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A new species of the sharpshooter genus Dasmeusa (Hemiptera: Cicadellidae: Cicadellini) from Central Amazon

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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

A

new

species

of

the

sharpshooter

genus

Dasmeusa

(Hemiptera:

Cicadellidae:

Cicadellini)

from

Central

Amazon

Nathalia

H.

Pecly

a,b

,

Daniela

M.

Takiya

c

,

Gabriel

Mejdalani

a,∗

aUniversidadeFederaldoRiodeJaneiro,MuseuNacional,DepartamentodeEntomologia,RiodeJaneiro,RJ,Brazil

bUniversidadeFederaldoRiodeJaneiro,MuseuNacional,ProgramadePós-graduac¸ãoemZoologia(PPgZoo),RiodeJaneiro,RJ,Brazil cUniversidadeFederaldoRiodeJaneiro,InstitutodeBiologia,DepartamentodeZoologia,RiodeJaneiro,RJ,Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received12July2019 Accepted3August2019 Availableonline21August2019 AssociateEditor:RodrigoFeitosa Keywords: AtlanticForest Cicadellinae Leafhopper Morphology Neotropicalregion

a

b

s

t

r

a

c

t

AnewspeciesofthegenusDasmeusaMelichar,1926isdescribedandillustratedfromspecimenscollected intheStateofAmazonas,NorthernBrazil.Dasmeusaimperialissp.nov.canbedistinguishedfromthefive knownspeciesofthegenus,aswellasfromthoseofcloselyrelatedgenera,bythefollowingcombination offeatures:dorsumyellowwithorange,preapicaltransverseirregularstripeonforewing;malepygofer moderatelyproducedposteriorly,withposteriormarginbroadlyrounded;stylewithoutpreapicallobe, narrowandtruncateapically;aedeaguswithrobustapicalprocessdirectedventrally,ventralmargin ofthisprocessdentate;paraphyseswithpairofdorsaldentiformprojectionsonstalk,ramislenderand directedposterodorsally;posteriormarginoffemalesterniteVIIwithsmallquadratelobe;firstovipositor valvulawithdentiformapex;secondovipositorvalvulawithapicalthirddirectedventrally.Thispaper includesthefirstdetaileddescriptionandillustrationsofthefemaleterminaliaofaDasmeusaspecies. Inaddition,theknowngeographicdistributionofthegenusispresented;D.pauperata(Fabricius,1803) isnewlyrecordedfromtheBrazilianstatesofRoraima,Amazonas,Pará,Sergipe,andBahia;therecords fromthelasttwostatesareinterestingbecausetheyarefromareasofAtlanticForest.Previously,the genuswasknownonlyfromtheAmazonForest.

©2019SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction

Cicadellidae(leafhoppers), oneof thelargestinsect families, comprisesmorethan22,000describedspeciescurrentlygrouped intoaboutthirtysubfamilies(Dietrich,2004,2005).Leafhoppers rangeinlengthfrom2to32mmandcharacteristicallyhavefour rows of enlarged spine-like setae on the hind tibiae that are employedinthepeculiarbehaviorsofbrochosomeanointingand grooming(Rakitov,2009; Bartlettetal., 2018).Many speciesof this familycan beabundantand causeconsiderabledamageto cropsbyfeedingdirectlyonplants orbybeingvectorsofplant pathogens(Nielson,1968;FreytagandSharkey,2002). Leafhop-persfeedviapiercing-suckingmouthparts,usuallyonthevascular fluidsofplants,andovipositdirectlyintothelivingtissueoftheir hostplants(Dietrich,1999).

The subfamily Cicadellinae comprises approximately 2400 species in about 330 genera (Wilson and Turner, 2007). This subfamilyis very largeand diverseand includes taxa fromall

∗ Correspondingauthor.

E-mail:mejdalan@acd.ufrj.br(G.Mejdalani).

zoogeographicalregions,beingespecially richintheNeotropics (Young,1968,1977;Mejdalani,1998).Allknownmembersofthe Cicadellinaearexylem-feeders(Young,1968).Currently,twotribes arerecognizedwithintheCicadellinae,aNewWorldProconiiniand acosmopolitanCicadellini(Young,1968,1977;Mejdalani,1998).

TheCicadellinigenusDasmeusaMelichar,1926isrecordedfrom NorthernBrazilandGuianas(Young,1977)andcurrentlycomprises fivespecies:D.bassetiCavichioliandChiamolera,1999,D.flavescens Metcalf,1965,D.isabellinaCavichioliandChiamolera,1999,D. men-dicaYoung,1977,andD.pauperata(Fabricius,1803)(typespecies) (CavichioliandChiamolera,1999;McKamey,2007).Accordingto Young(1977),DasmeusaisrelatedinmanyrespectstoParomenia Melichar,1926,butcanbedistinguishedbythefollowing combi-nationoffeatures:(1)dorsumusuallyyellow,oftenwithorange shadesor spotsatthebaseandneartheapexof theforewing; (2)bodyslender;(3)headwellproducedanteriorlyandwiththe anteriormarginrounded;and(4)maleterminaliawithparaphyses. ThetaxonomyoftheCicadellidaeisbasedmainlyon charac-tersofthemaleterminalia.Thefemaleterminaliahavenotbeen commonly studiedbecausetheircharacters are consideredless variable(CarvalhoandMejdalani,2014).However,several stud-ies have revealeduseful characters in thefemale terminalia of https://doi.org/10.1016/j.rbe.2019.08.002

0085-5626/©2019SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http:// creativecommons.org/licenses/by-nc-nd/4.0/).

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344 N.H.Peclyetal./RevistaBrasileiradeEntomologia63(2019)343–348 thesharpshootersforspeciesdelimitation(e.g.,Mejdalani,1998;

TakiyaandMejdalani,2004;CarvalhoandMejdalani,2014).The femaleterminaliainDasmeusaarepoorlyknown;Young(1977) illustratedonlythesterniteVIIofD.flavescensandthepygoferand secondovipositorvalvulaofDasmeusasp.,whereasCavichioliand Chiamolera(1999)illustratedthesterniteVIIofD.isabellina.Thus, detailedmorphologicalstudies,whichcouldprovideuseful charac-tersforunderstandingphylogeneticrelationshipswithinthegenus andamongmembersoftheParomeniagenericgroup(sensuYoung, 1977),areneeded.

Inthepresentpaper,anewspeciesofDasmeusafromtheState ofAmazonas,NorthernBrazil,isdescribedandillustratedbased onfemaleandmalespecimens.Inaddition,preliminarydataon thegeographicdistributionofthegenusareprovided;D. pauper-ata(Fabricius,1803)isnewlyrecordedfromtheBrazilianstatesof Roraima,Amazonas,Pará,Sergipe,andBahia.

Materialandmethods

Specimensstudiedaredepositedinthefollowinginstitutions: Colec¸ão Entomológica Pe. Jesus Santiago Moure, Departamento de Zoologia, Universidade Federal do Paraná, Curitiba (DZUP); Colec¸ãoEntomológicaProf.JoséAlfredoPinheiroDutra, Departa-mentode Zoologia,UniversidadeFederaldo Rio deJaneiro,Rio deJaneiro(DZRJ);Colec¸ãodeInvertebrados,InstitutoNacionalde PesquisasdaAmazônia,Manaus(INPA);Departamentode Ento-mologia,MuseuNacional,UniversidadeFederaldoRiodeJaneiro, RiodeJaneiro(MNRJ);andColec¸ãoEntomológica,MuseuParaense EmílioGoeldi,Belém(MPEG).

Terminaliastructureswereremoved,maceratedin10% KOH toeliminate unsclerotized tissues, and dissected (Oman, 1949; Mejdalani,1998).Dissectedpartswerestoredinsmallvialswith glycerin that were pinned beneath the specimen (Young and Beirne, 1958). Descriptive terminology followed mainly Young (1968,1977),exceptforthefacialareasofthehead(Hamilton,1981; Mejdalani,1993,1998)andthefemaleterminalia(Nielson,1965; Hill,1970).Useofthetermgonoplac(=thirdovipositorvalvula) andthenamesofthesculpturedareasofthefirstovipositorvalvula followedMejdalani(1998).Linedrawingsoftheanteriordorsum andterminaliastructureswerepreparedwiththeaidofa cam-eralucidaattachedto astereomicroscope and then inkedwith Indiaink.Photographsofthebodyatdifferentfocalplaneswere takenusing a digital cameraattachedtoa stereomicroscope; a compositeimagecreatedfromthein-focusareasoftheoriginal photographswasproducedbyCombineZP,afreesoftware devel-oped byAlanHadley (http://combinezp.software.informer.com). Photographsofthefirstandsecondovipositorvalvulaewere pre-paredwithadigitalcameraattachedtoalightmicroscope.Total lengthofspecimenswasmeasuredfromtheapexofthecrownto thetipsoftheforewingsatrestposition(Young,1977).Labeldata werequotedexactlywithareversedvirgule(\)separatinglineson thelabels.UsingtheonlinetoolSimpleMappr(Shorthouse,2010), wepreparedamaptoshowtheknowndistributionofDasmeusa speciesinSouthAmerica.Recordswereobtainedfromspecimens depositedinDZRJ,DZUP,INPA,MNRJ,andMPEG,aswellasfrom theliterature(Young,1977;ZanolanddeMenezes,1982;Cavichioli andChiamolera,1999;McKamey,2007;Wilsonetal.,2009).

Results

Dasmeusaimperialissp.nov.(Figs.1–17)

Length. Male holotype 8.1mm; male paratypes 7.8–8.0mm (n=5);femaleparatypes8.8–9.6mm(n=5).

Maleholotype

Head(Figs.1,17),indorsalview,stronglyproducedanteriorly; median lengthofcrown almost equalto interocularwidth and approximately5/10transocularwidth;anteriormarginrounded; withoutcarinaattransitionfromcrown toface;coronalsuture distinct,elongate,extendinganteriorlybeyondinterocellarline; frontogenal sutureextendingonto crownand attaining ocellus; ocellilocatedonimaginarylinebetweenanterioreyeangles,each ocellusapproximatelyequidistantbetweenmedianlineofcrown andadjacenteyeangle;surfaceofcrownflattened;antennalledge, in dorsalview,slightly protuberant;in lateralview,with ante-riormarginconvex.Frons,inanteriorview,convex;medianarea slightlypunctate;muscleimpressionsdistinct;inlateralview, infe-riorthirdslightlyangulate;epistomalsutureincompletemedially; clypeus, in lateralview, convex,continuing inferior contour of frons.

Thorax(Figs.1,17)withpronotum,indorsalview,withwidth approximatelyequaltotransocularwidthofhead;lateralmargins convergent anteriorly;posteriormargin rectilinear;dorsolateral carina complete, rectilinear, declivent anteriorly; disk without pubescenceorpunctures.Mesonotumwithscutellumnot transver-sally striate and without punctures. Forewing with membrane indistinct;veinsnotelevated;apexslightlyexpandedandobliquely truncate;withfourapicalcells,baseoffourthslightlymore prox-imal thanbase ofthird, and three closedanteapical cells, their baseslocatedmoreproximallythanclavalapex;costalapicalcell broadenedposteriorly;withoutanteapicalplexusofveins;texture subhyaline.HindwingwithveinR2+3 incomplete.Hindlegwith

femoralsetalformula2:1:1;firsttarsomerelongerthancombined lengthoftwomoredistaltarsomeres,withtwolongitudinalrows ofsmallsetaeonplantarsurface.

Terminaliawithpygofer(Fig.2),inlateralview,moderately produced posteriorly; posterior marginbroadly rounded; with-outprocesses;macrosetaedistributedonposteriorhalfbutsome locatedmoreanteriorly;microsetaedistributedonbasiventral por-tion.Subgenital plate(Fig.3), in ventralview, withbasal third broadanddistaltwo-thirdsstronglynarrowed;notfusedbasally toitscounterpart;withelongateuniseriatemacrosetaeonbasal third,microsetaedistributedalongouterlateralmargin;inlateral view,platenotextendingasfarposteriorlyaspygoferapex.Style (Fig. 4), indorsal view,extendingposteriorlyfartherthan apex ofconnective,withoutpreapicallobe, narrowandtruncate api-cally.Connective(Fig.4),indorsalview,T-shaped;stalkshort,arms broad.Aedeagus(Fig.5)symmetrical;shaftshort,withrobust api-calprocessdirectedventrally,ventralmarginofprocessirregularly dentate;gonoductdistinct,gonoporelocatedapically.Paraphyses (Figs.6,7)symmetrical,articulatedtoapexofconnective, extend-ingbeyondsubgenitalplates;indorsalview(Fig.6),stalklongand robust,withdorsoapicalpairofdentiformprojections;rami slen-derandwithacuteapexes,inlateralview(Fig.7)directeddorsally formostoftheirlengthbutwithapicalportiondirectedposteriorly. Color(Fig.17).Dorsumyellow.Forewingwithorange,preapical transverseirregularstripe,apexcolorless.Face,lateralandventral portionsofthorax,andlegspaleyellow.

Female

Externalmorphologyandcolorsimilartothoseofmale. Ter-minaliawithsterniteVII(Fig.8),inventralview,wellproduced posteriorly,narrowinggraduallytowardsapex;posteriormargin withsmallquadratelobe.Pygofer(Fig.9),inlateralview,well pro-ducedposteriorly;posteriormarginnarrowlyroundedtosubacute; surfacewithlargemacrosetaedistributedmostlyonposteriorhalf. “Internal”sterniteVIII,indorsalview,withoutsclerotizedareas. Firstvalvifer(Fig.10),inlateralview,subquadrate.Firstvalvula

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Figs.1–9.Dasmeusaimperialissp.nov.1–7,male.1,head,pronotum,andmesonotum,dorsalview.2,pygofer,lateralview.3,subgenitalplate,ventralview.4,connectiveand style,dorsalview.5,ejaculatorybulbandaedeagus,lateralview.6,paraphyses,dorsalview.7,paraphyses,lateralview.8–9,female.8,sterniteVII,ventralview.9,pygofer, lateralview.Scalebars:Figs.1,8,9=1mm,2,3,6,7=0.5mm,4,5=0.25mm.

10 VLI 11 DSA 12 VSA RAM VID 13 14 15 TOO DEN DUC RAM 16 DEN PPR

Figs.10–16.Dasmeusaimperialissp.nov.,female.10,ovipositorvalvulaI,lateralview(thebasalportionoftheramusisbroken).11,dorsalsculpturedarea.12,apical portion.13,ovipositorvalvulaII,lateralview.14,basalteeth.15,medianteeth.16,apicalportion.(DEN)denticle;(DSA)dorsalsculpturedarea;(DUC)duct;(PPR)preapical prominence;(RAM)ramus;(TOO)tooth;(VID)ventralinterlockingdevice;(VLI)valviferI;(VSA)ventralsculpturedarea.Scalebars:0.5mm.

(Figs. 10–12), in lateral view, abruptlynarrowed apically, ven-troapicalmarginsomewhatsinuous,apexacute,dentiform;dorsal sculpturedarea(Fig.11)extendingfrombasalportionofbladeto apex,formedmostlybyscale-likeprocessesarrangedinoblique lines(strigate);ventralsculpturedarea(Fig.12)restrictedto api-calportionofblade,formedmostlybyscale-likeprocesses;ventral interlockingdevicedistinctonbasalhalfofblade.Secondvalvula

(Figs.13–16),inlateralview,withdorsalmarginconvexand api-calthirddirectedventrally;withabout45non-contiguous,mostly subtriangularteeth;denticlesdistributedonteethandondorsal andventralapicalportionsofblade(ventraldentateapicalportion longerthandorsalone)(Figs.15,16);preapicalprominencedistinct (Fig.16);apexobtuse;ducts(Fig.15)extendingtowardsteethand apicalarea.GonoplacoftheusualCicadellinaetype:inlateralview,

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346 N.H.Peclyetal./RevistaBrasileiradeEntomologia63(2019)343–348 withbasalhalfnarrow;apicalhalfexpanded,graduallynarrowing

towardsapex;latterobtuse.

Etymology.Thenameofthenewspecies,imperialis,isatribute totheMuseuNacional(UniversidadeFederaldoRiodeJaneiro).The mainMuseumbuilding(SãoCristóvãoImperialPalace)wasalmost completelydestroyedbythefireduringthenightofSeptember2, 2018.Unfortunately,mostoftheentomologicalcollectionwasalso destroyed.

Typematerial.NorthernBrazil,AmazonForest.Maleholotype: “BR[Brazil],A.M.[StateofAmazonas],Manaus,\ReservaDucke \ 09/IX/1986 \ Ulisses, Luís” (DZUP). Paratypes: fifteen males and one female: “BRASIL, AM, 80km N \ Manaus, Reservado \PDBFF [ProjetoDinâmica Biológica de Fragmentos Florestais], Km41\02◦24S,59◦43W\22.xii-07.i.2005”(INPA);twomales andonefemale:same dataasprecedingexcept“09-10.vi.2004” (DZRJ); two males and one female: “10-12.xi.2004” (DZRJ); two males: “27-28.x.2004” (DZRJ); one male: “21-22.vii.2004” (DZRJ);ninemalesandonefemale:“02-04.iii.2005”(DZRJ);three males: “26-27.v.2004” (DZRJ); twelve males and two females: “16-18.iii.2005”(INPA);threemales:“02-04.ii.2005”(DZRJ);two malesandonefemale:“24-25.xi.2004”(DZRJ);fourmales: “30.iii-01.iv.2005”(DZRJ);onemale:“16-17.ii.2005”(DZRJ);onemale: “15-16.ix.2004”(DZRJ);threemales:“07-08.vii.2004”(DZRJ);one male:“12-13.v.2004” (DZRJ); ten males and two females: “08-09.xii.2004” (MNRJ); four males: “16-17.ii.2005” (DZRJ); eight males: “19-21.i.2005” (DZRJ); one male and one female: “23-24.vi.2005”(DZUP);onemale:“05-06.viii.2004”(DZRJ);twomales: “Brasil,Amazonas,Manaus,ZF2\KM-14,02◦3521S-60◦0655W\ 03–17.viii.2016\Malaisegrandenochão\J.A.Rafael&F.F.Xavier” (INPA);onemale:samedataasprecedingexcept“16-30.ix.2016” (INPA).

Discussion

Dasmeusaimperialissp.nov.canbedistinguishedfromtheother speciesofthegenus,aswellasfromthoseofcloselyrelatedgenera (e.g.,ParomeniaMelichar,AlochaMelichar,AlbinianaCavichioli,and JeepiulusCavichioli),bythefollowingcombinationoffeatures:(1) dorsumyellowwithorange,preapicaltransverseirregularstripe onforewing(Fig.17);(2)malepygofermoderatelyproduced pos-teriorly,withposteriormarginbroadlyrounded(Fig.2);(3)style withoutpreapicallobe,narrowandtruncateapically(Fig.4);(4) aedeagus withrobust apical process directed ventrally, ventral marginofthisprocessdentate(Fig.5);(5)paraphyseswithpair ofdorsaldentiformprojectionsonstalk,ramislenderanddirected dorsoposteriorly(Figs.6,7);(6)posteriormarginoffemalesternite VIIwithsmallquadratelobe(Fig.8);(7)firstovipositorvalvulawith dentiformapex(Fig.12);secondovipositorvalvulawithapicalthird directedventrally(Fig.13).Themaleterminaliaofthenewspecies aresimilartothoseofD.bassetiandD.isabellina.However,these threespeciescanbereadilydistinguishedfromoneanotherbythe shapeoftheparaphyses.InD.basseti,theramioftheparaphysesare bifidapically(seeCavichioliandChiamolera,1999),aconditionthat isnotobservedinthenewspeciesandinD.isabellina.Thepairof dentiformprojectionsofthestalkandtheposterodorsally-directed ramidistinguishtheparaphysesofthenewspeciesfromthoseofD. isabellina(seeCavichioliandChiamolera,1999).Thevastmajority ofD.imperialisspecimensfromthePDBFFreservewerecollected withsuspendedintercepttrapsplacedatunderstorylevel.Based onstatisticalanalysesconducted,thenewspeciesisanunderstory indicator(D.Takiya,unpublisheddata).

TheknowndistributionofDasmeusaspeciesisshowninFig.18 . Unfortunately, we have no detailed data on the distribution ofD.flavescens,which wasdescribedfromBrazil(Young, 1977; ZanolanddeMenezes,1982;McKamey,2007)andsubsequently

Fig.17.Dasmeusaimperialissp.nov.Maleholotype,body(totallength8.1mm), dorsalview(antennaeandlegsnotdepicted;thepinhasbeengluedtotheright sideofthethorax).

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Fig.18.DistributionofDasmeusaspecies(preliminarydata).RecordswereobtainedfromspecimensdepositedinDZRJ,DZUP,INPA,MNRJ,andMPEG,aswellasfromthe literature(Young,1977;ZanolanddeMenezes,1982;CavichioliandChiamolera,1999;McKamey,2007;Wilsonetal.,2009).Dasmeusaflavescensisnotincludedbecause theonlyrecordsavailableforthisspeciesare“Brazil”and“Suriname.”DasmeusapauperataisalsorecordedfromSuriname(McKamey,2007)andD.mendicaisalsorecorded fromFrenchGuiana(Wilsonetal.,2009).

recordedfromSuriname(Wilsonetal.2009).Basedonspecimens herein studied,we have firstlyrecorded D. pauperata fromthe BrazilianstatesofRoraima,Amazonas,Pará,Sergipe,andBahia(a recordfrom“Brazil”wasprovidedbyWilsonetal.,2009).Records fromthelasttwostates,whicharelocatedinNortheasternBrazil, areparticularlyinterestingbecausetheyarefromareasofAtlantic Forest.Previously,thegenuswasknownonlyfromtheAmazon Forest.Furthermore,thedistributionofD.pauperatainthe Brazil-ianAmazonregionstronglysuggeststhatthisspeciesalsooccurs inlowlandsofVenezuelaandColombia.

Additionalmaterialexamined(newBrazilianrecordsof

Dasmeusapauperata)

StateofRoraima:onemale:Amajari(DZRJ);onemale:Amajari

(DZUP);sixmalesandtwofemales:Amajari(INPA).Stateof

Ama-zonas:eightmales:SãoGabrieldaCachoeira(INPA);twomales:

Barcelos(DZUP);13malesand13females:Manaus(DZRJ);one male:Manaus(DZUP);sixmalesandsixfemales:Manaus(MNRJ); 16malesand20females:Manaus(INPA).StateofPará:onemale: Belém,Curió-Utinga(MPEG);twomales:Óbidos(DZUP).Stateof

Sergipe:onemaleandonefemale:SãoCristóvão(DZRJ).Stateof

Bahia:onefemale:Itabuna(DZRJ);onemaleandonefemale:

Bel-monte(DZRJ).

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest. Acknowledgements

LuizA. A.Costa (MNRJ)kindly inkedtheline drawings.The manuscriptbenefitedfromtheusefulcommentsofVictor Quin-tas(MNRJ)andGuilhermeMuricy(MNRJ).GabrielMejdalaniand DanielaM.TakiyaareresearchproductivityfellowsfromConselho NacionaldeDesenvolvimentoCientíficoeTecnológico(CNPq; pro-cesses303229/2018-7and313677/2017-4,respectively).Nathalia PeclyhasascholarshipfromCoordenac¸ãodeAperfeic¸oamentode

PessoaldeNívelSuperior (CAPES)in connectionwithherM.Sc. studiesatPPgZoo.ThisworkwassupportedbyFundac¸ãoCarlos ChagasFilhodeAmparoàPesquisado EstadodoRiodeJaneiro (FAPERJ;processE-26/200.082/2019;ApoioEmergencialaoMuseu Nacional). We are greatly indebted to Cristiano Moreira, Mar-cosRaposo Ferreira, and othercolleaguesof the Departamento de Vertebrados for the great support provided to us after the fireattheMuseuNacional(UFRJ).RosalyAle-Rocha(INPA),Greg Lamarre(INRA),StephaneBrule(SEAG),andRodneyR.Cavichioli (DZUP)kindlyprovided specimensforthis study.Several speci-mensfromAmazonasandRoraimastateswerecollectedthrough projectscoordinatedbyJoséAlbertinoRafael(INPA)andfinanced byCNPqandFundac¸ãodeAmparoàPesquisadoEstadodo Ama-zonas(FAPEAM).

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