REVISTA
BRASILEIRA
DE
Entomologia
AJournalonInsectDiversityandEvolutionw w w . r b e n t o m o l o g i a . c o m
Biology,
Ecology
and
Diversity
Biology
of
Bactrocera
carambolae
(Diptera:
Tephritidae)
on
four
hosts
Alison
Pureza
Castilho
a,
Joel
Pasinato
b,
Jhulie
Emille
Veloso
dos
Santos
c,
Analia
e
Silva
da
Costa
c,
Dori
Edson
Nava
d,
Cristiane
Ramos
de
Jesus
e,
Ricardo
Adaime
a,e,∗ aUniversidadeFederaldoAmapá,ProgramadePós-graduac¸ãodaRedeBionorte,Macapá,AP,BrazilbUniversidadeFederaldoRioGrandedoSul,ProgramadePós-graduac¸ãoemFitotecnia,PortoAlegre,RS,Brazil cFaculdadedeMacapá,Macapá,AP,Brazil
dEmbrapaClimaTemperado,Pelotas,RS,Brazil eEmbrapaAmapá,Macapá,AP,Brazil
a
r
t
i
c
l
e
i
n
f
o
Articlehistory: Received8March2019 Accepted6September2019 Availableonline17October2019 AssociateEditor:LeonardoBarbosa
Keywords: Carambolafruitfly Fruitflies Insect Quarantinepest
a
b
s
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c
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BactroceracarambolaeisaquarantinepestfoundinBrazil,restrictedtothestatesofAmapá,Paráand Roraima.Thisfruitflycanpotentiallycauseextensivesocioeconomicandenvironmentaldamageinthe country,ifitdisperseintoareaswherefruitisgrownforexporting.Theobjectiveofthisworkwasto studythebiologyofB.carambolaeonfruitsofAverrhoacarambolaL.(Oxalidaceae),PsidiumguajavaL. (Myrtaceae),SpondiasmombinL.(Anacardiaceae)andEugeniastipitataMcVaugh(Myrtaceae).The follow-ingparameterswereinvestigated:durationofegg-larva,pupal,egg-adult,pre-oviposition,oviposition andpost-ovipositionperiods,pupalweightandviability,sexratio,fecundity,fertilityandlongevity.All parametersexceptpupalweight,ovipositionandpost-ovipositionperiod,eggfertilityandsexratiowere influencedbythehostplantonwhichthelarvaewerereared.Thecarambolafruitflycompletesits developmentonallthosehostsstudiedhere,withthehighestfecunditiesonA.carambolaandP.guajava. ©2019SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction
BactroceracarambolaeDrew&Hancock(Diptera:Tephritidae), nativetoAsia,isaninvadingspeciesinSouthAmerica,whereit wascollectedforthefirsttimein1975inParamaribo,Suriname. InBrazil,itwasdetectedforthefirsttimein1996inthe munic-ipalityofOiapoque,stateofAmapá(Silvaetal.,2004).Bactrocera carambolaeisanimportantimpedimenttofruitexportation,due tothequarantinerestrictionsimposedbyimportingcountrieson regionswherethepestispresent(Godoyetal.,2011;Lemosetal., 2014;FerreiraandRangel,2015;MirandaandAdami,2015).This speciesiscurrentlyclassifiedasaquarantinepestpresentinBrazil, whereitisdistributedinthestatesofAmapá,ParáandRoraima andisunderofficialcontrolbytheMinistryofAgricultureandFood Supply(Brasil,2018).
Availability of information onthe population dynamics and demography of this fruit fly, as well as range and preference forhosts,areessentialfortheestablishmentofcontrolmeasures (Lemosetal.,2014).Bactroceracarambolaeisapolyphagousfruitfly with21reportedhostplantsinBrazil(Adaimeetal.,2016).Despite
∗ Correspondingauthor.
E-mail:ricardo.adaime@embrapa.br(R.Adaime).
existingreportsofB.carambolaeonnativeplantsoftheAmazon region,includingEugeniastipitataMcVaugh,Pouteriamacrophylla (Lam.)Eymaand Licaniasp.,it shouldbenotedthat allreports occurredinenvironmentsalteredbyhumanactivity(Lemosetal., 2014;Almeidaetal.,2016).Ontheotherhand,theconsiderable hostrangeofthispest(Adaimeetal.,2016)andtheirpotential foradaptationtootherregionsofBrazil,suchastheSãoFrancisco Valley(Pessoaetal.,2016),putfruitgrowingatrisk(Limaetal., 2018).
AmongthereportedhostsofB.carambolaeinBrazil,wechose two primary hosts – carambola [Averrhoa carambola L. (Oxali-daceae)] andguava [Psidiumguajava L.(Myrtaceae)] –and two alternativehosts–yellowmombin[SpondiasmombinL. (Anacar-diaceae)]and araza[EugeniastipitataMcVaugh(Myrtaceae)],as mentionedintheliterature(Lemosetal.,2010,2014;Adaimeetal., 2016;Almeidaetal.,2016;Brasil,2018).
AverrhoacarambolaisnativetotropicalAsiaanditsfruitscanbe consumedinnaturaorusedtomakejuicesandsweets(Cavalcante, 1996).Guavaoriginatedin tropicalforestsinLatinAmerica and isparticularlynotableforthehighnutritionalvalueofitsfruit,as wellasthemultipleformsinwhichitisused(GonzagaNeto,2001). IntheAmazon,itgrowsalongruralroads,nearnativevegetation, duetoitseaseseeddispersal(Cavalcante,1996).Yellowmombinis foundintheAtlanticForestandAmazoninuplandandfloodplain
https://doi.org/10.1016/j.rbe.2019.09.002
0085-5626/©2019SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisis anopenaccessarticleundertheCCBY-NC-NDlicense(http:// creativecommons.org/licenses/by-nc-nd/4.0/).
forestenvironments,andisalsopresentininhabitedareas,albeit inasubspontaneousstate.Itsfruitsareconsumedinnaturaor pro-cessedintojuices,icecreamsandpopsicles(SacramentoandSouza, 2009;Cavalcante,2010).ArazaisnativetothePeruvianAmazon, whereitiswidelyfoundacrosspracticallytheentireregion(Pinedo etal.,1981).Itspulpisusedinthepreparationofjuices,preserves, creams,jamsandsweets,butisrarelyconsumedinnaturadueto itsacidity(Falcãoetal.,1988;Cavalcante,1991).
Despite the undeniable importance of B. carambolae to the Brazilian fruit industry,no studieshave yetbeen conductedto investigateitsbiologyonmultiplehosts.Inlightofthis,ourstudy aimedtodeterminethebiologicalparametersofB.carambolaeon fruitsoffourplantspeciesunderlaboratoryconditions.
Materialandmethods
TheexperimentwasconductedinthePlantProtection Labo-ratoryatEmbrapaAmapá,whereacolonyofB.carambolaewas establishedin 2013, fromguava fruitscollectedin thestate of Amapá.Allprocedures usedforrearingaredescribedin Bariani etal.(2016)andsummarizedbelow.Larvaewerefedonan arti-ficialdiet containingsugarcane bagasse, soybean flour, sodium benzoate,sandingsugar,yeastextract,citricacid,Nipaginand dis-tilledwater,and weremaintainedina climate-controlledroom (28±1◦C;80±10% R.H.;nophotophase).Thepuparia obtained wereplacedinplasticbottles(500mL)containingvermiculiteand keptinaclimate-controlledchamber(26±1◦C;12-hphotophase) untiladultemergence.Theadultswerekeptinrearingcagesina climate-controlledroom(26±2◦C;70±10%R.H.and12-h pho-tophase),and theirdiet wascomposedof Bionis® YEMFyeast extractandrefinedsugar(1:3ratio),placedoncottoninPetridishes (5cmdiameter).Waterwasofferedbycapillarity,througha‘sponge cloth’(Esfrebom®,manufacturedbyBettaninIndustrialS.A.,Esteio, RioGrandedoSul,Brazil).
Infestationoffruits
Whentheadultflieshadreachedtheageof25–30days,cages weresetupforinfestationoffruitsofthefourhostplantspecies targetedinthisstudy,asfollows:
Psidiumguajava:twocagesweresetup(45cmlength×30cm width×35cmheight),eachcontaining50“green-ripe”fruitsand 100couplesof B. carambolae.The fruitshad a mean weightof 196.46±3.85gandwereobtainedinasupermarketinthecityof Macapá,vacuum-packedandconfirmedtobefreeofinfestationby fruitflies.
Averrhoacarambola:twocagesweresetup(45×30×35cm), eachcontaining50“green-ripe”fruitsand100couplesofB. caram-bolae.Thefruitshadameanweightof114.70±5.96gandwere obtainedat theExperimentalField for theCerradoat Embrapa Amapá,locatedintheruralareaofMacapá.
Spondiasmombin:onecagewassetup(45×30×35cm), con-taining135“green-ripe”fruitsand200couplesofB.carambolae. Thefruitshadameanweightof15.86±0.27gandwereobtained fromanagriculturalpropertyinthecityofPortoGrande.
Eugeniastipitata:30cagesweresetup(20×12×12cm),each containingone“green”fruitand10couplesofB.carambolae.The fruitshadameanweightof147.0±8.9gandwereobtainedfrom asmalldomesticorchardintheurbanareaofMacapá.
InthecaseofA.carambola,S.mombinandE.stipitata,thefruits werewrappedinfinemeshfabricattheearlystageofdevelopment, toavoidinfestationbyfruitflies.Toensureseparationbetweenthe fruitsandthefabric,plasticgarbagebinsventedatthebottomwere used,formingacage.
DeterminationofbiologicalparametersofB.carambolae
Attheendoftheperiodestablishedforoviposition(48h),the fruitswereremovedfromthecages andindividually placed on a thin layerof sterilized vermiculitein clearplastic containers (8–15cmdiameter,dependingonfruitsize)coveredwithorganza fabric and a vented lid, under controlled conditions (26±2◦C; 70±10%R.H.and12-hphotophase).Afterfivedays,thevermiculite ineachcontainerwasexaminedandanypupariawereremovedand transferredtoplasticvialscontainingmoistenedvermiculite.This procedurewasrepeateddailyuntildisposalofthefruits (approx-imately 20 to30 days).Thepuparia obtainedwereplaced in a climate-controlledchamber(26±2◦C;70±10%R.H.and12-h pho-tophase)untiladultemergence.Thefollowingparameters were assessed:durationofegg-larvaperiod(days),pupalstage(days) andegg-adultperiod(days),pupalviability(%),sexratio(number offemales/totalnumberofadults)andpupalweight.
Fromtheadultsthatemerged,individualcouplesrearedoneach hostplantwereplacedinplasticcages(20×12×12cm)withfood andwateradlibitum.Exactly25coupleswereformedforA. caram-bolaandP.guajava,20forE.stipitataand18forS.mombin.Artificial ovipositiondeviceswereplacedineachcage,eachdevice contain-ingafinelayerofpulpfromthefruitofthecorrespondingspecies (seedetailsin Barianietal.,2016).Toensuretheavailabilityof pulpduringtheexperiment,pulpfromthefruitsofthefourplant specieswasextractedandfrozen.Thecageswereinspectedona dailybasis,atwhichtimethenumberofdeadadultsandnumber ofeggsintheartificialovipositiondeviceswerecounted.The fol-lowingparametersweredetermined:dailyfecundity(numberof eggs/female/day),totalfecundity(numberofeggs/femaleduring lifetime),pre-ovipositionperiod(daysfromemergenceoffemaleto layingoffirstegg),ovipositionperiod(daysfromfirsttolast ovipo-sition),post-ovipositionperiod(daysfromlastegglaidtodeath offemale)andlongevityofmalesandfemales(periodoftimefrom emergencetodeathofindividual).Fertilitywasassessedby analyz-ingovipositionsmadewhencoupleswereapproximately30days old,theageofpeakovipositionforB.carambolaereportedby Jesus-Barrosetal.(2017).Eggswereplacedonfilterpaperin5cmPetri dishescontainingplant-basedspongematerial,moistenedandkept inaclimate-controlledenvironment(26±1◦C;80±10%R.H.;no photophase).Thenumberofeclosedlarvaewascounteddaily.
Dataanalysis
AlldatawereverifiedfornormalityusingtheShapiroWilktest; forhomoscedasticityusingtheBartletttest;andforindependence of residuals through graphicalanalysis.Box cox transformation wasappliedtopupalweightandfecundity.Pupalweight,periods ofpre-oviposition,ovipositionandpost-oviposition,fecundityand fertilitydataweresubmittedtovarianceanalysis(p≤0.05)and, in casesof statisticalsignificance, theeffects of thehosts were comparedbyTukeytest(p≤0.05).Dataofdurationofegg-larva period,pupalstageandegg-adultdidnotmetparametric assump-tionsandweresubmittedtoKruskal-Wallis(p≤0.05)andmeans werecomparedbyDunntest(p≤0.05),incasesofstatistical sig-nificance. Sexratiowascompared usingchi-squaretesting (x2) (p≤0.05).Longevityoffemalesandmaleswasanalyzedthrough survival curvesusing theKaplan-Meierestimator, comparedby log-ranktesting. Toanalyzepupalviability,arcsine transforma-tionwasappliedtothedataand themeanswerecomparedby Tukeytestingat5%probability,asdescribedbyPimentel-Gomes andGarcia(2002).AlldataanalyseswereconductedusingtheR softwarepackage(RDevelopmentCoreTeam,2015).
Table1
Mean±standarddeviationandintervalofvariationofbiologicalparametersofBactroceracarambolaerearedonfruitsofcarambola(Averrhoacarambola),guava(Psidium guajava),yellowmombin(Spondiasmombin)andaraza(Eugeniastipitata)..
Biologicalparameters Hosts
Averrhoacarambola Psidiumguajava Spondiasmombin Eugeniastipitata Durationofegg-larvaperioda(days) 16.00±3.30b
(9–28) 15.44±2.47c (11–23) 14.10±0.95d (10–15) 16.72±2.42a (12–28) Durationofpupalstagea(days) 9.79±1.73c
(4–16) 10.07±0.73b (6–13) 11.04±4.03a (9–14) 9.81±1.60bc (5–12) Durationofegg-adultperioda(days) 25.79±2.37b
(19–32) 25.69±2.38b (21–33) 24.10±0.95c (20–27) 26.44±1.82a (22–30) Pupalweightc(mg) 8.16±1.79 (5–12) 12.24±2.47 (8–19) 8.76±4.03 (4–24) 10.24±3.58 (5–22) Pupalviabilitya(%) 56.40a 57.74a 37.31b 40.64b Sexratioc 0.54 0.48 0.46 0.60
Durationofpre-ovipositionperiodb(days) 28.88±11.90a
(20–56) 15.20±8.09b (9–38) 17.53±8.26b (9–42) 21.56±9.19ab (12–43) Durationofovipositionperiodc(days) 47.37±36.41
(1–119) 39.45±26.41 (2–107) 63.73±42.72 (2–144) 45.37±34.18 (1–102) Durationofpost-ovipositionperiodc(days) 15.89±16.05
(0–46) 13.05±14.61 (0–49) 13.87±18.52 (0–51) 16.50±15.65 (0–47) Fecundityb(No.ofeggs) 502.95±436.88ab
(18–1439) 774.80±546.72a (55–2057) 293.93±311.42b (6–1097) 176.94±190.47b (16–575) Fertilityc(%) 38.02±27.89 (6.67–93.75) 33.52±28.13 (0–100) 50.51±31.93 (3.33–100) 43.09±16.75 (20.0–66.7)
aMeansfollowedbythesameletterinthecolumndidnotdifferbytheDunntest(p≤0.05). b MeansfollowedbythesameletterinthecolumndidnotdifferbytheTukeytest(p≤0.05). c Notsignificant.
Results
Egg-larvaperioddifferedamongtreatments(x2=155.3,df=3, p=0.001),beinglongestforfliesrearedonE.stipitata(16.72days) andshortestforthoserearedonS.mombin(14.10days)(Table1). Pupalstagedurationwaslonger(x2=47.19,df=3,p=0.00012)for fliesrearedonS.mombin(11.04days)andshorterforthosereared onA.carambola(9.79days).Adifferenceinegg-adultperiodwas alsoobserved(x2=3.97,df=3,p=0.2652),withthelongestperiod beingshown byfliesrearedonE.stipitata(26.44days)andthe shortestbythoserearedonS.mombin(24.10days);theperiods recordedforfliesrearedonA.carambola(25.79days)andP. gua-java(25.69days)wereintermediary.Therewasnodifferencein pupalweightamongtreatments.(F=0.54,df=3,p=0.464).
Significantdifferenceswereobservedinpupalviabilityon dif-ferenthosts.FliesrearedonA.carambolaandP.guajavaweremore viablethanthoserearedonS.mombinandE.stipitata(Table1).No significantdifferenceinsexratiowasobserved(X2=1.9567,df=3, p=0.1024),withobservedratiosrangingfrom0.46(S.mombin)to 0.60(E.stipitata).
Thepre-ovipositionperiodwaslonger(F3,66=7.40,p=0.00023) forfliesrearedonA.carambola(28.88days)incomparisontoS. mombin(17.53days)andP.guajava(15.20days),butfliesreared onE.stipitata(21.56 days)didnotdifferfromothertreatments (Table1).Nosignificantdifferencewasobservedinthe oviposi-tionperiod (F3,66=1.45, p=0.2358) and post-oviposition period (F3,66=0.18, p=0.9071). Oviposition periods rangedfrom 39.45 days(P.guajava)to63.73days(S.mombin),andpost-oviposition periods ranged from 13.05 days (P. guajava) to 16.50 days (E. stipitata).
Fecundity wasinfluenced by thehost plants used for larval development(F=11.07,df=3,p=0.0014),withthehighest num-berof eggs/femalebeingobservedfor fliesrearedonP.guajava (774.80eggs)andthelowestforthoserearedonS.mombin(293.93 eggs)andE.stipitata(176.94eggs)(Table1).Forfemalesrearedon P.guajava,therateofovipositionwasmorestronglyconcentrated inthefirst40daysoflife,whereasovipositionbyfemalesreared onotherhostswasmoreevenlydistributedovertime(Fig.1).
Asregardsmeanlongevityoffemales,asignificantdifference wasonlyobservedforfliesrearedonP.guajavawhencomparedto
A.carambolaandS.mombin(Fig.2).Overall,femalesurvival var-iedamongthefourhosts,withtheshortestsurvivalperiodbeing observedforfemalesrearedonP.guajavaandthelongestforS. mombin(Fig.2).Astatisticaldifferencewasfoundinmeanlongevity ofmalesrearedondifferenthosts(Fig.3).Longevityofmalesreared onS.mombinwasequaltothatofthoserearedonA.carambola,but higherthanthelongevityofmalesrearedonP.guajavaandE. stipi-tata.MalesrearedonE.stipitatahadequallongevitytothosereared onP.guajavaandlowerlongevitythanmalesrearedonA.carambola andS.mombin.
There was no significant difference in fertility of eggs (F3,41=3.11,p=0.0367)producedbyfemaleswhose larvaewere rearedondifferenthostplants,despiteanobservedfertilityrange of33.52%forP.guajavato50.51%forS.mombin(Table1).
Discussion
Thedifferences detectedin durationof egg-larva, pupaland egg-adultperiodsamongdifferenthostplantsmaybeassociated withthenutritionalqualityoftheirfruit.Somehostsmayhave providedresourcesforlarvaldevelopmentinamountsthatwere adequateand sufficientforcompletionofthebiologicalcyclein lesstime.Fruitsizemayalsohaveinterferedinthedurationof bio-logicalparameters,aslarvaldevelopmentcouldbeacceleratedby thelowerfoodavailabilityprovidedbysmallerfruits,asobserved forS.mombin,whosefruithadameanweightof15.86g,ninetimes lessthanE.stipitata(147.0g).Barianietal.(2016)describedrearing techniquesforB.carambolaeinthelaboratoryandreportedthatthe timeneededforegg-adultdevelopmentis22.5dayswhenlarvae arerearedonguavafruitsand19.5daysforlarvaefedan artifi-cialdiet,durationsthatareshorterthanthosereportedhere.This indicatesthatartificiallarvaldietstendtobemorenutritionally adequateforB.carambolae.
InBrazil,theexistingstudiesonB.carambolaebiologyarerecent. Jesus-Barrosetal.(2017)studiedthefecundityandlongevityof females ofB. carambolaeinthelaboratory, fed anartificialdiet atthelarvalstage(brewer’syeast,soybeanflour,sandingsugar, Nipagin,citricacid,sodiumbenzoate,groundanddriedsugarcane bagasse,anddistilledwater)andinadulthood(samedietusedin ourpresentstudy).Pre-ovipositionandovipositionperiodswere
P. guajava 80 60 40 20 0 80 60 40 20 0 80 60 40 20 0 80 60 40 20 0 1 NO. OF EGGS/DA Y NO. OF EGGS/DA Y NO. OF EGGS/DA Y NO. OF EGGS/DA Y 11 21 31 41 51 61 71 81 91 101 111 121 131 141 151 161 171 1 11 21 31 41 51 61 71 81 91 101 111 121 131 141 151 161 171 1 11 21 31 41 51 61 71 81 91 101 111 121 131 141 151 161 171 1 11 21 31 41 51 61 71 81 91 101 111 121 131 141151 161 171 AGE (DAYS) AGE (DAYS) AGE (DAYS) AGE (DAYS) A. carambola S. mombin E. stipitata
Fig.1.DailyrateofovipositionofBactroceracarambolaerearedonfruitsofcarambola(Averrhoacarambola),araza(Eugeniastipitata),guava(Psidiumguajava)andyellow mombin(Spondiasmombin).
Treatment A (Tms=92.05 a) Treatment B (Tms=57.92 b) Treatment C (Tms=95.13 a) Treatment D (Tms=83.37 ab) 0 0.0 0.2 0 .4 0.6 0.8 1.0 Estimated S(t) 50 100 Time (days) 150 200
Fig.2.SurvivalcurveoffemalesofBactroceracarambolae:TreatmentA(Averrhoacarambola),TreatmentB(Psidiumguajava),TreatmentC(Spondiasmombin)andTreatment D(Eugeniastipitata).Thearrowsindicatethemeansurvivaltime(Tms).
Treatment A (Tms = 87.2 6ab) Treatment B (Tms = 64.52 6 bc) Treatment C (Tms = 98.06 a) Treatment D (Tms = 54.02 c) 0 0.0 0 .2 0.4 0 .6 0.8 1 .0 Estimated S(t) 50 100 150 200 Time (days)
Fig.3. SurvivalcurveofmalesofBactroceracarambolae:TreatmentA(Averrhoacarambola),TreatmentB(Psidiumguajava),TreatmentC(Spondiasmombin)andTreatment D(Eugeniastipitata).Thearrowsindicatethemeansurvivaltime(Tms).
25.15daysand62.73days,respectively,andthemeanlongevity offemaleswas90.70days.Fecundityvariedovertime,withpeak ovipositiononthe28thdayandameanof1088.26eggsperfemale. InacomparisonofourworkwithJesus-Barrosetal.(2017),the onlydiscrepantfindingwasfecundity.Consideringthattheadults werefedthesamedietinbothstudies,wecanassumethatthe fruitsoftheplantspeciesusedin thisworkwereprobablyless nutritionallyrichthananartificialdiet,possiblyinterferinginthe reproductiveperformanceoftheflies.
Pasinatoetal.(2019)studiedbiologicalaspectsofB.carambolae rearedontablegrape(‘Italia’cultivar)andacerola,reportinglonger egg-larva,pupalandegg-adultperiodsforfliesrearedongrape.In thatstudy,diettypehadnoinfluenceonpre-oviposition, ovipo-sitionandpost-ovipositionperioddurations.Thenumberofeggs producedperfemalewashigherongrape(1663)thanonacerola andwashigherthanthevaluesreportedhere,whichrangedfrom 774.80eggs(onP.guajava)to176.94eggs(onE.stipitata).Among thebiologicalparametersassessedbyPasinatoetal.(2019),the strongestdiscrepancyinrelationtoourfindingsherewas fertil-ity,whichwas5.63%ongrapeand12.47%onacerola,lowerthan thelevelsobtainedinourstudy.Themethodologywasthesamein bothstudiesandsothisparametermayhavebeeninfluencedby theoriginofthefliesandaspectsrelatedtomatingbehavior.
Theegg-adultperiodsreportedhereforfliesrearedonA. caram-bolaandP.guajavaaresimilartothoseobservedbyPasinatoetal. (2019)ongrape(25.8days).For Ceratitiscapitata(Wiedemann), Krainackeretal.(1987)observedthatnutritionalqualityofthefruit isthemainfactoraffectinglarvalperformance.Inaddition,studies haveshownthatnutritionalqualitymayvarywithinasinglefruit andthisfactorismostexpressiveathighlevelsofinfestation,which leadstotheingestionoflessnutritiouspartsofafruit(Dukasetal., 2001).
Pupalviabilitywashigherforinsectsrearedoncarambolaand guava,however,thisparametercanalsobeinfluencedbyexternal factorsrelatedtotheenvironment,suchashumidity,asobserved byZart(2008).
Individuals reared on A. carambola exhibited longer pre-ovipositionperiodsthanthoserearedonS.mombinandP.guajava. Thisdifferencemayberelatedtovariousfactors,including matu-rationofsexualorgans,whichrequirestheingestionofaprotein source,asfemaletephritidsaresynovigenicandthereforerequire aprotein-richdiettopromoteoocytematurationoverthecourse oftheirlives(Tsiropoulos,1983;Zucoloto,2000).
Thepre-ovipositionperioddurationrecordedhereforB. caram-bolaeappearstobesimilartothatofotherspeciesinthesame group.FemalesofB.carambolaeobtainedfromcarambola,grape andacerolaplantsandmaintainedunderthesamelaboratory con-ditionsalsoexhibitedlongpre-ovipositionandovipositionperiods (Jesus-Barros etal., 2017;Pasinato etal., 2019),supportingthe resultsobtainedinthisstudy.
Theovipositionpatternobservedinthisworkissimilartothat reportedbyJesus-Barrosetal.(2017)andbyPasinatoetal.(2019) forthissamespecies,indicatingthatthelongovipositionperiodof B.carambolaecanexpressivelyincreaseitsdamageinthefield,and alsogivesitenoughtimetothoroughlyexploititsecologicalniche. AccordingtoGodoyet al.(2011) andMalavasiet al.(2013), femalesofB.carambolaecanlay1000–3000eggsovertheirlifetime inthelaboratory,andfrom1200to1500underfieldconditions.The meanfecundityoffemalesinthisstudywaslowerthanthelevels describedforthespecies,butneverthelessfollowedthesame pat-ternofproducinganelevatednumberofeggs. Consideringthat artificialsubstratescontainingfruitpulpwereusedforoviposition, theresultssuggest thatguavaismoreattractivetoB. carambo-lae.ForTephritidae,Broufasetal.(2009)reportedthathostquality affectsthedynamicsofovipositionandovarianmaturation.
Thehighlongevityobservedinthisstudyforfliesrearedonall thestudiedhosts(Fig.2)suggeststhatthecarambolafruitflyis abletosurviveforlongperiods,duringwhichitcannotonlycause damage,butalsoleaveagreatnumberofdescendants.Ourresults aresupportedbyJesus-Barrosetal.(2017),whoreportedsurvival upto150daysforfemalesofB.carambolae,andbyPasinatoetal. (2019),whoobservedlongevitiesofupto200and127daysforthis specieswhenrearedonacerolaandgrape,respectively.
ThisworkhasshownthatBactroceracarambolaecompletesits developmentonallfouroftheinvestigatedhosts(Psidiumguajava, Averrhoacarambola,SpondiasmombinandEugeniastipitata), con-firmingtheresultspublishedbyAdaimeetal.(2016).Also, our resultsshowthat thesefruitsare suitable forthe development ofB.carambolae,contributingtothemaintenanceandgrowthof populationsofthispestspecies.
Furtherstudiesofthisnatureneedtobecarriedoutinorder tobroadentheknowledgeofthecarambolafruitflybiologyand ecology.Additionally,resultssuchasthoseobtainedinourwork areusefulfordirectingactionstocombatthisimportantquarantine pest.
Authors’contribution
APC, RA, DEN, and CRJ conceived and designed the exper-iments and wrote the manuscript; APC, JP, JEVS, and ASC performed field and laboratory work and reviewed the manuscript.
Conflictsofinterest
Theauthorsdeclarenoconflictsofinterest.
Acknowledgments
TotheBrazilianFederalAgencyfortheSupportandEvaluation ofGraduateEducation(CAPES)fortheMaster’sDegreeScholarship grantedtoAlisonPurezaCastilho,andtotheNationalCouncilfor ScientificandTechnologicalDevelopment–CNPq,fortheResearch ProductivityFellowshipgrantedtoRicardoAdaime.ToAlexandra PeterKrüger,M.Sc.,andTiagoScheumemann,M.Sc.,forassistance withstatisticalanalysis.TotechnicalassistantJacivaldoBarbosada Costaforsupportduringfieldandlaboratorywork.TotheMinistry ofAgricultureandFoodSupplyforauthorizingpublicationofdata pertainingtothecarambolafruitfly,asprovidedinNormativeRule No.52/2007.
References
Adaime, R.,Jesus-Barros, C.R.,Bariani,A., Lima,A.L.,Cruz, K.R.,Carvalho,J.P., 2016.Novos RegistrosDeHospedeirosDaMosca-da-carambola (Bactrocera carambolae)No Estado Do Amapá. Embrapa Amapá, Comunicado Técnico 146, Macapá, Brasil, Available at: https://ainfo.cnptia.embrapa.br/digital/ bitstream/item/155953/1/CPAF-AP-2016-COT-146-Hospedeiros-mosca-v5.pdf
(Accessed12August2019).
Almeida,R.R.,Cruz,K.R.,Sousa,M.S.M.,Costa-Neto,S.V.,Jesus-Barros,C.R.,Lima,A.L., Adaime,R.,2016.Frugivorousflies(Diptera:Tephritidae,Lonchaeidae) associ-atedwithfruitproductiononIlhadeSantana,BrazilianAmazon.Fla.Entomol. 99,426–436.
Bariani, A., Jesus-Barros, C.R., Carvalho, J.P., Mota-Junior, L.O., Nascimento, P.R.,Cruz, K.R.,Facundes,V.S., 2016. TécnicasPara Criac¸ão Da Mosca-da-carambola (Bactrocera carambolae Drew & Hancock) EmLaboratório Para Pesquisa Científica. Embrapa Amapá, Documentos 97, Macapá, Available at: https://ainfo.cnptia.embrapa.br/digital/bitstream/item/157147/1/CPAF-AP-2016-DOC-97-Tecnicas-para-criacao-da-mosaca-carambola.pdf (Accessed 12 August2019).
Brasil. Ministério da Agricultura, Pecuária e Abastecimento. Instruc¸ão Nor-mativa n◦ 38, de 1 de outubro de 2018. Diário Oficial [da] República
Federativa do Brasil, Brasília, DF, 2 out. 2018. Sec¸ão 1. Available at:
http://www.in.gov.br/materia/-/assetpublisher/Kujrw0TZC2Mb/content/id/ 43461167/do1-2018-10-02-instrucao-normativa-n-38-de-1-de-outubro-de-2018-43461024(Accessed12August2019).
Broufas, G.D., Pappas, M.L., Koveos, D.S., 2009. Effects of relative humid-ity on longevity, ovarian maturation, and egg production in the olive fruit fly (Diptera: Tephritidae). Ann. Entomol. Soc. Am. 102, 70–75,
http://dx.doi.org/10.1603/008.102.0107.
Cavalcante,P.B.,2010.FrutasComestíveisNaAmazônia.MuseuParaenseEmílio Goeldi,Belém.
Cavalcante,P.B.,1996.FrutasComestíveisDaAmazônia.CNPq/MuseuParaense EmílioGoeldi,Belém.
Cavalcante,P.B.,1991.FrutasComestíveisDaAmazônia.CEJUS/MuseuParaense EmilioGoeldi,Belém.
Dukas,R.,Prokopy,R.J., Duan,J.J.,2001. Effectsof larvalcompetitionon sur-vivalandgrowthinMediterraneanfruitflies.Ecol. Entomol.26,587–593,
http://dx.doi.org/10.1046/j.1365-2311.2001.00359.x.
Falcão,M.A.,Chávez,F.W.B.,Ferreira,S.A.N.,Clement,C.R.,Barros,M.J.B.,Brito,J.M.C., Santos,T.C.T.,1988.Aspectosfenológicoseecológicosdoarac¸á-boi(Eugenia stip-itataMcVaugh)naAmazôniaCentral.I.Plantasjuvenis.ActaAmaz.18,27–38,
http://dx.doi.org/10.1590/1809-43921988183038.
Ferreira,M.E.,Rangel,P.H.N.,2015.Melhoramentogenéticopreventivo:obtenc¸ão deestoquesgenéticosresistentesapragasquarentenáriasdealtoriscoparaa agriculturabrasileira.In:Sugayama,R.L.,Silva,M.L.,Silva,S.X.deB.,Ribeiro,
L.C.,Rangel,L.E.P.(Eds.),DefesaVegetal:Fundamentos,Ferramentas,PolíticasE Perspectivas.SociedadeBrasileiradeDefesaAgropecuária,BeloHorizonte,pp. 275–292.
Godoy,M.J.S.,Pacheco,W.S.P.,Malavasi,A.,2011.Moscas-das-frutasquarentenárias paraoBrasil.In:Silva,R.A.,Lemos,W.P.,Zucchi,R.A.(Eds.),Moscas-Das-Frutas NaAmazôniaBrasileira:Diversidade,HospedeirosEInimigosNaturais.Embrapa Amapá,Macapá,pp.111–132.
GonzagaNeto,L.,2001.Importânciaeconômica,alimentaresocial.In:GonzagaNeto, L.(Ed.),Goiaba:Produc¸ão:AspectosTécnicos.EmbrapaInformac¸ãoTecnológica. Brasília;EmbrapaSemi-Árido,Petrolina,pp.13–14.
Jesus-Barros, C.R., Mota-Junior, L.O., Costa, A.S., Pasinato, J., Adaime, R., 2017. Fecundidade e longevidade de Bactrocera carambo-lae Drew & Hancock (Diptera: Tephritidae). Biotemas 30, 7–13,
http://dx.doi.org/10.5007/2175-7925.2017v30n4p7.
Krainacker,D.A.,Carey,J.R.,Vargas,R.I.,1987.Effectoflarvalhostonlifehistory traitsoftheMediterraneanfruitfly,Ceratitiscapitata.Oecologia73,583–590,
http://dx.doi.org/10.1007/BF00379420.
Lemos,L.N.,Adaime,R.,Jesus-Barros,C.R.,Deus,E.G.,2014.Newhostsof Bactro-ceracarambolae(Diptera:Tephritidae)inBrazil. Fla.Entomol.97,841–847,
http://dx.doi.org/10.1653/024.097.0274.
Lemos,L.N.,Lima,C.R.,Deus,E.G.,Silva,R.A.,Godoy,M.J.S.,2010.Novosregistros dehospedeirosparaBactroceracarambolae(Diptera:Tephritidae)noestadodo Amapá,Brasil.In:XXIIICongressoBrasileiroDeEntomologia,Natal,Resumos.
Lima, A.L., Bariani, A., Jesus-Barros, C.R., Costa, J.V.T.A., Melém-Júnior, N.J., Adaime,R.,2018. ImpactosDa PossívelDispersãoDa Mosca-da-Carambola ParaRegiõesExportadorasDeFrutasNoBrasil.EmbrapaAmapá,Nota Téc-nica 001, Macapá, Available at: https://www.alice.cnptia.embrapa.br/alice/ bitstream/doc/1098173/1/CPAFAP2018NT001Impactospossiveldispersao.pdf
(Accessed12August2019).
Malavasi, A., Midgarden, D., Meyer, M., 2013. Bactrocera species that pose a threat to Florida: B. carambolae and B. invadens. In: Pe ˜na, J. (Ed.), Potential Invasive Pests of Agricultural Crops. CABI, Homestead,
http://dx.doi.org/10.1079/9781845938291.0000.
Miranda,S.H.G.,Adami,A.C.O.,2015.Métodosquantitativosnaavaliac¸ãoderisco depragas.In:Sugayama,R.L.,Silva,M.L.,Silva,S.X.deB.,Ribeiro,L.C.,Rangel, L.E.P.(Eds.),Defesavegetal:fundamentos,ferramentas,políticaseperspectivas. SociedadeBrasileiradeDefesaAgropecuária,BeloHorizonte,pp.183–203.
Pasinato,J.,Redaelli,L.R.,Botton,M.,Jesus-Barros,C.R.,2019.Biologyandfertility lifetableofBactroceracarambolaeongrapeandacerola.Rev.Bras.Entomol.63, 217–223,http://dx.doi.org/10.1016/j.rbe.2019.06.001.
Pessoa,M.P.C.Y.,Marinho-Prado,J.S.,Mingoti,R.,Lovisi-Filho,E.,Silva,A.S.,Moura, M.S.B.,Silva-Filho,P.P.,Sá,L.A.N.,Prado,S.S.,Spadotto,C.A.,Farias,A.R.,2016. Estimativadepotencialadaptac¸ãodeBactroceracarambolaeDrew&Hancock (PragaQuarentenáriaA2):estudodecasoparadoisperímetrosirrigadosdo valedoRioSãoFrancisco.EmbrapaGestãoTerritorial,NotaTécnico-Científica, Campinas,http://dx.doi.org/10.13140/RG.2.2.26774.14401.
Pimentel-Gomes, F., Garcia, C.H., 2002. Estatística aplicada a experimentos agronômicoseflorestais:exposic¸ãocomexemploseorientac¸õesparausode aplicativos.FEALQ,Piracicaba.
Pinedo,M.,Ramirez,F.,Blasco,M.,1981.Notaspreliminaressobreelarazá(Eugenia stipitata),frutalnativodeLaamazoniaperuana.INIA/IICA,Lima.Publicación Miscelánea,pp.229.
RDevelopmentCoreTeam, 2015.R:Alanguageandenvironmentfor statisti-calcomputing.RFoundationforStatisticalComputing,Vienna,Availableat:
http://www.Rproject.org/(Accessed12August2019).
Sacramento,C.K.,Souza,F.X.,2009.Cajá.In:Santos-Serejo,J.A.,Dantas,J.L.L., Sam-paio,C.V.,Coelho,Y.S.(Eds.),FruticulturaTropical:EspéciesRegionaiseExóticas. EmbrapaInformac¸ãoTecnológica,Brasília,pp.83–106.
Silva,R.A.,Jordão, A.L.,Sá,A.L.N., Oliveira,M.R.V., 2004.Mosca-da-carambola: uma ameac¸a à fruticultura brasileira. Embrapa Amapá, Circular Técnica 31, Macapá, Available at: https://ainfo.cnptia.embrapa.br/digital/bitstream/ CPAF-AP/8417/1/Circular200431.PDF(Accessed12August2019).
Tsiropoulos,G.J.,1983.Theimportanceofdietaryaminoacidsonthereproduction andlongevityofadultDacusoleae(Gmelin)(Diptera:Tephritidae).Arch.Int. Physiol.Biochim.91,159–164.
Zart,M.,(Dissertac¸ãodeMestrado),2008.BioecologiadeAnastrephafraterculus (Wiedemann,1830)(Diptera:Tephritidae)emvideira.FaculdadedeCiências AgráriaseVeterinárias.UniversidadeEstadualPaulista“JuliodeMesquitaFilho”, Available at: https://repositorio.unesp.br/handle/11449/91339(Accessed 12 August2019).
Zucoloto,F.S.,2000.Nutric¸ãoealimentac¸ão.In:Malavasi,A.,Zucchi,R.A.(Eds.), Moscas-Das-FrutasdeImportânciaEconômicanoBrasil:ConhecimentoBásico eAplicado.Holos,RibeirãoPreto,pp.67–80.
