First record of Peridroma saucia Hübner (Lepidoptera: Noctuidae) in transgenic soybeans

RevistaBrasileiradeEntomologia63(2019)199–201

REVISTA

BRASILEIRA

DE

Entomologia

Short

Communication

First

record

of

Peridroma

saucia

Hübner

(Lepidoptera:

Noctuidae)

in

transgenic

soybeans

Tamara

A.

Takahashi

_,

_Guilherme

_Nishimura

_,

_Eduardo

_Carneiro

_,

_Luís

_A.

_Foerster

a_{UniversidadeFederaldoParaná,DepartamentodeFitotecniaeFitossanitarismo,Curitiba,PR,Brazil} b_{UniversidadeFederaldoParaná,DepartamentodeZoologia,Curitiba,PR,Brazil}

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r

t

i

c

l

e

i

n

f

o

Articlehistory: Received7June2018 Accepted31May2019 Availableonline12June2019

AssociateEditor:AdeneydeFreitasBueno Keywords:

Variegatedcutworm Btsoybean

Glyphosatetolerantsoybean

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s

t

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Thewidespreadcultivationoftransgenicsoybeanshascausedsignificantchangesinthespectrumof Lepidopteralarvae,bothinthenumberofspeciesaswellasontheirdensitiesinthefield.Transgeniccrops producingBacillusthuringiensis(Bt)insecticidalproteinshavesuccessfullyreducedtheincidenceofthe mostcommoncaterpillarsinfestingsoybeans,namelyAnticarsiagemmatalis(Lepidoptera:Erebidae)and Chrysodeixisincludens(Lepidoptera:Noctuidae).However,lepidopteranspeciesnotpreviouslyrecorded onthecrophavebeenrecentlyfound,andareofconcernduetothepossibilityofadaptationtothe geneticallymodifiedcultivars.TheoccurrenceofPeridromasauciaHübner(Lepidoptera:Noctuidae)is describedforthefirsttimeinBrazilfeedingongeneticallymodifiedsoybeancultivars.

©2019SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction

Soybean,Glycinemax(L.)Merrill(Fabaceae:Phaseoleae)isthe most important commodity crop in Brazil (Conab, 2017). The primarycaterpillarsthat attackleavesarethevelvetbean cater-pillar,Anticarsiagemmatalis(Hübner)(Lepidoptera:Erebidae)and thesoybeanlooper,Chrysodeixisincludens(Walker)(Lepidoptera: Noctuidae).Theintroductionofglyphosate-tolerantsoybeanand genetically modified insect-resistant plants which express the Cry1AcproteinfromthebacteriumBacillusthuringiensis(Berliner) (Eubacteriales:Bacillaceae),hasprovidedasatisfactorycontrolof thesepests(Bernardietal.,2012).However,insectspeciesnot sus-ceptibletotheexpressedtoxinmaydevelopintosecondarypests andcausedamagetothecrop(WuandGuo,2005;Zhaoetal.,2011; Catarinoetal.,2015).

The variegated cutworm Peridroma saucia (Hübner) (Lepi-doptera:Noctuidae)isapolyphagous,cosmopolitanspeciesthat damagesvariouscultivatedplantslikepeanuts,sunflowers, soy-beansandgrapevines(Álvarezetal.,2009).Larvaehaveavariable feeding behavior, damaging tubers underground and climbing orchard trees and attacking the fruits. In the UnitedStates the attacksofthiscutwormoccursporadicallyandinisolatedregions (Ringsetal.,1976).InTurkeyitisoneofthemostabundantand harmfulspeciesforagriculture(Yukseletal.,2018).InBrazil,the

∗ Correspondingauthor.

E-mail:tamaratakahashi@gmail.com(T.A.Takahashi).

presenceofP.sauciawasreportedbyKleseneretal.(2016)onapple orchardsinnorthernParanástate.

In South America, P.saucia is frequentlyrecorded attacking different food and ornamental plants (Quimbayo et al., 2010). InArgentinaP.sauciaisdescribedcausingdamagetoartichokes (Vasicek,1983)andalfalfa(Baudino,2004;BaudinoandVillareal, 2007).In Colombia, Fajardo and Cardona (2006) described the developmentoftheimmaturestagesandadultlongevityofP.saucia rearedduringthelarvalstageonflowersofthePeruvianlily, Alstroe-meriasp.(Alstroemeriaceae).Quimbayoetal.(2010)considerP. sauciaasoneofthemosteconomicallyimportantspeciesin Colom-biaduetoitswidedistributionandpolyphagoushabit.According toButinandPedigo(1985)larvaeofP.sauciahavenocturnalhabits, makingitdifficulttheirobservationinthefield.

WedescribeforthefirsttimeinBraziltheoccurrenceofP.saucia ongeneticallymodifiedsoybeansexpressingtheCry1Acproteinof B.thuringiensisaswellasona cultivartoleranttotheherbicide glyphosate(RRsoybean).

Materialandmethods

Thesurveywasconductedintwo14 hectare-areasof genet-ically modified soybeans in SãoJosé dos Pinhais(25◦3646.0S, 49◦0821.5W), Paranástate,BrazilbetweenJanuaryand March 2018. One area was planted with soybeans expressing toler-ance totheherbicideglyphosate,Roundup Ready® (RR)variety NA5909RGandtheotherwithvarietySyn13671IPROexpressing Cry1AcproteinofB.thuringiensis(Bt)whichconfersresistanceto https://doi.org/10.1016/j.rbe.2019.05.006

0085-5626/©2019SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http:// creativecommons.org/licenses/by-nc-nd/4.0/).

200 T.A.Takahashietal./RevistaBrasileiradeEntomologia63(2019)199–201

Fig.1. DevelopmentalstagesofPeridromasauciacollectedingeneticallymodifiedsoybeans:(A)eggs,(B)larvaeand(C)adultemergedinlaboratory(scale=1cm).

targetlepidopteranspeciesaswellastolerancetotheherbicide glyphosate.Noinsecticidetreatments weremadein bothareas, andonly fungicide(azoxystrobin+benzovindiflupyr; cyprocona-zole+difenoconazole;trifloxystrobin+protioconazole)and herbi-cide(glyphosate)wereappliedonbothareas.Samplingsweretaken weeklybythebeatclothmethod(Shepardetal.,1974)in20points withineachexperimentalarea.EggmassesandlarvaeofP.saucia weretakentothelaboratoryandindividualizedin4×7cmplastic flasksat25±2◦C,relativehumidityof60±10%and14:10(L:D) photophase.Fieldcollectedlarvaeand thosehatchedin labora-toryfromthefield-collectedeggswerefedwithRRandBtsoybean leaves;180larvae wereevaluated ineach treatment uptothe pupalstage.Afteradultemergence,mothswerekilledandpinned, andthespeciesidentifiedbasedonthespecializedbibliography (Lafontaine,2004).

Resultsanddiscussion

Duringthe2017–2018soybeancrop,38larvaewerecollected in RR and two in Bt-growing areas. Additionally, egg-masses (Fig. 1A) were collected in both areas during the vegetative (January)and reproductivestages of thecrop(January–March). Of the total collected larvae (Fig. 1B) and fed in laboratory with transgenic soybean tolerant to glyphosate (RR), 37% suc-cessfully completed larval development and reached the adult stage (Fig. 1C), 29% were parasitized, three by specimens of Hymenopteraand eight by specimens of Dipteraand 34% died ofnaturalcausesorbyentomopathogens.Bothlarvaefoundon Bt-soybeanandlarvaehatchedfromtheegg-massescollectedin thefield consumedleavesof Btsoybeansandcompleted devel-opment until the adult stage. Our results show that P. saucia can survive and reproduce on both RR and Bt soybeans, with potentialtocausedamagetothecrop.Sincetherewereno pre-viousreports of P.saucia feedingonsoybeans, it is reasonable toassumethat thespeciesis naturallytoleranttotransgenicBt

soybeans.However,therewasahighadaptativecosttothenew host,becauseoutof180larvaefeedingonRRsoybeans,97(53.9%) completedthelarvalstageandpupated,whileintheBttreatment only57(31.7%)reachedthepupalstage.Inordertoassessthe toxi-cityofthesecultivarstoasusceptiblespecies,60third-instarlarvae ofA.gemmataliswerefedontheCry1Achybrid,andtotal mortal-itywasrecordedbeforeecdysistothefourthinstar.Despitethe poorperformanceofthefirstgenerationofP.sauciaongenetically modifiedsoybeans,itispossiblethat,inthecourseofgenerations, theadaptationofthespeciestothenewhostwillbesignificantly improved.

ToleranceofinsectpeststoBtCryproteinscanimpairthe selec-tionadvantage of this technology, and favor otherspecies that aretoleranttoBtproteins.ThisisthecasewithSpodopteraspp. (Lepidoptera:Noctuidae)thatexhibitslowornosusceptibilityto Bt-soybeancontainingtheproteinCry1Ac(Bernardietal.,2014), andinsomesoybeanareasinBrazil,theyarealreadyconsidered keypestsinthecrop(Buenoetal.,2011).Whenthepopulations oftargetpestsareefficientlycontrolledbyaBttoxin,secondary non-susceptiblepestsmaybecomeprimarypests,occupyingthe ecologicalvacantnicheandusingtheavailableresource,causing significantdamage to thecrop(Wu and Guo, 2005; Gross and Rosenheim,2011).

Outbreaksofsecondarypestsareoccasionallyreportedin trans-genic soybeans in Brazil, and although they do not occur in extensiveareasanddonotcausedamageofeconomicrelevance, productionlossescanbeobservedinlocalizedareas(Buenoetal., 2011;Marquesetal.,2017).Therefore,itis necessarytosurvey thespecies and theiroccurrence along thecrop seasons, since rearrangementofprimarypestshasbeenpreviouslyrecordedin soybeans.Thiswasthecaseofthesoybeanlooper,C.includens, whichuntilthelate1990swasconsideredasecondarypest,but withthechangesinthephytosanitarymanagementofsoybeans, becameakeypestofthecrop(Moscardietal.,2012).Despitethe successincontrollingthetargetpests,thecultivationofBtsoybean

T.A.Takahashietal./RevistaBrasileiradeEntomologia63(2019)199–201 201 (Cry1Ac)alsochangedcropmanagementandmaycausechanges

inthepestpopulationovertheyears.

InformationabouttheimpactofBttechnologyonnon-target pestsisimportantforthedevelopmentofsuccessfulpest manage-mentprogramsontransgeniccrops.Morestudiesaboutthebiology ofP.sauciaareneededtoevaluateleafconsumption,development andreproductionofthisspecies.Itremainstobeinvestigatedif larvaeofP.sauciaareabletoconsumesoybeanpods

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgements

The authors thank André Valenga and Edson Kachinski for theassignmentof theexperimentalareatocarry outthework. Wethankanonymousreviewersforreadingthemanuscriptand improvingitsreadability.WeacknowledgetheCoordinationfor theImprovementofHigherEducationPersonnel(CAPES)forthe scholarshiptoT.A.T.andG.N.andtotheNationalCouncilfor Sci-entificandTechnologicalDevelopment(CNPq)toL.A.F.,andtothe teamoftheLaboratoryofIntegratedInsectControlforallaround help.

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