REVISTA
BRASILEIRA
DE
Entomologia
AJournalonInsectDiversityandEvolution w w w . r b e n t o m o l o g i a . c o m
Systematics,
Morphology
and
Biogeography
First
record
of
Cotesia
scotti
(Valerio
and
Whitfield,
2009)
(Hymenoptera:
Braconidae:
Microgastrinae)
comb.
nov.
parasitising
Spodoptera
cosmioides
(Walk,
1858)
and
Spodoptera
eridania
(Stoll,
1782)
(Lepidoptera:
Noctuidae)
in
Brazil
Josiane
Garcia
de
Freitas
a,
Tamara
Akemi
Takahashi
b,
Lara
L.
Figueiredo
a,
Paulo
M.
Fernandes
a,
Luiza
Figueiredo
Camargo
c,
Isabela
Midori
Watanabe
d,
Luís
Amilton
Foerster
e,
José
Fernandez-Triana
f,
Eduardo
Mitio
Shimbori
g,∗aUniversidadeFederaldeGoiás,EscoladeAgronomia,SetordeEntomologia,ProgramadePós-Graduac¸ãoemAgronomia,Goiânia,GO,Brazil bUniversidadeFederaldoParaná,SetordeCiênciasAgrárias,ProgramadePós-Graduac¸ãoemAgronomia–Produc¸ãoVegetal,Curitiba,PR,Brazil cUniversidadeFederaldeSãoCarlos,ProgramadePós-Graduac¸ãoemEcologiaeRecursosNaturais,SãoCarlos,SP,Brazil
dUniversidadeFederaldeSãoCarlos,DepartamentodeEcologiaeBiologiaEvolutiva,SãoCarlos,SP,Brazil eUniversidadeFederaldoParaná,DepartamentodeZoologia,Curitiba,PR,Brazil
fCanadianNationalCollectionofInsects,Ottawa,Canada
gUniversidadedeSãoPaulo,EscolaSuperiordeAgricultura“LuizdeQueiroz”,DepartamentodeEntomologiaeAcarologia,Piracicaba,SP,Brazil
a
r
t
i
c
l
e
i
n
f
o
Articlehistory:Received3December2018 Accepted6May2019 Availableonline27May2019 AssociateEditor:RegianeBueno Keywords: Biologicalcontrol Bt Parasitoid Pest Taxonomy
a
b
s
t
r
a
c
t
ThisisthefirstreportofCotesiascotti(ValerioandWhitfield)comb.nov.inBrazil,attackinglarvaeofthe blackarmyworm,Spodopteracosmioides,andthesouthernarmyworm,S.eridania.Themothlarvaewere foundrespectively,infestingaprotectedcroppingoforganictomatoinHidrolândia,Goiás,Brazil,anda transgenicsoybeancropinSãoJosédosPinhais,Paraná,Brazil.Biological,molecularandmorphological characterswereusedtoconfirmtheidentityofthespecimens.Parasitoididentificationpresenteda challengesincethespecieshasmostdiagnosticcharactersofthegenusCotesiaCameron,butfewin thepoorlydefinedgenusParapantelesAshmead.Basedonmorphologicalandmolecularevidence,we transferParapantelesscottitothegenusCotesia.Thenewcombinationisdiscussedbycomparisonwith morphologicallysimilarspeciesandavailablemoleculardata.
©2019SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction
The genus Spodoptera Guenée (Lepidoptera, Noctuidae, Amphipyrinae)comprises 31valid species (Pogue, 2002,2011), commonlyknownas‘armyworms’.It hasacosmopolitan distri-butionwithhigherdiversityfoundinthetropicsandsubtropics (Pogue,2002).MostoftheNewWorldspecieswithknownhosts are polyphagous on dicots, with the exception of Spodoptera frugiperda,commonlyknownas thefallarmyworm,which also feeds on monocots (Kergoat et al., 2012). Roughly half of the knownspecies are importantor even key pests inseveral cul-tivatedplants. Thisstatus can,in great extent,beattributedto theirhighbiotic potentialand polyphagy,frequentlyleadingto
∗ Correspondingauthor.
E-mail:shimbori@gmail.com(E.M.Shimbori).
populationoutbreaks.Theimportance ofsomespecies aspests isaggravatedbynaturaltoleranceorresistancetosomeCryand Vip3AproteinsofBacillusthuringiensis(Bt)Berliner(Eubacteriales: Bacillaceae)expressedintransgenicplants (Luttrelletal.,1999; Bernardietal.,2014;Horikoshietal.,2016).
Theblackarmyworm,Spodopteracosmioides(Walk,1858),isa polyphagousspecies,nativeofSouthAmerica,feedingonagreat varietyofcultivatedandnativeplants.InBrazil,itisapeston sev-eralcrops,especiallypineapple(seedlings),cotton(bolls),rice,and soybean(leavesandpods).SpechtandRoque-Specht(2016)list126 speciesin40differentplantfamiliesashostsforS.cosmioides,being Solanaceae(with15spp.)andFabaceae(14spp.),thefamilieswith mostspeciesrecorded.PreviousrecordsofS.cosmioidesfeedingon tomatocropsaregivenbyBiezankoetal.(1974),Pastrana(2004) andSilvaetal.(1968).Thesouthernarmyworm,Spodoptera erida-nia(Stoll,1782),occursthroughouttheAmericas,andisrecorded fromasmanyas202hostplantspecies,in58families(Montezano
https://doi.org/10.1016/j.rbe.2019.05.001
0085-5626/©2019SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisis anopenaccessarticleundertheCCBY-NC-NDlicense(http:// creativecommons.org/licenses/by-nc-nd/4.0/).
etal.,2014),beingAsteraceaeandFabaceaethemostfrequently recordedhosts(with20and19speciesrespectively).Itisreported aspestformanycrops,beingcottonandsoybeanthemost econom-icallyimportantinBrazil(Parraetal.,1977;Quintelaetal.,2007; Santosetal.,2005).
Alargenumberofdipteranandhymenopterousparasitoidsare knowntoattackspeciesofthegenusSpodoptera,inallimmature stagesofdevelopment.Molina-Ochoaetal.(2003)listedca.150 speciesparasitizingthefallarmyworm,ofwhich86aredescribed fromSouthAmerica.ComparedtoS.frugiperda,literatureon par-asitoidsof S.cosmioidesandS.eridania isscarcer,especially for theformer.Mostoftheparasitoidwasps(Hymenoptera)reported forthesetwospeciesareeitherhighlypolyphagous(e.g.Yuetal., 2016;Zachéetal.,2012)and/orassociatedwithS.frugiperdaas well(seeMolina-Ochoaetal.,2003).Forinstance,severalstudies report theegg parasitoidTelenomus remus Nixon, 1937 (Platy-gastridae)asapotentialbiologicalcontrolagentforthesethree Spodopteraspecies (Bortolotto etal., 2014;Goulartet al.,2011; Pomari et al., 2013).Larval parasitoids for S. cosmioides and S. eridaniaaremostlyrestrictedtoafewIchneumonoideaandone Eulophidae (Hymenoptera) species, all of them also associated withS.frugiperda (Capinera,2018;Tingleet al.,1978;Yuetal., 2016and referenceswithin). For Ichneumonoideathis includes theBraconidae:MeteorusautographaeMuesebeck,1923,Meteorus laphygmaeViereck,1913(Euphorinae),ChelonustexanusCresson, 1872(Cheloninae),Cotesiamarginiventris(Cresson,1865) (Micro-gastrinae),Aleiodeslaphygmae(Viereck,1912)(Rogadinae)forS. eridania,andAleiodesvaughani(Muesebeck,1960)(Rogadinae)for S.cosmioidesandS.eridania;andtheIchneumonidae:Campoletis flavicincta(Ashmead, 1890) (Campopleginae) (but seeCamargo etal.,2015foradiscussiononidentityofC.flavicinctaand Cam-poletis sonorensis (Cameron 1886), Ophion Fabricius, 1798 spp. (Ophioninae),andEiphosomadentator(Fabricius,1804) (Cremasti-nae),forS.eridania.
Microgastrinae(Hymenoptera,Braconidae)isthesecondlargest subfamilyofbraconids,andthesinglemostimportantgroupof par-asitoidsofLepidoptera,withmorethan100speciesbeingusedin biologicalcontrolprogramsworldwide(Whitfield,1997).Despite their ecological and economic importance, the majority of the speciesisstillunknown,andthelimitsofmanyofitsgeneraare blurredastheyaredefinedbyfewdiagnosticcharacters(Whitfield etal.,2018a).ThegenusCotesiaCameron,1891isoneofthelargest in Microgastrinae, withabout 300species described (Yu et al., 2016).Currently theirdiversity isconcentrated intheHolarctic region,wherespeciesaresomeofthemostcommonparasitoids ofmacrolepidopteranlarvae(Whitfieldetal.,2018b).Their impor-tanceasbiologicalcontrolagentsiswellillustratedbythebiological controlprogram withCotesia flavipesCameron,1891; imported fromtheOrientalregionforthecontrolofthesugarcaneborer, Dia-traeasaccharallis(Fabricius,1794)(Lepidoptera,Crambidae),this isconsideredthemostsuccessfulexampleofbiologicalcontrolin Brazil(Parra,2014).OtherexamplesintheNewWorldincludethe controlofthecabbagemoth,Pierisrapae(L.,1758)(Lepidoptera, Pieridae),byCotesiaglomerata(L.,1758)andCotesiarubecula (Mar-shal,1885),andthecontrolofthegypsymoth,Lymantriadispar(L., 1758)(Lepidoptera,Erebidae)byCotesiamelanoscela(Ratzeburg, 1844)(Vailetal.,2001).AllsevenspeciesofSpodopterarecordedas hostsforCotesiaintheNewWorldareparasitizedbyC. marginiven-tris,includingS.eridaniaandS.frugiperda.Thereisoneadditional recordofC.congregataonS.frugiperda(Yuetal.,2016),andanother twoexoticspeciesinthesamehost(Molina-Ochoaetal.,2003). Here,wepresentataxonomiccontributionandnewhostrecords fora potentiallyimportantbiological controlagentoftheblack armyworm,S.cosmioides,andthesouthernarmyworm,S.eridania.
Materialandmethods Sampling
AlargepopulationofS.cosmioideswasobservedinanorganic protected cropping of tomato – Lycopersicum esculentum Mill (Solanaceae) – at Fazenda Orgânica Nossa Senhora Aparecida, Hidrolândia,Goiás,Brazil(16◦5758S;49◦1113W), intheyear 2017.FromAugustofthatyear,manycaterpillarsproducedcocoon masses typicalof microgastrineparasitoids(Hymenoptera, Bra-conidae).Samplingofcaterpillarswasperformedweekly,untilthe endoftheoccurrenceofthetargetinsect.Thesamplesweretaken atrandom,walkinginsidethegreenhousewherethecaterpillars werehand-collectedandtakentotheEntomologyLaboratoryofthe PlantProtectionDepartmentoftheSchoolofAgronomyatthe Fed-eralUniversityofGoiás.Larvaewerekeptinindividual9×12cm plasticcontainersandfedwithtomatoleavesuntilemergenceof adultmothorparasitoid.Alongwiththecollectionofcaterpillars wealsocollectedcocoonmassesoftheparasitoidwhichweretaken tothelaboratoryuntiladultwaspsemerged.
Asurveyof caterpillarsandtheirlarvalparasitoidswas con-ducted in soybeans, Glycine max (L.) Merrill (Fabaceae) in the municipalityofSãoJosédosPinhais,Paraná,Brazil.Thecropwas sampledduringthe2016/2017season(fromJanuary4to Febru-ary 15, 2017), in an areaof approximately12ha(25◦3644.68 S 49◦0817.31 W) planted with the cultivar Syn13671 IPRO expressingtheCry1ActoxinfromB.thuringiensis.Samplingswere performed in ten random points using the beat cloth method (Shepardet al.,1974).Thecollectedcaterpillars were individu-alizedin3×7cmpolyethylenecontainersandfedwithsoybean leavesfromthesamecultivarinwhichtheywerecollected.Atotal of37 Spodopteracaterpillars werecollect;nineS.cosmioides,of whichsevenwereparasitized,and28S.eridania,20ofwhichwere parasitized.FromtheS.eridanialarvaecollected,asingleonewas parasitizedbyC.scotti.
Adult parasitoidswerepreservedin96% alcoholfor identifi-cation. Part of thematerial wasmounted and morphologically identified using keys to genera (Whitfield, 1997) and species (Muesebeck,1921;Papp,1987;Sharkeyetal.,2005;Valerioetal., 2009).For comparisonswithmost similarspecies inthe genus Cotesia, original descriptions and authenticated specimens (i.e. specimensidentifiedandcomparedwithholotype)wereexamined forallspecimenscitedinthediscussion.Authenticatedspecimens aredepositedattheCanadianNationalCollectionofInsectsand Arachnids(CNC),Ottawa,Canada.FivefemaleswereusedforDNA extractionandthenmounted.Thestudiedmaterialwasdeposited atColec¸ãoEntomológicadoDepartamentodeEcologiaeBiologiada UFSCar(DCBU),SãoCarlos,SP,andMuseudeEntomologiaESALQ (ESALQ),Piracicaba,SP,bothinBrazil.Colorimageoftheadult par-asitoidwascapturedwitha3MPLeicavideocameraandaLeica M205C stereomicroscope running LeicaApplication Suite (LAS) software,and focus-stackedusingthesamesoftware.Greyscale imagewastakenusingaScanningElectronicMicroscopeFEIQuanta 250.Caterpillarswerechosenfromamassrearing,atthe Labo-ratóriodeControleIntegradodeInsetosintheUniversidadeFederal do Paraná, and photographed usingSony Cyber Shot30x opti-calzoom.Picturesofcocoonmassesbeforeparasitoidemergence weretaken,attherearingsite (Fig.4);thecocoonmassreared fromS.eridania(Fig.2)wasphotographedusingaLeicaTMDMC
4500videocameraattachedtoaLeicaM205CwithaPlanapo1.0× objective,usingLeicaLAS(LeicaApplicationSuiteTMversion3.7)
MicrosystemsandthesoftwareSyncroscopy®Auto-montagePro® version5.03.0040.Minoradjustmentsinimagesandplate prepa-rationwereperformedinAdobePhotoshopversionCS4.
Laboratoryprocedures
GenomicDNAwasextractedfromwholewaspusingDNeasy Blood&TissueKit (QIAGEN Inc., Valencia,California) following manufacturer’sinstructions.SubsequentDNApurificationwas per-formedbyEthanolPrecipitation(SambrookandRussell,2001)and thenDNAextractswereresuspendedin50LofTEBuffer.COI fragmentbelongingtothebarcodinglocuswasamplifiedusing the universalLCO 1490 and HCO 2198primers (Folmer et al., 1994).PolymeraseChainReactionwascarriedin25uLfinalvolume (2.5mMMgCl2,2.5mMdNTPMix,0.2Meachprimer, 1×HOT
FIREPol® BufferB1and1UHOTFIREPol® DNAPolymerase,Solis Biodyne)andfollowedacyclingprocessofinitialdenaturationat 95◦Cfor15min;35cyclesofdenaturationat95◦Cfor45s, anneal-ingat56◦Cfor30sandextensionat72◦Cfor1min;andfinally afinal extensionat72◦Cfor 5min.PCRproductswerepurified byPEG(PolyethyleneGlycol)precipitation(LisandSchleif,1975) andsequencedatCentrodePesquisasobreoGenomaHumanoe Células-TroncoinUniversidadedeSãoPaulo,SãoPaulo,Brazil.
Sequenceanalyses
Sequenceswere edited using theprogram Sequencher 4.14, and then aligned and analyzed with all sequences of Cotesia andParapanteleswhichwereidentifiedatspecieslevelfoundon BOLD(BarcodeofLife Data System,http://v4.boldsystems.org/). ThealignmentwasmadeusingMAFFTversion7andthe phylo-geneticanalysisusingtheprogramMegaX(Kumaretal.,2018).A maximumlikelihood(ML)treewasreconstructedwiththesedata usingtheGeneralTimeReversible (GTR,Nei and Kumar, 2000) evolutionarymodel, which wasfound asthe most appropriate modelofnucleotidesubstitutionforourdatasetbyhierarchic like-lihoodratio testin MEGAX(−lnL=10642.625, BIC=27059.765, AIC=22258.441).Ageneticdistances tablewasgeneratedbased onthep-distancemodelwiththeprogramMEGAX(Kumaretal., 2018)forbetterspeciescomparison.WealsorefertotheBarcode IndexNumber(BIN)Systemtodiscussspecieslimits,followingthe BINconceptdetailedbyRatnasinghamandHebert(2013).
Resultsanddiscussion
Parasitoidswereobservedin98lastinstarcaterpillarsofS. cos-mioides(Fig.3)feedingontomato,whichdiedaftertheparasitoid larvaelefttheirbody.Soonafterleavingthebodyofthehost,the larvaebegan toformcocoonmassesinvolvingthebodyofeach caterpillar(Fig.4).Thepupalphaseoftheparasitoidlastedon aver-agefivedaysandanaverageof94.67±4.46pupae(varyingfrom 20to272)wereformedineachcocoonmassoftheparasitoidper caterpillar,with98% emergence.Fromtheemergedadults, 81% werefemalesand19%males.
ThesingleindividualofS.eridania(Fig.1)parasitizedwas col-lectedfromasoybeancropandyielded25cocoons(Fig.2),with emergenceof24femalesand1male.
AcomparisonofCOIsequences,usingtheBLASTtoolon Gen-Bank,retrieveda99%similaritywithParapantelesscottiValerioet al.,2009(Hymenoptera,Braconidae)(Fig.7).Theidentificationtool inBOLDSystems,alsoconfirmedtheidentityofourspecimensas P.scotti,with99.64–99.66%similaritywithotherpublicsequences withatleast500bp.OursequencesareclearlywithinaBINcluster (BINBOLD:AAB9141)formedexclusivelybyP.scotti(31sequences fromspecimensfromCostaRicaandArgentina).Treebased identi-ficationtoolalsoshowsthatallclosersequencesbelongstospecies ofCotesia.TheclosestBINwithsequencesdepositedinBOLD(BIN BOLD:ABZ0768)corresponds to Cotesia orobenae (Forbes, 1883)
(2.84%distance),agregariousparasitoidwhichattacksEvergestis rimosalis(Guenée,1854)(Pyralidae)inU.S.A.(Yuetal.,2016).
Results of the analyses of the five barcoding sequences of specimens parasitizing S. cosmioides (Genbank accession num-bers:MK239190,MK239191,MK239192,MK239193,MK239194), plusonebarcodingsequencefromspecimensonS.eridania (Gen-bankaccessionnumber:MK239195)retrievedvirtuallyidentical sequenceswhichareonly0.3-0.4%differentfromtheCOIsequence ofP.scotti(Table1 –SupplementaryAppendix).Themaximum likelihood(ML)treeincludingallgeneratedsequencesisshowed inFig.5,whiletheEstimatesofEvolutionaryDivergencebetween Sequences(Tamuraetal.,2011)withsamedataisshowninTable 1.
Amorphologicalidentification,followingValerioetal.(2009) wasperformed and theidentity of thespecies confirmed as P. scotti.MorphologyofcocoonmassescomparedwithphotosinACG Database(JanzenandHallwachs,accessJuly2018)alsoconfirmed identityofthenewlyrearedspecimens.Confirmationofthespecies, however,raisedthequestionofthegenericboundariesfor Para-pantelesandCotesia.Thisquestionwasacknowledgedandbriefly commentedbytheauthorsofP.scotti,mainlybecausethatsame specieswaspreviouslytreatedasCotesiasp.‘whitfield14’bySmith etal.(2008).Unfortunately,Valerioetal.(2009)refrainedto dis-cusstheirdecisiontodescribethisspeciesinadifferentgenus.It alsohappenstobethecaseforParapantelesmariae(Valerioetal., 2009),evidencingthedifficultyinseparatingtheaforementioned twogenera.Ourmolecularresults,aswellasthosepresentedby Smithetal.(2008),corroboratetheplacementofP.scottiinCotesia. ThegenusParapantelesispoorlydefined,andtheonlyavailable phylogenydoesnottestitsmonophyly(Whitfieldetal.,2002). Nev-ertheless,thegenusisrepeatedlyrecoveredascloselyrelatedto Hypomicrogaster,ratherthanCotesia,inmolecularand morpholog-icalanalyses(BanksandWhitfield,2006;Whitfieldetal.,2002). Contradictingresultsofthesepapers,P.scottiishardlydifferent fromCotesiaspecies,buteasilydistinguishedfromany Hypomi-crogaster. Based onthe definition of Parapanteles presented by Valerioetal.(2009),andonthemorphologymatrixinWhitfield etal.(2002),thereareupto13charactersseparatingParapanteles andCotesia.ForP.scotti,statesofatleastsixofthosecharacters aretheonesfoundinCotesia(e.g.:absenceofsublateralhairson metanotum–Fig.6),andfourcharactersareunknownor inter-mediate.Onlythreecharacterscouldjustifytheplacement ofP. scottiinParapanteles,allofthemonthepropodeum:presenceof propodealareola, presenceof transversecarina,and absenceof medianlongitudinalcarina(Fig.6).Infact,allkeysforgenera sep-arateParapantelesfromCotesiabythepresenceofawell-defined areolaonpropodeum(e.g.AustinandDangerfield,1992;Whitfield, 1997).However,areolaandtransversecarinaonpropodeumare difficulttoseeinP.scottiduetothestrongsculpturingonthis scle-rite.Morphologyofthecocoonmasses,whicharerelativelylarge andcoveredbyafluffysilkinP.scotti(Figs.2,4),unlikeusualmasses producedbyCotesia,couldbeaninformativecharacterfor distinc-tion.Thepossibilityofmisidentificationisanimportanttaxonomic issuethat needsattention,especially regarding theNeotropical fauna.Here,basedonmorphologyofadults andmoleculardata (Fig.7)wetransferParapantelesscottitoCotesiascotti(Valerioetal., 2009)comb.nov.
All sequences in BOLD cluster as a unique BIN (BIN BOLD:AAB9141; average distance: 0.16% p-dist), which trans-lates as a putative species according to a clustering algorithm (RatnasinghamandHebert,2013),andthereforecorroboratesthe hypothesisofthisspeciesasadistinctentitywithinCotesia.This aloneis notsufficientevidencetoseparateC.scotticomb.nov. fromotherCotesiaspecies,sincenotallofthemhavesequences depositedinthisdatabase.Cotesiaorobenaeistheclosestmatchfor C.scotti,butthetwospeciesdiffersignificantlyintheirbarcodes
Figs.1–4.1,Spodopteraeridaniacaterpillar,dorsalview,headatright;2,cocoonmassofCotesiascotticomb.nov.afterparasitoidemergence,rearedfromS.eridania;3, Spodopteracosmioides,caterpillar,dorsalview,headatright;4,cocoonmassofC.scottirearedfromoneS.cosmioidescaterpillar(imagetakenbeforeparasitoidemergence atrearingsite).
Figs.5and6. Cotesiascotticomb.nov.3,habitus,lateral;4,detailofmetanotumandpropodeum.
(2.84%distance).Thesetwospeciesarereadilydistinguishedbythe colorofmetacoxa,blacktodarkbrowninC.orobenaeandmostly yellowwithdarkbaseinC.scotti,andthesculpturingoftergite3, smoothinC.orobenaebutbasallystriateinC.scotti.
MorphologyofthespecieshereintransferredissimilartoCotesia delicata(Howard,1897),inhavingarugosepropodeum,metasomal terga1–2andbaseoftergite3rugosestriate,innerspurof metati-bialessthan0.5×themetabasitarsusandbarelylongerthanouter spur,andmesoscutumstronglypunctatewithlarger/coarser punc-tationatnotauli.Thetwospeciesdiffermainlyincolorfeatures, C.scottihavingmoreextensiveyellow(pale)colorationas com-paredwithC.delicata,includingallcoxa,trochanter,trochantellus, tegulaandhumeralcomplex,andbaseofantenna,allofwhichare darkbrowninC.delicata.InC.scotti,thepropodeumhasapoorly defined carinaontop of a stronglyrugose background, and no mediancarina,whileinC.delicatathepropodeumhasnoindication ofanareolaandthemediancarinaispresentatleastpartially,and tergite1isnearlyparallelsidedinC.scotti,butdistinctly widen-ingtowardapexinC.delicata,withapicalwidthabout1.5times basalwidth.Additionally,C.scottihasaNeotropicaldistribution (CostaRica,BrazilandArgentina),and parasitizesNoctuidae, in
comparisontoaNearcticdistribution,andErebidaehostsforC. del-icata.RegardingtheNeotropicalfauna,C.scottiresemblesCotesia ornatricis(Muesebeck,1958),whichisalsoagregariousparasitoid, however associatedwithUletheisaornatrix (L.,1758)(Erebidae: Arctiinae)(Muesebeck,1958).Althoughbothspecieshavearugose propodeum,inC.ornatricisthemediancarinaismoreorlessdistinct andthereisnoindicationofanareola,butinC.scottithemedian carinaisabsentandtheareolaismoreorlessdistinct.Thesetwo speciesalsodifferinthesculpturingoftergite3,smoothinC. orna-tricis,butrugose-striatebasallyinC.scotti,andinthecoloroftegula andhumeralcomplex,darkbrowninC.ornatricis,butyellowinC. scotti.
Forspecies witheconomicimportanceasnaturalenemiesof pests,coveredintheinteractivekeytospeciesbySharkey(2005),C. scottiissimilartoCotesiamarginiventris,aspecieswithwidespread distribution in the Americas and known to parasitize several speciesofagriculturalpests.Besidesmorphologicalresemblance, bothspeciesareknowntoparasitizeSpodopteraspp.(threeand sevenspecies respectively),andtheavailableDNA barcodesfor bothspeciesarerelativelysimilar(4.7%distance)(Table1– Supple-mentaryAppendix).Biologyisusefulforseparatingthetwospecies,
Cotesia enypiae|HYCNE247-11|paratype|canada Cotesia janzen200|/scadia argentea|ASHYD2512-10|costa rica Cotesia phobetri|HyCNE449-11|united states Parapanteles mariae|euglyphis maria|ASHYD969-08|costa rica
Cotesia lyciae|HYCNE384-11|canada Parapanteles polus|napata lelex|ASBR070-06|costa rica Cotesia lunata|HYCNE380-11|canada
Cotesia rubecula|HYCNE484-11|france Cotesia congregata|CNCHZ630-09|canada Cotesia isolde|WOMIA111-11|hungary Cotesia electrae|HYCNE236-11|united states Cotesia zygaenarum|CNBR611-09|sweden Cotesia eliniae|ASCNCO50-09|canada
Cotesia spuria|BCHYM7179-15|czech republic Cotesia selenevora|CNCBR641-09|sweden
Cotesia sibyllarum|ASQAS173-11|spain Cotesia pieridis|ASQSR300-11|greece
Cotesia koebelei|GBAH0946-06|united states Cotesia abjecta|WOMIA129-11|austria Cotesia fiskei|HYCNE271-11|canada Cotesia glomerata|CGBTA030-08|turkey Cotesia ayerzai|HYCNE181-11|chile Cotesia glomerata|GBAH2173-06| Cotesia smerinthi|HYCNE19-11|canada Cotesia obscuricomis|GBAH3172-08| Cotesia orabenae|CGBTB717-09|turkey Cotesia orabenae|SAHYM130-10|canada
Parapanteles scotti|ctenoplusia oxygramma|ASBA637-06|costa rica Parapanteles scotti|spodoptera androgea|ASBA637-06|costa rica Cotesia scotti|spodoptera eridania|MK239195|brazil GO ES06 Cotesia scotti|spodoptera cosmioides|MK239190|brazil GO ES06
Cotesia scotti|spodoptera cosmioides|MK239191|brazil GO ES06 Cotesia scotti|spodoptera cosmioides|MK239192|brazil GO ES06 Cotesia scotti|spodoptera cosmioides|MK239193|brazil GO ES06 Cotesia scotti|spodoptera cosmioides|MK239194|brazil GO ES06 Cotesia marginiventris|ASQAS169-11|united states
Cotesia marginiventris|SYC7726-14|french polynesia Cotesia marginiventris|HYCNE408-11|canada Cotesia urabae|NZHYM611-10|new zealand
Cotesia jft03|plutella xyllostella|HYLEP331-08|canada Cotesia ruficrus|mythimna impura|ASQSP562-08|united kingdom Cotesia telengia|CGBTA403-08|turkey
Cotesia ruficrus|GMEGA138-14|egypt Cotesia ruficrus|CNBA897-10|new zealand Cotesia ruficrus|MAMTK483-12|pakistan Cotesia lycophron|WOMIA134-11|spain Cotesia melitaearum|GBAH0933-06|italy Cotesia melitaearum|CGBTA450-08|turkey Cotesia melitaearum|ASQSR287-11|france Cotesia cynthiae|GBAH0942-06|france Cotesia plutellae|NZMG256-11|new zealand
Cotesia vestalis|GBMIN74199-17| Cotesia crambi|CGBTA439-08|turkey Cotesia crambi|CNCHZ1162-09|canada Cotesia sesamiae|KINS459-10|kenya Cotesia sesamiae|KINS471-10|kenya Cotesia chilonis|GBMIN23886-13| Cotesia flavipes|KINS468-10|kenya Cotesia nonagriae|GBMIN23885-13| Cotesia maculithorax|ASQS182-11|united kingdom Cotesia specularis|WOMIA124-11|spain Cotesia inducta|ASQAS168-11|united kingdom
Cotesia parastichtidis|ASWA947-08|canada Cotesia cf.numen|ASQSR302-11|united kingdom Cotesia pilicornis|WOMIC628-10|sweden
Cotesia jucunda|BCHYM7306-15|czech republic Cotesia tenebrosa|CGBTB713-09|turkey Cotesia eulipis|ASQSR294-11|norway
Cotesia sericea|BCHYM193-15|czech republic Cotesia selebrosa|SSJAE3068-13|canada
Cotesia saltatoria|WOMIA159-11|united kingdom Cotesia ancilla|ASQSR274-11|france Cotesia kazak|HYCNE346-11|russia Cotesia jfto9|ASWAU507-08|canada Cotesia cyaniridis|HYCNE216-11|canada Cotesia jft09|CNCHY183-07|canada Cotesia atalantee|HYCNE169-11|canada Cotesia tetricus|ASQSR267-11|austria Cotesia acuminate|GBAH00932-06|russia Cotesia eunomiae|ASQAS165-11|belgium Cotesia acuminated|GBAH0928-06|sweden Cotesia acuminated|WOMIA133-11|poland Cotesia bignellii|GBAH0948-06|finland Cotesia bignellii|ASQAS164-11|germany Cotesia rufocoxalis|CNCHX262-09|united states
Cotesia griffini|HYCNE309-11|canada Cotesia jft02|ASWA407-08|canada Cotesia laeviveps|paratype|HYCNE372-11|canada Cotesia acronyctae|HYCNE146-11|canada Cotesia halli|ASCNC045-09|canada Cotesia yakutatensis|ASWAS034-07|canada Cotesia jft06|CNCHY185-07|canada Cotesia jft06|TTHYB423-09|canada Cotesia yakutatensis|SSBAF2139-13|canada Cotesia vanessae|WOMIA097-11|spain Cotesia diversa|CNPPC872-12|canada Cotesia ofella|WOMIA115-11|hungary Cotesia tibialis|ASQSR255-11|austria Cotesia xylina|CNCHY039-07|canada Cotesia hyphantriae|SMTP08944-15|canada
Parapanteles gerontogeae|paratype|HYCNE1748-11|south africa Parapanteles continua|hylesia continua|ASBAC280-05|costa rica
Parapanteles tessares|hylesia continua|ASBAC369-05|costa rica Parapanteles sicpolus|lonomia concordia|ASBR060-06|costa rica
Parapanteles em|hemiceras consipirates|HSBA316-06|costa rica Parapanteles paradoxus DHJ02|tithaustes noctiluces|ASBC133-05|costa rica Parapanteles paradoxus DHJ02|dunama janecoxae|ASBAC387-05|costa rica
Capitonius sp.|JIAAL038-16| Notiospathius mariachi|ASDOR018-09| Meteoridea sp.|ASQSQ545-09| Aspilodemon sp.|GMHDN063-13|
Cardiochiles sp.|GMMCF101-14| Ephedrus incompletus|SSEIB11671-13|
0.05
Fig.7. MaximumlikelihoodtreebasedonpartialCOIsequences,usingGeneralTime Reversibleparameter.Terminaltaxalabelsinclude:speciesname|hostspecies/type status(whenavailable)|BOLDaccessionnumber|country(whenavailable);new sequenceslabelsareinboldandwithGenbankaccessionnumber.
sinceC.scottiisgregarious,and C.marginiventrisismainly soli-tary(Harrisetal.,2012),withonlyoccasionalreports,inlaboratory conditions,oftwoadultsemergingfromonehost(Kunnalacaand Mueller,1979;Riddick,2002).Colorinthesetwospeciesisvery similar,includingthemostlyyellowmetacoxa withdarkbrown base(notsharedwiththeothermentionedspecies),althoughthe antennaofC.marginiventrisisentirelydarkbrown(palebasallyinC. scotti)anditsmetasomausuallywithsomedegreeoforange-yellow onterga,usuallyvaryingfromentiremetasomatotergite1–3.Few specimensexaminedhavetheentiremetasomaltergablackasin C.scotti.Besidescolor,themaindifferenceisthelengthoftheinner spurofmetatibia,lessthan0.5timesbasitarsusandnearlyaslong asouterspurinC.scotti,comparedtomorethan0.5timesbasitarsus anddistinctlylongerthanouterspurinC.marginiventris
Bothspecies,S.cosmioidesandS.eridania,aregaining impor-tanceaspestsinrecentyears (Silva etal.,2017;Teodoroetal., 2013).Forinstance,S.cosmioidesusedtobeconsideredasporadic pest,witheconomicdamageregisteredindifferentcropsduring outbreaks(Habibetal.,1983).ThesamewastrueforS.eridania, con-sideredanincidentalpestinsoybean(Sosa-Gómezetal.,1993).The frequencyofoutbreaksofS.cosmioidesandS.eridaniaisincreasing, andcurrentlytheyareconsideredaskeypestsinsomegrain pro-ductionsystems,especiallysoybean,andcotton(Buenoetal.,2011; Favettietal.,2015;Link,2010;Quintelaetal.,2007;Santosetal., 2005,2010),aswellastomato,inwhichS.eridaniaisalready con-sideredthemainfruitborerpestforsomeregionsinBrazil(Miranda etal.,2005).Thevoracityofthesespecies(Buenoetal.,2011),and thewidespreaduseofBtcropsasthemaintacticforpestcontrol,for whichthesetwospeciesaretolerant(Bernardietal.,2014)arelikely themainreasonsfortheirrisingimportanceaspests(Chilcuttetal., 2007;Silvaetal.,2016).TheparasitoidCotesiascotticomb.nov.is recordedforthefirsttimeonthesetwospecies,andfrom agricul-turalsystems(i.e.organictomatoandBtsoybean),suggestingthe importanceofthisspeciesasanaturalenemyoftheblack army-wormandthesouthernarmyworm.Researchonnaturalenemies forspeciesofSpodopteraisparticularlyrelevantconsideringtheir demonstratednaturaltolerancetotransgenicBtcrops(Bernardi etal.,2014),atechnologywhichmaysuppressherbivoryformost defoliators,withoutcompromisingtheabilityofparasitoidstofind (Liuetal.,2015)andparasitizetheirhostcaterpillar.
Conflictsofinterest
Theauthorsdeclarenoconflictsofinterest. Acknowledgements
ToFazenda OrgânicaNossaSenhoraAparecida for providing informationtothegraduatestudentsoftheUniversidadeFederalde Goiás,AnnaPaulaAraújoeTássiadosSantos.SinvalSilveiraNetofor theconfirmationoftheLepidopteraidentity.Financialsupportwas providedbyCAPES(Coordenac¸ãodeAperfeic¸oamentodePessoalde NívelSuperior),andINCT-HYMPAR(InstitutoNacionaldeCiênciae TecnologiadosHymenopteraParasitoides).WethankAngélicaM. Penteado-Diasforprovidingsupportforthemolecularanalysesand LucianaB.R.FernandezfortheSEM(ScanningElectronMicroscope) photograph.
AppendixA. Supplementarydata
Supplementarydataassociatedwiththisarticlecanbefound,in theonlineversion,atdoi:10.1016/j.rbe.2019.05.001.
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