Parasitism rate of Myzus persicae (Sulzer) by Diaeretiella rapae (McIntosh) in the presence of an alternative, resistant host

REVISTA

BRASILEIRA

DE

Entomologia

w w w . r b e n t o m o l o g i a . c o m

Biological

Control

and

Crop

Protection

Parasitism

rate

of

Myzus

persicae

(Sulzer)

by

Diaeretiella

rapae

(McIntosh)

in

the

presence

of

an

alternative,

resistant

host

Samira

Evangelista

Ferreira

_,

_Marcus

_Vinicius

_Sampaio

_,

_Reinaldo

_Silva

_de

_Oliveira

_,

Heraldo

Luís

de

Vasconcelos

a_{UniversidadeFederaldeUberlândia,InstitutodeCiênciasAgrárias,Uberlândia,MG,Brazil} b_{InstitutoFederaldeEducac¸ão,CiênciaeTecnologiadoTriânguloMineiro,Uberlândia,MG,Brazil} c_{UniversidadeFederaldeUberlândia,InstitutodeBiologia,Uberlândia,MG,Brazil}

a

r

t

i

c

l

e

i

n

f

o

Articlehistory: Received19March2017 Accepted18October2017 Availableonline13November2017 AssociateEditor:LucasKaminski Keywords:

Aphid Aphididae Aphidiinae

Competitionmediatedbyparasitoid Indirectresistance

a

b

s

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r

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TheaphidsLipaphispseudobrassicae(Davis)andMyzuspersicae(Sulzer) (Hemiptera:Aphididae)are importantBrassicaceaepests,occurringworldwideandcausingsignificantdamagetocrops. Interspe-cificvariationsintheresistancetonaturalenemiescanpotentiallyimpacttheinteractionamongaphid populations.Hereweevaluatedthehypothesisofassociationalresistancebydeterminingifthepresence ofresistantaphids(L.pseudobrassicae)reducestherateofparasitismbyDiaeretiellarapae(McIntosh)on non-resistantaphids(M.persicae).Theexperimentwasconductedusingcollardgreenplantsinfested withM.persicaeandL.pseudobrassicaeeitherresistantorsusceptibletoD.rapae.Thepercentageof par-asitismbyD.rapaewasgreateronL.pseudobrassicaeinthesusceptiblethanintheresistanttreatment, butparasitismratesonM.persicaedidnotdifferbetweenthetreatments.Therewasnodifferencein averagegrowthratebetweenM.persicaeandsusceptibleL.pseudobrassicaepopulations,butresistantL. pseudobrassicaehadgreatergrowthratethanM.persicae.Theseresultssuggestthatoverashortperiod oftimethepresenceofresistantL.pseudobrassicaedoesnotaffecttherateofparasitismbyD.rapaeon M.persicae.

©2017SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction

Interactions involving a shared and limited resource may resultinexploitativecompetition,whenindividualsuseavailable resourcesandthusdeprivecompetitorsoftheseresources,orin interferencecompetition,in whichindividualsinflictdamageto eachotherthroughdirectcontact,thusdeprivingcompetitorsof accesstotheresource(Priceetal.,2011;Schoener,1983).

Whentwospeciesdonotcompeteforaresource,their popu-lationcanbechangedbyasharedpredator,parasite,orpathogen –aphenomenonknownas“competitionmediatedbyparasitesor naturalenemies”or“apparentcompetition”.Thistypeof compe-titionwasdefinedasareductioninpopulationofaspecieswhen thepopulationofasecondspeciesincreasesthroughitsinteraction withathirdspeciesofahighertrophiclevel(ChanetonandBonsall,

2000;Holt,1977;HoltandLawton,1994).Competitionmediated

byparasitesandnaturalenemiesareverycommoninnatureand

∗ Correspondingauthor.

E-mail:mvsampaio@ufu.br(M.V.Sampaio).

canbeconsideredoneofthemaintypesofinteractioninecological systems(Bhattaraietal.,2017;KaplanandDenno,2007;Priceetal.,

1986).

Thereareseveralcaseswhere theparasitoidspeciesare the samefortwohosts,buttheimpactofthisnaturalenemyisdifferent

ineachone(Frostetal.,2016;Holmes,1982;RiceandWestoby,

1982).For instance,ahostspecieswithalargepopulationmay sustaina largeparasitoidpopulationand, thus,indirectly affect theparasitismrateofasecondhostspecies(Asgarietal.,1998;

Blumberg,1997;Priceetal.,1986;vanVeenetal.,2006).

Ontheotherhand,thetheoryofoptimalforagingpredictsthat parasitoidsshouldovipositpreferentiallyinhostsofbetter qual-ityforthedevelopmentoftheiroffspring(Emlen,1966;Fellowes

etal.,2007;MacArthurandPianka,1966;MacArthurandWilson,

1967).However,someaphidparasitoids(Braconidae:Aphidiinae) maynotbeabletorecognizethebesthosts(Henryetal.,2005; Sam-paioetal.,2008)ormayevenovipositinhostsunsuitableforthe developmentoftheiroffspring(Sampaioetal.,2008;Star ´y,1989). Asaresult,eggsarelikelytobedepositedinboth,resistantand susceptiblehosts(Ferrarietal.,2001;Oliveretal.,2003;Oliveira

etal.,2013).

https://doi.org/10.1016/j.rbe.2017.10.003

0085-5626/©2017SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http:// creativecommons.org/licenses/by-nc-nd/4.0/).

Someparasitoidspeciesareabletorecognizetheresistanthosts

(Oliveretal.,2012).Diaeretiellarapae(McIntosh)(Hymenoptera:

Braconidae: Aphidiinae), however, deposit its eggs in resistant hostsatthesamefrequencyasitdoesinsusceptibleones, indi-catingthatthisparasitoidspeciescannotrecognizetheresistant

ones(Oliveiraetal.,2013).Thisway,thepresenceofaresistant

hostcanpotentiallyreducetheparasitoidpopulation,thus favor-ingthesusceptibleaphidcompetitorthroughindirectresistance

(Meisneretal.,2007),whichmayleadtoseriousconsequencesfor

thebiologicalcontrolofaphidpeststhatsharethesameparasitoid. TheaphidsLipaphispseudobrassicae(Davis)andMyzuspersicae (Sulzer)(Hemiptera:Aphididae)areimportantBrassicaceaepests, occurring worldwide and causing significant damage to crops

(BlackmanandEastop,2007).Studiesrevealthatthepopulationof

L.pseudobrassicaeinUberlândia,southeasternBrazil,has individ-ualsresistanttoD.rapae(Oliveiraetal.,2013),whichisthemain parasitoidpresentinBrassicaintheregion(Sampaioetal.,2017).

ThecauseoftheresistanceofL.pseudobrassicaetoD.rapaeisstill underinvestigation,butresistantindividualsaremoreabundant thansusceptibleonesinUberlandia’spopulation,whichmakesD. rapaeineffectiveincontrollingL.pseudobrassicae(Oliveiraetal.,

2013;Sampaioet al.,2017).In contrast,theparasitoidD. rapae

hasbeenfoundasthemainnaturalenemyofL.pseudobrassicaein regionswheretheaphidissusceptible,withhighratesofparasitism inthelaboratory(Silvaetal.,2011)andinfieldandgreenhouse conditions(DeshandChand,1998;Jeonetal.,2005).

HereweevaluatedifresistantL.pseudobrassicaepopulationscan changetheparasitismrateofasecondhostspecies,M.persicae, throughindirectresistancetotheirsharedparasitoid(D.rapae).

Materialandmethods

Hostplantmaterial

Collardgreenseedlings(Brassicaoleraceavar.acephalaL., cul-tivarManteigadaGeorgia)weregrowninagreenhouseinplastic potscontainingthecommercialorganicsubstrateBioplant®.Plants usedforrearingtheaphidsandparasitoidswerekeptin3-Lplastic pots(15cmtalland20cmdiameter),whereasplantsusedforthe experimentwerekeptin14.5Lplasticpots(27cmtalland30cm diameter).Leavesweredetachedfromplantsandtakentothe lab-oratorytoobtainleafdiscs,whichwerethenplacedonPetridishes withagarsolutiontoreartheaphids.Thirtyfivedaysoldseedlings, withsixexpandedleaves,werecoveredwithananti-aphidcagefor theexperiment.Theexperimentwasconductedinagreenhouse fromNovember10toDecember1,2012,withanaverage temper-atureof28◦C,andtheminimumandmaximumaveragesof19◦C and37◦C,respectively.

Aphidrearing

TwoclonesofL.pseudobrassicae,B3(resistant)andB6 (suscep-tible),werecollectedincollardgreenplants,selectedandrearing forfive monthsinlaboratoryprior totheexperiment (Ferreira, 2013).Aphidsweregrownoncollardgreenleafdisksplacedon 1%agar/watersolutioninPetridishes(10cmdiameter).ThePetri dishesweremaintainedinaclimatecontrolledchamber(23±1◦C, 12hphotoperiod,50–55%humidity)andaphidsweretransferred tonewPetri dishes containingfresh foliage everyfourdays to ensureagoodqualityofthehostplant.

ToconfirmtheresistanceofthecloneB3incomparisonwith thesusceptibleB6,60secondinstarnymphsofL.pseudobrassicae ofeachclonewereplacedindividuallyinPetridisheswithacollard greenleafdisk.AmatedD.rapaefemalewasreleasedonevery PetridishuntilitovipositedonsixL.pseudobrassicaenymphs.A

totaloftenD.rapaefemaleswereusedtoparasitize60aphidsof eachclone.Subsequently,thesenymphswerekeptinaclimatic controlledchamberandobserveddaily.NoneoftheB3nymphs parasitizedbyD.rapaemummified,indicatingthatallindividuals wereresistant.Incontrast,40outofthe60parasitizedB6nymphs weremummified,confirmingthesusceptibilityofB6.

TheresistantcloneB3wasthenrearedinthelaboratoryforfive monthsandusedtoobtainsusceptibleindividualswithinits pop-ulation.Resistancetoparasitoidsin aphids,associated withthe presenceof secondarysymbionts, maybelostin some individ-ualseven iftheyareclones froma singleresistantfemale.This happensbecausesecondarysymbiontsassociatedwithaphidsare transmittedviamother’sovariestoheroffspring;however,this transmissionisnotperfect,whichresultsinresistancelossbysome individuals(ChenandPurcell,1997;Fukatsuetal.,2000;Oliver

etal.,2010;Dykstraet al.,2014).Eventhoughthecauseofthe

resistanceofL.pseudobrassicaetoD.rapaeisstillunknown,itwas possibletoobtainsusceptibleindividuals fromthecloneB3.To obtainsusceptibleindividuals,60nymphsofL.pseudobrassicaeof fourthinstarwereplacedindividuallyinPetridisheswitha col-lardgreenleafdiskandweresubjectedtoasingleovipositionof D.rapae(aspreviouslydescribedabove).ParasitizedL. pseudobras-sicaenymphsoffourthinstarareabletoreproducebeforedying, eventhesusceptibleones.Whentheparasitizedaphid(fouraphids) developedtoaregularmummy(normaldevelopmentofthe par-asitoid),heroffspringwasselectedandkeptforcolonyformation ofsusceptibleL.pseudobrassicae.Similarly,nymphsproducedby aparasitizedaphidwhoseparasitoiddidnotdevelop(49aphids) wereusedtoformcoloniesofresistantL.pseudobrassicae.After thetest,theB3offspringpopulationwasdividedbetweenthose thatlostresistanceandthosethatwerestillresistant.Thesetwo groupsweremaintainedinPetridishes(100mm)tobeusedinthe experiment.

Myzuspersicaeaphidswerecollectedincollardgreenplantsin agreenhouseoftheFederalUniversityofUberlândiaandreared inPetridishes,aspreviouslydescribed.Acolonyofapproximately 50individualsofvariousinstarswaskeptineachPetridish.Thirty PetridisheswithM.persicaewereusedintheexperimentandtwo dishesofthisaphidspecieswereusedforrearingD.rapae. Parasitoidrearing

The parasitoids were obtainedfrom Brevicoryne brassicae L. mummiescollectedinacommercialcollardgreencropatthe Fed-eralUniversity ofUberlândia. Themummies weretakentothe laboratory,placedindividuallyinEppendorftubesandkeptat23◦C andphotoperiodof12h.Onceparasitoidsemerged,theywerefed with50%honeyandwater.TwoPetridisheswithapproximately 50individualsofM.persicaewereusedforrearingD.rapae.One matedfemaleofD.rapaewasreleasedineachPetridishand main-tainedfor24hforoviposition.Afterthisperiod,thefemaleswere removedandparasitizedaphidskeptat23±1◦C,50–55%RHand photophaseof12h.Themummifiedaphidswereplacedin Eppen-dorftubes and,afteremergence,theparasitoidsfedand mated. Aftermatingwasobserved,maleswereremovedfromthetubes andthefemaleswereusedintheexperiment24hafteremergence. Experimentalprotocol

On thefirstdayof theexperiment, theaphidcolonieswere reducedto30individualsofseveralinstars.Toensureauniform stand,smallernymphs(1stand2ndinstar)wereremoved,leaving onlythelargestnymphs(3rdand4thinstars)andadults.Theleaf diskcontainingtheaphidswasremovedfromthePetridishand placedonaplantinsideananti-aphidcage.Twoleavesin oppo-sitepositionswereinfestedperplant.Eachplantreceivedaleaf

diskcontaining30resistantor30susceptibleL.pseudobrassicaeon aleafandaleafdiskwith30M.persicaeonanotherleaf,totaling 60aphidsperplant.Theleafdiscswiththeaphidswereplacedon fullydevelopedleaveslocatedinthemedianregionoftheplants becausethisisthepreferredleafpositionofbothaphidspeciesin fieldconditions(CividanesandSouza,2004;Sampaioetal.,2017). Theparasitoidswerereleasedinthecages48hafterinfestingthe plantswithaphids.

Parasitoid release took place as follows: two females were releasedpercage,oneinthethirdandanotherinthefourthday afterthebeginningoftheexperiment;bothwerereleasedlaterin theday(mildertemperatures)tofacilitatetheacclimationofthe parasitoid.Femaleswereleftinside thecagesuntiltheirnatural death.

Observationsweremadedaily,inordertomonitorthe devel-opmentoftheparasitoidsandthusdeterminethedurationofthe experiment.Thefirstmummieswereformedaftersevendaysand F1adultsemerged10daysafterthereleaseofthefirstD.rapae female.Thus,themummiesoftheF2generationofD.rapaebegan tobeformed17 daysafterthereleaseof thefirstfemale para-sitoid.Inthe21stdayafterthebeginningoftheexperiment(19 daysafterthereleaseofthefirstD.rapaefemale)plantsweretaken tothelaboratoryforevaluation,withsufficienttimetocomplete themummy’sformationoftheF2generation.Thenumberoflive andparasitizedaphidsfromthreefullydevelopedleaves(located inthemiddleregionofeachcollardgreen)werecountedusinga stereoscopicmicroscope.

Plantsfromtwocages,onefromeachtreatment,werelostdue tothehighaphidpopulationandthusthesewereremovedfrom theanalyses.Thus,intotal,therewereninereplicatesofresistant and11ofsusceptibleL.pseudobrassicae.

Dataanalysis

NormalityofresidualswasevaluatedbyShapiroWilk’stestand homogeneityofvariancebyLevene’stest,usingSPSS16.0software atfivepercentprobability.Theproportionofparasitizedindividuals wascalculatedastheratiobetweenthenumberofparasitized indi-vidualsandthetotalnumberofindividualsoneachplant21days afterthebeginningoftheexperiment.Therelativegrowthrateof eachaphidpopulationwascalculatedas(T1−T0)/T0,where:T1is thenumberofnon-parasitizedaphidspresentoneachplantafter 21daysandT0istheinitialnumberofindividualsplacedineach plant(30individuals).Wecomparedtheproportionofparasitism andthegrowthratesofM.persicaegrowinginplantswithor with-outresistantL.pseudobrassicaepopulationsusingthet-testfortwo independentsamples.Thesametestwasusedtocomparethe

resis-tantandsusceptiblepopulationsofL.pseudobrassicae.Inorderto meettheassumptionsofthet-test,weusedlogarithm(Zar,1984) andlogit(WartonandHui,2011)transformation,respectively,for dataonrelativegrowthratesandproportionofparasitism.Wealso comparedtheproportionofparasitismonM.persicaegrowingin plantswithorwithoutresistantL.pseudobrassicaeusingAnalysis ofCovarianceinwhichthenumberofparasitizedindividualsof L.pseudobrassicae(logtransformed)wastreatedasthecovariate. Growthrateofthetwoaphidspecieswascomparedusingpaired t-test,andseparatetestswereperformedforplantswiththe sus-ceptibleandresistantpopulationsofL.pseudobrassicae.Allanalyses wereconductedusingSystat10.2(SPSS,2000).

Results

ThepercentageofparasitismbyD.rapaeonM.persicaevaried morethan10-foldinourexperimentalplants(range=4.5–62.2%), and therewasnodifferencein thepercentageof parasitismon M.persicaebetweenplantswithsusceptibleorresistantL. pseu-dobrassicae(t=0.64,df=18,p=0.53)(Fig.1A).Thepercentageof parasitisminL.pseudobrassicaevariedfrom0.9to40%.Parasitism byD.rapaewasgreaterinthesusceptiblethanintheresistant pop-ulationofL.pseudobrassicae(t=4.67,df=18,p<0.001).Onaverage, parasitisminthesusceptiblepopulationwas3.5timesgreaterthan intheresistantone(mean±SD:susceptible=23.3±9.7%;resistant 6.6.±5.9%)(Fig.1B).

WhenweusedtheabsolutenumberofL.pseudobrassicae para-sitizedineachplantascovariateintheanalysiswedidnotdetect anydifferencesinparasitismonM.persicaebetweenplantswith susceptible or resistantL. pseudobrassicae (F1,16=1.63, p=0.22).

Furthermore, there was no effect of the covariate (F1,16=2.75,

p=0.12),i.e.thepercentageofparasitismonM.persicaeinagiven plantwasnotrelatedtothenumberofparasitizedL. pseudobrassi-caeinthatsameplant(Fig.2).

Therelative growthrate ofL.pseudobrassicae resistanttoD. rapaewasgreaterthanthatofM.persicae(pairedt-test,t=2.42, df=8,p<0.041)(Fig.3A),whereastherelativegrowthrateofL. pseudobrassicaesusceptibletoD.rapaewasnotdifferentfromthat ofM.persicae(pairedt-test,t=1.37,df=10,p=0.20)(Fig.3B).Also, whencomparingthegrowthrateofthesameaphidspeciesinplants withresistantorsusceptiblepopulationswefoundnodifferences forM.persicae(t=0.10,df=18,p=0.93)norforL.pseudobrassicae (t=1.41,df=18,p=0.18).

Fig.1. (A)ProportionofM.persicaeparasitizedbyD.rapaeinplantswithresistantorsusceptibleL.pseudobrassicaepopulations.(B)ProportionofresistantorsusceptibleL. pseudobrassicaeparasitizedbyD.rapaeinplantswithM.persicae.

Fig.2.RelationshipbetweentheabsolutenumberofL.pseudobrassicaeparasitized byD.rapaeandthepercentageofparasitismonM.persicae.Eachsymbolrepresents adifferentplant.

Discussion

TherewasnodifferenceinthepercentageofparasitismofM. persicaebyD.rapaebetweenplantswithsusceptibleorresistantL. pseudobrassicae.AnindirectresistanceofM.persicaewasexpected inthepresenceofresistantL.pseudobrassicaeduetothereduction inparasitoidpopulationbytwoeffects:areductioninparasitoid foragingcapabilityandgreaterparasitoidmortality.

Thepresenceofanon-susceptiblespeciescanreducethe forag-ingcapabilityoftheparasitoid.TheparasitoidAphidiuserviHaliday, forexample,ovipositsonTherioaphismaculata(Buckton),andthe presenceofthisaphiddecreasestheforagingcapacityofthe par-asitoidonasuitablehost,Acyrthosiphonpisum(Harris),reducing thepopulationoftheparasitoid(Meisneretal.,2007).AsD.rapae ovipositsatequalrateswhenM.persicaeandresistantL. pseudo-brassicaearesimultaneouslyexposed totheparasitoid(Oliveira etal.,2013),adecreaseintheparasitoidpopulationwasexpected, becauseresistantaphids preventthedevelopmentof the para-sitoideggs(Oliveiraetal.,2013).However,theparasitismofM. persicaewasnotchangedinthepresenceofresistantL. pseudobras-sicae.Therefore,wedidnotfindsupporttotheindirectresistance hypothesis.

Overshorttimeperiods,thepresenceofacompetitorofgreater potentialgrowthratecandecreasetheeffectoftheparasitoidonthe specieswiththelowergrowthpotentialrateduetothewiderange ofhosts(Gonzálesetal.,2002;HoltandKotler,1987).However,

thiseffecttendstobereversedovertime,sincealargerpopulation oftheparasitoidwillbeformed(HoltandKotler,1987).Infact,the presenceofanotherhostspeciesmayincreasethecontrolefficiency oftheparasitoidonbothaphidspecies(LangerandHance,2004).

Parasitismrateswerelowerintheresistantthaninthe suscep-tiblepopulationofL.pseudobrassicae.Parasitismintheresistant populationofL.pseudobrassicaecanbeexplainedduetothelossof resistanceintheoffspring,thusparasitizedindividualsinthis pop-ulationweresusceptibleoffspringoftheoriginalresistantclone

(Oliver etal., 2010).In addition, becauseparasitoidswere

con-finedwithinalimitedspacetogetherwiththeresistanthosts,the chanceoffindingapreviouslyparasitizedhostincrease,leadingto “superparsitism”(vanLenterenandBakker,1976;Kantetal.,2011). Furthermore,thegreaterthenumber of ovipositionsina given resistanthost,thegreaterthechanceofbreakingtheresistance

(Oliveretal.,2012).

Inthepresentstudy,theresistantpopulationofL. pseudobrassi-caeshoweda greatergrowthratethanM.persicae,whereasthe susceptibleonedidnot.Studiesindicatethat,intheabsenceof competitorsandnaturalenemies,thepopulationgrowth poten-tial of L. pseudobrassicae on collard green is greater than that ofM.persicae(CividanesandSouza,2003;GodoyandCividanes, 2002).ThelowerparasitismratefoundinresistantL. pseudobras-sicaemayhavebeenthefactorforthegreaterpopulationgrowth ofthisaphidspecies.Typically,whenparasitizedduringthe sec-ondinstar,aphidsbecomemummiesanddiebeforereproducing, andevenparasitizedaphidsthatsurviveuntiladulthooddonot reproduce.Therefore,susceptibleaphidswhenparasitizedduring earlyinstarsdo not contributetothegrowthof thepopulation

(Sampaioetal.,2007;vanSteenisandEl-Kawass,1995)and

resis-tant L.pseudobrassicae populationshave a positive growthrate even whenparasitized duringthesecondinstar (Oliveira etal.,

2013).

However,thepresenceoftheparasitoidcanbethereasonwhy wefoundnodifferencesingrowthratesbetweenresistantand sus-ceptiblepopulationsofL.pseudobrassicae.Althoughbeingableto reproduce,theintrinsicrateofpopulationincrease(rm)of

resis-tantL.pseudobrassicaeparasitizedbyD.rapaeisonly63%thatof non-parasitizedaphids(Oliveiraetal.,2013).Therefore,the para-sitoidcanreducethepopulationgrowthrateofboth,resistantand susceptiblepopulationsofL.pseudobrassicae.

ThepopulationsofL.pseudobrassicaeandM.persicaedocompete sincebothhaveapreferenceforfeedingoncollardgreenleaves intheintermediateandlowerregionsoftheplant(Cividanesand

Souza,2004;Sampaioetal.,2017).Astheaphidsdonothavea

mechanismtoremovethecompetitorfromthefavoritespots,the specieswiththegreatestpopulationgrowthpotential,andthatis abletooccupytheseplacesfirst,willprobablyhaveacompetitive

Fig.3. (A)RelativegrowthratesofM.persicaeandresistantL.pseudobrassicaepopulations.(B)RelativegrowthratesofM.persicaeandsusceptibleL.pseudobrassicae populations.

advantage(Crawley,1983;Dennoetal.,1995;PetersenandHunter,

2001;Schoener,1983).Evenwhenthis competitionismediated

byparasitoids,insectsthathaveagreaterpotentialofpopulation growthtendtosupportalargerpopulationofparasitoidsandgain competitiveadvantageoverspecieswithalowergrowthpotential

(HoltandLawton,1994).

Thisis thefirststudyevaluating theinfluenceof aresistant aphidpopulationontheparasitismofitssusceptiblecompetitor. Althoughadditional,longtermstudiesareneededtoruleoutthe hypothesis of indirectresistance, we showed that over a short periodoftimethepresenceofresistantL.pseudobrassicaedoesnot affecttherateofparasitismbyD.rapaeonM.persicae.

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgments

Wethank theFundac¸ãodeAmparoa Pesquisado Estadode MinasGerais(FAPEMIG)for thefinancialsupport(Project APQ-01744-12). We also thank the National Council for Scientific andTechnologicalDevelopment(CNPq)andtheSãoPauloState ResearchFoundation(FAPESP)forprovidingfinancialsupportto theINCT-HYMPAR/SUDESTEandCoordinationforImprovementof HigherEducationPersonnel(CAPES)forthegraduatescholarship forSamiraEvangelistaFerreiraandReinaldoSilvadeOliveira.

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