Insect galls on Bauhinia cupulata (Fabaceae): morphotypes characterization and description of a new species of Schizomyia (Cecidomyiidae, Diptera)

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RevistaBrasileiradeEntomologia63(2019)356–362

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

Insect

galls

on

Bauhinia

cupulata

(Fabaceae):

morphotypes

characterization

and

description

of

a

new

species

of

Schizomyia

(Cecidomyiidae,

Diptera)

Débora

Santarém

da

Silva

dos

Santos

b

_,

_Valéria

_Cid

_Maia

b

_,

_Daniéla

_Calado

a,∗ a_Universidade_Federal_do_Oeste_da_Bahia,_Barreiras,_BA,_Brazil

b_Universidade_Federal_do_Rio_de_Janeiro,_Rio_de_Janeiro,_RJ,_Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received24April2019 Accepted19July2019 Availableonline2August2019 AssociateEditor:MarciaSoutoCouri Keywords:

Cerrado Gallmidge

Insect–plantinteraction

a

b

s

t

r

a

c

t

GallsonBauhiniacupulata(Fabaceae)wereinvestigatedintwophysiognomiesoftheCerrado,riparian anddryforest,inthemunicipalityofBarreiras(WesternBahia,Brazil)fromOctober2012toJuly2014. Fourinsectgallmorphotypeswerefound.Theywerecharacterizedbasedonshape,color,indumentum, plantorganofoccurrenceandgallingtaxon.Anewgallingspecies,Schizomyiabarreirensis,isdescribed, illustrated(larva,pupa,male,femaleandgall)andcomparedtootherNeotropicalcongenericspecies.

Introduction

ManyBrazilianinventoriespointouttheFabaceaeasoneofthe plantfamilieswiththehighestnumberofinsectgalls(Araújoetal., 2011,2014,2015;Coelhoetal.,2009;Fernandesetal.,1988,1997; Gonc¸alves-AlvimandFernandes,2001;Luzetal.,2012;Maiaand Fernandes,2004;Santosetal.,2012;Urso-Guimarãesand Scareli-Santos,2006).

Amongthis family, Bauhinia Plum.ex L. Plum. isa speciose pantropicalgenus,within150–160species(VazandTozzi,2003). ItismoreabundantintheNeotropicswitharound110species,98 ofthemrecordedinBrazil(VazandTozzi,2003).Only13speciesof thisgenus,B.acuruanaMoric,B.brevipesVogel,B.cheilantha(Bong.) Steud., B. curvula Benth.,B. forcicataLink., B. holophylla(Bong.) Steud.,B.longifolia(Bong.)Steud.,B.mollis(Bong.),B.cf.outimouta Aubl.,B.pulchellaBenth.,B.rufaGraham,B.ungulataL.andBauhinia cupulataBenth.hostinsectgallsinBrazil(Araújoetal.,2011,2015; Coelhoetal.,2009;Costaetal.,2014;Fernandesetal.,1988,1997; Gonc¸alves-AlvimandFernandes,2001;Luzetal.,2012;Saitoand Urso-Guimarães,2012;Urso-GuimarãesandScareli-Santos,2006; Urso-Guimarãesetal.,2003;LimaandCalado,2018).Additionally, morphotypeswererecordedonundeterminedspeciesofBauhinia (Araújoetal.,2012,2015;Carneiroetal.,2009;Fernandesetal.,

∗ Correspondingauthor.

E-mail:daniccalado@gmail.com(D.Calado).

1997;Maia,2014;MaiaandCarvalho-Fernandes,2016;Nogueira etal.,2016;Ribeiroetal.,2019;Santosetal.,2012;Silvaetal.,2018). AccordingtoSilvaetal.(2018),Bauhiniahostsagreatdiversityof insectgalls,whichprobablyisduetogenusbeveryspeciose. Nev-ertheless,onlythreegallingspecieswereidentiﬁed:Asphondylia micropillataMaia,2005,SchizomyiamacropillataMaia,2005andS. tuiuiuUrso-GuimarãesandAmorim,2002.Theothergallerswere identiﬁedinorderorfamilylevel.

Inthepresentstudy,BauhiniacupulataBenth.(Fabaceae), pop-ularlyknownas“pata-de-vaca”,wassurveyedforinsectgalls.Itis anativeshruborasmalltreethatoccursinthestatesofAlagoas, Bahia,Ceará,Maranhão,Paraíba,Pernambuco,Piauí,RioGrandedo Norte,Sergipe,Goiás,Pará,Tocantins,DistritoFederal,MatoGrosso, andMatoGrossodoSulandcanbefoundinthreephytogeographic domains:Amazon,Cerradoand Caatinga(Vazand Tozzi,2003). GallsonBauhiniacupulatahave beencited byLimaand Calado (2018).

ThisstudyaimstocharacterizetheinsectgallsinBauhinia cupu-lataanddescribeanewspeciesofSchizomyia,whichinducesaleaf gallonthishostplant.

Materialandmethods

Studiedarea:TwophysiognomiesofCerradowereinvestigated inthemunicipalityofBarreiras (westernportionof thestateof Bahia,Brazil):ariparianforestareaatRiodeOndasinFazendado Gentil(45◦1435.17Wand12◦1246.51S)andadryforestareain

https://doi.org/10.1016/j.rbe.2019.07.002

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D.S.Santosetal./RevistaBrasileiradeEntomologia63(2019)356–362 357

Figs.1–6.DifferentdevelopmentstagesofgallsinducedbySchizomyiabarreirensis,sp.n.(1)Firststage.(2)Secondstage.(3)Thirdstage.(4)Fourthstage.(5)Fifthstage.(6) Laststage(gallcutopentoshowthelarvalchamber).

theCampusReitorEdgardSantos,UniversidadeFederaldoOeste daBahia–UFOB(45◦0106.54Wand12◦0853.05S).

FieldworksweredevelopedmonthlyfromOctober2012toJuly 2014.Fertilebranchesofthehostplantwerecollectedanddried. TheexsiccatewasidentifiedbyJulianaRibasdeMenezes(UFOB) asBauhiniacupulataandthevouchermaterialwasdepositedin theherbariumofUFOB.Fiftyindividualsofthehostplantwere surveyedforinsectgalls.Eachgallmorphotypewasphotographed andcharacterizedbyshape,color,organplant,presence/absenceof trichomes,numberofinternalchambersandgallinginsect.Forleaf galls,theoccurrenceintheadaxialorabaxialsurfacewasobserved. Toobtaintheadults,twogalledbranchesofeachindividualof thehostplantwererandomlybaggedinthefieldwith“voil”until thegallsputrefaction.Thebagswereweeklychecked.Other sam-plesweretakentothelaboratory,wheretheyweredissectedto obtainlarvaeandpupaeofeachgallinginsect.Adultsand imma-turestageswerefixedin70%alcoholinlabeledtubes.Later,they weremountedonslides,followingthemethodologyoutlinedby

Gagné(1994).KeyspresentinGagné(1994)wereusedtoidentify thegenera.PartofthematerialisdepositedintheEntomological ColletionofMuseuNacional,RiodeJaneiro(MNRJ)andpartinthe

EntomologicalCollectionoftheUFOB.Morphologicalterminology foradultsandimmaturestagesfollowsthatofGagné(1994).

Results

FourgallmorphotypeswerefoundonBauhiniacupulata.Oneis globoid,one-chambered,ontheleafadaxialsurface.Itisinduced bySchizomyiasp.(Diptera,Cecidomyiidae).Thisgallsuffers mor-phologicalchangesduringitsdevelopment.Intheearlystage,itis greenandglabrous.Later,itbecomesentirelycoveredwithred tri-chomes.Then,thetrichomesbecomewhiteandﬁnallybrowninthe maturegall(Figs.1–6).Theotherisfusiform,brown,glabrous, one-chambered,onstems.Itsinducerwasnotdetermined,asthegalls werealreadyemptywhencollected,presentingseveralemergence holes(Fig.7).Thethirdmorphotypeisgloboid,brown,glabrous, one-chambered,onstems.ItisinducedbyAsphondyliasp.(Diptera, Cecidomyiidae) (Figs. 8–10).The fourth is globoid, greenish or yellowish,withtrichomes,projectedsimultaneouslyontheleaf adaxialandabaxialsurfaces.ItisinducedbyAlycaulini(Diptera, Cecidomyiidae)(Figs.11and12).Consideringthehighspeciﬁcity

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358 D.S.Santosetal./RevistaBrasileiradeEntomologia63(2019)356–362

Figs7–12.GeneralviewofgallsinBauhiniacupulata(Fabaceae).(7)Fusiformstemgall,inducernotdetermined;(8–10)GloboidstemgallinducedbyAsphondyliasp.;(11–12) GloboidleafgallsinducedbyAlycauliniontheadaxialandabaxialsurfaces,respectively.

ofthegallingspecies,theseinducersareprobablynew,asthereisno describedgallmidgespeciesinassociationwithBauhiniacupulata. Amore detailed morphological studyof Schizomyia sp. con-ﬁrmedthatitbelongstoanewspecies,whichisdescribedherein. SchizomyiaKieffer,1889ischaracterizedbypresentingneedlelike ovipositor,four-segmentedpalpi,andlarvawithfourpairsof ter-minalpapillae(Gagné,1994).Thisisacosmopolitangenuswith 55species,elevenNeotropical,namely:S.ipomoeaeFelt,1910;S. lorocoGagné,2008;S.manihotiTavares,1925;S.maricaensisSouza andMaia,2007;S.microcapillataMaia,2005;S.rivinaeFelt,1908; S.santosiMaiaandAraújo,2009;S.serjaniaeMöhn1960;S. spher-icaMaiaandOliveira,2007;S.stachytarphetaeBarnes1932;and S.tuiuiuUrso-GuimarãesandAmorim2002(GagnéandJaschhof, 2017).

Schizomyiabarreirensissp.nov.

Description.Adult.Bodylength,1.36–1.80mminmale (n=12); 1.72–2.0mminfemale(n=11).Head(Fig.13).Occipitalprocess present.Eyesfacets hexagonal.Antennae: scapecylindrical and setose;pedicelglobularsetose;12ﬂagellomeresbandedinboth sexes (yellowish onproximal 1/2 to 1/3and fuscous ondistal 1/2), allcylindrical with bare neck.Circumﬁla sinuous in male (Fig.14)andlinearinfemale(Fig.15).Frontoclypeuswith8–9setae perside(n=5).Labrumtriangularwith3pairsofsetae.Labellae

elongatedandconvexinfrontalview,eachwith5lateralsetaeand threeshortmesalsetae(n=3).Palpus4-segmented;theﬁrst seg-mentovoidandotherscylindrical,increasinginlength,allsetose. Lengthofpalpus:segmentI:0.03mm;II:0.05–0.06;III:0.07–0.08 andIV:0.09(n=2).Hypopharynxsimilartothelabrumand setu-loseapically.Thorax.Scutumwith2longitudinalcentralrowsof setaewithafewscalesintermixed,2longitudinallateralrowsof setaealongmostofscutallengthwithafewscalesintermixed; scutellumwithsingleposteriorrowofsetae,somescatteredsetae atmidlengthandfewscales;anepimeronwithalongitudinalsingle rowofsetae,exceptanteriorly,wherethesetaearemorenumerous, otherpleurabare.Wing.Length(fromarculustotheapex):male, 1.36–1.92mm(n=10);female,1.72–2.32mm(n=8).Tarsalclaws simpleinalllegs,7.5timesaslongaspulvilli,empodiumlongand welldevelopednotexceedingthecurvatureofclaws(Fig.16).

Maleabdomen(Fig.17):Firstthroughsixthtergitesentire, rect-angular,eachwithsingle,uninterrupted,posteriorrowofsetae, no lateralsetae, a pair of trichoid sensillaon anterior margin, andotherwiseevenlycoveredwithscales.Seventhtergiteentire, rectangularwithmorenumerousposteriorsetae,irregularly dis-tributed,not forminga row, nolateralsetae,a pairof trichoid sensillaonanteriormargin,and otherwiseevenlycovered with scales.Eighth tergitepigmented,narrow,withonlytheanterior pairoftrichoidsensilla.Secondthroughsixthsternites rectangu-lar,morestronglypigmentedatmidlengthandposteriorly,with singleposteriorrowofsetae,separatedfromahorizontalgroupof

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Figs.13–18.Schizomyiabarreirensissp.n.(13)Male,head(frontalview);(14)Male,ﬂagellomere3;(15)Female,ﬂagellomere2;(16)Tarsalclawsandempodium;(17)Male, abdominalsegments3–8(lateralview);(18)Male,terminalia(dorsalview).Scalebarsinmm.

setaeatmidlength,lateralsetae,aanteriorpairofclosely approxi-matedtrichoidsensilla,andotherwiseevenlycoveredwithscales. Seventhandeigthsternitessimilartoprecedingexceptforits uni-formpigmentationandmorenumeroussetaenearmidlength,and

theanteriorpairofthetrichoidsensillaoftheeigthsternitewidely separatedfromoneanother.Maleterminalia(Figs.18). Gonocox-itenarrowandsetose,elongated,about2.3timeslongerthanwide, producedposteroventrally,proximomediallobesetose,gonostylus

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Figs.19and20.Schizomyiabarreirensis,sp.n.(19)Female,abdominalsegments7–8(lateralview);(20)Ovipositor(ventralview).Scalebarsinmm.

rectangular,abouttwiceaslongerthanwide,setose,apicaltooth coveringalmostallapicaledge;cercuswide,setose,with triangu-larlobes,approximatelyaslongashypoproct;hypoproctnarrow, approximatelyaswideasaedeagus,apicallydividedintotwolobes eachwithanapicalwithseta;aedeagusgraduallytaperingfrom widebasetonarrow,acuteapically,longerthanhypoproct.Female abdomen(Fig.19):tergites1–7asinmale,tergite8sclerotized, withalateralreentrance,abasalpairoftrichoidsensilla,caudal rowsofsetae,somelateralsetaeandscatteredscales.Firstthrough sixthtergitesasformale.Seventhtergitewithsingle,fullrowof posteriorsetaeandseverallateralsetae.Eighthtergitewith ante-riorpairoftrichoidsensillaastheonlyvestiture,posteriormargin deeplyconcaveonlateralthirdandshallowlyconcavemedially, theconcavityaccommodatingpairofsmalldorsallobesbetween tergiteandovipositor.Secondthroughsixthsternitesasformale. Seventhsterniteenlarged,morestronglysclerotizedthan preced-ingandcompletelycoveredwithsetae.

Ovipositor(Figs. 19 and 20).Elongate,protrusible, needle part about1.8timeslengthofseventhsternite;cerciseparate,withsetae atmidlengthandapically.

Pupa. Weakly sclerotized with light brown color. Body length 1.84–2.2mm (n=3). Head (Fig. 21): base of antenna obtusely

quadrangularatapexinventralview,cephalicsetae0.09mmlong (n=1),tegumentgrainy,3 pairsof lateralfacial papillae (1pair withshortseta and theothers asetose);2 pairs oflower facial papillae(1pairwithlongsetae,andotherasetose).Thorax: Protho-racicspiracleelongate,setiform,0.16–0.19mmlong(n=4)(Fig.21). Wingsheath reachingthedistalmargin ofthethird abdominal segment; foreleg,midlegand hindleg sheathsreaching, respec-tively the distal 1/5 of theﬁfth abdominal segment, the distal 1/4ofthesixthabdominalsegmentand perpassingslightlythe 1/2oftheseventhabdominalsegment.Abdomen(Fig.22): Seg-ments2–7with dorsal spines ofthe varyingsizes inthe basal half,onlyonthedisk,followed bymanytinyspinules through-outtherestof thesegment,exceptinthedistalquarter, where there are soft sculptures. Segment 8 with at least four dorsal short spines in the basal half, on thedisc, many tiny spinules elsewhere.

Larva. Color orange. Body elongate and fusiform. Length: 2.73–3.6mm (n=15). Integument completely grainy. Spatula (Fig. 23)robust with2 teeth,with0.18–0.20mm (n=9). Apical teethspacedout,stalkstriatedandelongated.Lateralpapillaeinto twogroups ofthreepapillae each,onebare andtheotherwith seta.Abdominalsegment8withmedialprojectionbearingpairof

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Figs.21–24.Schizomyiabarreirensis,sp.n.,immaturestages.(21–22)Pupa.(21)Headpupal(frontalview).(22)Abdominalsegment6(dorsalview);(23–24)Larva.(23) Prothoracicspatula,sternalandlateralpapillae(ventralview).(24)Terminalsegmentwithterminalpapillae(dorsalview).Scalebarsinmm.

papillaesetose.Terminalsegmentconvexwithfourpairsof papil-lae:onerecurvedandcorniformandthreewithshortsetae(oneof themwithsetalongerthantheothers)(Fig.24).

Material examined. Holotype male. BRAZIL, Bahia: Barreiras, 11.XI.2013.D.Santoscol.(MNRJ).Paratypes: samedata,1male (MNRJ), 1female (MNRJ);same localityand collector: 3males, 26.X.2013 (MNRJ); 2 females and 4 pupal exuviae, 10.X.2013 (MNRJ); 1 female, 03.XI.2012 (UFOB); 1 female and 1 male,

11.XI.2013 (UFOB);1 male,26.X.2013 (UFOB); 2pupalexuviae, 13.VII.2014 (MNRJ);2 pupalexuvia,13.II.2014 (MNRJ);1 larva, 19.VI.2013(MNRJ);2larvae,20.VI.2013(MNRJ);1larva,14.VI.2013 (MNRJ);1 larva,03.VII.2013(MNRJ);1 larva,18.V.2014 (MNRJ). Additionalmaterial:BRAZIL,Bahia:Barreiras,samelocalityand col-lector,4males,2females,10.X.2013,1pupalexuvia,28.X.2012;1 larva,20.VI.2013;1larva,18.II.2014;2larvae,23.II.2014;2larvae, 18.V.2014(MNRJ).

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Etymology.Thespeciﬁcepithet“barreirensis”referstothe type-locality:Barreiras,Bahia,Brazil.

Remarks.TheSchizomyiaspeciesknownfromtheWestern Hemi-spherecanbedividedintotwogroupsbasedonacropodfeatures, onewithfalcateclawsandempodianomorethan1/3thelengthof theclawsandtheotherwithhook-liketarsalclawsandempodia nearlyaslongastheclaws.Thenewspeciesbelongstothesecond group,whichalsoincludesS.ipomoeaeFelt,1910,S.maricaensis Souza&Maia,2007,S.macrocapillataMaia,2005,S.santosiMaia& Araújo,2009,S.serjaniaeMöhn,1960,S.sphericaMaia&Oliveira, 2007,S.stachytarphetaeBarnes,1932,andS.tuiuiuUrso-Guimarães &Amorim,2002.Onlytwoofthem,S.macrocapillataandS.tuiuiu, inducegallsonthesameplantfamilyandsameplantgenusofthose ofS.barreirensis,butindifferenthostspecies:B.brevipesVogel,B. rufa(Bong.)Steud.,andB.cupulatarespectively.Thesethreespecies werecollectedinCerradoareas.

Amongthesecondgroupofspecies,S.barreirensispresentsmore morphologicalsimilaritiestoS.macropillataregardingtheadults’ characters.Thenumberoffrontoclipealsetaeis14–18inS. bar-reirensis,14–16inS.macropillata,53inS.maricaensis,13–24inS. santosi,20inS.spherica,14inS.tuiuiu,nodataonS.serjaniae).The gonostyliarerectangulartoovoidinS.barreirensis,S.macropillata, S.maricaensisandS.macropillata,conicalinS.santosi,;claviformin S.spherica,biﬁdinS.ipomoeae;themalesofS.tuiuiuandofS. serja-niaeareunknown.Theneedlepartoftheovipositoris1.8timesas longasthe7thsterniteinS.barreirensis,1.9inS.macropillata,2.6in S.spherica,2.8inS.maricaensis,5.0inS.tuiuiu,5.8inS.santosi,no dataonS.serjaniae).ImmaturephasesofS.barreirensisandthose ofS.macropillataalsopresentmorphologicalsimilarities,suchas: lengthoftheapicalseta(pupa)–0.09mmlonginS.barreirensis, 0.09–0.10mminS.tuiuiu,0.02–0.04mminS.maricaensis,0.07mm inS.santosi,0.12mminS.spherical,0.08mminS.tuiuiu,nodataonS. serjaniae),lengthoftheprothoracicspatula(pupa)–0.18–0.20mm inS.barreirensis,0.20mminS.macropillata,0.14mminS.santosi, 0.17mminS.spherical,0.28–0.58mminS.serjaniae,thelarvaeof S.maricaensisandofS.tuiuiuareunknown.

ManyofthesecharacterswerenotdescribedforS.serjaniae,whose pupaandmaleareunknown.Nevertheless,thefollowing charac-terscanbeusedtodistinguishthenewspeciesfromS.serjaniae: shapeandproportionsofthelasttwoﬂagellomeres(11thand12th cylindricalandgraduallyshorterthantheprecedentinS. barreiren-sis;11thovoid,12thgloboid,bothconspicuouslyshorterthanthe precedentinS.serjaniae),shapeofthetarsalclaws(almoststraight inS.barreirensisandaccentuallycurvedinS.serjaniae),andshape ofthespatula(anteriorteethwithconcaveoutermargininS. bar-reirensis;anteriorteethwithconvexoutermargininS.serjaniae). ThenewspeciesdiffersfromS.macropillatainthefollowing char-acters:in adults– palpiwithﬁrstsegment obconical(spherical inthelatter),labellaewithacuminateapex(roundededgeinthe latter),longergonocoxites,inpupae–longerprothoracicspiracle (0.16–0.19mminS.barreirensisand0.06–0.09mminS. macropil-lata)anddorsalspinesfromthe2ndto7thabdominalsegments (fromthe3rdto9thabdominalsegmentsinS.macropillata).

Conﬂictsofinterest

Theauthorsdeclarenoconﬂictsofinterest.

Acknowledgments

VCMthankstoConselhoNacionaldeDesenvolvimento Cien-tíﬁco e Tecnológico (CNPq) (Process. 301481/2017-2) for the

financial support. This study was financed in part by the CoordenaçãodeAperfeiçoamentodePessoaldeNívelSuperior -Brasil(CAPES)-FinanceCode001.

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