Each female was placed in a Duran type tube 1.5mL containingadropletofhoneyasfood,andofferedapproximately 100S.frugiperdaeggsupto24holdgluedtowhitecardboard cards2.5×5cmsixreplicatespert
Trang 1REVISTA BRASILEIRA DE
EntomologiaAJournalonInsectDiversityandEvolution
w w w r b e n t o m o l o g i a c o m
Ana Paula de Queiroza, Adeney de Freitas Buenob,∗, Aline Pomari-Fernandesc,
Orcial Ceolin Bortolottod, Adriana Yatiem Mikamid, Lopes Olivee
a Instituto Agronômico do Paraná, Londrina, PR, Brazil
b Empresa Brasileira de Pesquisa Agropecuária, Londrina, PR, Brazil
c Universidade Federal da Fronteira Sul, Laranjeiras do Sul, PR, Brazil
d Universidade Federal do Paraná, Setor de Ciências Biológicas, Departamento de Biologia, Curitiba, PR, Brazil
e Universidade Federal de Rondônia, Porto Velho, RO, Brazil
a r t i c l e i n f o
Article history:
Received 6 September 2016
Accepted 16 December 2016
Available online xxx
Associate editor: Daniel Sosa Gómez
Keywords:
Arrhenotokous parthenogenesis
Optimal number
Phenological stages
Preimaginal conditioning
a b s t r a c t
Weevaluatedtheinfluenceofhostpreference,mating,andreleasedensityonTelenomusremus(Nixon, 1937)(Hymenoptera:Platygastridae)parasitizingeggsofSpodopterafrugiperda(Smith,1797) (Lepi-doptera:Noctuidae).First,wetestedhostpreferenceofT.remus(freechoicetest)offeredachoicebetween eggsofCorcyracephalonica(Stainton,1865)(Lepidoptera:Pyralidae)andS.frugiperda.Parasitism capac-ityandhostpreference(S.frugiperda)ofT.remusrearedoneitherofthetwohostsdidnotdiffer.Secondly,
weevaluatedtheinfluenceofmatingbehaviorofT.remusfemalesonitsparasitism.Onlytheoffspring sexratiodifferedbetweentreatments,indicatingthatthespeciesreproducesbyparthenogenesisofthe arrhenotokytype.Finally,weevaluatedtheinfluenceofreleasedensityonT.remusparasitism.Thiswas testedbyreleasingdifferentnumbersoftheparasitoidperS.frugiperdaeggusingT.remusrearedfor differentnumbersofgenerationsonC.cephalonicaeggs.Theregressionanalysisbetweenpercentageof parasitismanddensityofreleasedT.remusfemalesshowedaquadraticeffectforalltestedparasitoid generations(F35,F40,andF45)withmaximumparasitismfrom65.07%to71.69%.Ourresultsallowthe conclusionthat(a)T.remusprefersS.frugiperdaeggs,regardlessofthehostonwhichthisparasitoidwas reared,showingnopreimaginalconditioning;(b)Matingdoesnotaffectthenumberofeggsparasitized
byT.remusorthedevelopmentofitsoffspring;and(c)TheoptimalT.remusreleasedensitywhenreared
onC.cephalonicaisbetween0.133and0.150females/S.frugiperda
©2016SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/)
Introduction
Telenomusremusparasitizeseggsofvariousspeciesoftheorder
Lepidoptera, manyof whichare globalcroppests(Cave,2000)
Despitepossessingtraitsfavorablefortheiruseasbiological
con-trol,thisparasitoidiscurrentlyonlyrearedonasmallscaledueto
thedifficultiesofrearingitonitsnaturalhostSpodopterafrugiperda
(Pomari-Fernandes et al., 2015) Alternatively, T remus can be
rearedonafactitioushoststhatmaynotbetheparasitoid’s
pref-erencebutisstilladequateforitssuccessfuldevelopment(Parra,
1997).Inthiscontext,Corcyracephalonica,whichcanberearedin
thelaboratorymoreeasilyandatalowercostthanS.frugiperda
(Kumaretal.,1986), hasbeensuggestedasapossiblefactitious
hostofT.remus(Kumaretal.,1986;Pomarietal.,2012).However,
∗ Corresponding author.
E-mail: adeney.bueno@embrapa.br (A.F Bueno).
continuousrearingofaparasitoidonafactitioushostmayaffectits parasitismorhostpreference,andmaydirectlyinfluenceits effi-ciencyagainstthetargetpest.Thisisprobablyduetopreimaginal conditioningoccurringduringlarvaldevelopment(Cobert,1985),
abiologicalprocesswhichneedsfurtherstudyforT.remusreared
onC.cephalonicaeggs
Knowledgeofthebiologyandecologyofinsectsandtheir natu-ralenemiesisaprerequisiteforthesuccessofbiologicalcontrolin IntegratedPestManagement(IPM)(Cave,2000).Adultmatingcan impactparasitism,andshouldbetakenintoaccountwhentesting theuseofaneggparasitoidinmassivefieldreleases(Pratissolietal.,
2009).MalesofT.remushaveonelarvalinstarlessthanfemales (Cave,2000),andthereforeemergeearlierthanfemalesfromthe samehosteggmass.Thenewlyemergedmalesguardeggmasses
toensuretheirmatingwithfemalesassoonastheyemerge(Cave,
2000).Becauseparasitismcapacitymaydifferbetweenmatedand unmatedT remusfemales, the influenceof matingat thetime
ofemergenceshouldbeassessedpriortoadoptingtherecently http://dx.doi.org/10.1016/j.rbe.2016.12.004
0085-5626/© 2016 Sociedade Brasileira de Entomologia Published by Elsevier Editora Ltda This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/).
Trang 2emergence
Additionally,superparasitismcandecreasethenumberof
par-asitized eggs, and may occur when an excessive number of
parasitoidsperhosteggisreleased(Cave,2000).Researchisneeded
totesttheinfluenceofreleasedensityonparasitismwiththe
long-termgoalofdeterminingtheoptimalnumberofparasitoidstobe
releasedintothefield(SáandParra,1993).Tothisend,thisstudy
evaluatestheinfluenceofhostpreference,mating,andrelease
den-sityonT.remusparasitismoneggsofS.frugiperda.Theresultsyield
crucialinformationforthesuccessofrearingT.remusanditsrelease
inthefield
Material and methods
Thestudies(bioassay1and2)werecarriedoutundercontrolled
laboratoryconditions (25◦C±2◦C, relative humidity 80%±10%,
photoperiod14/10h[light/dark])andinasemifield(greenhouse)
(bioassay3)atEmbrapaSoybean,Londrina,StateofParaná,Brazil
Thisworkinvolvedthreeindependentbioassays.Inthefirst
bioas-sayweassessedhostpreferenceoftheparasitoidT.remusoffered
achoicebetweeneggsofC.cephalonicaandS.frugiperda.Inthe
secondbioassayweevaluatedtheinfluenceofmatingonT.remus
parasitismofS.frugiperdaeggs.Inthethirdbioassaywedetermined
theoptimalnumberofparasitoidstobereleasedforthe
success-fulcontrolofS.frugiperdainmaize.Allhostsandparasitoidsused
intheexperimentswereobtainedfromtherearinglaboratoryat
EmbrapaSoybean
Bioassay1:hostpreferenceofTelenomusremus
All T remus colonies evaluated in the host preference test
originatedfrominsectsrearedonC.cephalonicaeggsattheF40
generationandonS.frugiperdaeggsattheF350generation(Parra,
1997)inordertocomparethetwoinsectpopulations.The
exper-imentwascarriedoutinacompletelyrandomized2×2factorial
design(2parasitoidcoloniesby2hosteggs)and15replicates.Each
replicateconsistedofanarenaaccordingtoThuleretal.(2007):a
polyethylenebottle(4and2cmindiameter)forparasitoidrelease
wasplacedinthemiddleofthearenaaroundwhichfourtubes
(vol-ume1.5mL)containingthehostspecimenswerearrangedatequal
distances
Approximately 150 eggs of a single host (C cephalonica or
S frugiperda) were glued to labeled, white cardboard cards
(2.5×5cm)withwhiteglue(Tenaz®).Twocardsperhostwere
individuallyintroducedintothetubeslocatedonoppositesides
ofthearena.Next,fournewly emerged (24h)T.remus females
fedonhoneywerereleasedintothearenafromthecentral
bot-tle.After24h,thecardswereremovedandplacedindividuallyin
1.5mLDurantubesuntiltheemergenceofadults.Atthisstep,the
numberofparasitizedeggswasrecorded
Theresults(Table1)wereanalyzedfornormality(Shapiroand
Wilk,1965)andhomogeneityofvarianceoftreatments(Burrand
Foster,1972)and, whenevernecessary,transformedtoperform
ANOVA.Thenumberofparasitizedeggswastransformedbylog
(x+1).ThetreatmentmeanswerecomparedusingTukey’stestat
aprobabilitylevelof5%(SASInstitute,2009)
Bioassay2:influenceofparasitoidmatingonitsparasitism
MatedandunmatedT.remusfemalesrearedonC.cephalonica
eggs(F40generation)wereofferedeggsofS.frugiperdafora24h
period Each female was placed in a Duran type tube (1.5mL)
containingadropletofhoneyasfood,andofferedapproximately
100S.frugiperdaeggs(upto24hold)gluedtowhitecardboard
cards(2.5×5cm)(sixreplicatespertreatment).Afterwards,cards
Table 1
Bioassay 1: number of eggs (Spodoptera frugiperda and Corcyra cephalonica) para-sitized by Telenomus remus from different colonies (reared on S frugiperda and C cephalonica eggs) Temperature 25 ± 2◦C, relative humidity of 80% ± 10%, and the photoperiod of 14/10 h (light/dark).
Host Parasitoid colony
T remus reared
on C.
cephalonica
T remus reared
on S frugiperda
Mean
C cephalonica 2.29 ± 1.03 0.00 ± 0.00 1.19±0.57 b
S frugiperda 94.36 ± 12.71 81.08 ± 13.53 87.96 ± 9.18 a Mean 48.32 ± 10.85 A 40.53 ± 10.47 A
CV (%) 39.15
F host 259.46
p host <0.0001
DF host 1
Means (±SE) followed by identical upper-case letters within a row (different par-asitoid colonies), and lower-case letters within a column (different egg hosts) did not statistically differ according to Tukey’s Studentized range test at 5% probability Original data followed by statistics performed on data transformed in log (x + 1).
wereremovedandplacedindividuallyinDuran-typetubesuntil theemergenceofadults Thenumberof parasitizedeggs, para-sitoidemergence(%),sexratio,andlongevityofparentalfemales wasrecorded The results(Table 2)were analyzed for normal-ity (Shapiro and Wilk, 1965) and homogeneity of variance of treatments(BurrandFoster,1972)and,whenevernecessary, trans-formedtoperformANOVA.Thenumberofparasitizedeggswas transformed by log (x+1) and parasitoid emergence (%) trans-formedbyarcsin
X/100.Then,treatmentmeanswerecompared
byTukey’stestataprobabilitylevelof5%(SASInstitute,2009) Bioassay3:influenceofT.remusreleasedensityonitsparasitism Theinfluence oftherelease density ofT remusonits para-sitismwasdeterminedbyreleasingdifferentnumbersofT.remus
inrelationtoagivennumberofeggsofS.frugiperda,usingT.remus rearedforadifferentnumberofgenerations(F35,F40,andF45)onC cephalonicaeggs.WechoseT.remusrearedonC.cephalonicaeggs becausethisparasitoidisplannedtobereleasedinthefieldona largescaleforbiologicalcontrolprograms.Anindependenttrial wascarriedoutforeachparasitoidgenerationundergreenhouse conditions,usingafullyrandomizedexperimentaldesignwithten treatments(0,0.017,0.033,0.050,0.067,0.083,0.100,0.117,0.133, and0.150T.remusfemalesperS.frugiperdaegg)andfivereplicates Eggs of the pest species were obtained from laboratory rearing and exposed to treatments inside iron-framed cages (40cm×40cm×120cm)coveredwithvoilefabricineach repli-cate A pot of40-cm diameter withtwo hybridIPR 114maize plantswasplaced insideeach ofthesecages, attachinga white cardboardcardwith150eggstothewhorlofeachplant.Different numbers(5,10,15,20,25,30,35,40and45)ofpreviouslymated females(Pomarietal.,2013)werereleased,representingthe pro-portionsof0.017,0.033,0.050,0.067,0.083,0.100,0.117,0.133,and 0.150T.remusfemalesperS.frugiperdaegg.Noparasitoidswere releasedinthecontroltreatment.Parasitismwasallowedfor24h, andtemperatureandhumiditywererecordedusingadigitaldata logger(InstruthermHT-500)(Table3).Next,eggswerecollected andmaintainedinPetridishesat25◦Cuntiltheydarkenedand parasitoidsemergedforsubsequentevaluation.Werecordedtotal percentofparasitismperreplicate.Thisprocedurewasrepeated
Trang 3Table 2
Bioassay 2: biological parameters of mated and unmated Telenomus remus females (from Corcyra cephalonica eggs) that parasitized Spodoptera frugiperda eggs [Temperature
of 25 ± 2◦C, relative humidity of 80% ± 10%, and the photoperiod of 14/10 h (light/dark).].
Treatment Number of parasitized eggs 1 Parasitoid emergence (%) 2 Sex ratio Longevity of parental females (days) Mated females 53.33 ± 5.68 ns 99.13 ± 0.26 ns 0.61 ± 0.04 a 5.63 ± 0.34 ns
1 Means (±SE) followed by identical upper-case letters within a row (different parasitoid colonies), and lower-case letters within a column (different egg hosts) did not statistically differ according to Tukey’s Studentized range test at 5% probability Original data followed by statistics performed on data transformed in log (x + 1).
2 Original data followed by statistics performed on data transformed by arcsin
X/100.
ns ANOVA not significant.
Table 3
Weather data recorded by a data Logger during bioassay 3 (influence of the T remus release density on its parasitism).
Phenological Minimum Maximum Average Minimum Maximum Average
atvariousdevelopmentalstagesoftheplants(V2/V3,V4/V5,and
V8/V9accordingtoMagalhãesandDurães,2006)becausedifferent
leafsurfacesmightprovidedifferentsizesofareaforaparasitoid
tofindeggsandthereforemayimpactitsparasitism.Theaverage
parasitismobservedforeach parasitoiddensityduringdifferent
plantstages wasusedintheanalyses(Fig.1).ThenumberofT
remusfemalespereggofS.frugiperdaandpercentageofparasitism
wereusedinaregressionanalysis(SASInstitute,2009).Parasitism
datawas analyzed fornormality (Shapiro and Wilk, 1965)and
homogeneityofvarianceoftreatments(BurrandFoster,1972),and
whenevernecessarytransformedtoperformANOVA.Parasitism
valuesofT.remusgenerationsF40 andF45 weretransformedby
(x+1)0.5.ThetreatmentmeanswerethencomparedbyTukey’stest
ataprobabilitylevelof5%(SASInstitute,2009)
Results
Bioassay1:hostpreferenceofTelenomusremus
TherewasnointeractionbetweenT.remuscolonies(T.remus
reared on C cephalonica or S frugiperda eggs) and parasitized
hosts (C cephalonica or S frugiperda) (pparasitoid*host=0.1950,
Fparasitoid*host=1.73) (Table 1) Telenomus remus reared on C
cephalonicaeggsandS.frugiperdaeggsexhibitedsimilarparasitism
capacityregardlessofthehostspeciestheywererearedon.The
numberofparasitizedeggswassimilarforbothparasitoidcolonies
(48.32 and 40.53 eggs for parasitoids reared on C cephalonica
andS.frugiperda,respectively,pparasitoid=0.2161,Fparasitoid=1.57)
(Table 1) In contrast, higher numbers of S frugiperda eggs
(87.96)wereparasitizedcomparedwithC.cephalonicaeggs(1.19)
(phost<0.0001,Fhost=259.46)(Table1 indicatingaclear
prefer-enceforS.frugiperdaeggsregardlessofthehosttheparasitoidwas
rearedon
Bioassay2:influenceofparasitoidmatingonitsparasitism
No differences were found between mated and unmated
femaleswithrespecttothenumberofparasitizedeggs,parasitoid
emergence(%)andlongevityofparentalfemales(days)(Table2).In contrast,offspringsexratiodifferedbetweentreatments(0.61for matedfemalesand0.00forunmatedfemales,Table2 indicating thatT.remusreproducesparthenogeneticallywithcharacteristics
ofthearrhenotokytype
Bioassay3:influenceofthereleasedensityofT.remusonits parasitism
For S frugiperda eggsattached tomaize leaves, we founda quadraticeffectfortheregressionanalysisbetweenthepercentage
ofparasitismanddensityofreleasedT.remusfemales(numberof parasitoidperpestegg)inallparasitoidgenerationstested(Fig.1) Maximumparasitismwas71.69%,71.69%,and65.07%forF35,F40, andF45,respectively.Themaximumparasitismratewasreached
atdensitiesbetween0.133and 0.150ofT.remusfemalesperS frugiperdaegg(Fig.1).Throughoutthestudy,climaticdatawere recordedwithadataloggeratgreenhouseconditions.Differences
intemperatureandrelativehumiditybetweenallevaluatedgrowth stagesareshowninTable3
Discussion
Parasitoidrearingonfactitioushostsisessentialforthesuccess
ofitsmass releasein augmentativebiologicalcontrolprograms (Buenoetal.,2008)andrequirestheestablishmentofprocedures
tomonitorthequalityoftheproducedinsect.AccordingtoCobert (1985),continuousrearingofparasitoidsonfactitioushostscan causethelossoftheirabilitytorecognizeandchooseahostand thereforereducetheirefficiencyagainstthetargetedpestspecies
In ourstudy,this negativeeffectwasnot observedforT.remus rearedonC.cephalonicaeggs.Parasitismofeggsofthetargetfield pest (S.frugiperda)was similarin parasitoidfemales reared on both C.cephalonica andS.frugiperda However,theinfluenceof thefactitioushostonparasitoidqualitymightalsodependonthe numberofgenerationstheparasitoidisrearedonthesamehost Pratissolietal.(2004)reportedthatparasitismcapacityofspecies rearedonfactioushostswasinverselyproportionaltothenumber
Trang 4100 A: F35
B: F40
C: F45
90
80
70
60
50
40
30
20
10
19.5 23.32
35.36 47.99
Parasitism (%)=4.5 + 675.19 (parasitoid number) - 1753.92
(parasitoid number) 2
R 2 =0.8131
Parasitism (%)=1.40 + 90.20 (parasitoid number) - 302.55
(parasitoid number) 2
R 2 =0.9226
Parasitism (%)=1.47 + 72.82 (parasitoid number) - 209.47
(parasitoid number) 2
R 2 =0.8997
53.73
65.02
47.92 47.07
71.69
0
0.017 0.033 0.050 0.067 0.083 0.100 0.117 0.133 0.150
0 0.017 0.033 0.050 0.067 0.083 0.100 0.117 0.133 0.150
0 0.017 0.033
T remus density/ S.frugiperda eggs
0.050 0.067 0.083 0.100 0.117 0.133 0.150
100
90
80
70
60
50
40
30
20
10
0
100
90
80
70
60
50
40
30
20
10 8.02
13.16
23.28 32.17 34.18
42.99
38.62 53.46 65.07
0
7.15
18.34
35.11 41.16
51.18 62.11 71.69
64.75
27.62
Fig 1. Bioassay 3: parasitism (%) in Spodoptera frugiperda eggs after the release of
different densities of Telenomus remus per host egg using parasitoids from different
colonies T remus reared on Corcyra cephalonica for 35 generations (A), 40
gener-ations (B) and 45 generations (C) Average values from trials repeated at maize at
V2/V3, V4/V5 and V8/V9 development stage.
ofgenerationsforwhichtheywerekeptonthesamehostspecies
inthelaboratory.Therefore,qualitycontrolmustassessparasitism
capacity of all generations throughout parasitoid rearing We
observedsimilarparasitismforT.remusonS.frugiperdaregardless
oftheoriginoftheparasitoid(rearedoneitherC.cephalonicaorS
frugiperdaeggs)evenafterrearingitonC.cephalonicaeggsfor45
generations(F45generation).Theseresultshighlightthepotential
ofC.cephalonicaasafactitioushostforT.remusrearing
Inaddition,S.frugiperdaeggscontinuedtobepreferredbyT
remusrearedonC.cephalonicaeggsinthefree-choicetest
sup-portingthehypothesis thatitconstitutesanadequatefactitious
host.Thisresultalsosuggeststhatthehostacceptancebehavior
ofT.remusfemales cannotbeattributedtoexperienceacquired
duringlarval development(preimaginal conditioning) as
previ-ouslydescribed by Cobert (1985) and Kaiser et al (1989) and
morerecentlybyPomari-Fernandesetal.(2015).Ourfindingalso
excludeslearningor␣-conditioning,wherefemalesassociatenew
stimuli(acquired) withinnatestimuli and thuscan adapttheir
behaviortotheenvironmentinwhichtheylivedasadultsoryoung
individuals(Kaiseretal.,1989;Nurindahetal.,1999).Theabsence
ofpreimaginalconditioningorlearningwaspreviouslyreportedfor
T.remusrearedonS.frugiperdaeggsand,whentestedfordifferent hosts(S.frugiperdaversusS.cosmioides,S.frugiperdavs.S.albula, andS.cosmioidesvs.S.albula)thisspeciespreferredS.cosmioides
asahost(Goulartetal.,2011).ThissupportstheuseofT.remusin biologicalcontrolbecauseofthepossibilityofrearingitona sin-glehostforseveralgenerationswithoutreducingitseffectiveness againstdifferenttargetpestsinthefield
This host preference of T remus is probably related to the nutritionalqualityofthehost.Addingmorecomplexitytothis phe-nomenon,Molinaetal.(2005)claimthatnotonlythenutritional qualityofthefuturehostbutalsooftheprevioushostonwhichthe parasitoidwasrearedmightinfluencehostpreference.Eggsurface, colorandothertraitsofthehostcanalsoinfluencehostpreference
inamorecomplexdecision-makingprocess(Cônsolietal.,1999) However,thepreferenceofT.remusforS.frugiperdaeggswhen rearedonC.cephalonicamaybemorecloselyrelatedtothesuperior nutritionalvalueofS.frugiperdacomparedtoC.cephalonica Theimportanceofadultmatingmustalsobeconsideredwhen rearingT.remus,becauseitcancompromisethemaintenanceofthe parasitoidinthefield(Pratissolietal.,2009;Farrokhietal.,2010)
Arecentstrategytoreleaseeggparasitoidsinthefieldhasbeento useisolatedpupaethataresprayedonplants,forexampleof Tri-chogrammaspp.inBrazil.However,malesofT.remuswhichemerge earlierthanfemalesduetotheirshorterlifecycleawaitfemalesto emergefromthesameparasitizedeggmass(Cave,2000), allow-ingforhighmatingratesdirectlyafteremergence.Therefore,the sprayingofT.remusindividualpupaeinthefieldcouldnegatively impactthereproductivebehavioroftheparasitoid,highlightingthe importanceofevaluatingmatingdeprivation
Theabsenceofmatingdirectlyinfluencedoffspringsexratio, leadingtotheproductionofmalesonly.However,otherbiological parameterswerenotaffected.Theobservedreproductionmodeof
T.remusviaparthenogenesisofthearrhenotokytype(i.e.fertilized femalesgiverisetodiploidfemales,whereasunfertilizedfemales giverisetohaploidmales),hasbeendescribedasthemostcommon reproductivetypeforinsectsoftheorderHymenoptera(Pratissoli
etal.,2014)
Incontrasttosex ratio,thenumbers ofparasitizedeggsper matedand unmatedfemale were similar,as wellas parasitoid emergence(%)andlongevityofparentalfemales.Itshouldbenoted thatinourstudythelongevityoftheparentalfemaleswassimilarto thatobservedforT.remusofgenerationF19rearedonC.cephalonica eggsasreportedbyPomari-Fernandesetal.(2015).Theseresults differfromPratissolietal.(2014)whoobservedaninfluenceof matingonfemalelongevityof theeggparasitoidTrichogramma pretiosum (Riley, 1879) (Hymenoptera: Trichogrammatidae) In addition,Stouthamer (1993)reports that field releasesof para-sitoids(genusTrichogramma)reproducingbyparthenogenesisof thethelytokytypeweremoreefficientcomparedwithparasitoids withthose reproducing by parthenogenesis of thearrhenotoky type,illustratingtheimportanceofstudyingthereproductivemode
ofeachparasitoidspecies
OurresultssuggeststhatalthoughparasitismofT.remus,and thereforeitscontrolefficiency,wasnotaffectedbymating, par-asitoidpermanenceinthefieldmaybeimpactedwhenunmated femalesarereleased.Somestudiesreportedthefailuretoestablish
T.remusinthefieldafteritsrelease(VanWaddillandWhitcomb, 1982;Figueiredoetal.,1999).Sinceadditionalreleasemightbe alwaysnecessarywhenpestpopulationincrease,thereleasingof matedfemalesmightnotbeimportantconsideringthatthe para-sitismoftheavailableeggsinthefieldwouldbethesame(Carneiro
etal.,2009)
Additionally, the success of T remus as biological control depends ontheappropriate parasitoiddensityper S.frugiperda
Trang 5par-asitoidsinrelationtoa givennumber ofpesteggs Westudied
parasitoidrelease inmaize,usingdifferentdensitiesofT.remus
femalesoftheF35,F40,andF45generation.Parasitismoffemales
of all tested generations was positively related to the density
of females perS frugiperda egg,reachingmaximum parasitism
between 0.133 and 0.150 T remus/S frugiperda egg (40–45 T
remusfemalesper300eggsofS.frugiperda).Ina similarstudy,
theoptimaldensitywasalmost 50%less thanin ourstudy(25
T.remusfemales/300 S.frugiperdaeggsof T.remusrearedonS
frugiperdareportedbyPomarietal.,2013).Giventhatparasitism
canstronglydependontheparasitoidspeciesand/orstrains(Sá
andParra,1993),thesediscrepanciesmaybeduetodifferent
par-asitoidcoloniesusedinbothtrials.TherearingofT.remusonC
cephalonicaeggsfor manygenerations seemstogenerate
para-sitoidswithlowerparasitismcapacitycomparedwiththosereared
onS.frugiperdaeggs,requiringahigherdensityofT.remusfemales
toeffectivelycontrolthepest.Althoughagreaternumberof
par-asitoidsperpesteggareneededwhentheparasitoidisrearedon
afactitioushost,severalotherfactors,suchastheeaseofrearing
andlowcostoftheparasitoid,shouldbeconsidered.Overall,our
resultsallowtheconclusionthat(a)T.remuspreferstoparasitizeS
frugiperdatoC.cephalonicaeggs,despitetheabsenceof
preimagi-nalconditioning;(b)matingdoesnotaffectparasitismcapacityand
developmentofT.remus;(c)theoptimalreleasedensityofT.remus
rearedonC cephalonicais between0.133and 0.150females/S
frugiperdaeggs,whichishigherthantheoptimalreleasedensityof
T.remusrearedonitsnaturalhostS.frugiperda.Theseresults
impor-tantlycontributetoexistingknowledgeonthesuccessfulrearing
ofandfieldreleasestrategiesforT.remus
Conflict of interest
Theauthorsdeclarenoconflictofinterest
Acknowledgments
TheauthorswouldliketothankEmbrapaSojaandthesponsor
agenciesCAPESand CNPqfortheirfinancialsupportand
schol-arships.ThispaperwasapprovedforpublicationbytheEditorial
BoardofEmbrapaSoja
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