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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

Diolcogaster

flammeus

sp.

nov.

from

Brazil,

a

new

Microgastrinae

wasp

(Hymenoptera:

Braconidae)

of

importance

in

biological

control

Geraldo

Salgado-Neto

a

,

José

L.

Fernández-Triana

b

,

Wagner

de

Souza

Tavares

c

,

José

Cola

Zanuncio

d,∗

aUniversidadeFederaldeSantaMaria,DepartamentodeDefesaFitossanitária,Pós-Graduac¸ãoemAgronomia,SantaMaria,RS,Brazil

bCanadianNationalCollectionofInsects,Arachnids,andNematodes,Ottawa,Ontario,Canada

cUniversidadeFederaldeVic¸osa,DepartamentodeFitotecnia/InstitutodeBiotecnologiaAplicadaàAgropecuária,Vic¸osa,MG,Brazil

dUniversidadeFederaldeVic¸osa,DepartamentodeEntomologia/InstitutodeBiotecnologiaAplicadaàAgropecuária,Vic¸osa,MG,Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received7March2018

Accepted5June2018

Availableonline15June2018

AssociateEditor:BernardoSantos

Keywords: Agaraeaminuta Costaceae Costus Erebidae Ichneumonoidea

a

b

s

t

r

a

c

t

AnewspeciesofDiolcogaster(Ashmead,1900)(Hymenoptera:Braconidae)isdescribedandillustrated. Additionally,akeytoallNewWorldspeciesformallypublishedofthexanthaspisspecies-group(towhich thenewspeciesbelongs)isprovided.ThesolitarylarvalparasitoidDiolcogasterflammeussp.nov.was collectedinVic¸osa,MinasGeraisState,Brazil.ThisnaturalenemywasrearedfromcaterpillarsofAgaraea minuta(Schaus,1892)(Lepidoptera:Erebidae)feedingonplantsofspikedspiralflagginger,Costus spi-catus(Jacq.)Sw.andgingerspiral,Costusspiralis(Jacq.)Roscoevar.spiralis(Costaceae).Thefaunaofthe xanthaspisgroupintheNewWorldincludedjustthreepublishedspeciespriortothispublication. Diolco-gasterflammeussp.nov.istheonlyyellow-orangespeciesofthexanthaspisgrouprecordedintheNew Worldthusfar.

©2018SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

ThesubfamilyMicrogastrinae(Hymenoptera:Braconidae) com-prises2700+describedspecies (Yuet al.,2016; Whitfieldetal., 2018)andmanythousandadditionalundescribedones(Rodriguez etal.,2013;Fernández-TrianaandBoudreault,2016;Moghaddam and Mokhtari, 2017). Microgastrinae is the singlemost impor-tantgroupofparasitoidwaspsattackingcaterpillars(Avilaetal., 2013;Fiaboeetal.,2017),withmanyspeciesusedorbeing consid-eredasbiocontrolagentsagainstlepidopteranpestsinagriculture and forestry (Smith et al., 2013; Pintoet al., 2014).The genus Diolcogaster(Ashmead,1900)iscurrentlythesixthlargestof Micro-gastrinae,with98speciesdescribedworldwide(Zengetal.,2011; Fernández-Triana,2015)andhundredsawaitingdescription.This genushas17speciesrecordedfromtheNewWorld,10beingfrom theNeotropicalregion,andfourinBrazil(Guptaand Fernández-Triana,2014,2015;Yuetal.,2016).

Nixon(1965)includedsixDiolcogasterspeciesinthexanthaspis species-group:Diolcogasterxanthaspis(Ashmead,1900)fromthe WestIndies(Saint Vincentand Grenada)andfive otherspecies fromtheOldWorldtropics (thePhilippines).Later,Choi(2005)

also considered two additional species from the New World: Diolcogasterbakeri(Muesebeck,1922)andDiolcogasteriridescens (Cresson,1865)tobelongtothatgroup.Basedonspecimensseen

∗ Correspondingauthor.

E-mail:zanuncio@ufv.br(J.C.Zanuncio).

incollectionsworldwide,manymorespeciesremainundescribed (infact,Choi,2005describedsixadditionalNewWorldspeciesfor thegroup,butunfortunatelyhisPh.D.thesishasneverbeen pub-lishedandthusthosespeciesnamesarenotvalid–andarenot consideredhere).

Diolcogaster parasitizes early larval stages of Lepidoptera (Yeargan and Braman, 1986)including Agaraeaminuta(Schaus, 1892)(Lepidoptera:Erebidae)(synonym=AgoraeaminutaSchaus, 1892), a major pest of spiked spiralflag ginger, Costus spicatus (Jacq.) Sw. and ginger spiral, Costus spiralis (Jacq.) Roscoe var. spiralis (Costaceae) plants (Tavares et al., 2012).It is unknown otherhostplantspeciesofA.minuta.Costusspicatusisnativeto theCaribbean,includingDominica,Guadeloupe,Hispaniola, Mar-tinique,and PuertoRico(Kelleretal.,2009), whileC. spiralisis presentintropicalSouthAmerica(deAraújoandOliveira,2007). CostusspicatusandC.spiralisareeconomicallysignificantdueto theirpharmacologicalandmedicinalproperties(Sulakshanaetal., 2013;PawarandPawar,2014;Alonso-Castroetal.,2016)aswell asornamentalvalue(Castroetal.,2011;Skinner,2016).Agaraea minutaisfoundfromMexicotoBrazil(VincentandLaguerre,2014). ThisstudyaimstodescribeanewspeciesofDiolcogasterfrom Brazil.Thispreviouslyundescribedspecieshadalreadybeenfound inastudyonbiologicalinteractions,whereitwasfoundtoattackA. minuta(accordingtoTavaresetal.,2012,parasitismofDiolcogaster sp.onA.minutawas90.0%inthemunicipalityofVic¸osa,Minas GeraisState,Brazil).Hereinwedescribethenewtaxonandplace

https://doi.org/10.1016/j.rbe.2018.06.001

0085-5626/©2018SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisis anopenaccessarticleundertheCCBY-NC-NDlicense(http://

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Fig.1.GeographicallocationoftheBrazilianmunicipalityofVic¸osa(MinasGerais

State,Brazil).

itintoataxonomiccontextbyprovidingakeytoallNewWorld speciesformallypublishedofthexanthaspisspecies-group.

Materialsandmethods

AplantofC.spicatusandanotherofC.spiralisvar.spiraliswere sampledin May2011.Plantssampled wereapproximatelyfive yearsoldintheherbariumoftheFederalUniversityofVic¸osa(UFV) inVic¸osa,MinasGeraisState,Brazil(20◦45S×42◦ 51W,651m abovesealevel)(Fig.1).OnehundredlastinstarcaterpillarsofA. minutawerecollected,50fromC.spicatusandanother50fromC. spiralis.

TheoccurrenceofdefoliatingcaterpillarsofA.minutawas mon-itoredintheplantsofC.spicatusandC.spiralisvar.spiralisinMay 2011duetotheoccurrenceoftheseinsectsduringthatmonthin 2009and2010(Tavaresetal.,2012).

Thecaterpillarswerecollectedwithafine-tippedbrush,placed in500mLplasticcontainerslinedwithfilterpaperandwiththe lidaerated(20caterpillarsperplasticcontainerintwocontainers andanotheronewith10caterpillars)withleavesadlibitumofthe respectivehostplantssuppliedasfoodandsubstrateforpupation (Tavaresetal.,2012).TheywerebroughttotheLaboratoryof Bio-logicalControlofInsects–UFVinVic¸osa,MinasGeraisState,Brazil wheretheywerekeptat25±1◦C,12:12h(L:D)photoperiodand 70±10%RH.Theplasticcontainerswereopenedandcleanedwhen needed(Tavaresetal.,2012).Theleafpetiolesweremoistenedto avoiddesiccation(Tavaresetal.,2012).

SomepupaeofA.minutawereobtainedandindividualizedina 50mLplasticcontaineruntiltheemergenceofadultsofthisinsect, whichweremountedwithentomologicalpinsandfour individu-als(twomalesandtwofemales)senttoDr.VitorOsmarBecker, ofthe Uirac¸u InstituteinCamacan,Bahia State,Brazil,to iden-tifythespecies.Adultsoftheparasitoid,obtainedfromA.minuta caterpillars,weretransferredtoplasticEppendorfTMvialswith70%

ethanolandmountedwithentomologicalpins.Fourmaleandfour femaleoftheparasitoidweredepositedintheRegional Entomolog-icalMuseum–UFV.Adultsoftheparasitoidwereidentifiedbythe secondauthorofthisstudy(JLF-T).Thespecimensusedtodescribe theparasitoidinthepresentstudywerepartoftheonesusedfor thebiologicalstudybyTavaresetal.(2012).

AwealthofinformationonA.minuta,includingadditional pic-tures(eggs,larvae,pupae,cocoons,andadultsofA.minutaaswellas damagecausedbyitslarvae)wasprovidedbyTavaresetal.(2012).

PhotoswerepreparedusingaKeyenceVHX-1000Digital Micro-scope(KeyenceCorporationofAmerica;Illinois,UnitedStatesof America),usingalenswitharangeof10–130×.Multipleimages weretakenofastructurethroughthefocalplaneandthen com-bined to produce a single in-focus image using the software associatedwiththeKeyenceSystem.Plateswerepreparedusing MicrosoftPowerPoint2010.

Results

DiolcogasterflammeusSalgado-Neto&Fernández-Trianasp. nov.

Description.Diagnosis.Thisistheonlyyellow-orangespecies

of thexanthaspisgrouprecordedin theNew Worldthus far.It ispossiblethatmore yellow-orangeNewWorldspecies willbe discoveredina nearfuture.Female(Fig.2).Bodycolorentirely yellowtoorangeyellow,exceptfordarkbrowntoblackon flag-ellomeres,parts ofthescape,andmostoftheinterocellararea, andmostofT2–T4brown.Forewingwithpterostigmaandveins brown. Headmostly with striatesculptureon face,frons, gena andvertex;occiputstronglyconcaveandsmooth.Mesosomawith anteromesoscutumand scutellardiskrugose-punctate,scutellar diskposteriorlywithakeel;propodeumwithstrongandcomplete mediancarina,andadditionaltransverserugosityonposterior0.6 ofpropodeum.MetasomawithT1slightlywideningtoward pos-teriormarginand withstrongand deepmediansulcusrunning throughout the entire tergite; T2 subtriangular, withrelatively strongsulcusdelimitinglateralmarginsandacentralareathatis slightlyraisedanddelimitedlaterallybypunctures;T3+smooth; ovipositorsheathswithafewsetaeonapical0.3.Metacoxa rela-tivelylarge,morethanhalfthelengthofmetasoma.Measurements (allin mm).Bodylength:3.50.Forewinglength:3.4.Metacoxa length:0.96.Metafemurlength/width:1.12/0.31.Metatibialength: 1.22.Lengthofinner/outerspursofmetatibia:0.53/0.30.Length of first segment of metatarsus: 0.70. Ovipositor sheath length: 0.25. T1 length: 0.60; T1 width at anterior margin/maximum width0.20/0.28.T2length/widthatposteriormargin:0.24/0.50. T3 length: 0.36. Lengthof flagellomeres:F1/F2/F3/F14/F15/F16: 0.26/0.26/0.26/0.15/0.15/0.16.

Male(Fig.3).Identicaltofemale.

Remarks. Accountingfor the newspecies fromBrazil being

describedinthisstudy,thefaunaofthexanthaspisgroupinthe NewWorldnowincludesfourspecies(Table1).AkeytoallNew Worldspeciesisprovidedbelow.

1-Bodyalmostentirelyyellowtoorange-yellow(exceptforflagellomeres,

partofscapeandmostofinterocellarareablack,andmostofT2–T4partially

brown)...DiolcogasterflammeusSalgado-Neto&Fernández-Trianasp.nov.

-Bodymostlytopartiallydarkbrowntoblack...2

2(1)Femaleantennarelativelyshort,aslongasforewinglength,andwith

apical8–9flagellomereswithonlyoneplacoderank;metacoxayellowor

white-yellow...Diolcogasteriridescens(Cresson,1865)

-Femaleantennalongerthanforewing,mostflagellomereswithtworanksof

placodes;metacoxablacktodarkbrown...3

3(2)Secondsubmarginalcellofforewingtriangularandrelativelylargein

size,withoutdefinedveinRS+r−m;tergite20.5×aslongastergite3....

Diolcogasterbakeri(Muesebeck,1922)

-Secondsubmarginalcellofforewingrelativelysmallinsize,slit-like,with

shortveinRS+r−m;tergite20.6–0.7×aslongastergite3...Diolcogaster

xanthaspis(Ashmead,1900)

Typematerial. Holotype.Female,“MuseuRegional de

Ento-mologia – UFV, 20◦ 45S×42◦ 51W, 651m above sea level, 18.V.2011,WagnerdeSouzaTavares&JoséColaZanuncio. Holo-type locality: Vic¸osa,MinasGerais State,Brazil.Holotypelabel: WAG01.18.05.2011.Hostplants:C.spicatusandC.spiralisvar. spi-ralis.Hostcaterpillar:A. minuta.Paratypes.Samelocalityasfor holotype,fivefemalesandfivemales(allin“MuseuRegionalde Entomologia–UFV”,exceptonefemaleandonemaleinCanadian NationalCollectionofInsects,Arachnids,andNematodes(CNC),

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Fig.2.(A)Femaleparatype.(B)Head,ventralview.(C)Head,frontalview.(D)Foreandhindwings.(E)Propodeumandmetasomaltergites,dorsalview.(F)Mesosoma,dorsal

view.(G)Miasma,lateralview.(H)Metasoma,dorsalviewofDiolcogasterflammeussp.nov.(Hymenoptera:Braconidae).

Ottawa,Ontario.Labels:Brazil,MinasGerais,Vic¸osa-MinasGerais, 2012, ex. Agarea minuta, coll. G. Salgado-Neto, voucher codes: CNC649489,CNC649490).

Etymology.Thespecificepithet,flammeus,comesfromLatin,

referringtothespeciescolorandmeans“flame”.

Biology.Asolitaryparasitoid,rearedfromA.minuta.The infor-mationavailablesuggeststhatitisextremelyefficientasanatural enemy.LastlarvalinstaroftheparasitoidemergedfromA.minuta caterpillarsandpupatedatthebottomoftheplasticcontaineron filterpaperinthelaboratory.Parasitoidlarvaeproducedacocoon madeofwhitecoloredsilk.Thesilkwaswrappedaroundtheleaves causingthemtofoldandbecomecone-shaped.Parasitized cater-pillarssurvivedonlylongenoughtobuildanextraprotectionlayer fortheparasitoidsandthendied.Caterpillarsofdifferentageswere foundinasamesamplingwhichsuggestsovipositionsatdifferent timesandoverlappinggenerations.

Distribution.SofaronlyfoundinVic¸osa,MinasGeraisState,

Brazil;themunicipalityisinland,300kmnorthofRiodeJaneiro Stateandwestofthecoastby250km.

Discussion

Thefaunaof thexanthaspisgroupin theNewWorldnow is representedbyfourspecies,includingD.bakeri.Astudyrecording theD.bakeri fromPeruisquestionable(sensuFernández-Triana etal.,2009)becauseitwasreportedpreviouslyasaNorth Ameri-canparasitoidspecies(Muesebeck,1922).Diolcogasterhasbeenat timesdividedinspecies-groups(e.g.,Saeedetal.,1999;Whitfield etal.,2009;Zengetal.,2011).Oneofsuchgroups,the xanthap-sisgroup (sensuSaeed et al., 1999), is characterizedbyhaving thehead,anteromesoscutumandscutellardiskrugose-punctate, mediotergite1parallel-sidedand2.0–3.0×aslongasmaximum width,mediotergite2withmoreorlessdistinctmedianfield indi-catedbygrooves(ifnot,thenmedianfield smoothand convex, distinguishedbylongitudinalpits),vannallobeofhindwing con-vexwithmarginalsetae,andpostocellarvertexconcaveindorsal view(Nixon,1965;Mason,1981).Thisgroupwasoriginallyerected byNixon(1965:240),whoconsideredit“anartificialsegregation withinalargecomplexofspecies”.Morphologicaldifferencesand

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Fig.3.(A)Maleparatype.(B)Head,frontalview.(C)Habitus,dorsalview.(D)Propodeumandmetasomaltergite,dorsalview.(E)Forewing.(F)Metasoma,dorsalviewof

Diolcogasterflammeussp.nov.(Hymenoptera:Braconidae).

Table1

Hostcaterpillar(Lepidoptera)(author;family)anditsgeographicaldistribution,hostplant(author;family),andreferenceofspeciesofDiolcogaster(Hymenoptera:Braconidae)

(author).

SpeciesofDiolcogaster Hostcaterpillar Geographicaldistribution Hostplant Reference

D.flammeusSalgado-Neto& Fernández-Trianasp.nov.

Agaraeaminuta(Schaus,1892; Erebidae)

MexicotoBrazil Costusspicatus(Jacq.)Sw.and

C.spiralis(Jacq.)Roscoevar. spiralis;Costaceae

Presentstudy

D.iridescens(Cresson,1865) AsciodesgordialisGuenée, 1854;Crambidae

CubaandsouthernUSA (Florida)

SpeciesofBougainvillea; Nyctaginaceae

Patton(1958)

D.bakeri(Muesebeck,1922) Ponometiacandefacta(Hübner,

[1831])andP.erastrioides

(Guenée,1852;Noctuidae)

Canada(Ontario,Quebecand

Saskatchewan),USA(Arkansas,

Florida,Georgia,Illinois,Iowa,

Kansas,Louisiana,andTexas)

Asteraceaeincludingspeciesof

AsterandAmbrosia

Pogue(2010)and

Stojanovi ´cetal.(2011)

D.xanthaspis(Ashmead,1900) Unknown SaintVincentandthe

Grenadines

Unknown Ashmead(1900)

thedisparatearrangeofhosts knownfor thedescribed species, indeedsuggestthatthisgroupisfarfrommonophyletic(Whitfield etal.,2009),anditisverylikelythatitwillbesplitinthefuture whenmorestudiesoftheworldfaunaofDiolcogasteraredone. Diolcogasterflammeussp.nov.isextremelyefficientasanatural enemy,asitwasrecordedparasitizing90%oftheA.minuta cater-pillarpestscollectedin2010and2011(Tavaresetal.,2012).Inthe field,pupationoftheparasitoidoccurredontheabaxialsurfaces

oftheleavesofC.spicatusandC.spiralisvar.spiralis(Tavaresetal., 2012).AgareaminutaisaseverepestofCostusspeciesbecauseit canreduceplantbiomass(stemheights,leavesperstem,largest widthandgreaterlengthofleaves)(Tavaresetal.,2012).

Conflictsofinterest

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Acknowledgements

WearegratefultoDr.PaulusJohannesMariaMaas(Wageningen University,TheNetherlands)foridentifyingthevarietyofCostus spiralisandDr.AlexandreIgordeAzevedoPereiraforpreparing

Fig.1.Thisstudywassupportedby“ConselhoNacionalde Desen-volvimento Científico e Tecnológico (CNPq)”, “Coordenac¸ão de Aperfeic¸oamentodePessoaldeNívelSuperior(CAPES)”,“Fundac¸ão deAmparoàPesquisadoEstadodeMinasGerais(FAPEMIG)”,and “ProgramaCooperativosobreProtec¸ãoFlorestal(PROTEF)”ofthe “InstitutodePesquisaseEstudosFlorestais(IPEF)”.

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