1
2
3
2019—FloridaEntomologist—Volume102,No.1 59
Helicoverpaarmigera
Victor Hugo Duarte da Costa1, Marcus Alvarenga Soares1,*, Francisco Andrés
Rodriguez Dimate2, Veríssimo Gibran Mendes de Sá2, José Cola Zanuncio2,
and Fernando Hercos Valicente3,*
Helicoverpaarmigera(Hübner)(Lepidoptera:Noctuidae)larvaearepolyphagous,aggressive,andhavebeenfoundinmanyofBrazil’sagriculturalareas.Biologicalcontrolwithbaculovirusesispartofanintegratedpestmanagement(IPM)strategytomanagethisinsect.Threeisolatesofnucleo
H.armigera (animportednucleopolyhedrovirus),andtoNucleopolyedrovirusspodoptera(SPNPV)thatwaspassedseriallythroughH.armigera
andlef9genesrevealedthattheBrazilianisolateswerecloselyrelatedtonucleopolyhedrovirusspeciesfromAustralia,SouthAfrica,China,andIndia.TheisolatescausedhighmortalityratesinthirdinstarH.armigeralarvae.Themeanlethaldose(LD50 50
H.armigerainBrazil.
LagartasdeHelicoverpaarmigera
áreasdeproduçãoagrícola.Ocontrolebiológicodebaculovírusfazpartedomanejointegradodepragas(MIP).Trêsisoladosdenucleopoliedrovírus
(NPV)foramcoletadosempopulaçõesbrasileirasdeH.armigera ,combaseNucleopolyedrovirusspodoptera(SPNPV)emH.armigera.Foramrealizadostestes
Austrália,Índia,ÁfricadoSuleChina.TodososisoladostestadospossibilitaramocontroledelagartasdeterceiroinstardeH.armigera.Analisesbiológicasdadoseletalmédia(DL50)edotempoletalmédio(TL50)variaramentreosisoladostestados.OisoladoHearNPVBR2apresentouos
H.armigeranopaís.
Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) is apolyphagous insect, and one of the most important agriculturalpestsworldwide(Cunningham&Zalucki2014).Itslarvaepreferentiallyfeedonthereproductivestructuresofagriculturalplants(Fitt
H.armigera areestimated tobemorethan$2billionannually,inadditiontosocioeconomicandenvironmentalcosts(Tayetal.2013).HelicoverpaarmigeranowhasspreadthroughmostofBrazil,and ispresent inParaguayandArgentina,andrecentlywasdetected(thoughnotestablished)inFlorida,USA
al.2014;Hayden&Brambila2015).
Bacillus thuringinsis (Bt)proteins,
ofH.armigera
inAustralia,China,andIndia(Tabashniketal.2009;Liuetal.2010;
usedforbiologicalcontrol(Rollieetal.2013).Baculovirusbasedin
2019—FloridaEntomologist—Volume102,No.1
pestssuchas Hübner(Lepidoptera:Erebidae)
andCydiapomonella(Linnaeus)(Lepidoptera:Tortricidae)(Moscardi
doetal.2000;Chenetal. 2002;Arrizubietaetal. 2013).This is es
more,Haaseetal.(2015)reportedthatthesearchforlocalisolatesis
uctsbasedonforeignisolateshavebeenregisteredforcommercialuse
againstH.armigera
H.armigeralarvae.
LarvaeofH.armigerawereobtainedfromtheBiologicalControl
LaboratoryofAppliedBiologyCenter“EmbrapaMilhoeSorgo”inSete
25±2°C,with70±10%RH,anda12:12h(L:D)photoperiod,andfed
Fivevirusisolateswereobtained;3werefromH.armigeralarvae,
Threelarvae(1collectedinFeb2013and2inApr2014)showedbe
insectsdiedwithinafewdoftheintegumentrupturing.Theother2
LC,ef
H.armigera(HzSNPV)orBaculovirusspodop
teraSpNPVBR4.Onewasconsideredthereference isolate,whereas
theotherwasobtainedbyserialpassageofaBaculovirusspodoptera
SpNPVBR4throughH.armigera
SpodopterafrugiperdaSfNPV,which
wasisolatedfromSpodopterafrugiperdaSmith&Abbot(Lepidoptera:
Noctuidae) larvae,wasobtained fromthe“EmbrapaMilhoeSorgo”
baculovirusbank,andsprayedoncornleavescontainingH.armigera
H.armigerapopula
larvalmortality in the third passage, andwas thereforeused in the
bioassays.
H.armigera
9polyhedrapermLper
obtainedfromthisstepwereusedinthebioassays.
encesofthe“UniversidadedeBrasília”inBrasilia,DistritoFederal,Brazil.
totheBasicProgramLocalAlignmentSearchTool(BLAST)(Altschuletal.
ment. The alignments were trimmed to the size of the partial
4(Tamuraetal.2011).Thetreeswerebuiltby1,000replicatesof
stepwiseaddition.
HELI
COVERPAARMIGERALARVAE
H. armigera larvaewereheldwithout food
3 4 5 7 polyhedra
minedinadvanceusingahemocytometer(Neubauerchamber,Kasvi,
pathogen.Eachtreatmenthad32larvae.Controlleafdiscsweretreat
.Helicoverpaarmigeramortality
hosts(Rowleyaetal.2011).
Isolated Insectspecies
HearNPVBR1 Helicoverpaarmigera
HearNPVBR2 Helicoverpaarmigera
HearNPVBR3 Helicoverpaarmigera
SfNPVBR4 Spodopterafrugiperda Cascavel,Paraná,Brazil
Helicoverpazea USA,imported
Costaetal.:BaculovirusHearNPVfromHelicoverpaarmigera
Themedian lethaldose (LD50)wascalculated foreach isolateus
(LT50
polyhedrapermL.Thiswasthelowestdosedeterminedto
isolates.
is closely related tobaculovirusHearNPVofother regions.BR1 (Ac
relatedtonucleopolyhedrovirusfromAustralia(HearNPVAus,Acces
(AccessionNos.MF542297andMF542301)wascloselyrelatedtonu
cleopolyhedrovirusfromSouthAfrica(HearNPVNNg1,AccessionNo.
AP010907.2),HearNPVAus,HearNPVCI(AccessionNo.AF303045.2),
notrelatedtoanyHearNPV,butwascloselyrelatedtoisolatedcontrol,
nucleopolyhedrovirus from India (HearNPVFaridkot, Accession No.
KM357512.1)(Fig.1).
HELICOVERPAARMIGERALARVAE
H.
armigera
ages.TheLD50
4 4 4 5,and5
theLD50
TheBR3andBR4isolatesshowedhigherlimits,withvaluesabovethe
virulentbasedonassessmentofmortality.
TheLT50valuerangedfrom7to10d.WiththeBR1andBR2isolates,
curvereachedLT50
,BR3,andBR4iso
encesbetweentheisolatesintermsofLT50values,withfasterreplica
TherecentpresenceofH.armigerainBrazilindicatesthatitmay
2013;Costaetal.2015),commonlycollectedduringpestoutbreaks,
world(Wyckhuysetal.2013;Luoetal.2014).Naturallyoccurringiso
latesofpathogenicH.armigerabaculovirusinBrazilcouldallowforthe
inSpain(Arrizubietaetal.2013),China(Luoetal.2014),andAustralia
H.armigera
manceforbiologicalcontrol(Coryetal.2005;Baillie&Bouwer2012).
virusisolates,asreportedforthoseusedinChinaagainstH.armigera
(Tangetal.2012).
The high degree of relatedness among BrazilianH. armigera vi
rus isolates and those of Australia (HearNPVAus), China (HearNPV
H.armigerainBrazil.
HearNPVbaculovirushadnotbeenreportedpreviouslyinthiscountry,
andthereforetheymayhavebeenintroducedbyH.armigerapopula
pest indicates that thesemicroorganisms and their insect hosts can
overcome geographical barriers and colonizenewhabitats (Mazzi&
hedrovirusshowsthattheywereintroducedbyvariousmeans,asre
portedforH.armigera
H.armigera
Thenaturaldispersionofbaculovirusispossibleduetotheirability
al.2010).Thisoccurswhenvirusesareingestedatsublethalconcen
diseasesigns(Burdenetal.2003;Cory&Myers2003).Thelatentvirus
The tree is drawn to scale,withbranch lengthsmeasured in thenumberof
2019—FloridaEntomologist—Volume102,No.1
imposedonH.armigera
Bom
byxmori(L.)(Lepidoptera:Bombycidae)larvaewithadultsproducing
progenyinfectedwiththesameisolateastheirancestors(Khuradet
al.2004).Similarly,30.9±2.9%H.armigeraprogenywereinfecteddue
dosesofPlodiainterpunctella(Hübner)(Lepidoptera:Pyralidae)virus
(Burdenetal.2002).
TheBR4isolatemayhaveoriginatedfromalatentbaculovirusac
H.
armigera
Mam
estrabrassicae(L.)(Lepidoptera:Noctuidae)whenalatentbaculovirus
Autographacalifor
nica(Speyer)(Lepidoptera:Noctuidae)nucleopolyhedrovirusisolates
rusisolatesofM.brassicae)](Hughesetal.1993).Ontheotherhand,
ity of the alphabaculovirus isolated fromdead Lymantria dispar (L.)
tobaculoviruspreviouslyisolatedfromLymantriamonacha(L.)(Lepi
doptera:Lymantriidae).
VirusisolatescausedthirdinstarH.armigeralarvalmortalityatthe
evaluateddoses.AnalysisofLD50valuesindicatedthattheBR2isolate
wasmorevirulentascomparedwiththeotherisolates.TheLD50values
were similar to those reported in screening tests for biological pest
controlprogramsofH.armigerainSpain(Arrizubietaetal.2013).The
H.armigeraissimilartothatreportedin
virusisolates(Ogemboetal.2005;Arrizubietaetal.2013).
H.armigeralar
drovirusisolatesareinaccordancewithresultsofbaculovirusstrains
collectedintheIberianPeninsulaonsecondinstarH.armigeralarvae,
whichshowedthattheisolateHearSNPVSP1causedmorerapidmor
talitythantheotherIberianstrainstested(Arrizubietaetal.2013).
H.armigerainBrazilim
latesinH.armigera
H.armigera.
dePessoaldeNívelSuperior(CAPES),”“ConselhoNacionaldeDesen
EstudosFlorestais(IPEF)forfundingandsupport.
HelicoverpazeasinglenucleopolyhedrovirusisolatedinHelicoverpaarmig
era
ResponsedoseandmortalityofthirdinstarHelicoverpaarmigera(Lepidoptera:Noctuidae)larvaewithnucleopolyhedrovirusisolates.
Isolate N Slope±SE X² LD50
Range P df
192 4 4 5 <0.001 4
BR1 192 4 4 5 <0.001 4
BR2 192 4 4 4 <0.001 4
BR3 192 5 5 <0.001 4
BR4 192 5 5 <0.001 4
50
thelowestandthehighestvalueforLD50;P
SurvivalcurvesofHelicoverpaarmigera
feedingoncornleavesinoculatedwith1×10 polyhedrapermLofbaculovirusLC,BR1,BR2,BR3,BR4,andincontrolobtainedwithKaplan
Costaetal.:BaculovirusHearNPVfromHelicoverpaarmigera
hedrovirus isolatefromHelicoverpaarmigeraasthebasis forabiological
Helicoverpa
armigera
Spodopterafru
giperda
Plodiainterpunc
tella
Spodopteraexiguanuclearpoly
Helicoverpa zea and Helicoverpa armigera
CostaVHD,SoaresMA,RodriguezFAD,ZanuncioJC,SilvaIM,ValicenteFH.2015.
Nomuraea rileyi (Hypocreales: Clavicipitaceae) in Helicoverpa armigera
CraveiroSR,MeloFL,RibeiroZMA,RibeiroBM,BáoSN,InglisPW,CastroMEB.
2013.Pseudoplusiaincludens
ty,phylogenyandhypervariabilityofthepif2gene.JournalofInvertebrate
CunninghamJP,ZaluckiMP.2014.Understandingheliothine(Lepidoptera:He
liothinae)pests:whatisahostplant?JournalofEconomicEntomology7:
edoccurrenceofHelicoverpaarmigera(Hübner)(Lepidoptera:Noctuidae)
Helicoverpaarmigera
Heliothis
ofTrichoplusiani
Spodoptera
frugiperda
Hayden JE, Brambila J. 2015. Pest alert: the Old World bollworm. (online)
lovirusresemblingMamestrabrassicaenuclearpolyedrosisvirusinM.bras
sicae
Khurad AM, Mahulikar A, Rathod MK, Rai MM, Kanginakudru S, Nagaraju J.
Bom
byxmori
forcontrolofCydiapomonella
LeiteNA,AlvesPereiraA,CorrêaAS,ZucchiMI,OmotoC.2014.Demograph
Helicoverpazea)
andtheOldWorldbollworm(Helicoverpaarmigera)inBrazil.PLoSONE9:
He
licoverpaarmigera(Lepidoptera:Noctuidae)innorthernChina.PestMan
lovirusonthetomatomothLacanobiaoleracea.Journalof Invertebrate
MazziD,DornS.2012.Movementofinsectpestsinagriculturallandscapes.
Cabbage looper
(Lepidoptera: Noctuidae) lines to a nuclear polyhedrosis virus. Environ
Spodopteraexiguanucleopolyhedrovirus.Bio
Helicoverpaarmigera(Lepidoptera:
bollworm,Helicoverpaarmigera
nucleopolyhedrosisvirusthroughanalternatehostsystem.Entomophaga
alphabaculovirusisolatedfromdeadLymantriadisparlarvaeshowshigh
Lymantriamo
nacha
droviruscontrolwithresistanceforBacillusthuringiensis
crossresistancestudieswiththediamondbackmoth,Plutellaxylostella.
ppat.1003729]
worm,Spodopterafrugiperda
ofnucleopolyhedrovirusesisolatedworldwidefromtheheliothinepests
Helicoverpaarmigera,Helicoverpazea,andHeliothisvirescens.Journalof
Helicoverpaarmigera(Lepi
TabashnikBE,VanRensburgJBJ,CarriereY.2009.Fieldevolvedinsectresis
TakatsukaJ,OkunoS,IshiiT,NakaiM,KunimiY.2007.Hostrangeoftwomul
Spodoptera litura.Biological
cleopolyhedrovirusisolatedfromHelicoverpaarmigera.VirologyJournal
2019—FloridaEntomologist—Volume102,No.1
New World for an Old World pest: Helicoverpa armigera (Lepidop
VilaplanaL,WilsonK,RedmanEM,CoryJS.2010.Pathogenpersistenceinmi
nandezLM.2013.Currentstatusandpotentialofconservationbiological
Helicoverpa
armigera
ZhouM,SunX,SunX,Vlak JM,HuZ,vanderWerfW.2005.Horizontaland
Helicoverpaarmigera
singlenucleocapsidnucleopolyhedrovirus. Journalof InvertebratePathol
