New species of Lopesia Rübsaamen (Diptera: Cecidomyiidae) associated with Andira humilis Mart. ex Benth. (Fabaceae)

RevistaBrasileiradeEntomologia61(2017)239–242

REVISTA

BRASILEIRA

DE

Entomologia

Systematics,

Morphology

and

Biogeography

New

species

of

Lopesia

Rübsaamen

(Diptera:

Cecidomyiidae)

associated

with

Andira

humilis

Mart.

ex

Benth.

(Fabaceae)

Carolina

de

Almeida

Garcia

_,

_Valdeir

_Pereira

_Lima

_,

_Daniéla

_Cristina

_Calado

_,

Maria

Virginia

Urso-Guimarães

a_{UniversidadeFederaldeSãoCarlos,DepartamentodeBiologia,LaboratóriodeSistemáticadeDiptera,Sorocaba,SP,Brazil} b_{UniversidadeFederaldoOestedaBahia,CentrodasCiênciasBiológicasedaSaúde,LaboratóriodeZoologia,Barreiras,BA,Brazil}

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r

t

i

c

l

e

i

n

f

o

Articlehistory: Received24March2017 Accepted8June2017 Availableonline21June2017 AssociateEditor:MarciaSoutoCouri Keywords: Cerrado Gallmaker Insect–plantinteraction Neotropicalregion Taxonomy

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b

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AnewspeciesofLopesiaRübsaamen,1908inducesleafgallsonAndirahumilis(Fabaceae)intheCerrado biome(Braziliansavanna)ofBahia,MatoGrossoandSãoPaulostates,Brazil.Larva,pupa,female,and maleofthisnewspeciesofgallmidgearedescribedandillustratedinthispaper.

©2017SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction

LopesiaRübsaamen,1908isagenuswith25describedspecies, mainlydistributedinNeotropicalregion,butalsoregisteredinthe Nearctic,Afrotropical,andAustralasiaregions(GagnéandJaschhof, 2014;Urso-Guimarãesetal.,2014;MaiaandMonteiro,2017). Lope-siahas20describedspeciesreportedtoBrazilinAmazonas,Minas Gerais,RiodeJaneiro,Pernambuco,andSãoPauloStates(Gagnéand Jaschhof,2014;Urso-Guimarãesetal.,2014;MaiaandMonteiro, 2017).

In Brazil, eleven families of plants are referred as hosts of Lopesia galls: Burseraceae, Clusiaceae, Chrysobalanaceae, Erythroxylaceae,Euphorbiaceae,Fabaceae,Melastomataceae, Nyc-taginaceae,Sapotaceae(GagnéandJaschhof,2014),Pontederiaceae (Urso-Guimarãesetal.,2014),andDilleniaceae(MaiaandMonteiro, 2017).Six described speciesof LopesiaareknownonFabaceae, LopesiaarmataGagné,1993onAcaciatortilis(Forsk.)Hayne; Lope-sianiloticaeGagné,1993onAcacianilotica(L.)Willd.exDel;Lopesia grandisMaia,2001onDalbergiaecastaphyllum(L.)Taub.;Lopesia mimosae Maia,2010and LopesiapernambucensisMaia,2010 on Mimosatenuiflora(Willd.)Poir;andLopesiaaldinaeFernandesand Maia,2010onAldina heterophyllaSpruceex Benth.(Gagné and

∗ Correspondingauthor.

E-mail:carolina.dag@hotmail.com(C.A.Garcia).

Marohasy,1993;Maia,2001;Maiaetal.,2010;Fernandesetal., 2010).ThisisthefirstreportofLopesiainducinggallsonAndira species.

Here,wedescribedanewspeciesofLopesia,basedon mate-rialcollectedinthreelocalitiesofCerradobiome(Brazil)fromleaf gallsonAndirahumilisMart.exBenth.Andiraspeciesarepopularly knownas“angelimrasteiro”,“angelim-do-campo”or“mata-barata nocampo”(roachkiller),duetoitsuseasaninsecticide.Also,itisa commontreeorshrubendemictoBrazil,foundinAmazonForest, Caatinga,andCerradobiomes.Andiraspeciescanreachonemeter in heightand hasdemonstrated allelopathic potential(Periotto etal.,2004).

Blister-shaped leaf gall on Andira humilis was previously described by Saitoand Urso-Guimarães (2012) and Isaiasetal. (2014)withoutassociationwithitsinducer.Thisisthefirstformal recordofaLopesiaspeciesinducinggallsonAndirahumilis.

Materialandmethods

Brancheswithblister-shapedleafgallofAndirahumiliswere collectedfromthreelocalitiesoftheCerradobiomeinBrazil: Par-que Nacional da Chapada dos Guimarães (PNCG),Chapada dos Guimarães,MatoGrosso,Brazil(15◦2610S,055◦4723W), dur-ingtheSisbiota-DipteraProgram,14-22.i.2013;Estac¸ãoEcológica deJataí(EEJ), LuizAntônio,SãoPauloState(21◦3619.44Sand 47◦4728.86W),19-21.iv.2010;andCampusReitorEdgardSantos http://dx.doi.org/10.1016/j.rbe.2017.06.001

0085-5626/©2017SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http:// creativecommons.org/licenses/by-nc-nd/4.0/).

240 C.A.Garciaetal./RevistaBrasileiradeEntomologia61(2017)239–242

Figs.1–6.Lopesiaandiraesp.nov.1.Malehead(frontalview).2.Thirdmaleflagelomere(frontalview).3.Thirdfemaleflagelomere(frontalview).4.Twelfthfemale flagelomerewithapicalprocess.5.Maletarsalclawandempodia.6.Malewing.

oftheUniversidadeFederaldoOestedaBahia(UFOB),Barreiras, Bahia(12◦0851.4Sand45◦0117.3W),June2015.Thegallswere keptinplasticpotsforrearingofinsects.Larvaeandpupaewere obtainedbydissectingthegalls.Allspecimenswerepreservedin 70%alcoholandposteriorlymountedinslidesfollowingthe tech-niqueandterminologyofGagné(1994).

ThetypesaredepositedattheMuseudeZoologiaofthe Univer-sidadedeSãoPaulo,SãoPaulo,Brazil(MZSP).Additionalmaterial wasdepositedatColec¸ãodoLaboratóriodeZoologiaofthe Univer-sidadeFederaldoOestedaBahia.Ingrid Koch(IB/UNICAMP)and AnaCarolinaDevidesCastelo(UNESP/Botucatu)identifiedtheplant species.

Figs.7–10.Lopesiaandiraesp.nov.7.Malepostabdomem(lateralview).8.Femalepostabdomen(ventro-lateralview).9.Maleterminalia(ventralview).10.Femaleovipositor (lateralview).

C.A.Garciaetal./RevistaBrasileiradeEntomologia61(2017)239–242 241

Figs.11–13.Lopesiaandiraesp.nov.11.Pupalhead(ventralview).12.Prothoracic spatulaandlateralpapillae.13.Larvalterminalsegment(ventralview).

Taxonomy

CecidomyiidaeMacquart,1838 CecidomyiinaeRondani,1840 LopesiaRübsaamen,1908

Diagnosis. R5 joining C beyondthewing apex;Rs closerto

theendofR1thantothearculus;palpithreeorfour-segmented;

antennaewithbinodalandtricircunfilarflagellomeres(inmale), orinterconnectedcircumfila(infemale);tarsalclawscurvednear basalthird,generallytoothed;ovipositorshort,barelyprotrusible andfemalecerciseparate(Maiaetal.,2010;Maia,2015).

Description.Adult–Body:1.4mmlong(male,n=14),1.9mm long(female,n=18).Head(Fig.1):eyesblack,holoptic,facets circu-lar,closelyadjacent.Occipitalprocesspresent.Frontoclypeuswith 10setae;labrumtriangularwiththreepairsofsetae; hypophar-ynxofthesameshapeaslabrum;labellaelongate-convex,each withseverallonglateralsetae;palpitotallength,0.1mm,palpi 4-segmented.Antennaetotallength,0.8mm(female);scapeand pedicellongandmaximumwide,0.05mm;scapebroaderdistally; 12binodaltricircumfilarflagellomeres;circumfilawhorlsirregular inlengthin males,medialwhorlsshorter thandistal and basal whorls(Fig.2),cylindricalflagellomereswithinterconnected cir-cumfilainfemales(Fig.3),apicalprocesspresent(Fig.4),setulose necksinbothsexes.Thorax:scutumandscutelumbrown.Scutum withtworowsofdorsocentralandonerowofnotopleuralsetae; anepimeronwith16setae;laterotergitewithtwolongtrichoid sen-silla,otherscleritesbare.Legs:tarsalclawsbendnearmidlength and2-toothed(Fig.5);empodiashorterthanclaws.Wing1.25mm longand0.5mmwide(male,n=14),1.7mmlongand0.6mmwide

(male,n=14);venationasinFig.6.Abdomen.Male(Fig.7):Tergites 1–7rectangularwithacompleterowofposteriorsetae;irregular mesalrowsofsetae;Tergite8setose,weaklysclerotized. Stern-ites1–7astergites1–7.Sternite8rectangularandsetose.Trichoid sensillaabsentintergitesandsternites.Female(Fig.8):Tergites 1–7rectangularwithacompleterowofposteriorsetae;irregular mesalrowsofsetae;Tergite8setoseandnotsclerotized. Stern-ites1–7astergites 1–7.Sternite8astergite8.Trichoid sensilla absentintergitesandsternites.Maleterminalia(Fig.9): gonocox-itessplayed;wideandroundedwithmesobasallobediscreet;setae placed onlyonexternalsurface;gonostyluselongated,widerat baseandapicallynarrow;shorterthangonocoxite,sparsely cov-eredwithsetaeandmicrosetulae,teethentireandstrong;cercus setoseandbilobed(outerlobelittlelongerthantheinner),irregular margin;hypoproctdeeplybilobed,setose,andlongerthancerci; aedeaguslarge,elongate,taperinggraduallytotheapex,and1.5 longerthanhypoproct.Ovipositor(Fig.10):0.18mmlong;slightly protrusible, female cerci separate,ovoid and setose; hypoproct shortandsetose.

Pupa. Yellowish.Body2.18mm long(n=31).Head(Fig.11): antennalhorns,0.12mmlong,triangular,sclerotized,threelateral papillaepresent,twowithsetaeandoneasetose,twopairsoffacial papillaepresent,onepairsetoseandoneasetose.Cephalicsetae 0.06mmlong.Thorax: wingreachingthirdabdominalsegment; firstpairoflegsreachingtheposteriormarginoffifthabdominal segment,secondpairreachingthe1/3ofsixthabdominalsegment, andthirdpairsreachingtheposteriormarginofsixthabdominal segment.Prothoracicspiraclesetiform,0.16mmlong.Abdomen: abdominaltergiteswithdorsalspinesabsent,spiculespresent. Ter-minalsegmentas0.15mmlongaswide(n=31).Pupationingall.

Larva3rdinstar.Yellowish.Body1.5mmlong(n=2). Integu-ment rough. Spatula 2-toothed with long stalk (0.1mm long), pointedteethfarapartfromeachother(Fig.12).Twogroupsof threepapillaeperside,twoofeachgroupsetoseandoneasetose. Terminalsegmentconvexwiththreepairsofcorniformpapillae, onelongerthantheothertwo(Fig.13).

Types.Holotype:Brazil,MatoGrosso,ChapadadosGuimarães (Parque Nacional Chapada dos Guimarães) (15◦2610S, 055◦4723W), reared from leaf galls of Andira humilis, col-lectedin14.i.2013,emergedin17.vii.2013,M.V.Urso-Guimarães col.(♂MZSP).

Paratypes.MatoGrossoState–ChapadadosGuimarães(Parque Nacional Chapada dos Guimarães) (15◦2610S, 055◦4723W): 16 ♂, 15♀, 31 pupalexuvia,2larvae; rearedfrom leafgallsof Andirahumilis,collectedin14.i.2013,emergedin17.vii.2013,M.V. Urso-Guimarãescol.(MZSP);BahiaState–Barreiras(12◦0851.4S and45◦0117.3W):3♂,10♀, 3pupalexuviae,2larvae,reared fromleaf gallsof Andirahumilis, collectedinvi.2015, V.P.Lima col.(UFOB);SãoPauloState– LuizAntônio(21◦3619.44Sand 47◦4728.86W): leaf galls of Andira humilis, collected in 19-21.iv.2010,V.S.SaitoandM.V.Urso-Guimarãescol.

Etymology.Thespeciesnamereferstothegenericnameofthe hostplant.

Gallandbiology(Fig.14).Blister-shaped,green,andbareleaf gall occurs only onthe upper surface of leaf in Andira humilis (Fabaceae).Pupationingall.

Remarks.ThenewgallmidgediffersfromotherknownLopesia inhavingthelarvalterminalsegmentwiththreepairsof corni-formpapillae,onelongerthantheothertwoinaroundedterminal segmentandawideaedeagusinmales.

ThekeytosegregationofLopesiaspeciesofRodriguesandMaia (2010)indicatesthatL.andiraespnov.resemblesL.ellipticaMaia, 2003,insuchcharacteristics:setuloseflagellomerenecks,narrow gonocoxites,malebinodalflagelomeres,wingwithRsjoiningR1

242 C.A.Garciaetal./RevistaBrasileiradeEntomologia61(2017)239–242

Fig.14.LeafgallsofLopesiaandiraesp.nov.onAndirahumilis(Fabaceae).

aftermidlength,and2-toothedtarsalclaws,however,Lopesia ellip-ticahasanarrowaedeagus,whilethenewspeciespresentsalarge aedeagus.

ThepupaeofthenewspeciessharewithL.similisMaia,2004 theantennalhorndeveloped,theconspicuousapicalsetae,dorsal abdominalspinesabsent,andcephalicspinesabsent,butthe anten-nalbaseofthepupaeofL.similishasasmalldenticle,absentinthe L.andiraesp.nov.

L.andiraesp.nov.isalsocloselyrelatedtoL.singularisMaia,2001 andL.eichhorniaeUrso-Guimarães,2014bythefollowing charac-ters:prothoracicspatulawithtwo teethspaced apartand three pairsofcorniformpapillae,butbothspeciesdiffersfromL. andi-raesp.nov.inhavingbilobedterminalsegmentinsteadofrounded terminalsegment.

Itisknownthatthereisahighspecificitybetweengall mak-ersandtheirhostplants.Asaresult,gallmorphotypesassociated withhostplantsareusedtodistinguishtheirinducerspecies.Thus, despitethemorphologicalfeaturesshownbetweenL.andiraesp. nov.andthespeciesmentionedabove,thisspeciesinduces blister-shapedgallsontheupperleafsurfaceofAndirahumilis(Fabaceae).L. ellipticamakesaparenchymaticgallthatformsanelliptical disten-sionoftheleaf’sepidermisofCalophyllumbrasiliense(Clusiaceae). L.similisinducesagreenleafwitharolled-marginofProtium hepta-phyllum(Aubl.)(Burseraceae)(Naraharaetal.,2004).ThegallsofL. singularisareinducedonPouteriavenosa(Mart.)Bahni(Sapotaceae) andL.eichhorniaecausesswollenrhizomegallsonEichhorniaazurea (Sw.)Kunth(Pontederiaceae).

The association between the host plant Andira humilis (Fabaceae)andthegallmakerLopesiaandiraesp.nov.isreported forthefirsttime,aswellasthegeographicaldistributionofthe LopesiagenustoMatoGrossoandBahiaStates.

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgements

The authorsacknowledgethe supportfrom SisbiotaDiptera Project–Fapesp/CNPq563256/2010-9andCNPq154204/2012-9. Dra.IngridKoch(IB/UNICAMP),MSc.AnaCarolinaDevidesCastelo (UNESP/Botucatu)andRaymondJ.Gagné(SystematicEntomology Laboratory,USDA,Washington,DC,USA)forhiscommentsona draftofthemanuscript.

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