Cotesia invirae, sp. nov., from South Brazil: a new gregarious microgastrine wasp (Hymenoptera: Braconidae) reared from Opsiphanes invirae (Nymphalidae) feeding on palms

REVISTA

BRASILEIRA

DE

Entomologia

w w w . r b e n t o m o l o g i a . c o m

Systematics,

Morphology

and

Biogeography

Cotesia

invirae,

sp.

nov.,

from

South

Brazil:

a

new

gregarious

microgastrine

wasp

(Hymenoptera:

Braconidae)

reared

from

Opsiphanes

invirae

(Nymphalidae)

feeding

on

palms

Geraldo

Salgado-Neto

_,

_James

_Bryan

_Whitfield

_,

_Flávio

_Roberto

_Mello

_Garcia

b_{UniversityofIllinoisatUrbana-Champaign,DepartmentofEntomology,Urbana,USA}

c_{UniversidadeFederaldePelotas,DepartamentodeEcologia,ZoologiaeGenéticaPelotas,LaboratóriodeEcologiadeInsetos,Pelotas,RS,Brazil}

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received12October2018 Accepted23February2019 Availableonline12March2019 AssociateEditor:BernardoSantos Keywords: Palmaceae Nymphalidae Opsiphanesinvirae Taxonomy

a

b

s

t

r

a

c

t

Anewspeciesofmicrogastrinewasp,CotesiainviraeSalgado-Neto&Whitfield,sp.nov.,isdescribedfrom southernBrazilinSantaMaria,RioGrandedoSul.Thisspeciesisakoinobiontgregariouslarval endopar-asitoidandspinsacommonmassofcocoonsunderneaththehostcaterpillarsofOpsiphanesinvirae (Huebner,1818)(Lepidoptera:Nymphalidae),feedingonthepalmtreesSyagrusromanzoffianum(Cham.) Becc.;Livistonachinensis(N.J.Jacquim)R.Brown;Roystonearegia(HBK)O.F.Cook;Archontophoenix cunninghamianaWendland&Drude(Palmaceae).Morphological,molecular,biological,ecologicaland geographicaldataareintegratedtodescribethenewspecies.

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

Introduction

CotesiaCameron,1891(Braconidae:Microgastrinae)isthe sec-ondlargestgenusofmicrogastrinewaspsintermsof described species,encompassingroughly300–400describedspecies(Shaw andHuddleston,1991;Yuetal.,2016).However,thisnumberwill increaseinthecomingyears,sinceithasbeenestimatedthatnearly 1000species ofCotesia exist worldwide (Mason,1981; Michel-SalzatandWhitfield,2004).Thisincreasewillincreaseespecially intheNeotropicalregion,wherearelativelysmallnumberof stud-iesrecording species of Cotesia and their biology are available (Whitfield,1997),particularlyinSouthAmerica.

Cotesiaisrecognizableamongthemicrogastrinesbythe follow-ingfeatures:(1)forewingwithsecondr-mveinabsent,sothatthe smallareoletisopendistally;(2)propodeumcoarselysculptured, withmediallongitudinalcarinaratherthanmedialareola;(3)first andsecondmetasomaltergitesusuallyratherquadrateinformand coarselysculptured;and(4)ovipositorandsheathsshortandbarely exserted(Whitfieldetal.,2009).Thesewaspshaveakoinobiont habit(KankareandShaw,2004)andcanproducebothsingleadults orgregariousbroodsofoffspring.Thenewspeciesdescribedhere

∗ Correspondingauthor.

E-mail:gsalgado@bol.com.br(G.Salgado-Neto).

wasrecordedfromcaterpillarsof Lepidoptera(Nymphalidae)in Brazil,PeruandVenezuela(Yuetal.,2016).

Opsiphanesinvirae(Huebner1818)iswidespreadinBrazilbut is mostcommonly found betweenthe States of Rio de Janeiro (SoutheasternRegion)andRioGrandedoSul(SouthernRegion) (Silvaetal.,1968;Ferreiraetal.,1998).Thisspeciesisconsidered apestofthe“ac¸aí”palmtree(Euterpeoleraceae)inEastern Brazil-ianAmazonia(Northern Region),accordingtoSouzaandLemos (2007).InRio Grandedo Sul,this specieswasrecordedbyLink and AlvarezFilho (1979) and Link et al.(1980), morerecently,

Lamas (2004) also reported the occurrence of this species in Paraguay.

Fivespecies of Braconidaehavebeenrecorded as endopara-sitoidsofOpsiphanes(larvaestage):ApantelesbiezankoiBlanchard 1954, Apanteles opsiphanis Schrottky 1909, Cotesia sp., Cotesia alius(Muesebeck,1958a,b)(Penteado-Dias,1987;DeSantis,1989; Mason,1981),Rhysipolissp.(Sauer,1946;CostaLima,1950,1962; Silvaetal.,1968;Brice ˜no-Vergara,1978;DeSantis,1980; Penteado-Dias,1987;Mason,1981;Brice ˜no-Vergara,1997;Mexzón,1997; Rodríguezetal.,2006).

AsCotesiaspecieshaveappearedtobehighlyhostspecialized (KankareandShaw,2004),withmanycrypticspeciesandallopatric distributions(Fiaboeetal.,2017),theuseofanintegrative tax-onomicapproach(combiningmorphological,molecular,biological andgeographicaldata)iscriticalforrecognizinganddistinguishing theseparasitoidwasps(Smithetal.,2008;Kaiseretal.,2017).

https://doi.org/10.1016/j.rbe.2019.02.003

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

Usinganintegrativetaxonomicapproach,thispaperprovides a description of a new species of Cotesia, whose brood was producedfromOpsiphanesinvirae(Huebner,1818)(Lepidoptera: Nymphalidae), feeding on palm trees (Palmaceae) in southern BrazilinSantaMaria, RioGrandedoSul.Additionally,we com-pareditwithotherformallydescribedspeciesfortheNeotropical region.

Materialsandmethods

BetweenMarch2006andMarch2007,wecollected35larvaeof Opsiphanesinvirae.Thissurveywascarriedoutonnativeandexotic palmsintheUniversidadeFederaldeSantaMaria(UFSM)campus (29◦4219S,53◦4257W–90m.elev.).AvenidaRoraima(Campus –UFSM),JardimdaEscolaAgrícola(Campus–UFSM).Thelarvae ofO.inviraewerefoundonSyagrusromanzoffianum(Cham.)Becc. (Arecaceae;Gerivá);Livistona chinensis(N.J.Jacquim)R.Brown (ChineseRange); Roystonea regia (HBK) O.F. Cook(Cuban Real Palm);andArchontophoenix cunninghamianaWendland&Drude (AustralianRealPalm).

Uponcollection,larvaewerekeptinanenvironmentalchamber (25±1◦C;70%UR;photoperiodof14hoflight)andobserveddaily untiltheemergenceofthebutterfliesorparasitoids,whichwere preservedin70%ethanol.Voucherspecimensweredepositedin thecollectionoftheLaboratóriodeBiologiaEvolutivaoftheCentro deEducac¸ão,UniversidadeFederaldeSantaMaria(UFSM).(Rocco A.DiMarecurator),numberGSAL10.01.2006.

Illustrations were made using digital camera photography setupsattachedtostereoscopicmicroscopes, bothin Braziland attheUniversity of Illinois.Morphologicalterms and measure-mentsofstructuresare mostlythose usedbyFernandez-Triana etal.(2014).

To checkthe molecular-specificcharacterization of thenew species, the mitochondrial gene Cytochrome Oxidase I (COI) was analyzed. For the amplification of a fragment of approx-imately 460bp of this gene, we used the following primer pair: COI-F (5-GATTTTTTGGKCAYCCMGAAG-3) and COI-R (5 -CRAATACRGCTCCTATWGATAAWAC-3)(Gusmãoetal.,2010).DNA extraction of one specimen was performed with the GenElute MammalianGenomicDNAMiniprepKit(Sigma–Aldrich®)and fol-lowed the manufacturer’s protocol. The product was amplified viaPolymerase ChainReaction(PCR)accordingtothefollowing schedule: 94◦C for 2min,40 cyclesof 94◦C for 30s, 54◦C for 30s,72◦Cfor40sand72◦Cfor4min.ThenthePCRproductwas purifiedusingpolyethyleneglycolprecipitation(PEG;Schmitzand Riesner,2006).ThesesamplesweresequencedusingtheBigDye 3.1reagent(LifeTechnologies®)and3500×Lautomaticsequencer (LifeTechnologies®).

Descriptivetaxonomy

CotesiainviraeSalgado-Neto&Whitfield,sp.nov. (Figs.1and2)

Holotype.Female,Brazil:RioGrandedoSul,SantaMaria, Uni-versidadeFederaldeSantaMaria(UFSM)(29◦4219S,53◦4257W –90m.elev.).DepositedintheCollectionofEntomophagousInsects “OscarMonte”oftheInstitutoBiológicodeCampinas,SãoPaulo. (IB-CBE; Valmir Antônio Costa curator), number IB-CBE#215-C, GSAL10.01.2006andalsodepositedintheHymenopteracollection oftheMuseumofZoologyoftheUniversityofSãoPaulo(MZUSP; Carlos Brandão curator), number MZSP62057, September 2018, coll.G.Salgado-Neto,exlarvaOpsiphanesinvirae(Huebner,1818) (Lepidoptera:Nymphalidae).

Paratypes.2males,depositedinMZUSP,numbersMZSP62066 andMZSP62067.Samedataasholotype.

Diagnosis.Thecombinationofcharacterspresentedbelowis sufficient to separateC. invirae fromall other described native species of Cotesia for theNeotropical region.In particular, few neotropicalCotesia havetheanterior metasomaltergiteslargely orangish rather than black (and even those are mostly unde-scribed). However, several widespread agricultural species, C. marginiventris(Viereck) and C.flavipes(Cameron),have current distributionsextendingintoBrazilandareknowntobehighly vari-ableintergitecolour.C.marginiventrisdiffersinhavingtheanterior margin(roughly1/3oflength)oftergite3withroughersculpture (smoothinC.invirae),andC.flavipes(alongwithothermembers ofitsspeciescomplex)isextremelydistinctiveinhavinga rela-tivelydepressedmesosomathatisusuallysignificantlynarrower indorsalviewthanthewidthofthehead(inadditiontohaving thefacesomewhatbulgingbelowtheantennaeinlateralview). C.alius,previouslyrecordedfromthesamehost,hasessentially blacktergites,althoughthelaterotergitesarebrightyellowishas inC.invirae.C.aliusalsoappearstohaveaslightlylongerfirst ter-gitethanC.invirae,butotherwisethetwospeciesarequitesimilar morphologically.

Description. Female(Fig.1a). Body colour:head and meso-soma mostly black except pale, almost whitish palpi, most of all legs honey-yellow except darkened junction of trochanter withfemur,distal quarterofhind femur,distal 0.3–0.4ofhind tibia, and most of hind tarsus; metasoma mostly light honey-yellowtoorange exceptdarkbrownfirsttergiteand orange to brownsecondtergite.Antennacolour:scape,pedicelandflagellum dark.Tegulaecolour:darkbrown,relativelyopaque.Pterostigma colour: dark greyish brown. Fore wings colour: partially pig-mented but pigmented veins darkbrown(a few veins may be dark butmost pale).Antenna length/bodylength: antennajust slightly shorter than body (head to apex of metasoma). Body in lateral view: not distinctly flattened dorso-ventrally. Body

Fig.1.(a)LateralviewoffemaleCotesiainvirae;(b)viewofthelabrum,mandiblesandlabialpalps;(c)frontviewoftheface;(d)lateralviewoftheantenna;(e)dorsalview ofthemesosoma;(f)dorsalviewofabdomen;(g)viewoftheforewinginsitu;(h)detailsofthespursofthetibia(innerandouter);(i)larvaeofC.invirae;(j)frontviewofthe pupaofC.invirae;(k)dorsalviewofpupaofC.invirae;(l)lateralviewofthepupaofC.invirae;(m)frontviewofhead,thelarvaeofC.invirae;(n)viewofthecocoonsofC. invirae,arrangedregularlyandsecuredwithsilkthreadstoeachotherintheformofpalisadesonthehost.SomematerialherepreviouslyreportedinSalgado-Neto(2013) asfromC.alius.

Fig.2.(a)DorsalhabitusoffemaleCotesiainvirae,showingsculpturingofmesoscutum,scutellum,propodeumandanteriormetasomaltergites;(b)lateralhabitusofC. invirae;(c)wingsofC.invirae.

length (head to apex of metasoma): 2.5 – 2.7mm. Fore wing length:2.4–2.6mm.Ocular-ocellarline/posteriorocellusdiameter 1.7–1.9.Interocellardistance/posteriorocellusdiameter:1.9–2.1. Antennalflagellomere2 length-width: 2.9–3.1.Antennal flagel-lomere14length/width1.4–1.6.Lengthofflagellomere2/lengthof flagellomere14:2.2–2.3.Metafemurlength/width3.0–3.2. Metat-ibia inner spur length/metabasitarsus length: roughly 0.5–0.6.

Anteromesoscutum:anteriorlywithdistinctdensepunctures,with only a very narrow smooth band posteriorly anterior to scu-toscutellar sulcus. Mesoscutellar disc: sparsely punctured and mostly shiny. Number of pits in scutoscutellar sulcus: 8–10. Propodeumcarina:withcompletemediallongitudinalcarinathat isnearlyobscuredbycoarsebackgroundsuggestingmedial are-ola.Propodeumbackgroundsculpture:mostlycoarselyrugulose.

Mediotergite1length/widthatwidestpoint:1.0–1.1. Medioter-gite1shape:evenlywideningfromanteriormarginto0.8–0.9of mediotergitelength(widestpoint),thenroundingtowards pos-teriormargin.Mediotergite1sculpture:mostly ruguloseexcept anteromediallysmooth.Mediotergite2nearlyquadratewithwidth at posterior margin/length: 2.1–2.3. Mediotergite 2 sculpture: mostlyrugose,smoewhatpolishedlaterally.Hypopygium:evenly sclerotized but folded medially, posteriorly forming a strongly obtuseangleinlateralview.Ovipositorthickness:tapering grad-uallytotip.Ovipositorsheaths:short,approximately1/3ofhind tibialengthbutonlyslightlyexposedtowardstip.Lengthoffore wingveinsr/2Rs:1.0–1.1.Pterostigmalength/width2.0–2.2.Point ofinsertionofveinrinpterostigma:justbeyondhalfwaypointof pterostigmalength.Angleofveinrwithforewinganterior mar-gin:angling5–10degreestowardswingtipposteriorly.Shapeof junctionofveinsrand2RSinforewing:rweaklyarched,junction distinctlyangled.

Moleculardata.COIbarcodedepositedinGenBank(Accession MK040535).WhentheBarcodeofLifeDatabase(BOLD)was inter-rogatedwiththissequence,theclosestmatches(between1and2% sequencedivergence)weretwocurrentlyundescribedspeciesfrom theJanzenandHallwachsACGproject(Janzenetal.,2009).Bothof thesespecieswererearedfromOpsiphanesonpalms(albeit differ-entspecies).TheyarereferredtoinformallyasCotesiaWhitfield78 andCotesiaWhitfield20inSmithetal.(2008).AsC.aliusisalso fromthesamebasichostgroup,itappearsthatthereisan interna-tionalclusterofcloselyrelatedspecies,stillmostlyundescribed,to besortedouteventuallybasedonabroadstudy.

Host: Opsiphanes invirae (Huebner, 1818) (Lepidoptera: Nymphalidae).

Biology/ecology.Cotesiainviraeisagregariousparasitoidwasp thatoccursmainlyinthewetseason(March–May);however,its host,O.invirae,occursthroughouttheyear,mainlyintheautumn season(March–April–May).Cotesiainviraelarvaekillthehostlarva beforetheendofthelastinstarandformtheircocoonsinregular massofdirtywhitishcocoons,regularlyarrangedunderthehost. Thelarvaeofthisgregariousspeciesallemergefromthehostin ashorttimethroughmanydifferentholesinthehostcuticleand spinacommonwoollycocoonmass,withinwhichtheindividual cocoonscanbedistinguished.Somepreviousrecordsattributed to C. alius (e.g. Salgado-Neto, 2013) actually refer to this new species.

Basedon35analyzedreared broods,eachonereferring toa larva of O. invirae fromnature, were 4581 registered cocoons, averaging130.88±49.02per host.Takinginto accountthatthe number of cocoons is the number of eggs laid per host-larva, whoseaveragenumberofeggslaidwas87.Basedonsevenbroods, witha total of789cocoons (112.71±31.21cocoons/posture),it wasfoundthat 104 cocoons(13%) from two broods of C. invi-raewereparasitizedbyEulophidae.Weobservedfourspeciesof hyperparasitoids (Eulophidae)exploiting thecocoon massof C. inviraecollectedinthefield,twofromtheEntedoninae(Horismenus opsiphanisSchrottky,1909andHorismenussp.nov.)andtwofrom Tetrastichinae(OomyzussokolowskiiKurdjumov,1912and Aprosto-cetussp.nov.).AllhyperparasitoidswereidentifiedbyDr.Christer Hansson(LundUniversity,Sweden)andDr.ValmirAntonioCosta (InstitutoBiológicodeCampinas,Brazil)(Salgado-Neto&DiMare, 2010).

Distribution.KnownsofarfromSantaMaria,RioGrandedoSul, Brazil.

Etymology.Thespecificepithetinvirae,fromtheLatin mean-ingturnaround, (thesame as: bickering,return, bend,reverse, spin,putyourselfinanewposition)isareferencetoOpsiphanes invirae(Huebner,1818)(Lepidoptera:Nymphalidae)intributeto themovementofthehostcaterpillartoavoidtheovipositionof parasitoids.

Discussion

UnliketherecentlydescribedCotesiaspeciesfromGeometridae, C.itororensisSousa-LopezandWhitfield(Sousa-Lopesetal.,2016;

Souza-Lopesetal.2018),Cotesiainviraefallssquarelywithinthe usualmorphologicalanddefinitionofCotesia,ratherthan some-whatintermediatebetweenthecloselyrelatedgeneraCotesiaand Protapanteles.CotesiaareoftenrearedfromNymphalidae,although theonlyspeciessofarrecordedfromSouthAmericaisa Protapante-les,P.eryphanidis(Whitfield),rearedfromEryphanisgreeneyi(Penz andDevries,2008)(Nymphalidae)inEcuador(Greeneyetal.,2011). Withrespecttomoleculardata,C.inviraealsofitssquarelywithin CotesiaaccordingtoBLASThits,closelyrelatedtotwoecologically similarspeciesfromCentralAmerica.

Species of Cotesia are importantagents of biological control againstpestinsects,sothatthecorrectidentificationofthemis criticaltosuccessinpestmanagementprogrammes.Wereiterate herethattheuseofanintegrativetaxonomicapproach (combin-ingmorphological,molecular,biologicalandgeographicaldata)is essentialforaccuratespeciesdelineation.

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgments

WearegratefultoDr.RoccoAlfredoDiMare(inmemorian)for photographsframeinFig.2ofCotesia(Braconidae)specimens,Dr. ValmirAntônioCostaofInstitutoBiológicodeCampinasforCotesia (Braconidae)genusidentification,Dr.ChristerHanssonofLund Uni-versity,SwedenforhyperparasitoidEulophidaeidentificationand Dr.RicardoHarakavaofInstitutoBiológicodeSãoPaulofor analy-sesoftheCOIbarcode.JBWwouldliketothankTylerBlackwellfor producingthephotographsinFig.1.

References

Brice ˜no-Vergara,A.J.J.,1997.Perspectivasdeunmanejointegradodelgusanoverde delplatano,OpsiphanestamarindiFelder(Lepidoptera:Brassolidae).Rev.Fac. Agron.14(5),475–590.

Brice ˜no-Vergara, A.J., 1978. Algunos parasitos y depredadores de Opsiphanes tamarindiFelder(Lepidoptera:Brassolidae)enVenezuela.Rev.Fac.Agron.26, 117–128.

CostaLima,A.M.,1950.InsetosdoBrasil,Lepidopteros.6◦_tomo,2a_{parte,SérieDidática}

daEscolaNacionaldeAgronomia.UniversidadeRural,RiodeJaneiro,420pp. CostaLima,A.M.,1962.InsetosdoBrasil,Himenópteros.12◦_tomo,2◦_parte.Escola

NacionaldeAgronomia,RiodeJaneiro,393pp.

DeSantis,L.,1980.Catalogodeloshimenópterosbrasilenosdelaserieparasitica: incluyendobethyloidea.EditoradaUniversidadeFederaldoParaná,Curitiba, 395pp.

DeSantis,L.,1989.CatalogodelosHimenopterosCalcidoides(Hymenoptera)alsur delosEstadosUnidos,segundosuplemento.ActaEntomol.Chil.15,12. Fernandez-Triana, J.L.,Whitfield,J.B., Rodriguez,J.J.,Smith, M.A., Janzen,D.H.,

Hallwachs,W.,Hajibabaei,M.,Burns,J.M.,Solis,M.A.,Brown,J.,Cardinal,S., Goulet,H.,Hebert,P.D.N.,2014.ReviewofApanteles(Hymenoptera,Braconidae, Microgastrinae)fromAreadeConservacionGuanacaste,CostaRica,withkeys toalldescribedspeciesfromMesoamerica.ZooKeys383,15–65.

Ferreira,J.M.S.,Lima,M.F.,Santana,D.L.Q.,Moura,J.I.L.,Souza,L.A.,1998.Pragasdo coqueiro,p.189-267.In:Ferreira,J.M.S.,Warwick,D.R.N.,Siqueira,L.A.(Eds.),A culturadocoqueironoBrasil.2ed.rev.ampl.Embrapa-SPI/Aracaju,Embrapa CPATC,Brasília,p.292.

Fiaboe,K.K.M.,Fernandez-Triana,J.L.,Nyamu,F.W.,Agbodzavu,K.M.,2017.Cotesia icipesp.n.,anewMicrogastrinaewasp(Hymenoptera,Braconidae)of impor-tanceinthebiologicalcontrolofLepidopteranpestsinAfrica.J.Hymenopt.Res. 61,49–64.

Greeney,H.F.,Whitfield,J.B.,Stireman,J.O.,Penz,C.M.,Dyer,L.A.,2011.Natural His-toryofEryphanisgreeneyi(Lepidoptera:Nymphalidae)andItsEnemies,Witha DescriptionofaNewSpeciesofBraconidParasitoidandNotesonItsTachinid Parasitoid.Ann.Entomol.Soc.Am.104(6),1078–1090.

Gusmão,F.A.,Harakava,R.,Campos,A.E.C.,2010.Fire-antsoftheSolenopsis saevis-simaspecies-group(Hymenoptera:Formicidae)nestinginparksinthecityof SãoPaulo:identificationbasedonmtDNAsequencesandmorphological char-acters.Sociobiology56,353–362.

Janzen,D.H.,Hallwachs,W.,Blandin,P.,Burns,J.M.,Cadiou,J.-M.,Chacon,I., Dap-key,T.,Deans,A.R.,Epstein,M.E.,Espinoza,B.,Franclemont,J.G.,Haber,W.A., Hajibabaei,M.,Hall,J.P.W.,Hebert,P.D.N.,Gauld,I.D.,Harvey,D.J.,Hausmann, A.,Kitching,I.J.,LaFontaine,D.,Landry,J.-F.,Lemaire,C.,Miller,J.Y.,Miller,J.S., Miller,L.,Miller,S.E.,Montero,J.,Munroe,E.,RabGreen,S.,Ratnasinghsm,S., Rawlins,J.E.,Robbins,R.K.,Rodriguez,J.J.,Rougerie,R.,Sharkey,M.J.,Smith,M.A., Solis,M.A.,Sullivan,J.B.,Thiaucourt,P.,Wahl,D.B.,Weller,S.J.,Whitfield,J.B., Willmott,K.R.,Wood,D.M.,Woodley,N.E.,Wilson,J.J.,2009.IntegrationofDNA barcodingintoanongoinginventoryofcomplextropicaldiversity.Mol.Ecol. Resour.9(Suppl.1),1–26.

Kaiser,L.,Fernandez-Triana,J.,Capdevielle-Dulac,C.,Chantre,C.,Bodet,M.,Kaoula, F.,Benoist,R.,Calatayud,P.A.,Dupas,S.,Herniou,E.A.,Jennette,R.,Obonyo, J.,Silvain,J.F.,Ru,B.L.,2017.SystematicsandbiologyofCotesiatyphaesp.n. (Hymenoptera,Braconidae,Microgastrinae),apotentialbiologicalcontrolagent againstthenoctuidMediterraneancornborer,Sesamianonagrioides.Zookeys 682,105–136.

Kankare,M.,Shaw,M.R.,2004.MolecularphylogenyofCotesiaCameron,1891 (Insecta:Hymenoptera:Braconidae: Microgastrinae)parasitoids associated withMelitaeinibutterflies(Insecta:Lepidoptera:Nymphalidae:Melitaeini). Mol.Phylogenet.Evol.32,207–220.

Lamas,G.,2004.AtlasofNeotropicalLepidoptera.Checklist: part4A, Hesperi-oidea&Papilionoidea.AssociationofTropicalLepidoptera,ScientificPublishers, Gainesville,USA,439pp.

Link,D.,AlvarezFilho,A.,1979.PalmeirasatacadasporlagartasdeBrassolidae (Lep-idoptera)emSantaMaria,RS.Rev.CentroCiênc.Rurais9(2),221–225. Link,D.,Biezanko,C.M.,Carvalho,S.,Tarragó,M.F.S.,1980.LepidopteradeSanta

MariaeArredores.III.MorphidaeeBrassolidae.Rev.CentroCiênc.Rurais10(2), 191–195.

Mason,W.R.M.,1981.ThepolyphyleticnatureofApantelesFoerster(Hymenoptera: Braconidae):aphylogenyandreclassificationofMicrogastrinae.Mem.Entomol. Soc.Canada115,1–147.

Mexzón,R.G.,1997.Entomofaunaprejudicial,enemigosnaturalesymalezasútiles enpal-.maaceiteraenAméricaCentral.ManejoIntegradodePlagas(C.R.)20/21, 1–7.

Michel-Salzat,A.,Whitfield,J.B.,2004.Preliminaryevolutionaryrelationshipswithin theparasitoidwaspgenusCotesia(Hymenoptera:Braconidae:Microgastrinae): combinedanalysisoffourgenes.System.Entomol.29,371–382.

Muesebeck, C.F.W., 1958a. New neotropical wasps of the family braconidae (hymenoptera)intheU.S.NationalMuseum.Proc.U.S.Natl.Mus.107,405–461. Muesebeck,C.F.W., 1958b. New Neotropical wasps of the family Braconidae (Hymenoptera) in theU.S. National Museum. Proc. U. S.Natl. Mus.107, 405–461.

Penteado-Dias,A.M.,1987.Contribuic¸ãoparaoconhecimentodamorfologiae biologiadeCotesiaalius(Muesebeck,1958)(Hymenoptera:Braconidae, Micro-gastrinae).Rev.Bras.Entomol.31(3),439–443.

Rodríguez,G.,Fari ˜nas,J.,Díaz,A.,Silva-Acu ˜na,R.,Pi ˜na,E.,2006.Plantasatrayentes de enemigos naturales de insectos plaga en palma aceitera. Rev. Digit.

CENIAPHOY10,Maracay,Aragua,Venezuela.ISSN1690-4117, Depósitole-gal:00302AR1449.http://www.ceniap.gov.ve/ceniaphoy/articulos/n10/arti/rod riguezg/arti/rodriguezg.htm[Accessed:05/11/2007].

Salgado-Neto,G.,DiMare,R.A.,2010.HiperparasitóidesemCotesiaalius(Mues.) (Hymenoptera;Braconidae)noestadodoRioGrandedoSul,Brasil.Magistra22 (3/4),210–212.

Salgado-Neto,G.,2013. Aspectsofbiology ofCotesiaalius(Muesebeck,1958) (Hymenoptera:Braconidae:Microgastrinae)onOpsiphanesinviraeamplificatus Stichel(Lepidoptera:Nymphalidae)forRioGrandedoSul,Brazil.Est.Biol.35 (84),35–41,http://www2.pucpr.br/reol/index.php/bs.

Sauer,H.F.G.,1946.Constatac¸ãodehimenópterosedipterosEntomófagosnoEstado deSãoPaulo.Bol.Fitossanit.3(1),7–23.

Schmitz,A.,Riesner,D.,2006.Purificationofnucleicacidsbyselectiveprecipitation withpolyethyleneglycol6000.Anal.Biochem.354,311–313.

Shaw,M.R.,Huddleston,T.,1991.Classification andbiologyofbraconidwasps (Hymenoptera,Braconidae).HandbooksfortheIdentificationofBritishInsects. R.Entomol.Soc.Lond.7,1–126.

Silva,A.G.,de,A.,Gonc¸alves,C.R.,Galvão,D.M.,Gonc¸alves,A.J.L.,Gomes,J.,Silva, M.N.,Simoni,L.,1968.Quartocatálogodosinsetosquevivemnasplantasdo Brasil;seusparasitasepredadores.MinistériodaAgricultura,tomo1,part.2, RiodeJaneiro,622pp.

Smith,M.A.,Rodriguez,J.J.,Whitfield,J.B.,Deans,A.R.,Janzen,D.H.,Hallwachs,W., Hebert,P.D.N.,2008.Extremediversityoftropicalparasitoidwaspsexposed byiterativeintegrationofnaturalhistory,DNAbarcoding,morphology,and collections.Proc.Natl.Acad.Sci.U.S.Am.105(35),12359–12364.

Sousa-Lopes,B.,Bächtold,A.,Del-Claro,K.,2016.Biology,naturalhistoryand tem-poralfluctuationofthegeometridOospilapallidariaassociatedwithhostplant phenology.Stud.Neotrop.FaunaEnviron.51(2),135–143.

Sousa-Lopes, B., Whitfield, J.B., Salgado-Neto, G., Del-Claro,K., 2018. Cotesia itororensis, sp. nov., from Brazilian savanna: a new reared microgas-trinae wasp (Hymenoptera: Braconidae) described using an integrative taxonomic approach. Zootaxa 4544 (3), 437–445, https://www.mapress. com/j/zt/article/view/zootaxa.4544.3.9.

Souza, L.A., Lemos, W.P., 2007. Sistema de produc¸ão do ac¸aí. Embrapa Amazônia Oriental, http://sistemasdeproducao.cnptia.embrapa.br/ FontesHTML/Acai/SistemaProducaoAcai 2ed/paginas/pragas.htm (accessed 03.11.07).

Whitfield,J.B.,1997. SubfamilyMicrogastrinae.In:Wharton, R.A.,Marsh,P.M., Sharkey,M.J.(Eds.),IdentificationManualtotheNewWorldGeneraofthe Fam-ilyBraconidae(Hymenoptera).InternationalSocietyofHymenopteristsSpecial Publication,pp.333–364.

Whitfield,J.B.,Rodriguez,J.J.,Masonick,P.K.,2009.Rearedmicrogastrinewasps (Hymenoptera:Braconidae)fromYanayacuBiologicalStationandenvirons (NapoProvince,Ecuador):diversityandhostspecialization.J.InsectSci.9(1), http://dx.doi.org/10.1673/031.009.3101(article31).

Yu,D.S.K.,VanAchterberg,C.,Horstmann,K.,2016.Taxapad,Ichneumonoidea2015. Ottawa,Ontario,Canada,Availablefrom:http://www.taxapad.com.