genetic improvement in biological controlAgriculture Ecosystems amp Environment15(2ndash3)109ndash119httpsdoiorg1010160167-8809(86)90084-8

HusseinHMHabustovaOSPuzaVampZemekR(2016)Laboratoryevaluation of Isaria fumosorosea CCM 8367 and Steinernema fel-tiaeUstinov against immature stages of theColoradopotato bee-tle PLoS ONE 11(3) e0152399 httpsdoiorg101371journalpone0152399

IacovoneAGirodPRisNWeydertCGibertPPoirieacuteMampGattiJL(2015)WorldwideinvasionbyDrosophila suzukiiDoesbeingtheldquocousinrdquoofamodelorganismreallyhelpsettingupbiologicalcontrolHopesdisenchantmentsandnewperspectivesRevue drsquoEcologie- La Terre et la Vie70207ndash214

Ideo S Watada M Mitsui H amp Kimura M T (2008) Host rangeof Asobara japonica (hymenoptera Braconidae) a larval parasit-oid of drosophilid flies Entomological Science11 1ndash6 httpsdoiorg101111j1479-8298200700244x

Jackson S A Iwata A Lee S Schmutz J amp Shoemaker R(2011) Sequencing crop genomes Approaches and ap-plications New Phytologist 191(4) 915ndash925 httpsdoiorg101111j1469-8137201103804x

Janssen A (1989) Optimal host selection by Drosophila parasit-oids in the field Functional Ecology 3 469ndash479 httpsdoiorg1023072389621

JanssenADriessenGDeHaanMampRoodbolN (1987)The im-pact of parasitoids on natural populations of temperatewoodlandDrosophila Netherlands Journal of Zoology38(1)61ndash73httpsdoiorg101163156854288X00049

KacsohBZampSchlenkeTA (2012)Highhemocyte load is associ-atedwith increased resistanceagainstparasitoids inDrosophila su-zukiiarelativeofDmelanogaster PLoS ONE7e34721httpsdoiorg101371journalpone0034721

Kaiser L Perez-Maluf R Sandoz J amp Pham-Delegue M (2003)Dynamics of odour learning in Leptopilina boulardi a hymenopter-ous parasitoid Animal Behaviour 66(6) 1077ndash1084 httpsdoiorg101006anbe20032302

Kasuya N Mitsui H Ideo S Watada M amp Kimura M T (2013)Ecological morphological and molecular studies onGanaspis indi-viduals(hymenopteraFigitidae)attackingDrosophila suzukii(dipteraDrosophilidae)Applied Entomology and Zoology4887ndash92httpsdoiorg101007s13355-012-0156-0

KaurRSioziosSMillerWJampRota-StabelliO(2017)Insertionse-quencepolymorphismandgenomicrearrangementsuncoverhidden

WolbachiadiversityinDrosophila suzukii and D subpulchrella Scientific Reports7(1)14815httpsdoiorg101038s41598-017-13808-z

KaweckiTJLenskiREEbertDHollisBOlivieriIampWhitlockMC (2012)ExperimentalevolutionTrends in Ecology amp Evolution27(10)547ndash560httpsdoiorg101016jtree201206001

Keebaugh E S amp Schlenke T A (2014) Insights from natural hostndashparasite interactions The Drosophila model Developmental amp Comparative Immunology42(1)111ndash123httpsdoiorg101016jdci201306001

KnollVEllenbroekTRomeisJampCollatzJ(2017)Seasonalandre-gionalpresenceofhymenopteranparasitoidsofDrosophila inswit-zerlandandtheirabilitytoparasitizetheinvasiveDrosophila suzukii Scientific Reports740697httpsdoiorg101038srep40697

Kolseth A DrsquoHertefeldt T Emmerich M Forabosco F MarklundS Cheeke T E hellip Weih M (2015) Influence of geneticallymodified organisms on agro-ecosystem processes Agriculture Ecosystems amp Environment 214 96ndash106 httpsdoiorg101016jagee201508021

Komeza N Fouillet P Bouletreau M amp Delpuech J (2001)Modification by the insecticide chlorpyrifos of the behavioral re-sponse to kairomones of a parasitoid wasp Leptopilina boulardi Archives of Environmental Contamination and Toxicology41(4)436ndash442httpsdoiorg101007s002440010269

Koppik M Hoffmeister T S Brunkhorst S Kiess M amp Thiel A(2015)IntraspecificvariabilityinassociativelearningintheparasiticwaspNasonia vitripennis Animal Cognition18(3)593ndash604httpsdoiorg101007s10071-014-0828-y

KraaijeveldA RampGodfrayH (1997) Trade-off between parasitoidresistanceand larvalcompetitiveability inDrosophila melanogaster Nature389(6648)278ndash280httpsdoiorg10103838483

Kraaijeveld A R Hutcheson K A Limentani E C amp Godfray HC J (2001) Costs of counterdefenses to host resistance in aparasitoid of Drosophila Evolution 55 1815ndash1821 httpsdoiorg101111j0014-38202001tb00830x

Kraaijeveld A R Limentani E C amp Godfray H C (2001) Basis ofthe trade-offbetweenparasitoid resistanceand larvalcompetitiveability in Drosophila melanogaster Proceedings Biological Sciences268(1464)259ndash261httpsdoiorg101098rspb20001354

Lee M J Kalamarz M E Paddibhatla I Small C Rajwani R ampGovindS(2009)VirulencefactorsandstrategiesofLeptopilinasppSelectiveresponsesinDrosophilahostsAdvances in Parasitology70123ndash145httpsdoiorg101016S0065-308X(09)70005-3

LeftwichPTBoltonMampChapmanT (2016)EvolutionarybiologyandgenetictechniquesforinsectcontrolEvolutionary Applications9(1)212ndash230httpsdoiorg101111eva12280

vanLenteren J C (2012a) IOBC internet book of biological control Retrieved from httpwwwiobc-globalorgdownloadIOBC_InternetBookBiCoVersion6Spring2012pdf

van Lenteren J C (2012b) The state of commercial augmenta-tive biological control Plenty of natural enemies but a frustrat-ing lack of uptake BioControl 57 1ndash20 httpsdoiorg101007s10526-011-9395-1

vanLenterenJCBolckmansKKoumlhlJRavensbergWJampUrbanejaA(2018)BiologicalcontrolusinginvertebratesandmicroorganismsPlentyofnewopportunitiesBioControl6339ndash59

LommenSTE(2013)Exploring and Exploiting Natural Variation in the Wings of a Predatory Ladybird Beetle for Biological Control Doctoral ThesisUniversityofLeidenLeidenTheNetherlands

LommenSTEdeJongPWampPannebakkerBA(2017)Itistimetobridge thegapbetweenexploringandexploitingProspects forutilizing intraspecific genetic variation to optimise arthropods foraugmentative pest control ndash A review Entomologia Experimentalis Et Applicata 162(2) 108ndash123 httpsdoiorg101111eea12 510


MackauerM (1976)Geneticproblems in theproductionofbiologicalcontrolagentsAnnual Review of Entomology21(1)369ndash385httpsdoiorg101146annureven21010176002101

MacQuarrieC J LyonsD SeehausenM Lamp Smith SM (2016)AhistoryofbiologicalcontrolinCanadianforests1882ndash2014The Canadian Entomologist1481ndash31

Marchiori CampBarbaresco L (2007)Occurrence ofPachycrepoideus vindemmiae (rondani1875)(hymenopteraPteromalidae)asapara-sitoidofMegaselia scalaris(loew1866)(dipteraPhoridae)inBrazilBrazilian Journal of Biology67(3)577ndash578httpsdoiorg101590S1519-69842007000300025

Markow T A amp OrsquoGrady P (2008) Reproductive ecology ofDrosophila Functional Ecology 22(5) 747ndash759 httpsdoiorg101111j1365-2435200801457x

Martinez J Duplouy A Woolfit M Vavre F OrsquoNeill S L ampVaraldi J (2012) Influenceof the virus LbFVandofWolbachia in a host-parasitoid interaction PLoS ONE 7(4) e35081 httpsdoiorg101371journalpone0035081

Martinez J Lepetit D Ravallec M Fleury F amp Varaldi J (2016)Additionalheritablevirus in theparasiticwaspLeptopilina boulardi PrevalencetransmissionandphenotypiceffectsJournal of General Virology97(2)523ndash535httpsdoiorg101099jgv0000360

MazzettoFGonellaEampAlmaA(2015)Wolbachiainfectionaffectsfemale fecundity in Drosophila suzukii Bulletin of Insectology 68153ndash157

Mazzetto F Marchetti E Amiresmaeili N Sacco D Francati SJucker C hellip Tavella L (2016)Drosophila parasitoids in northernItaly and their potential to attack the exotic pest Drosophila su-zukii Journal of Pest Science89837ndash850httpsdoiorg101007s10340-016-0746-7

Meijer K Smit C Schilthuizen M amp Beukeboom L W (2016)FitnessbenefitsofthefruitflyRhagoletis alternataonanon-nativerose host Oecologia 181(1) 185ndash192 httpsdoiorg101007s00442-015-3524-y

MeshrifWSRohlfsMampRoederT (2016)TheeffectofnutritiveyeastsonthefitnessofthefruitflyDrosophila melanogaster(DipteraDrosophilidae) African Entomology 24(1) 90ndash99 httpsdoiorg1040010030240090

Mesquita A amp Lacey L (2001) Interactions among the entomo-pathogenic fungus Paecilomyces fumosoroseus (Deuteromycotina Hyphomycetes) the parasitoid Aphelinus asychis (HymenopteraAphelinidae) and their aphid host Biological Control 22(1) 51ndash59httpsdoiorg101006bcon20010950

MeuwissenTampWoolliamsJ(1994)Effectivesizesoflivestockpopula-tionstopreventadeclineinfitnessTheoretical and Applied Genetics89(7)1019ndash1026

MichaelTPampJacksonS(2013)Thefirst50plantgenomesThe Plant Genome6(2)1ndash7

Miller B Anfora G Buffington M Daane K M Dalton D THoelmerKMhellipWaltonVM(2015)Seasonaloccurrenceofres-identparasitoidsassociatedwithDrosophila suzukiiintwosmallfruitproductionregionsof ItalyandtheUSABulletin of Insectology68 255ndash263

MitsuiHampKimuraMT(2010)Distributionabundanceandhostas-sociationoftwoparasitoidspeciesattackingfrugivorousdrosophi-lidlarvaeincentralJapanEuropean Journal of Entomology107535httpsdoiorg1014411eje2010061

MitsuiHTakahashiKHampKimuraMT(2006)Spatialdistributionsand clutch sizes ofDrosophila species ovipositing on cherry fruitsof different stagesPopulation Ecology48(3) 233ndash237 httpsdoiorg101007s10144-006-0260-5

MitsuiHvanAchterbergKNordlanderGampKimuraMT (2007)GeographicaldistributionsandhostassociationsoflarvalparasitoidsoffrugivorousdrosophilidaeinJapanJournal of Natural History411731ndash1738httpsdoiorg10108000222930701504797

MortimerNT(2013)Parasitoidwaspvirulenceawindowintoflyim-munity Fly7(4)242ndash248httpsdoiorg104161fly26484

NansenCCoelhoAJrVieiraJMampParraJR(2014)Reflectance-basedidentificationofparasitizedhosteggsandadultTrichogramma specimensThe Journal of Experimental Biology217(7) 1187ndash1192httpsdoiorg101242jeb095661

NansenCRibeiroLPDadourIampRobertsJD(2015)DetectionoftemporalchangesininsectbodyreflectanceinresponsetokillingagentsPLoS ONE10(4)e0124866httpsdoiorg101371journalpone0124866

NomanoFYKasuyaNMatsuuraASuwitoAMitsuiHBuffingtonM L amp KimuraM T (2017) Genetic differentiation ofGanaspis brasiliensis (Hymenoptera Figitidae) from East and SoutheastAsia Applied Entomology and Zoology 52 429ndash437 httpsdoiorg101007s13355-017-0493-0

NomanoFYMitsuiHampKimuraMT(2015)CapacityofJapanese Asobara species (hymenoptera braconidae) to parasitize a fruitpest Drosophila suzukii (diptera Drosophilidae) Journal of Applied Entomology139105ndash113httpsdoiorg101111jen12141

NystrandMampDowlingD (2014)Dose-dependenteffectsofanim-munechallengeatbothultimateandproximatelevelsinDrosophilamelanogasterJournal of Evolutionary Biology27(5)876ndash888httpsdoiorg101111jeb12364

Oliai S amp King B (2000) Associative learning in response tocolor in the parasitoid wasp Nasonia vitripennis (HymenopteraPteromalidae) Journal of Insect Behavior 13(1) 55ndash69 httpsdoiorg101023A1007763525685

OliveiraCMAuadAMMendesSMampFrizzasMR(2013)EconomicimpactofexoticinsectpestsinBrazilianagricultureJournal of Applied Entomology137(1ndash2)1ndash15httpsdoiorg101111jen12018

PapajDRampVetLE(1990)OdorlearningandforagingsuccessintheparasitoidLeptopilina heterotoma Journal of Chemical Ecology16(11)3137ndash3150httpsdoiorg101007BF00979616

Perez-Maluf R Rafalimanana H Campan E Fleury F amp Kaiser L(2008)Differentiationof innate but not learnt responses to host-habitat odours contributes to rapid host finding in a parasitoidgenotype Physiological Entomology 33(3) 226ndash232 httpsdoiorg101111j1365-3032200800636x

Pimentel D McNair S Janecka J Wightman J Simmonds COrsquoConnell C hellip Tsomondo T (2001) Economic and environmen-talthreatsofalienplantanimalandmicrobeinvasionsAgriculture Ecosystems amp Environment84(1)1ndash20httpsdoiorgdoi101016S0167-8809(00)00178-X

PimentelDZunigaRampMorrisonD(2005)Updateontheenviron-mentalandeconomiccostsassociatedwithalien-invasivespeciesintheUnitedStatesEcological Economics52(3)273ndash288httpsdoiorg101016jecolecon200410002

Poirieacute M Carton Y amp Dubuffet A (2009) Virulence strategiesin parasitoid Hymenoptera as an example of adaptive diversityComptes Rendus Biologies332 311ndash320 httpsdoiorg101016jcrvi200809004

PoyetM Eslin P Chabrerie O Prudrsquohomme SM Desouhant EampGibertP (2017)TheinvasivepestDrosophila suzukiiusestrans-generationalmedicationtoresistparasitoidattackScientific Reports743696httpsdoiorg101038srep43696

PoyetMEslinPHeacuteraudeMLeRouxVPreacutevostGGibertPampChabrerie O (2014) Invasive host for invasive pest When theAsiatic cherry fly (Drosophila suzukii) meets the American blackcherry (Prunus serotina)inEuropeAgricultural and Forest Entomology16(3)251ndash259httpsdoiorg101111afe12052

PoyetMHavardSPrevostGChabrerieODouryGGibertPampEslinP (2013)ResistanceofDrosophila suzukiitothelarvalpar-asitoids Leptopilina heterotoma and Asobara japonica is related tohaemocyte load Physiological Entomology 38 45ndash53 httpsdoiorg101111phen12002


PoyetMLeRouxVGibertPMeirlandAPreacutevostGEslinPampChabrerieO(2015)ThewidepotentialtrophicnicheoftheAsiaticfruitflyDrosophila suzukiiThekeyofitsinvasionsuccessintemper-ateEuropePLoS ONE10(11) e0142785httpsdoiorg101371journalpone0142785

RafalimananaHKaiserLampDelpuechJ(2002)Stimulatingeffectsofthe insecticide chlorpyrifosonhost searchingand infestationeffi-cacyofaparasitoidwaspPest Management Science58(4)321ndash328httpsdoiorg101002ps454

Reynolds D amp Riley J (2002) Remote-sensing telemetric andcomputer-based technologies for investigating insect movementA survey of existing and potential techniques Computers and Electronics in Agriculture35(2ndash3)271ndash307httpsdoiorg101016S0168-1699(02)00023-6

Ris N Allemand R Fouillet P amp Fleury F (2004) The joint effectof temperature and host species induce complex genotype-by-environment interactions in the larval parasitoid of DrosophilaLeptopilinaheterotoma(HymenopteraFigitidae)Oikos106(3)451ndash456httpsdoiorg101111j0030-1299200413274x

Rossi-Stacconi M V Panel A Baser N Ioriatti C Pantezzi T ampAnfora G (2017) Comparative life history traits of indigenousItalian parasitoids of Drosophila suzukii and their effectiveness atdifferent temperatures Biological Control 112 20ndash27 httpsdoiorg101016jbiocontrol201706003

RouchetRampVorburgerC (2014)Experimentalevolutionofparasit-oidinfectivityonsymbiont-protectedhostsleadstotheemergenceof genotype specificity Evolution 68(6) 1607ndash1616 httpsdoiorg101111evo12377

Sampson B JMallette T Addesso KM Liburd O E Iglesias LE Stringer S J hellip Adamczyk J J Jr (2016) Novel aspects ofDrosophila suzukii(DipteraDrosophilidae)biologyandanimprovedmethodforculturingthis invasivespecieswithamodifiedD mela-nogaster diet Florida Entomologist 99(4) 774ndash780 httpsdoiorg1016530240990433

Segura D F Viscarret M M Paladino L Z C Ovruski S M ampCladera J L (2007) Role of visual information and learning inhabitat selection by a generalist parasitoid foraging for concealedhosts Animal Behaviour 74 131ndash142 httpsdoiorg101016janbehav200612005

Shapiro-IlanDIJacksonMReillyCCampHotchkissMW(2004)EffectsofcombininganentomopathogenicfungiorbacteriumwithentomopathogenicnematodesonmortalityofCurculio caryae (cole-opteraCurculionidae)Biological Control30(1)119ndash126httpsdoiorg101016jbiocontrol200309014

SioziosSCestaroAKaurRPertot IRota-StabelliOampAnforaG(2013) Draft genome sequence of theWolbachia endosymbiont ofDrosophila suzukii Genome Announcements1e00032-13

SmidHMWangGBukovinszkyTSteidleJLBleekerMAvanLoonJJampVetLE(2007)Species-specificacquisitionandcon-solidationoflong-termmemoryinparasiticwaspsProceedings of the Royal Society of London B Biological Sciences274(1617)1539ndash1546httpsdoiorgC71V7N73169V3613

Snyder W amp Ives A (2003) Interactions between specialist andgeneralist natural enemies Parasitoids predators and pea aphidbiocontrol Ecology 84(1) 91ndash107 httpsdoiorg1018900012-9658(2003)084[0091IBSAGN]20CO2

SoslashrensenJGAddisonMFampTerblancheJS(2012)Mass-rearingofinsectsforpestmanagementChallengessynergiesandadvancesfromevolutionaryphysiologyCrop Protection3887ndash94httpsdoiorg101016jcropro201203023

SouleM (1967)Pheneticsofnaturalpopulations IPhenetic relation-ships of insular populations of the side-blotched lizard Evolution21(3)584ndash591httpsdoiorg1023072406618

StacconiMVRBuffingtonMDaaneKMDaltonDTGrassiAKacarGhellipAnforaG (2015)Host stagepreferenceefficacy

andfecundityofparasitoidsattackingDrosophila suzukii in newly in-vadedareasBiological Control8428ndash35httpsdoiorg101016jbiocontrol201502003

StacconiMVRGrassiADaltonDMillerBOuantarMLoniAhellipAnforaG(2013)FirstfieldrecordsofPachycrepoideus vindemiae as aparasitoidofDrosophila suzukii inEuropeanandOregon smallfruitproductionareasEntomologia1(1)3httpsdoiorg104081entomologia2013e3

StewartAOhkuraMampMcleanK(2010)Targetedscreeningformi-crobialbioactivityInSMZydenbosampTAJackson(Eds)Microbial products Exploiting microbial diversity for sustainable plant production (pp11ndash19)AucklandNewZealandNewZealandPlantProtectionSocietyInc

Stiling P amp Cornelissen T (2005)Whatmakes a successful biocon-trol agent A meta-analysis of biological control agent perfor-mance Biological Control34(3)236ndash246httpsdoiorg101016jbiocontrol200502017

TeixeiraLFerreiraAacuteampAshburnerM(2008)ThebacterialsymbiontWolbachia induces resistance toRNAviral infections inDrosophila melanogaster PLoS Biology6(12)e1000002

ThomasMBampBlanfordS(2003)Thermalbiologyininsect-parasiteinteractionsTrends in Ecology amp Evolution18(7)344ndash350httpsdoiorg101016S0169-5347(03)00069-7

TimmerenSVampIsaacsR(2013)ControlofspottedwingDrosophilaDrosophila suzukiibyspecific insecticidesandbyconventionalandorganic crop protection programs Crop Protection 54 126ndash133httpsdoiorgdoi101016jcropro201308003

TochenSDaltonDTWimanNHammCShearerPWampWaltonVM(2014)Temperature-relateddevelopmentandpopulationpa-rametersforDrosophila suzukii(dipteraDrosophilidae)oncherryandblueberry Environmental Entomology 43(2) 501ndash510 httpsdoiorg101603EN13200

Tochen S Woltz J Dalton D Lee J Wiman N amp Walton V(2016)HumidityaffectspopulationsofDrosophila suzukii (DipteraDrosophilidae) inblueberryJournal of Applied Entomology140(1ndash2)47ndash57httpsdoiorg101111jen12247

UenoHDeJongPampBrakefieldP(2004)Geneticbasisandfitnessconsequences of winglessness in the two-spot ladybird beetleAdalia bipunctata Heredity93(3)283ndash289httpsdoiorg101038sjhdy6800502

Vagravezquez-Salat N Salter B Smets G amp Houdebine L (2012) Thecurrent state of GMO governance Are we ready for GM ani-mals Biotechnology Advances 30(6) 1336ndash1343 httpsdoiorg101016jbiotechadv201202006

Wajnberg E (2004) Measuring genetic variation in natural ene-mies used for biological controlWhy and how In L E Ehler RSforza amp T Mateille (Eds) Genetics evolution and biological con-trol (pp 19ndash37) Wallingford UK CAB International httpsdoiorg10107997808519973530000

WajnbergEPrevostGampBouleacutetreauM(1985)Geneticandepigen-etic variation in Drosophilalarvaesuitabilitytoahymenopterousen-doparasitoidBioControl30(2)187ndash191

WalshDBBoldaMPGoodhueREDrevesAJLeeJBruckDJhellipZalomFG(2011)Drosophila suzukii (dipteraDrosophilidae)Invasivepestof ripening soft fruit expanding its geographic rangeanddamagepotentialJournal of Integrated Pest Management2G1ndashG7httpsdoiorg101603IPM10010

WangXGKacarGBiondiAampDaaneKM(2016a)Life-historyandhostpreferenceofTrichopria DrosophilaeapupalparasitoidofspottedwingDrosophila Journal of Integrated Pest Management61387ndash397

WangXGKacarGBiondiAampDaaneKM(2016b)Foragingef-ficiency andoutcomesof interactionsof twopupal parasitoids at-tackingthe invasivespottedwingDrosophila Biological Control9664ndash71httpsdoiorg101016jbiocontrol201602004


WangXGampMessingRH(2004a)TheectoparasiticpupalparasitoidPachycrepoideus vindemmiae (Hymenoptera Pteromalidae) attacksotherprimarytephritidfruitflyparasitoidsHostexpansionandpo-tentialnon-targetimpactBiological Control31(2)227ndash236httpsdoiorg101016jbiocontrol200404019

WangXGampMessingRH(2004b)Twodifferentlife-historystrat-egies determine the competitive outcomebetweenDirhinus giffar-dii (chalcididae) and Pachycrepoideus vindemmiae (pteromalidae)ectoparasitoidsof cyclorrhaphousdipteraBulletin of Entomological Research94(05)473ndash480

WangJNakanoKOhashiSTakizawaKampHeJ(2010)Comparisonofdifferentmodesofvisibleandnear-infraredspectroscopyforde-tectinginternalinsectinfestationinjujubesJournal of Food Engineering101(1)78ndash84httpsdoiorg101016jjfoodeng201006011

WebberBLRaghuSampEdwardsOR (2015)Opinion IsCRISPR-based gene drive a biocontrol silver bullet or global conservationthreat Proceedings of the National Academy of Sciences of the United States of America 112(34) 10565ndash10567 httpsdoiorg101073pnas1514258112

Werren JHBaldo LampClarkME (2008)WolbachiaMasterma-nipulatorsofinvertebratebiologyNature Reviews Microbiology6(10)741httpsdoiorg101038nrmicro1969

WertheimBVetLampDickeM(2003)Increasedriskofparasitismasecological costsofusingaggregationpheromonesLaboratoryandfieldstudyofDrosophila-Leptopilina interaction Oikos100(2)269ndash282httpsdoiorg101034j1600-0706200311579x

WeselohRM(1986)Artificialselectionforhostsuitabilityanddevelop-mentlengthofthegypsymoth(LepidopteraLymantriidae)parasiteCotesiamelanoscela(HymenopteraBraconidae)Journal of Economic Entomology79(5)1212ndash1216httpsdoiorg101093jee7951212

WhiteJWAndrade-SanchezPGoreMABronsonKFCoffeltTAConleyMMhellipHunsakerDJ(2012)Field-basedphenom-ics forplantgenetics researchField Crops Research133101ndash112httpsdoiorg101016jfcr201204003

Xie J Butler S SanchezGampMateosM (2014)Male killing spiro-plasmaprotectsDrosophila melanogasteragainsttwoparasitoidwaspsHeredity112(4)399ndash408httpsdoiorg101038hdy2013118

XuYLuYXieCGaoSWanJampPrasannaBM (2012)Whole-genome strategies for marker-assisted plant breeding Molecular Breeding29(4)833ndash854httpsdoiorg101007s11032-012-9699-6

Young Y Buckiewicz N amp Long T A (2018) Nutritional geome-try and fitness consequences in Drosophila suzukii the Spotted-WingDrosophilaEcology and Evolution8 2842ndash2851 httpsdoiorg101002ece33849

van de Zande L Ferber S de Haan A Beukeboom L W vanHeerwaarden J amp Pannebakker B A (2014) Development ofa Nasonia vitripennis outbred laboratory population for geneticanalysis Molecular Ecology Resources 14 578ndash587 httpsdoiorg1011111755-099812201

ZhaoHZengLXuYLuYampLiangG(2013)Effectsofhostageon the parasitism of Pachycrepoideus vindemmiae (HymenopteraPteromalidae) an ectoparasitic pupal parasitoid of Bactrocera cu-curbitae (DipteraTephritidae)Florida Entomologist96(2)451ndash457httpsdoiorg1016530240960209

ZhouZZangYYanMampLuoX(2014)Quantityestimationmodel-ingofthericeplant-hopperinfestationareaonricestemsbasedona2-dimensionalwaveletpackettransformandcornerdetectionalgo-rithm Computers and Electronics in Agriculture101102ndash109httpsdoiorg101016jcompag201312013

ZhuCLiJWangHZhangMampHuH (2017)Demographicpo-tentialofthepupalparasitoidTrichopria Drosophilae(HymenopteraDiapriidae) reared on Drosophila suzukii (Diptera Drosophilidae)Journal of Asia- Pacific Entomology 20(3) 747ndash751 httpsdoiorg101016jaspen201704008

How to cite this articleKruitwagenABeukeboomLWWertheimBOptimizationofnativebiocontrolagentswithparasitoidsoftheinvasivepestDrosophila suzukiiasanexampleEvol Appl 2018111473ndash1497 httpsdoiorg101111eva12648

Evolutionary Applications 2018111473ndash1497 emsp|emsp1473wileyonlinelibrarycomjournaleva

Received30October2017emsp |emsp Revised3May2018emsp |emsp Accepted8May2018DOI 101111eva12648

R E V I E W S A N D S Y N T H E S E S

Optimization of native biocontrol agents with parasitoids of the invasive pest Drosophila suzukii as an example

Astrid Kruitwagen emsp|emspLeo W Beukeboomemsp|emspBregje Wertheim

ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicensewhichpermitsusedistributionandreproductioninanymediumprovidedtheoriginalworkisproperlycitedcopy2018TheAuthorsEvolutionary ApplicationspublishedbyJohnWileyampSonsLtd

GroningenInstituteforEvolutionaryLifeSciencesUniversityofGroningenGroningenTheNetherlands

CorrespondenceAstridKruitwagenGroningenInstituteforEvolutionaryLifeSciencesUniversityofGroningenGroningenTheNetherlandsEmailajkruitwagenrugnl

Funding informationNederlandseOrganisatievoorWetenschappelijkOnderzoekGrantAwardNumberALWGR20156

AbstractThedevelopmentofbiological controlmethods for exotic invasivepest specieshas becomemore challenging during the last decade Compared to indigenousnaturalenemiesspeciesfromthepestareaoforiginareoftenmoreefficientdueto their long coevolutionary history with the pest The import of these well-adaptedexoticspecieshoweverhasbecomerestrictedundertheNagoyaProtocolonAccessandBenefitSharingreducingthenumberofavailablebiocontrolcandi-datesFindingnewagentsandwaystoimproveimportanttraitsforcontrolagents(ldquobiocontroltraitsrdquo)isthereforeofcrucialimportanceHerewedemonstratethepotentialofasurprisinglyunder-ratedmethodforimprovementofbiocontroltheexploitationofintraspecificvariationinbiocontroltraitsforexamplebyselectivebreedingWe propose a four-step approach to investigate the potential of thismethodinvestigationoftheamountof(a)inter-and(b)intraspecificvariationforbiocontroltraits(c)determinationoftheenvironmentalandgeneticfactorsshap-ingthisvariationand(d)exploitationofthisvariationinbreedingprogramsWeillustrate this approachwith a case studyonparasitoids ofDrosophila suzukii ahighly invasivepestspecies inEuropeandNorthAmericaWereviewallknownparasitoidsofD suzukiiandfindlargevariationamongandwithinspeciesintheirabilitytokillthisflyWethenconsiderwhichgeneticandenvironmentalfactorsshapetheinteractionbetweenD suzukiianditsparasitoidstoexplainthisvaria-tion Insight into thecausesofvariation informsusonhowand towhatextentcandidateagentscanbe improvedMoreover itaids inpredictingtheeffective-nessoftheagentuponreleaseandprovidesinsightintotheselectiveforcesthatare limiting the adaptation of indigenous species to the new pestWe use thisknowledge to give future research directions for the development of selectivebreedingmethodsforbiocontrolagents

K E Y W O R D S

artificialselectionbiologicalcontrolagentcoevolutionexoticspecieshostndashparasiteinteractionspestmanagementphenomicsspottedwingDrosophila



















































(Continues)








Environmentalsafety






















































Pupalparasitoids



Cancinoetal(2015)




Mediuminfestation







Milleretal(2015)




Wangetal(2016b)


Stacconietal(2013)


Milleretal(2015)



Stacconietal(2015)



Cancinoetal(2015)



Chabertetal(2012)





(Continues)








Wangetal(2016b)


Knolletal(2017)







Cancinoetal(2015)



Larvalparasitoids


Chabertetal(2012)










Verylowinadequacy



Mediuminadequacy







(Continues)









Mediuminadequacy


Milleretal(2015)



Milleretal(2015)




Stacconietal(2015)


Mediuminadequacy






Knolletal(2017)


Mediuminadequacy



Cancinoetal(2015)




Highinfestation





Mediuminadequacy



(Continues)












Mediuminadequacy



Mediuminadequacy




Mediuminadequacy



Mediuminadequacy









Mediuminadequacy









Pupalparasitoids




Larvalparasitoids



Mitsuietal(2007)




Nomanoetal(2015)



Chabertetal(2012)



Yes Daaneetal(2016)



Daaneetal(2016)



Mitsuietal(2007)



Nomanoetal(2015)



Nomanoetal(2015)



Nomanoetal(2015)







Mitsuietal(2007)





Kasuyaetal(2013)


Nomanoetal(2015)


(Continues)
















Kasuyaetal(2013)















































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S






















































































































































































































































(Continues)








Environmentalsafety






















































Pupalparasitoids



Cancinoetal(2015)




Mediuminfestation







Milleretal(2015)




Wangetal(2016b)


Stacconietal(2013)


Milleretal(2015)



Stacconietal(2015)



Cancinoetal(2015)



Chabertetal(2012)





(Continues)








Wangetal(2016b)


Knolletal(2017)







Cancinoetal(2015)



Larvalparasitoids


Chabertetal(2012)










Verylowinadequacy



Mediuminadequacy







(Continues)









Mediuminadequacy


Milleretal(2015)



Milleretal(2015)




Stacconietal(2015)


Mediuminadequacy






Knolletal(2017)


Mediuminadequacy



Cancinoetal(2015)




Highinfestation





Mediuminadequacy



(Continues)












Mediuminadequacy



Mediuminadequacy




Mediuminadequacy



Mediuminadequacy









Mediuminadequacy









Pupalparasitoids




Larvalparasitoids



Mitsuietal(2007)




Nomanoetal(2015)



Chabertetal(2012)



Yes Daaneetal(2016)



Daaneetal(2016)



Mitsuietal(2007)



Nomanoetal(2015)



Nomanoetal(2015)



Nomanoetal(2015)







Mitsuietal(2007)





Kasuyaetal(2013)


Nomanoetal(2015)


(Continues)
















Kasuyaetal(2013)















































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S















































































































































































































































(Continues)








Environmentalsafety






















































Pupalparasitoids



Cancinoetal(2015)




Mediuminfestation







Milleretal(2015)




Wangetal(2016b)


Stacconietal(2013)


Milleretal(2015)



Stacconietal(2015)



Cancinoetal(2015)



Chabertetal(2012)





(Continues)








Wangetal(2016b)


Knolletal(2017)







Cancinoetal(2015)



Larvalparasitoids


Chabertetal(2012)










Verylowinadequacy



Mediuminadequacy







(Continues)









Mediuminadequacy


Milleretal(2015)



Milleretal(2015)




Stacconietal(2015)


Mediuminadequacy






Knolletal(2017)


Mediuminadequacy



Cancinoetal(2015)




Highinfestation





Mediuminadequacy



(Continues)












Mediuminadequacy



Mediuminadequacy




Mediuminadequacy



Mediuminadequacy









Mediuminadequacy









Pupalparasitoids




Larvalparasitoids



Mitsuietal(2007)




Nomanoetal(2015)



Chabertetal(2012)



Yes Daaneetal(2016)



Daaneetal(2016)



Mitsuietal(2007)



Nomanoetal(2015)



Nomanoetal(2015)



Nomanoetal(2015)







Mitsuietal(2007)





Kasuyaetal(2013)


Nomanoetal(2015)


(Continues)
















Kasuyaetal(2013)















































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S







































































































































































































































(Continues)








Environmentalsafety






















































Pupalparasitoids



Cancinoetal(2015)




Mediuminfestation







Milleretal(2015)




Wangetal(2016b)


Stacconietal(2013)


Milleretal(2015)



Stacconietal(2015)



Cancinoetal(2015)



Chabertetal(2012)





(Continues)








Wangetal(2016b)


Knolletal(2017)







Cancinoetal(2015)



Larvalparasitoids


Chabertetal(2012)










Verylowinadequacy



Mediuminadequacy







(Continues)









Mediuminadequacy


Milleretal(2015)



Milleretal(2015)




Stacconietal(2015)


Mediuminadequacy






Knolletal(2017)


Mediuminadequacy



Cancinoetal(2015)




Highinfestation





Mediuminadequacy



(Continues)












Mediuminadequacy



Mediuminadequacy




Mediuminadequacy



Mediuminadequacy









Mediuminadequacy









Pupalparasitoids




Larvalparasitoids



Mitsuietal(2007)




Nomanoetal(2015)



Chabertetal(2012)



Yes Daaneetal(2016)



Daaneetal(2016)



Mitsuietal(2007)



Nomanoetal(2015)



Nomanoetal(2015)



Nomanoetal(2015)







Mitsuietal(2007)





Kasuyaetal(2013)


Nomanoetal(2015)


(Continues)
















Kasuyaetal(2013)















































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S











































































































































































































Environmentalsafety






















































Pupalparasitoids



Cancinoetal(2015)




Mediuminfestation







Milleretal(2015)




Wangetal(2016b)


Stacconietal(2013)


Milleretal(2015)



Stacconietal(2015)



Cancinoetal(2015)



Chabertetal(2012)





(Continues)








Wangetal(2016b)


Knolletal(2017)







Cancinoetal(2015)



Larvalparasitoids


Chabertetal(2012)










Verylowinadequacy



Mediuminadequacy







(Continues)









Mediuminadequacy


Milleretal(2015)



Milleretal(2015)




Stacconietal(2015)


Mediuminadequacy






Knolletal(2017)


Mediuminadequacy



Cancinoetal(2015)




Highinfestation





Mediuminadequacy



(Continues)












Mediuminadequacy



Mediuminadequacy




Mediuminadequacy



Mediuminadequacy









Mediuminadequacy









Pupalparasitoids




Larvalparasitoids



Mitsuietal(2007)




Nomanoetal(2015)



Chabertetal(2012)



Yes Daaneetal(2016)



Daaneetal(2016)



Mitsuietal(2007)



Nomanoetal(2015)



Nomanoetal(2015)



Nomanoetal(2015)







Mitsuietal(2007)





Kasuyaetal(2013)


Nomanoetal(2015)


(Continues)
















Kasuyaetal(2013)















































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S
































































































































































































































Pupalparasitoids



Cancinoetal(2015)




Mediuminfestation







Milleretal(2015)




Wangetal(2016b)


Stacconietal(2013)


Milleretal(2015)



Stacconietal(2015)



Cancinoetal(2015)



Chabertetal(2012)





(Continues)








Wangetal(2016b)


Knolletal(2017)







Cancinoetal(2015)



Larvalparasitoids


Chabertetal(2012)










Verylowinadequacy



Mediuminadequacy







(Continues)









Mediuminadequacy


Milleretal(2015)



Milleretal(2015)




Stacconietal(2015)


Mediuminadequacy






Knolletal(2017)


Mediuminadequacy



Cancinoetal(2015)




Highinfestation





Mediuminadequacy



(Continues)












Mediuminadequacy



Mediuminadequacy




Mediuminadequacy



Mediuminadequacy









Mediuminadequacy









Pupalparasitoids




Larvalparasitoids



Mitsuietal(2007)




Nomanoetal(2015)



Chabertetal(2012)



Yes Daaneetal(2016)



Daaneetal(2016)



Mitsuietal(2007)



Nomanoetal(2015)



Nomanoetal(2015)



Nomanoetal(2015)







Mitsuietal(2007)





Kasuyaetal(2013)


Nomanoetal(2015)


(Continues)
















Kasuyaetal(2013)















































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S



























































































































































































































Pupalparasitoids



Cancinoetal(2015)




Mediuminfestation







Milleretal(2015)




Wangetal(2016b)


Stacconietal(2013)


Milleretal(2015)



Stacconietal(2015)



Cancinoetal(2015)



Chabertetal(2012)





(Continues)








Wangetal(2016b)


Knolletal(2017)







Cancinoetal(2015)



Larvalparasitoids


Chabertetal(2012)










Verylowinadequacy



Mediuminadequacy







(Continues)









Mediuminadequacy


Milleretal(2015)



Milleretal(2015)




Stacconietal(2015)


Mediuminadequacy






Knolletal(2017)


Mediuminadequacy



Cancinoetal(2015)




Highinfestation





Mediuminadequacy



(Continues)












Mediuminadequacy



Mediuminadequacy




Mediuminadequacy



Mediuminadequacy









Mediuminadequacy









Pupalparasitoids




Larvalparasitoids



Mitsuietal(2007)




Nomanoetal(2015)



Chabertetal(2012)



Yes Daaneetal(2016)



Daaneetal(2016)



Mitsuietal(2007)



Nomanoetal(2015)



Nomanoetal(2015)



Nomanoetal(2015)







Mitsuietal(2007)





Kasuyaetal(2013)


Nomanoetal(2015)


(Continues)
















Kasuyaetal(2013)















































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S





















































































































































































































Pupalparasitoids



Cancinoetal(2015)




Mediuminfestation







Milleretal(2015)




Wangetal(2016b)


Stacconietal(2013)


Milleretal(2015)



Stacconietal(2015)



Cancinoetal(2015)



Chabertetal(2012)





(Continues)








Wangetal(2016b)


Knolletal(2017)







Cancinoetal(2015)



Larvalparasitoids


Chabertetal(2012)










Verylowinadequacy



Mediuminadequacy







(Continues)









Mediuminadequacy


Milleretal(2015)



Milleretal(2015)




Stacconietal(2015)


Mediuminadequacy






Knolletal(2017)


Mediuminadequacy



Cancinoetal(2015)




Highinfestation





Mediuminadequacy



(Continues)












Mediuminadequacy



Mediuminadequacy




Mediuminadequacy



Mediuminadequacy









Mediuminadequacy









Pupalparasitoids




Larvalparasitoids



Mitsuietal(2007)




Nomanoetal(2015)



Chabertetal(2012)



Yes Daaneetal(2016)



Daaneetal(2016)



Mitsuietal(2007)



Nomanoetal(2015)



Nomanoetal(2015)



Nomanoetal(2015)







Mitsuietal(2007)





Kasuyaetal(2013)


Nomanoetal(2015)


(Continues)
















Kasuyaetal(2013)















































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S










































































































































































































Pupalparasitoids



Cancinoetal(2015)




Mediuminfestation







Milleretal(2015)




Wangetal(2016b)


Stacconietal(2013)


Milleretal(2015)



Stacconietal(2015)



Cancinoetal(2015)



Chabertetal(2012)





(Continues)








Wangetal(2016b)


Knolletal(2017)







Cancinoetal(2015)



Larvalparasitoids


Chabertetal(2012)










Verylowinadequacy



Mediuminadequacy







(Continues)









Mediuminadequacy


Milleretal(2015)



Milleretal(2015)




Stacconietal(2015)


Mediuminadequacy






Knolletal(2017)


Mediuminadequacy



Cancinoetal(2015)




Highinfestation





Mediuminadequacy



(Continues)












Mediuminadequacy



Mediuminadequacy




Mediuminadequacy



Mediuminadequacy









Mediuminadequacy









Pupalparasitoids




Larvalparasitoids



Mitsuietal(2007)




Nomanoetal(2015)



Chabertetal(2012)



Yes Daaneetal(2016)



Daaneetal(2016)



Mitsuietal(2007)



Nomanoetal(2015)



Nomanoetal(2015)



Nomanoetal(2015)







Mitsuietal(2007)





Kasuyaetal(2013)


Nomanoetal(2015)


(Continues)
















Kasuyaetal(2013)















































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S











































































































































































































Wangetal(2016b)


Knolletal(2017)







Cancinoetal(2015)



Larvalparasitoids


Chabertetal(2012)










Verylowinadequacy



Mediuminadequacy







(Continues)









Mediuminadequacy


Milleretal(2015)



Milleretal(2015)




Stacconietal(2015)


Mediuminadequacy






Knolletal(2017)


Mediuminadequacy



Cancinoetal(2015)




Highinfestation





Mediuminadequacy



(Continues)












Mediuminadequacy



Mediuminadequacy




Mediuminadequacy



Mediuminadequacy









Mediuminadequacy









Pupalparasitoids




Larvalparasitoids



Mitsuietal(2007)




Nomanoetal(2015)



Chabertetal(2012)



Yes Daaneetal(2016)



Daaneetal(2016)



Mitsuietal(2007)



Nomanoetal(2015)



Nomanoetal(2015)



Nomanoetal(2015)







Mitsuietal(2007)





Kasuyaetal(2013)


Nomanoetal(2015)


(Continues)
















Kasuyaetal(2013)















































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S












































































































































































































Mediuminadequacy


Milleretal(2015)



Milleretal(2015)




Stacconietal(2015)


Mediuminadequacy






Knolletal(2017)


Mediuminadequacy



Cancinoetal(2015)




Highinfestation





Mediuminadequacy



(Continues)












Mediuminadequacy



Mediuminadequacy




Mediuminadequacy



Mediuminadequacy









Mediuminadequacy









Pupalparasitoids




Larvalparasitoids



Mitsuietal(2007)




Nomanoetal(2015)



Chabertetal(2012)



Yes Daaneetal(2016)



Daaneetal(2016)



Mitsuietal(2007)



Nomanoetal(2015)



Nomanoetal(2015)



Nomanoetal(2015)







Mitsuietal(2007)





Kasuyaetal(2013)


Nomanoetal(2015)


(Continues)
















Kasuyaetal(2013)















































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S















































































































































































































Mediuminadequacy



Mediuminadequacy




Mediuminadequacy



Mediuminadequacy









Mediuminadequacy









Pupalparasitoids




Larvalparasitoids



Mitsuietal(2007)




Nomanoetal(2015)



Chabertetal(2012)



Yes Daaneetal(2016)



Daaneetal(2016)



Mitsuietal(2007)



Nomanoetal(2015)



Nomanoetal(2015)



Nomanoetal(2015)







Mitsuietal(2007)





Kasuyaetal(2013)


Nomanoetal(2015)


(Continues)
















Kasuyaetal(2013)















































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S









































































































































































































Pupalparasitoids




Larvalparasitoids



Mitsuietal(2007)




Nomanoetal(2015)



Chabertetal(2012)



Yes Daaneetal(2016)



Daaneetal(2016)



Mitsuietal(2007)



Nomanoetal(2015)



Nomanoetal(2015)



Nomanoetal(2015)







Mitsuietal(2007)





Kasuyaetal(2013)


Nomanoetal(2015)


(Continues)
















Kasuyaetal(2013)















































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S



















































































































































































































Kasuyaetal(2013)















































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S











































































































































































































































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S
































































































































































































































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S























































































































































































































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S
















































































































































































































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S









































































































































































































ACKNOWLEDG EMENTS



Nonedeclared

DATA ARCHIVING


ORCID


R E FE R E N C E S



































































































































































































































































































































































































































































































































































































































































































































































































































Documents

Optimization of native biocontrol agents, with parasitoids ... · Optimization of native biocontrol agents, with parasitoids of the invasive pest Drosophila suzukii as an example