Lopesia indaiensis (Diptera, Cecidomyiidae), a new species of gall midge feeding on Andira fraxinifolia Benth (Fabaceae), an endemic plant in Brazil

REVISTA

BRASILEIRA

DE

Entomologia

Systematics,

Morphology

and

Biogeography

Lopesia

indaiensis

(Diptera,

Cecidomyiidae),

a

new

species

of

gall

midge

feeding

on

Andira

fraxinifolia

Benth

(Fabaceae),

an

endemic

plant

in

Brazil

Valéria

Cid

Maia

_,

_Lázaro

_Araújo

_de

_Oliveira

a_{MuseuNacional,QuintadaBoaVista,RiodeJaneiro,RJ,Brazil}

b_{FaculdadedeFilosofia,CiênciaseLetrasdoAltoSãoFrancisco,DepartamentodeCiênciasBiológicas,Luz,MG,Brazil}

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received14November2017 Accepted12January2018 Availableonline12February2018 AssociateEditor:MarciaSoutoCouri Keywords: Insect–plantinteraction Morphology Neotropical Taxonomy

a

b

s

t

r

a

c

t

Lopesiaindaiensis(Diptera,Cecidomyiidae),anewspeciesofgallmidgefoundcausinggallsonAndira fraxinifolia(Fabaceae),anendemicplantspeciesinBrazil,isdescribedbasedonlarva,pupa,maleand female.L.indaiensisgallswerecollectedinDoresdoIndaiá,StateofMinasGerais,SoutheasternBrazil. Larvaewereremovedfromthegallsandpupaeandadultswereobtainedbyrearing.Thespecimenswere mountedonslidesandthemostimportantmorphologicalcharacterswereillustrated.Thenewspecies wascomparedtotheotherspeciesofLopesia.

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

Introduction

AndirafraxinifoliaBenth(Fabaceae)isaheliophytic,evergreen, woodyplant,whichisendemicinBrazil(Lorenzi,1992).Itoccursin theAtlanticforest,CerradoandCaatingaandhasbeenfoundfrom RioGrandedoSultoPiauíStates.Duetoitsgoodpropagationand fastgermination,thisspecieshasgreatimportanceforrecovering disturbedareas(BackesandIrgang,2004).

Fourgallmorphotypeshavebeenrecordedonthisplantspecies. One of them (Fig.1) is a vermiform leaf fold foundin several areasofAtlanticforest(SoutheasternBrazil:Bertioga/StateofSão Paulo,MangaratibaandMaricá/StateofRiodeJaneiro; Northeast-ernBrazil:Tamandaré/StateofPernambuco),aswellasinaCerrado area(SoutheasternBrazil:DoresdoIndaiá,StateofMinasGerais) (Table1).ThisgallisinducedbyanewspeciesofLopesia Rübsaa-men,1908(Diptera,Cecidomyiidae).

SimilargallshavebeenrecordedonAndirasp.inBahia (North-eastern)(Tavares,1920)andAndirahumilisMart.exBenth.inMato Grosso(Midwestern), SãoPauloand Bahia(Garcia et al.,2017). Theformer is inducedby AndirodiplosisbahiensisTavares,1920

(Cecidomyiidae)andthelatterbyLopesiaandiraeGarcia,Lima, Cal-adoandUrso-Guimarães,2017.

∗ Correspondingauthor.

E-mail:maiavcid@acd.ufrj.br(V.C.Maia).

Fig.1.GallsofLopesiaindaiensis,sp.n.,onleafofAndirafraxinifoliaBenth(Fabaceae), generalaspect.

Inthisstudy,wedescribeanewspeciesofLopesiathatinduces vermiformgallsonleavesofA.fraxinifoliabasedonmaterialfrom MinasGerais.Thisgenusisknownfrom25describedspecies,20 ofthemfromtheNeotropics.TheotherspeciesareAfrotropical (threespp.),Nearctic(onesp.)andAustralasian(onesp.)(Gagné andJaschhof,2017;MaiaandMonteiro,2017).

https://doi.org/10.1016/j.rbe.2018.01.001

0085-5626/©2018SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http:// creativecommons.org/licenses/by-nc-nd/4.0/).

126 V.C.Maia,L.A.Oliveira/RevistaBrasileiradeEntomologia62(2018)125–130

Table1

InsectgallsinAndirafraxinifoliaBenth(Fabaceae):characterization,localityandreference.

Galledorgan Gallshape Gallinginsect Locality Domainphytogeopraphic Reference Leaf Vermiform Cecidomyiidi Bertioga/SP Atlanticforest Maiaetal.(2008)

Lopesiasp. Mangaratiba/RJ Atlanticforest Rodriguesetal.(2014)

Cecidomyiidae Tamandaré/PE Atlanticforest Santosetal.(2012)

Lopesiaindaiensis,sp.n. DoresdoIndaiá/MG Cerrado Presentwork

Leaf Globoid Asphondyliina Bertioga/SP Atlanticforest Maiaetal.(2008)

Asphondyliasp. Mangaratiba/RJ Atlanticforest Rodriguesetal.(2014)

Asphondyliina SantaTeresa/ES Atlanticforest Maiaetal.(2014)

Stem Fusiform Curculionidae Bertioga/SP Atlanticforest Maiaetal.(2008)

Notdetermined Tamandaré/PE Atlanticforest Santosetal.(2012)

Curculionidae SantaTeresa/ES Atlanticforest Maiaetal.(2014)

Leaf Lenticular Meunieriellasp. Maricá Atlanticforest Maiaetal.(2002)

Meunieriellasp. AraruamaandArraialdoCabo/RJ Atlanticforest Carvalho-Fernandesetal.(2016)

Materialandmethods

BranchesofA.fraxinifoliawithleafgallswerecollectedatPorcos Farm(19◦3018.99S–45◦4100.88W),municipalityofDoresdo Indaiá,StateofMinasGerais(SoutheasternBrazil),inAprilof2009. Gallswerefoundonanindividualplantsituatedintheborderofa Cerradofragment.Mostleavesweregalledandleafletshostedone toseveralgalls.Thepresenceofmorethanthreegallsonthesame leafletcauseditsdistortion.

Galledbrancheswereremovedfromthehostplantand trans-portedin plasticbags tothelaboratoryof theDepartamentode CiênciasBiológicas/FaculdadedeFilosofia,CiênciaseLetrasdoAlto SãoFrancisco,wheresomegallsweredissectedunderastereoscopic microscopetoobtainlarvaeandpupae.Othergalledbrancheswere wrappedinwetcottonatthebasisandkeptinplasticpotscovered byafinescreeninguntiladults’emergence,whenthesepotswere putinarefrigeratortocauseinsects’lethargy.Then,midgeswere collectedusinga70%ethanolsoakedpaintbrush.

Allspecimenswerefirstpreservedin70%ethanol,thenmounted onmicroscopeslides, followingthemethodsoutlinedbyGagné (1994)anddepositedintheEntomologicalCollectionoftheMuseu Nacional/UniversidadeFederaldoRiodeJaneiro(MNRJ).

Samplesofthehostplantwerepressed,dried,identifiedbyDr. FernandoAugusto deOliveiraeSilveira(UniversidadeFederalde MinasGerais)andkeptinhislaboratoryasavouchermaterial.

Results

Lopesiaindaiensis,sp.n.(Figs.2–13)

ThenewspecieswasplacedinLopesiaduetofour-segmented palpi, R5 curved at its juncture with Rs, Rs situated near the midlengthofR1,shortfemalepostabdomenanditscerciwithmany short,sensorysetae,andlarvawithcorniformterminalpapillae, eachonaterminalprojection.

Diagnosis.Adultswith1st–11thantennalflagellomeresneck partiallysetuloseinbothsexes,12thflagellomerewithapical pro-cessentirelysetuloseinboth sexes,four-segmentedpalpi,male circumfilawithallloopssimilarin length,tarsalclawwithtwo teeth,8thmaletergitenarrow,elongated,withonlybasalpairof trichoidsensilla;pupawithantennalbasismodifiedinto anteri-orlypointedprojection,withinnermarginslightlyserrated,apical platedeeplybilobed,prothoracicspiraclelongandabdominal dor-salspinesabsent;larvawithspatulatwo-toothedandfourpairsof corniformterminalpapillae.

Larva. Fusiform and cylindrical body; 1.90–2.60mm long (n=05). Integumentrough. Spatula(Fig.2): 0.17–0.26mm long (n=05),two-toothed,apicalteethtriangular,stalklong.Twogroups ofthreelateralpapillaeoneachsideofspatula(twopairssetoseand asinglesetosepapillaineachgroup)(Fig.2).Terminalsegment (Fig.3):fourpairsofcorniformpapillaesimilarinlength.

2

3

0.04

0.05

Figs.2–3.Lopesiaindaiensis,sp.n.2.Larva,sternalspatulawithadjacentpapillae

(ventralview).3.Larva,terminalsegments(dorsalview).

Pupa.Bodylength:3.10–4.40mm(n=17).Head(Fig.4):apical setae0.07–0.13mmlong(n=11);verticalplatedeeplybilobedat uppermargin,antennalprojectionsslightlyserrated,0.10–0.17mm long(n=17)(fromapextotheupperantennalmargin);twopairs oflowerfacialpapillae(oneasetoseandtheothersetose),three pairs of lateral facial papillae, one pair setose and two with-outseta.Prothoracicspiracle(Fig.4)elongate0.25–0.35mmlong (n=17),sclerotized.Prothoracicintegumentpartiallyrough(Fig.5). Abdominalsegments2–8withoutdorsalspines.

Male. Body length 2.70–3.80mm long (n=12) (including terminalia).Head(Fig.6): apicalprocess absent.Eye facets cir-cular,allcloselyapproximated.Antenna(n=05):scapeobconical,

4

5

0.20

0.20

Figs.4–5.Lopesiaindaiensis,sp.n.4.Pupa,face(ventralview).5.Pupa,anteriorpart(dorsalview).Scalebarsinmm.

pedicel globose,flagellomeres binodaland tricircumfilar;nodes andinternodessetulose,neckspartiallysetulose;threecircumfila ofeachflagellomerewithloopsregularinlength(Fig.7);1stand 2ndflagellomeresconnate,12thflagellomere0.20mmlong(n=5), withapicalprocess entirelysetulose.Frontoclypeus with10–12 setae(n=10).Labrumtriangular,long-attenuate,with3pairsof ventralsensorysetae.Hypopharynxwithanteriorlydirected lat-eralsetulae.Labellaelongate-convex,eachwithlonglateralsetae andthreepairsofshortmesalsensorysetae.Palpus(n=07)with foursegments,allcylindricalwithsetae,1stsegmentshorterthan

theothers,0.03–0.04mmlong,2ndsegment0.08–0.09mmlong, 3rdsegment0.08mmlong,and4thsegment0.08mmlong. Thorax.Wings:length:2.40–2.70mm(n=12).Venation:R5and Rsasinthegenusdiagnosis,CuAforked,M3+4present.Scutum with4longitudinalrowsofsetaewitha fewscalesintermixed, the2dorsocentralrowsbroadestanteriorly,formingasinglerow posteriorly,andthe2lateralasasinglerow.Scutellumwith sev-eralsetae.Anepisternumbare.Anepimeronwithsetae.Tarsalclaws bentnearbaseandtwo-toothed,toothbasalshorterthanthedistal; empodiumshort,notreachingbentinclaws(Fig.8).

128 V.C.Maia,L.A.Oliveira/RevistaBrasileiradeEntomologia62(2018)125–130

6

7

8

0.20

0.05

0.05

0.10

0.05

9

10

Figs.6–10.Lopesiaindaiensis,sp.n.6.Malehead(frontalview).7.Maleflagellomere5.8.Malehindleg,tarsalclawandempodium.9.Maleabdominalsegments7–8(lateral

view).10.Maleterminalia(dorsalview).Scalebarsinmm.

Abdomen(Fig.9):1st–6thtergitessclerotized,rectangular,with asingledistalrowofsetae,fewsetaemesallyandlaterally,basal pairoftrichoidsensilla,andscatteredscales;7thtergitesclerotized, rectangular,withadoubledistalrowofsetae,fewsetaemesallyand laterally,basalpairoftrichoidsensilla,andscatteredscales;8th

tergitesclerotized,narrow,elongated,withonlybasalpairof tri-choidsensilla.2nd–7thsternitessclerotized, rectangular,witha singledistalrowofsetae,manysetaemesallyandlaterally,basal pairoftrichoidsensilla,andscatteredscales;8thsternite sclero-tized,withscatteredsetaeat½distal,lateralsetae,basalpairof

12

13

11

Figs.11–13.Lopesiaindaiensis,sp.n.11.Femaleflagellomere5.12.Femaleabdominalsegments7–8(lateralview).13.Ovipositor(ventralview).Scalebarsinmm.

trichoidsensillaandscatteredscales.Terminalia(Fig.10): gono-coxite partially setose, 0.21–0.22mm long, 0.07–0.08mm wide (n=07),withsetuloseroundedmesobasallobe;gonostylussetulose basally,striatedbeyondbasis,0.11–0.12mmlong,0.02–0.03mm wide(n=07);cerciapicallyroundedwithsetaeandsetulae,cercal lobesconvergent;hypoproctdeeplybilobed,withsetaeand setu-lae,lobeswidelyseparatedandroundedapically;hypoproctmuch longerthancercus;aedeagusaccentuatelylongerthanhypoproct, widerthangonostylus,taperedtoapex,roundedapically,bearing severalasetosepapillae.

Female. Body length 3.90–4.20mm long (n=8) (including ovipositor).Antenna:scapeandpedicelasinmale,flagellomeres cylindrical;nodesentirelysetuloseand neckspartiallysetulose; circumfilamadeoftworings,connectedhorizontally,slightly sin-uous(Fig.11),12thflagellomere0.11–0.13mmlong(n=6),entirely

setulose,apicalprocess0.05–0.07mmlong(n=6)withbasalnode 0.02mmlong(n=6).Frontoclypeuswith10–14setae(n=9). Pal-pus(n=9):1stsegmentshorterthantheothers,2nd–4thsegments subequalinlength,1stsegment0.04–0.05mmlong,2ndsegment 0.09–0.10mmlong,3rdsegment0.08–0.09mmlong,4thsegment 0.09–0.10mmlong.

Thorax.Wings:length:3.00–3.30mm(n=8).

Abdomen(Fig.12):1st–7thtergitesasinmale;8thtergitenot scle-rotized,withbasalpairoftrichoidsensillaanddistalrowofsetae. 2nd–7thsternitesasinmale,8thsternitenotsclerotized,withbasal pairoftrichoidsensillaandarowofdistalsetae.

Ovipositor(Fig.13)barelyprotrusible,0.18–0.21mmlong(from basal margin ofsegment 9 tocerci apex)(n=3),cerci separate elongate-ovoid,0.07–0.08mmlong(n=4)andsetose,hypoproct widewithsetaeandsetulae.

130 V.C.Maia,L.A.Oliveira/RevistaBrasileiradeEntomologia62(2018)125–130 Etymology.Thenameindaiensisreferstothetypelocality.

Materialexamined.Holotypemale.Brazil,MinasGerais:Dores do Indaiá, IV.2009, L. Oliveira col., MNRJ. Paratypes, data as holotype–10 males,9females, 18pupalexuviae and06larvae, MNRJ.

Distribution.Brazil:Pernambuco(Tamandaré),RiodeJaneiro (Mangaratiba)andSãoPaulo(Bertioga)inAtlanticforestareas,and MinasGerais(DoresdoIndaiá)inCerradoareas.

Comments.Lopesiaincludesadultswithbareorsetulose flagel-lomerenecks.Thenewspecieshassetuloseflagellomeresneckas inL.andirae,L.brasiliensisRübsaamen, 1908;L.caulinarisMaia, 2003;L.conspicuaMaia,2003;L.davillaeMaia,2017;L. eichhor-niaeUrso-Guimarães,2014;L.ellipticaMaia,2013;L.erythroxyli Rodrigues&Maia,2010;L.linearisMaia,2003;L.marginalisMaia, 2001;L.maricaensisRodrigues&Maia,2010;L.similisMaia,2004; L.simplexMaia,2002;andL.tibouchinaeMaia,2004.Amongthem, ninespecies have male flagellomereswithbasal and distal cir-cumfilawithwelldevelopedloopsandmidcircumfilawithshorter loopsorwithoutloops(linearcircumfila), namely:L.andirae,L. conspicua,L.davillae,L.eichhorniaeUrso-Guimarães,2014,L. lin-earis,L.marginalis,L.similis,L.simplexandL.tibouchinae;twohave gynecoidcircumfila(L.caulinarisandL.elliptica),threeincludingthe newspecieshaveallcircumfilawithdevelopedloops(L.erythroxyli, L.brasiliensisandthenewspecies)andasingleone,L.maricaensis, hasallcircumfilawithreducedloops.

AdultsofthenewspeciesdifferfromthoseofL.erythroxyliandL. brasiliensismainlybytheshapeofmaleterminalia.Gonocoxites, gonostyliandaedeagusarewiderinL.indaiensisthaninthe oth-ers;thehypoproctofthenewspecieshaslongerlobesthanthose oftheothers,anditscercallobesareconvergent(divergentinthe twootherspecies).Pupaediffermainlyintheshapeandlengthand oftheantennalprojections (slightlyserratedand conspicuously longerinL.indaiensis,notserratedandshorterintheothers),shape oftheapicalplate(deeplybilobedonlyinthenewspecies),and numberofabdominaldorsalspines(noneinL.indaiensis,severalin L.brasiliensisandL.erythroxyli).Besides,theprothoracicspiracles areclearlyshorterinthenewspeciesthaninL.brasiliensis.

AsL.andiraeandL.indaiensisaretheonlytwocongenericspecies associatedwithAndiraLam.,botharecompared:larva–thespatula teethofL.andiraearefarapartfromeachother,whilethoseofL. indaiensisaremorecloselyapproximatedandthespatulabasisof theformerisnarrowwhileinthelatterisanchor-shaped;pupa –theverticalplateconspicuouslymoredeeplybilobedatupper margininL.indaiensis,theantennalprojectionshaveserratedinner marginonlyinthenewspecies,theprothoracicspiracleisclearly longerinthenewspecies(0.16mminL.andiraeand0.25–0.35mm inL.indaiensis),aswellastheapicalsetae(0.06mminL.andiraeand 0.07–0.13mminL.indaiensis);male–themedialcircumfilumhas

shortwhorlswhileinthenewspeciestheyarelong,the8thtergite ofL.andiraeissetosewhereasthatofL.indaiensishasnosetae,the cercusofL.andiraeismoreacutethanthatofthenewspeciesand thehypoprocthassinuousmarginwhileinL.indaiensisitsmarginis rounded;andfemale–thecircunfilaofL.andiraearemoresinuous thanthatofthenewspecies,the8thtergiteofL.andiraehasno setaewhereasthatofL.indaiensishasadistalrowofsetaeanda basalpairoftrichoidsensilla(notdescribedinL.andirae). Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest. Acknowledgments

WearegratefultoDr.FernandoAugustodeOliveiraeSilveira (UFMG)forplantidentification.

References

Backes,P.,Irgang,B.,2004.Mataatlântica:asárvoreseapaisagem.PaisagemdoSul, PortoAlegre.

Carvalho-Fernandes,S.P.,Ascendino,S.,Maia,V.C.,Couri,M.S.,2016.Diversityof insectgallsassociatedwithcoastalshrubvegetationinRiodeJaneiro,Brazil. An.Acad.Bras.Ciênc.88(3),1407–1418.

Gagné,R.J.,1994.TheGallMidgesoftheNeotropicalRegion.CornellUniversityPress, Ithaca,NewYork.

Gagné,R.J.,Jaschhof,M.,2017.ACatalogoftheCecidomyiidae(Diptera)oftheWorld. DigitalVersion,4thedition.

Garcia,C.,de,A.,Lima,V.P.,Calado,D.C.,Urso-Guimarães,M.V.,2017.Newspecies ofLopesiaRübsaamen(Diptera:Cecidomyiidae)associatedwithAndirahumilis Mart.exBenth.(Fabaceae).Rev.Bras.Entomol.61,239–242.

Lorenzi,H.,1992.Árvoresbrasileiras:manualdeidentificac¸ãoecultivodeplantas arbóreasnativasdoBrasil.EditoraPlantarum,NovaOdessa.

Maia,V.C.,Monteiro,R.F.,2017.Lopesiadavillae(Diptera.Cecidomyiidae),anew speciesofgallmidgefromBrazilassociatedwithDavillarugosa(Dilleniaceae). Braz.J.Biol.,http://dx.doi.org/10.1590/1519-6984.13815.

Maia,V.C.,Azevedode,M.A.P.,Couri,M.S.,2002.Newcontributiontotheknowledge ofthegallmidges(Diptera,Cecidomyiidae)fromtherestingaofBarradeMaricá (RiodeJaneiro,Brazil).Stud.Dipterol.9(2),447–452.

Maia,V.C.,Magenta,M.A.G.,Martins,S.E.,2008.Ocorrênciaecaracterizac¸ãodegalhas deinsetosemáreasderestingadeBertioga(SãoPaulo,Brasil).BiotaNeotrop.8 (1),167–197.

Maia,V.C.,Cardoso,L.J.T.,Braga,J.M.A.,2014.InsectgallsfromAtlanticForestareas ofSantaTeresa,EspíritoSanto,Brazil:characterizationandoccurrence.Bol.Mus. Biol.MelloLeitão33,47–129.

Rodrigues,A.R.,Maia,V.C.,Couri,M.S.,2014.InsectgallsofrestingaareasofIlhada Marambaia,RiodeJaneiro,Brazil.Rev.Bras.Entomol.58(2),173–197. Santos,J.C.,Almeida-Cortez,J.S.,Fernandes,G.W.,2012.Gall-inducinginsectsfrom

Atlanticforest ofPernambuco, NortheasternBrazil. BiotaNeotrop. 12(3), 197–213.

Tavares, J.S., 1920. Cecidologia brazileira. Cecídias que se criam em plantas das famílias das Leguminosae, Sapotaceae, Lauraceae, Myrtaceae, Puni-caceae, Aurantiaceae, Malpighiaceae, Sapindaceae, Umbelliferae, Loran-thaceae,Apocynaceae,Urticaceae,SalicaceaeeGraminae.Brotéria(Zool.)18, 82–125.