A new species of Youngomyia Felt from Brazil and new morphological data on Youngomyia pouteriae Maia (Insecta, Diptera, Cecidomyiidae)

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RevistaBrasileiradeEntomologia63(2019)130–135

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

A

new

species

of

Youngomyia

Felt

from

Brazil

and

new

morphological

data

on

Youngomyia

pouteriae

Maia

(Insecta,

Diptera,

Cecidomyiidae)

Barbara

Proenc¸

a

,

Valéria

Cid

Maia

∗

DepartamentodeEntomologia,LaboratóriodeDiptera,MuseuNacional,QuintadaBoaVista,SãoCristóvão,20940-040RiodeJaneiro,RJ,Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received27September2018 Accepted12January2019 Availableonline10February2019 AssociateEditor:ClaudioCarvalho Keywords: Cerrado Gallinginsect Gallmidge Morphology Taxonomy

a

b

s

t

r

a

c

t

YoungomyiamatogrossensisProenc¸a&MaiaanewspeciesofCecidomyiidae(Insecta:Diptera)thatinduces cylindricalhairygallsonleavesofPouteriatorta(Mart.)Radlk.(Sapotaceae)ishereindescribedand illustrated(larvae,pupalexuviae,maleandfemale).Thegaller,gallandhostplantwerecollectedat ParqueNacionaldaChapadadosGuimarães,inthestateofMatoGrosso(Brazil).Newmorphological dataandphotographsofpupalexuviae,maleandfemaleofYoungomyiapouteriaeMaia,2001arealso provided.

Introduction

Pouteriatorta (Mart.)Radlk (Sapotaceae) is a perennialtree, nativetoBrazil,distributedfromCentraltoSouthAmerica.InBrazil, itpresentsawidedistributionbeingfoundinNorth,Northwest, Midwestand Southeast areas,includingfourphytogeographical domains:Amazonrainforest,Caatinga (dryforest),Cerrado and Atlanticforest(FloradoBrasil,2018).Thisplantiscommonlycalled “guapeva”,“curiola”,“acáferro”,“abiudocerrado”,and“grãode galo”, and it is used both as food resource and antidysenteric medicine(Perfeitoetal.,2005).

AsingleinsectgallmorphotypeattackingleavesofP.tortahas beenreported sofar. It was record for theﬁrst time by

Urso-GuimarãesandScareli-Santos(2006)inPé-de-GiganteReserve,a

CerradoareainthemunicipalityofSantaRita doPassaQuatro, inSãoPauloState,Brazil.Thegallerwasidentiﬁedasaprobably newspeciesofYoungomyiaFelt,1908.Later,Urso-Guimarãesetal.

(2017)recordedthissamegallmorphotypeinaCerradoareain

Aquidauana,MatoGrossodoSul,Brazil.

Youngomyia Felt, 1908 have been recorded in the Nearctic, NeotropicalandOrientalregions.Onlysixspeciesareknownso farand four of them are fromthe Neotropics, one fromBrazil (YoungomyiapouteriaeMaia,2001).Themajorityofthespeciesare

∗ Correspondingauthor.

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

inquilinous,possiblypredaceous,ingallsofothercecidomyiids,but someoftheminducegall(GagnéandJaschhof,2017).

Thisgenusischaracterizedasfollows:incompleteRssituated beforeorafterthehalfofthelengthofR1;longtricircumfilarmale flagellomeres;femalewithnumerousconnectivecircumfila;neck oftheflagellomerescoveredwithsetaeinbothsexes;tarsalclaws stronglycurvedafterthebasalthird;gonocoxitewithasetulose mesobasallobe;longgonostyle;hipoproctwithcloselyapressed spinesattheposteriorhalf,andvariableaedeagus(Gagné,1994).

Theobjectivesofthisstudyaretodescribeanewspeciesof Youn-gomyiathatinducesgallsonleavesofPouteriatorta(Mart.)Radlk. (Sapotaceae)andtoprovidenewmorphologicaldataonpupal exu-viae,maleandfemaleofYoungomyiapouteriaeMaia,2001.

Materialandmethods

Thisstudyispartoftheproject“DipteradosestadosdoMato Grosso,MatoGrossodoSuleRondônia:diversidade,sistemáticae limitesdistribucionais”.Theaimofthisprojectistoinventorythe diversityofDipterafromBrazil’sNorthandMidwestareas.

Thespecies describedin thepresent studywascollectedon Sep.2011atParqueNacionaldaChapadadosGuimarães(National ParkofChapadadosGuimarães)inMatoGrosso(Brazil).Thegall (Fig.1)wasphotographedusingadigitalcameraandcharacterized bytheplantorganofoccurrence,shape,color,presenceorabsence oftrichomes,andnumberofinternalchambers.

Thecollectedmaterialwaslabeledandtransportedtothe Labo-ratóriodeDiptera(MuseuNacional/UFRJ,RiodeJaneiro).Samples https://doi.org/10.1016/j.rbe.2019.01.002

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Fig.1.Cylindricalgall,green,one-chambered,withbrownishtrichomesonleavesofPouteriatorta(Mart.)Radlk.(Sapotaceae).(A)Viewofthegallsontheleave’sadaxial side;(B)gallsonleaves’abaxialside;(C)detailofthegall;(D)openedgall,showingtheinnerchamberandayoungpupaofYoungomyiamatogrossensisProenc¸a&Maia.

ofthegallwereplacedinplasticpotsatroomtemperaturetorear adults.Othersamplesweredissectedtoobtainlarvaeandpupaeof theinducer.Thespecimenswerepreparedandmountedonslides followingthemethodsoutlinedinGagné(1994).

ThegallmidgegenuswasidentiﬁedusingGagné’s(1994)key toNeotropicalgeneraandthespecieswasdeterminedtobenew to science aftercomparison with theoriginal descriptions and illustrationsoftheknownspecies,andwithspecimensfromthe CecidomyiidaecollectionoftheMuseuNacional(MNRJ).The diag-nostic characters were illustrated with an optical microscope. PhotographsweretakenbyaNIKONeclipsee200cameracoupledto anopticalmicroscope.Alldrawingswerescannedandprocessedin AdobeIllustratorCC2015®andbothdraw’splatesandphotographs wereprocessedinPhotoshopCS6®.

Wedesignatedamaleasholotypeandalsomales,females,pupal exuviaeandlarvaeasparatypes.Allmaterial,includingthetypes, isdepositedintheCecidomyiidaecollectionofMuseuNacional, RiodeJaneiro(MNRJ).MorphologicalterminologyfollowsGagné

(1994).TheﬁeldworkwasdonebyMaia,V.C.andAscendino,S.,

andthedescriptionofthenewspeciesbyProenc¸a,B.andMaia,V.C. The host plant wasidentiﬁed by Dr. Gracialda Ferreira and ManuelCordeiro(UniversidadeFederalRuraldaAmazônia),and theexsiccatewasdepositedintheherbariumofthatinstitution.

Type-materialofY.pouteriaedepositedintheCecidomyiidae collection of theMuseuNacional (MNRJ) wasexaminedin the presentstudy.

Results

Youngomyiamatogrossensissp.nov.(Figs.2–18)

Diagnosis.Adult:clawstwo-toothed;empodiashort,not reach-ingbendinclaws;claviformgonostylus;setuloseandovalcerci; hypoproctslightlylongerthancerci;aedeaguslongand triangu-lar.Ovipositorshort,slightlyprotrusible,with1.6timesthelength ofsternite 7;ovaland separatedcerci.Pupal exuviae:antennal basesshortandtriangular;prothoracicspiraclelong;abdominal

segments2–8withserrated dorsal spines. Larvae:two-toothed spatulawithtaperedend;threepairsofsetuloseterminalpapillae. Description. Adult. Body length: 2.9–3.4mm in males (n=4), 3.9–4.6mminfemales(n=3).Head(Figs.2–6):Frontoclypeuswith 5–9 setae(n=5); labrum long-attenuated with 2 pairs of ven-tralsensorysetaeclosetotheapex(n=3),hypopharynxapically setulose,slightlylongerthanlabrum(n=3),labellaelong,convex, setulose,withtwo pairsofsetae(n=3);palpustwo-segmented, cylindrical,thesecondtwotimeslongerthanthefirstone. Occip-italprocessabsent.Eyesfacetshexagonal,closelyapproximated. Antenna 2+12: scape obconicalwith 2–3 setae (n=4), pedicel globosewith2–5setae(n=4)(Fig.2).Maleflagellomeres:distal circumfilumwithloopslongerthanthoseoftheothersand mid-dlecircumfilumwithloopsshorter than thoseof thebasalone (Fig.3).Femaleflagellomere1slightlylongerthantheothers; cir-cumfilaintworingsslightlysinuous,oneringdistalandtheother subbasal,interconnectedbyalongitudinalslightlysinuousstrand (Fig.4).Antennaewithlongandsetulosenecksandflagellomere12 withapicalprocessinbothsexes(Figs.5and6).Apicalprocess7.0 timesshorterthanflagellomere12inmales(n=1)and6.5timesin females(n=1).Thorax(Figs.7and8):Malewingswith2.3–2.5mm in length (n=4),female wings 2.9–3.0mm in length (n=4).Rs evanescent,reachingR1beforethemidlength;theotherveinsasin thegenericcharacterization(Fig.7).Anepimeronwith7–10setae. Scutumwithlateralanddorsalsetae,scutelumwithfewsubapical setae.Tarsalclawsrobust,stronglysclerotized,bendatthebasal third,two-toothed,thesuperiortoothconspicuouslylongerthan theinferiorone;setuloseempodia,notreachingthebendinclaws (Fig.8).Maleabdomen(Fig.9):tergites1–7sclerotized, rectangu-lar,withoneanteriorpairoftrichoidsensilla.Tergites1–6with singlerowof posteriorsetae;somesparsesetaeirregularly dis-tributedandscaleselsewhere.Tergite7evenlysclerotized,with setaeirregularlydistributed. Tergite8notsclerotized withonly one anteriorpair oftrichoid sensillaas vestiture.Sternites 2–8 sclerotized,rectangular,withonepairoftrichoidsensilla,scales elsewhere.Sternites2–4withasimplerowofposteriorsetaeand scatteredmesalsetae;sternites5–7withmorethantwoposterior

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132 B.Proenc¸aandV.C.Maia/RevistaBrasileiradeEntomologia63(2019)130–135 2 3 4 5 6 7 ₈ 0.01 mm 0.01 mm 0.01 mm 0.1 mm 0.1 mm 0.1 mm 0.1 mm

Figs.2–8.YoungomyiamatogrossensisProença&Maia.(2)Malehead(frontalview); (3)maleflagellomere;(4)femaleflagellomere;(5)maleflagellomere12;(6)female flagellomere12;(7)malewing;(8)femalemidleg:clawsandempodium(lateral view). 9 10 11 ₁₂ 0.1 mm 0.1 mm 0.1 mm 0.1 mm

Figs.9–12.YoungomyiamatogrossensisProenc¸a&Maia.(9)Maleabdomen, seg-ments6–8(lateralview);(10)maleterminalia(dorsalview);(11)femaleabdomen, segments6–8(lateralview);(12)ovipositor(lateralview).

rowsofsetaeandscatteredsetaeontherestofthesternites. Stern-ite8reduced,about0.10–0.12mminlength(n=7),withscattered setaeonposteriormargin,moreconcentratedfromdistalhalfto posteriormargin.Stenite8about0.45–0.65mmaslongassternite 7. Male terminalia (Fig. 10): gonocoxiteoval, not splayed, cov-eredwithsetae,withspinyandroundedmesobasallobes,slightly shorterthanthehypoproct;gonostylusclaviform,1.5–1.6times shorterthangonocoxite(n=2),withstronglypronunciatedstriae atallextension,delimitingelongatedcells,eachonewithaseta attheapex;setuloseatbasal1/5.Cercioval,setulose,withapical setae;hypoproctslightlybilobated,setulose,andslightly longer thancercus;aedeagusverylong,triangular,stronglysharpatthe apex,withlateralpittedsensorialfromtheapextomiddlelength. Female(Fig.11):tergites1–7andsternites2–7sclerotized,with scatteredscalesandanteriorpairoftrichoidsensilla.Tergites1–6 rectangular,withroundedmargins,singlerowposteriorsetaeand scatteredmesalsetae.Tergite7withsetaemoreconcentratedatthe posteriormargin.Tergite8notsclerotized,withonlyoneanterior pairoftrichoidsensillaasvestiture.Sternites2–7quadrangular, withscatteredscalesandanteriorpairoftrichoidsensilla. Stern-ites2–5withrowofposteriorsetaeandlateralsetae.Sternite6 withadoublerowofposteriorsetae,rowoflateralsetaeandmesal setae.Sternite7withsetaeconcentratedposteriorly,laterallyand mesally.Sternite8notsclerotized,withonlyoneanteriorpairof trichoidsensillaasvestiture.Ovipositor(Fig.12):short,slightly protrusible,about1.6timesaslongassternite7;cercioval, setu-lose,withdorsalsetaelongerthantheventralsetae;hypoproct tiny,glossiformandsetulose.Segment9withscatteredsetaequite variedinsize,moreabundantventrally.

Pupal exuviae (Figs. 13 and 14): Length:3.2–3.9mm (n=5). Cephalicregion(Fig.13):cephalicsetashortwith0.03–0.05mm inlength(n=9);apicalplatewithroughintegumentinall exten-sionexceptapically;anteriormarginwithabundantshortspines. Antennal bases sclerotized, triangular, smooth and short, with 0.03–0.05mmlong(n=8).Upperandlateralcephalicmargin thick-ened.Twopairsoflowerfacialpapillae,onesetoseandoneasetose; twogroupsofthreelateralfacialpapillae:onepairbiggerand ase-tose,andtwo setose.Thorax:prothoracicspiraclelong,strongly sclerotized,triangular,bentatthe5thdistalportionandslightly bentsubapically,0.32–0.49mmlong(n=7);outermarginserrated fromthedistalhalf.Forelegsheathreachingtheanteriormargin ofabdominalsegment 5;midlegsheath reachingthemiddle of abdominalsegment5;hindlegsheathreachingthedistalmarginof abdominalsegment5.Abdomen(Fig.14):spinyintegument. Seg-ment1coveredwithsmallspines.Anteriormarginofabdominal segment2–8witharowofirregularserratedspinesofdifferent sizes.Segments2–8sclerotizedfromtheanteriormarginuntilthe endofthespinyarea.

Larvae (Figs. 15–18): Length: 1.1–2.7mm (n=13). Fusiform body, white coloration. Integumentdorsal and ventrally rough.

(Figs.15and16).Spatulastronglysclerotized,with0.2–0.3mmin

length(n=13),withtwowelldevelopedteeth,parallel,well sep-aratedfromeachother,apicalmarginserratedbetweentheteeth. Spatulashaftreducedinlength,withabout1/4ofthespatulatotal lengthandweeklysclerotizedattheend.Oneasetosepairof ster-nalpapillae;twopairsofsetoselateralpapillaeoneachsideofthe spatula(Fig.17);fourpairsofsetoseterminalpapillae:twopairs smallerthantheothers(Fig.18).

Etymology. The speciﬁc name matogrossensis refers to Mato Grosso,theBrazilianstatewherethisspecieswascollected. Materialexamined.Holotype.BRAZIL:♂(slide),MidwestBrazil, MatoGrosso,ParqueNacionaldaChapadadosGuimarães,Caminho VéudaNoivatrail,15◦2420S;55◦4947W,5Sep.2011,Maia,V.C. andAscendino,S.col.,Pouteriatorta(Mart.)Radlk.(Sapotaceae), (MNRJ).

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13 14 15 16 17 18 0.1 mm 0.1 mm 1.0 mm 0.1 mm 0.1 mm

Figs.13–18.YoungomyiamatogrossensisProenc¸a&Maia.(13)Pupa:cephalicregionandprothoracicspiracle(frontalview);(14)pupa:abdominalsegment5(dorsal/lateral view);(15)larva,generalaspect(ventralview);(16)larva,generalaspectphotomicrograph(ventralview);(17)larvalspatula(ventralview);(18)larva:terminalsegment (ventralview).

Paratypes.BRAZIL:Midwest Brazil,12 ♂♂,10 ♀♀,5pupal exu-viae and 9 larvae in permanent slides, same data as holotype (MNRJ).

AdditionalFigs. 19, 20, 21, 22 and 23 showing respectively, oneadultfemale,onelarva, oneyoungpupa,onematurepupa ofYoungomyiamatogrossensis and onemicrohymenopterapupa (parasitoid).

Gall. Thegalls ofYoungomyiamatogrossensis areinitially green, brownishwhenmature,andbrownish-redwhensenescent.Brown trichomesareobservedthroughoutthegalls,beingmoreabundant

attheapex.Thegallsarefoundonyoungormatureleaves,onboth adaxialandabaxialsurfaces,beingmoreabundantontheabaxial surface.

Hostplant.Pouteriatorta(Mart.)Radlk(Sapotaceae).

Distribution.Sofar,Youngomyiamatogrossensis occursin three Brazilianstates:MatoGrosso,presentstudy,MatoGrossodoSul, in Aquidauana municipality(Urso-Guimarães etal. (2017))and SãoPaulo,inEcologicalStationofJataí(SaitoandUrso-Guimarães, 2012)andinPé-de-GiganteReserve,SantaRita doPassa-Quatro

(Urso-GuimarãesandScareli-Santos,2006).AllareasintheCerrado

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134 B.Proenc¸aandV.C.Maia/RevistaBrasileiradeEntomologia63(2019)130–135

Figs.19–23. YoungomyiamatogrossensisProenc¸a&Maia.(19)Larvainsidegall’schamber;(20and21)youngandmaturepupainsidegall’schamber;(22)undetermined hymenopteraparasitoidinthegall;(23)adultfemale.

24 25

0.05 mm 0.05 mm

.Youngomyia matogrossensis proença & maia sp.nov .Youngomyia pouteriae maia, 2001

Figs.24and25.(24)Palpustwo-segmentedofYoungomyiamatogrossensisProenc¸a&Maia(blackarrow);(25)palpusone-segmentedofYoungomyiapouteriaeMaia,2001 (blackarrow).

Comments.Urso-GuimarãesandScareli-Santos(2006)recorded leafgallsonPouteriatorta,inMinasGeraisState,Brazil,and sug-gestedthattheywereinducedbyanewspeciesofYoungomyia.

Scareli-Santosetal.(2008)describedthestructureaswellasthe

histochemistryofthesegalls.Later,theinducerwasidentiﬁedas Youngomyiapouteriae Maia,2001 by Saito and Urso-Guimarães

(2012).Aftercomparingthespecimensthatwehaveobtainedfrom

PouteriatortawiththetypespecimensofY.pouteriae,werealized thattheformerisanewspeciesofYoungomyia.Thenewspecies wasincludedin Youngomyiabasedonthefollowingcharacters: necksoftheﬂagellomeressetulose;gonocoxiteswithspinesonthe mesobasallobes;gonostylusstriated;andlarvaewithtwo-toothed spatulawithtaperedend.

Among thepreviously known species, three have elongated cerci:Y.pouteriae Maia, 2001;Y. podophylla(Felt,1907) and Y. knabi(Felt,1912)aswellasthenewspecies.However,onlyinY.

pouteriaeandY.matogrossensisthespinesonmale’shypoproctare absent.

DespitethesesimilaritiesY.pouteriaeandY.matogrossensis dif-ferinthefollowingaspects:adults–two-segmentedpalpiinthe newspecies(Fig.24)andone-segmentedinY.pouteriae(Fig.25); male cercusshorter and aedeagus narrower in Y. matogrossen-sis(Fig.26)thanthoseofY.pouteriae(Fig.27);malehypoproct slightlybilobatedinthenewspeciesandsimpleinY.pouteriae; mesobasal lobes of Y. pouteriae more pronunciated than those of Y. matogrossensis. Pupal exuviae: Lateral facial papillae are presentinthenewspeciesbutabsentinY.pouteriae.Larval spat-ulawithoutindentationatexternalmarginofthelateralsideinY. matogrossensis(Fig.28),butthisindentationispresentinY. poute-riae(Fig.29).

ThisisthesecondYoungomyiaspeciesdescribedfromBraziland theﬁrstfromCerrado.Thepreviousknownspecies,Youngomyia

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26 27

0.05 mm _{0.05 mm}

.Youngomyia matogrossensis proença & maia sp.nov Youngomyia pouteriae maia, 2001

Figs.26and27.(26)MaleterminaliaofYoungomyiamatogrossensisProenc¸a&Maia.(27)MaleterminaliaofYoungomyiapouteriaeMaia,2001.Thearrowspointouttothe followingstructures:blackarrow:mesobasallobe;redarrow:cerci;greenarrow:hypoproct.

28 29

0.05 mm _{0.05 mm}

.Youngomyia matogrossensis proença & maia sp.nov Youngomyia pouteriae maia, 2001

Figs.28and29. Larvalspatulaof(28)YoungomyiamatogrossensisProenc¸a&Maia;(29)YoungomyiapouteriaeMaia,2001.Thearrowsshowthedifferencebetweenthelarval spatulaofbothspecies.AnindentationattheexternalmarginoftheteethisonlyobservedinY.pouteriae.

pouteriaeMaia,2001,wasfoundinAtlanticforestareasofRiode Janeiro(Brazil).

YoungomyiapouteriaeMaia,2001(Figs.25and27)

Newmorphologicaldata.Adult:Head(Fig.25).Bothsexeswith flagellomeres1–2connatedandneckoftheflagellomeressetulose. Maleflagellomereswithbasalloopslongerthanthemedialand dis-talloops;flagellomere12withapicalprocess.Femaleflagellomere 1longerthantheothers;circumfilaintworingsslightlysinuose, oneringdistalandtheothersubbasal,interconnectedbya lon-gitudinalslightlysinuosestrand.Hypopharynxtriangular,longer thanlabrumandapicallysetulose.Labellawith2pairsofventral sensorialsetae.Palpuswithapicalsetae.Thorax:Wing:Rsbent atits juncturewithR5.Legs: Tarsal claws wellsclerotized and two-tootched.Maleterminalia(Fig.27).Gonostylussmallerthan gonocoxite,withstronglypronouncedstriae,delimitingelongated cells,eachonewithabristleatitsbase;separatedcerci,setosein alllength,withsixpairsoflongersetaeattheapex;aedeagus elon-gatedandclaviform.Ovipositor:femalecercioval.Pupalexuviae. Antennalbasesshort,triangular;cephalicsetashort.Twopairsof lowerfacialpapillae,onesetoseandoneasetose.Prothoracic spir-aclelong,triangular,stronglysclerotized,andslightlyserratedat themargin.Abdominalsegments2–8sclerotizeddorso-anteriorly, sclerotizedareacontiguouswithspines.

Materialexamined.3♂♂,6♀♀,3pupalexuviaeand5full-grown larvaefromRestingadaBarradeMaricáeItaipuac¸uinMaricáand ArraialdoCabomunicipality,RiodeJaneiro,Brazil,depositedinthe CecidomyiidaecollectionatMNRJ,RiodeJaneiro,Brazil.

Conﬂictsofinterest

Theauthorsdeclarenoconﬂictsofinterest. Acknowledgments

WethanktoSharleneAscendinofortheﬁeldworkandallthe researchersinvolved ontheSisbiotaDipteraproject. Thisstudy wassupportedbyCNPq(ConselhoNacionaldeDesenvolvimento CientíﬁcoeTecnológico,Proc.563256/2010-9).

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