ww w . r b e n t o m o l o g i a . c o m
REVISTA
BRASILEIRA
DE
Entomologia
AJournalonInsectDiversityandEvolution
Systematics,
Morphology
and
Biogeography
Redescription
of
the
adult
male
and
description
of
the
puparium
of
Hirmoneuropsis
luctuosa
(Philippi)
(Diptera,
Nemestrinidae)
from
central
Chile
Christian
R.
González
∗,
Camila
Carvacho
InstitutoEntomología,FacultaddeCienciasBásicas,UniversidadMetropolitanadeCienciasdelaEducación,Santiago,Chile
a
r
t
i
c
l
e
i
n
f
o
Articlehistory:Received21August2015 Accepted22November2015 Availableonline18December2015 AssociateEditor:SarahSiqueiradeOliveira Keywords: Flies Immaturestages Neotropicalregion Taxonomy
a
b
s
t
r
a
c
t
ThemaleofHirmoneuropsisluctuosa(Philippi,1865)isredescribedandthepupariumisdescribedand illustratedforthefirsttime.Hirmoneuropsisluctuosaiscomparedwithotherspeciesofthegenus. Illus-trationsofdiagnosticcharactersofthemaleandpupaarealsoprovided.
©2015SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction
TheNemestrinidaeortangle-veinedfliesareasmallgroupof brachycerousflieswithabout300extantandfossilspeciesinmore than20genera;thefamilyhasaworldwidedistribution(Bernardi, 1973),butspecimensaresometimeshardtofindinsomeregions. The adultfliesare usually moderate tolargestout flieswith a denselypilosebody.Adultsfrequentvisitflowers,feedinguponthe nectar.Nemestrinidlarvaeareinternalparasitoidsofotherinsects –suchasOrthoptera(Greathead,1958),Coleoptera(Richter,1997), andMantodea(HaenniandBorer,2007).Thespeciesof Hirmoneu-ropsisBequaertdevelopin larvaeofscarabaeidbeetles(Richter, 1997).Theyhaveapeculiarwingvenationwithacompound diag-onalcrossveinand theapicalveinsrunningparalleltothehind marginofthewingandterminatinganteriortoitsapex.
ThefamilywasrevisedworldwidebyBernardi(1973).Inthe Neotropicsthefamilyisrepresentedbyfoursubfamilies,six gen-era,and 64 species (Papaveroand Bernardi,2009a).In Chile,4 generaand39speciesareknown(PapaveroandBernardi,2009a) withthegenusTrichophthalma Westwoodthemost diversified. ThenemestrinidshavebeenstudiedinChilebyPhilippi(1865),
Stuardo(1930a,b,1932,1934,1935,1936),Wagenknecht(1940),
andAngulo(1971,1976).
∗ Correspondingauthor.
E-mail:[email protected](C.R.González).
ThegenusHirmoneuropsisBequaert(1932)wasdescribedasa subgenusofHirmoneuraMeigenbelongstosubfamily Hirmoneuri-nae, tribe Hyrmophlaebini,and comprises 35 species (Bernardi,
1976, 1977; Papavero and Bernardi, 2009a)with most species
distributed inArgentinaand Chile(Angulo,1971;Papaveroand
Bernardi,2009a;Kosmannetal.,2014).
Knowledge of the immaturesof Neotropicalspecies is poor
(PapaveroandBernardi,2009b);immaturesonlyoffourspeciesare
known–Neorhynchocephalussackenii(Williston)(Prescott,1960, 1961),Neorhynchocephalussulphureus(Wiedemann)(Crouzeland
Salavin,1943),thepupalskinofHirmoneuropsisarticulata(Philippi)
(Stuardo,1936),andthelarvaeofFalleniinae,whichforma
respira-torytube(Léonide,1962;Prescott,1955,1961);thattubeislacking
inthelarvaofHirmoneuraobscuraMeigen(Handlirsch,1882,1883). Theobjectiveofthepresentworkistoredescribethemaleandto describeforthefirsttimethepupariumofHirmoneuropsisluctuosa, thenbycontributingtoourknowledgeofthebiodiversityofthe DipteraofChile.
Materialandmethods
Morphological terminology follows Teskey (1969) for pupal exuviaeandtoCummingandWood(2009)foradults.Thecentral zoneofChilehasamediterraneanclimatewithsevenmonthsof dryconditionsandfivemonthswithrains.Broadsclerophyll ever-green treesand shrubs dominatethevegetation.Thepuparium werefound3–5cmbeneath thesoilsurfaceofa Lithraeaforest,
http://dx.doi.org/10.1016/j.rbe.2015.11.011
0085-5626/© 2015 Sociedade Brasileira de Entomologia. Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
PhotographsweretakenusingaNikontrinocularstereomicroscope SMZ1500anddigitalcameraDS-Fi2.Depthoffieldwasenhanced byNikonTDACT-2Usoftwarestackingmultipleimages.Terminalia weremaceratedin10%KOHatapprox.95◦Cfor3htoremovesoft tissue,thenrinsedindistilledwateranddiluteglacialaceticacid, anddissectedinwater.
Results
Hirmoneuropsisluctuosa(Philippi)
(Figs.1–8)
HermoneuraluctuosaPhilippi,1865:661 Hirmoneuropsisluctuosan.comb.Bernardi,1977
Materialexamined
Región de Valparaíso, 1 male El Granizo 2.XII.1952, E.Z.R. col.; 1 male El Salto 19.XII.1964 C. Vivar col. Región Metropolitana: Cordillera Province,1 male Qda.LosAlmendros (33◦4350S/70◦2923W) elevation 959m, Reserva Nacional Río Clarillo, 4.XI.1997, P. Estrada col. Material examined depositedintheInstitutodeEntomologíaCollection,Universidad Metropolitana.
Diagnosis
Bodycolor grayish. Scutumdark-brownpollinose with long blackhairs.Wingsmokywithoutsectorialvein.Legsbrownish-gray pollinose.Abdomendarkgray;firstsegmentwithtuftofyellowish,
Male.Bodylength:10.5–13.5mm;winglength:12.5–13.5mm. Head.Holopticeyesslightlytouchinginupper¼withshort abun-dantwhitish hairs, ommatidia largerin upper2/3–3/4; occiput grayishpollinose,withshortwhitishhairs,largerlateralto com-pound eye; ocellar tubercle raised, polished dark gray, with proclinatedarkhairs;fronsdark-graypollinose;facebrownish pol-ishedgray,withlongwhitishhairsaroundoralmarginandlong blackhairsnearmarginofcompoundeyes andbaseof antenna (Fig.2).Genawithlongwhitishhairs.Antennadark-graypollinose; scapewithblackhairsondorsalandventralsurface(Fig.3); pedi-celcylindrical,withlong,thinblackhairs;firstflagellomereovoid andslightlyflattened,3×longerthanpedicel;proboscisshort,½ thelengthoftheeyes;palpusshort,brownish-graypollinose,with short,thinandsparselight-brownhairs.Thoraxdorsalview: scu-tumdark-brownpollinose,withlong,thinandsparseblackhairs; notopleurondark-brownpollinosewithlongblackandyellowish hairs;scutellumdark-brownpollinose,withverylongblackhairs, andthinwhitishhairsonbase(Fig.4).Pleura:postpronotallobe graypollinose,withdenselong,thinwhitishhairs;anepisternum graypollinose,withdenselong,thinyellowishhairs,andveryfew blackhairs;katepisternumgraypollinose,withlongwhitishhairs; anepimeron,meropleurite,mediotergite,laterotergite, metepister-numand metepimeron withlong whitish hairs. Wing (Fig. 5): smoky,darkerincostalmargin;Cwithdelicateblackbristles sur-roundingwing;cellscandr1brownishcompletely;R1,R2+3,R4,
R5,M1,andM2 straightandalmostparalleltoeachother;
with-outsectorialvein;CuA2 andA1 touchingwingmargin,cellcup
open;alulahyaline;wing3xlongerthanwide.Stalkofhalterdarker brownwithdelicateyellowbristlesnearbase;knobdarkbrownon
Figs.5–8.Hirmoneuropsisluctuosa(Philippi,1865).5.Wing;6.Abdomenindorsalview;7.Epandriumandcerci(ce);8.Gonocoxite(gc),innergonocoxalprocess(igp)and gonostylus(gs).Scalebar=1mm.
dorsalsurfaceandlightbrownonventralsurface.Legs: grayish-brownpollinose;coxaegrayishpollinose,withlong,thinwhitish hairsonanteriorsurface;trochanterswithshortwhitehairs on anteriorsurface;femoragrayishpollinosewithshort,thinwhitish
hairsonanteriorsurfaceandlong,thinhairsonposteriorsurface; tibiaeIandIIwithdelicateshortblack bristlesonanterior sur-face;tibiaeIIIwithabundantshortblackhairs;tarsuswithshort, delicatelightbrownbristlesonanteriorsurface,andshort,strong
Figs.9–12.PupaofHirmoneuropsisluctuosa(Philippi,1865).9.Lateralview;10.Headinfrontalview(vt,verticaltubercle;as,antennalsheaths;es,epicranialsuture;cs,
Figs.13–15.PupaofHirmoneuropsisluctuosa(Philippi,1865).13.Analsegmentinlateralview(ds,dorsalspine;vpc,ventralpreanalcomb;vt,ventraltubercle;dt,dorsal tubercle);14.Analsegmentinventralview(fs,fringespines;vt,ventraltubercle;dt,dorsaltubercle)(scalebar=0.5mm);15.Analsegmentofthepupainposteriorview (ds,dorsalspines;fs,fringespines;dt,lateraltubercle).Scalebar=1mm.
dark-brownbristlesonposteriorsurface, firsttarsomere longer thanothers;pulvillussmallerthanclaws.Abdomen(Fig.6):dark gray;first segmentwithtuftofyellowish longerand thin hairs onlateralmargin; lateralmarginoftergites II–V withlong and thinwhitishhairs;tergitesIII–Vwithlongandthinwhitishhairs; sterniteslight gray, sterniteswith thin whitish hairs. Termina-lia:dorsalview:epandrium short,broaderthanlong,withlong blackbristles,basalmarginconcave,apicalmarginrounded; cer-cusovoid-rectangular(Fig.7).Gonocoxitebasebroadwithbristles elongated;innergonocoxalprocessslendertaperedapicallywith apexandcurvedupwards.Gonostyluselongated,slightlybroader basally.Aedeaguswithapicalregionupwardlyarcheddowncurved withroundedapex(Fig.8).
Descriptionofthepuparium(Figs.9–15).
Dimensions: body length 16.5–17.5mm, maximum width 4.0–4.5,obtect,4× longerthan theirgreatestdiameter, slightly archeddorsallyandcompletelycoloredbrown,moredarkinthe aster(Fig.9).
Head: narrower and shorter than thorax; vertical tubercle prominent and developed 0.86–1.06mm arising at the base of antennal sheaths,antennal sheaths 0.74mmlong and 0.29mm wide not touchingtheepicranial suture,prominent,irregularly annulate,widelyseparated,ventrolaterallydivergent,longerthan theirbasaldiameter;maxillarypalppoorlydifferentiated(Fig.10). Thorax: each wing sheath with one tubercles positionedon thecostalmarginofthewingsheath(Fig.11).Thoracicspiracle 0.67mmlongand0.21mmwide,touchingcephalothoracicsuture, prominent.Legs reachinghalfwings sheaths;forelegs touching thoracicspiracle(Fig.11).Withoutothersetae.
Abdomen:abdominalsegments1–7eachencircledbyarowof spines;abdominalsegments1–7withreniformspiraclesinpleural region.T1–T3withtransverserowof20–25strongsetae differ-entsizeonanteriormargineithersideofmidline;T4–T6withtwo strongspinesmedially,and3–4smallerspines,tergite7smaller. Pleuronofabdominalsegments1–6with4–5long,strongsetae, and2–3smaller.Pleuronofabdominalsegment7witha5strong setae,hookedapically,and2–3smaller.Sternites2–7witharowof 5–7strongsetaeclosetoposteriormargin,smallerthanthe pleu-ron.Sternites5–6shortandwithdifferent-sizedspines;sternite 7withspinesmoredeveloped,andtwolonger(Fig.12).Tergite8 terminatesinanasterofpaireddorsalandventralsharplypointed sclerotizedtubercles;dorsaltubercleslongest(Figs.13and 14); analtuberclewithventralpreanalcombprominent,withtwo well-developedspines(Fig.15).
Discussion
FivespeciesofHirmoneuropsislackthesectorialvein:H.orellanai (Stuardo),H.silvai(Stuardo),H.brevirostrata (Bigot),H.strobelii
(Rondani),andH.luctuosa(Philippi).However,thesefivespecies exhibitsubstantialmorphologicaldifferencesbetweenthem (gen-eralcolorationofthebody, colorofhairsof beardand thoracic pleura,wings, abdominal tergites) and probably have noother relations.H.luctuosaismorphologicallyclosetoH.paraluctuosa (Angulo)ingeneralappearanceandcolor.H.luctuosa(Philippi)can bedistinguishedfromH.paraluctuosa(Angulo)bythelackof sec-torialvein,yellowish legs,andthecolorofthefronsandpleura
(Angulo,1971).
Knowledgeoftheimmaturestagesoftangle-veinedfliesisvery limited,asisinformationonthehostrelationsofthespecies.The importanceoftheseparasiteshasbeendemonstratedintheiruse tosuppresspopulationsofOrthoptera(Prescott,1960).
Ofthe36speciescitedforChile(Angulo,1971),theimmature stagesofonlyonespeciesareknown,viz.Hyrmophlaebaarticulate (Philippi),reflectingthelimitedknowledgeofaspectsofthebiology ofimmaturestagesandknowledgeofthehost.
ThepupalmorphologydescribedhereissimilartothatofH. articulate(Philippi)describedbyStuardo(1936)witha few dif-ferencesin the verticaltubercles– larger and sclerotized inH. articulate,andfewerspinesindorsalfringe,butverydifferentofthe pupalskinofAtriadopsvespertilio(HaenniandBorer,2007)which lackspleuralandsternalsetaeorareveryshort,replacedbyshort spinesinsternum;andabdominaldorsalspinesarethicker.
Thepupaof Hirmoneuropsis ismorphologicallycomplex and presentssignificanttaxonomicandphylogeneticcharacters. Conflictsofinterest
Theauthorsdeclarenoconflictsofinterest. Acknowledgments
WethankDr.StephenM.Smith(Biology,Universityof Water-loo)for helpinrevisingthemanuscriptandediting theEnglish version.
References
Angulo,A.O.,1971.LosNemestrinidosdeChile(Diptera:Nemestrinidae).Gayana Zoología19,1–175.
Angulo,A.O.,1976.TrichophthalmajaffueliStuardo:NuevoparaMagallanesyalgunas consideracionessistemáticassobreTrichophthalmaamaenaBigoty Eurygas-tromyiasexmaculata(Edwards)(Diptera,Nemestrinidae).An.Inst.Patagon.7, 197–199.
Bequaert,J.,1932.TheNemestrinidae(Diptera)intheV.vonRoderCollection.Zool. Anz.100(1–2),13–33.
Bernardi,N.,1973.ThegeneraofthefamilyNemestrinidae(Diptera:Brachycera). Arq.Zool.24(4),211–309.
Bernardi, N., 1976. Classificac¸ão da subfamilia Hirmoneurinae (Diptera, Nemestrinidae).PapéisavulsosZool.,SãoPaulo30(2),25–33.
Bernardi,N.,1977.AtriboHyrmophlaebini(Diptera,Nemestridae,Hirmoneurinae), comtrezeespéciesnovasdaAméricadoSul.PapéisavulsosZool.,SãoPaulo30 (16),239–259.
Crouzel,I.S.,deSalavin,R.G.,1943.Contribuciónalestudiodelos Neorhyncho-cephalus argentinos(Diptera: Nemestrinidae).An. Soc. Cient. Argent. 136, 145–177.
Cumming,J.M.,Wood,D.M.,2009.Adultmorphologyandterminology.In:Brown, B.V.,Borkent,A.,Cumming,J.M.,Wood,D.M.,Woodley,N.E.,Zumbado,M.(Eds.), ManualofCentralAmericanDiptera,vol.1.NRCResearchPress,Ottawa,Ontario, Canada,pp.9–50.
Greathead,D.J.,1958.NotesonlifehistoryofSymmictusflavopilosusBigot(Diptera: Nemestrinidae)asaparasiteofSchistocercagregaria(Forskal)(Orthoptera: Acri-didae).Proc.R.Ent.Soc.Lond.Ser.A33,107–119.
Haenni,J.P.,Borer,M.,2007.FirstreportofaNemestrinidae(Diptera)parasitoidof theMantodea.Stud.Dipterol.14,61–65.
Handlirsch,A.,1882.DieMetamorphoseundLebensweisevonHirmoneuraobscura Meig.,einemVertretelderDipteren-FamilieNemestrinidae.Wien.Ent.Zeitg.l, 224–227.
Handlirsch,A.,1883.DieMetamorphoseundLebensweisevonHirmoneuraobscura Meig.,einemVertreterderDipteren-FamilieNemestrinidae.Wien.Ent.Zeitg.2, 11–15.
Kosmann,C.,Lamas,C.J.E.,Pujol-Luz,J.R.,2014.Nemestrinidae.In:Roig-Ju ˜nent,S., Claps,L.E.,Morrone,J.J.(Eds.),BiodiversidaddeArtrópodosArgentinosvolumen 4.EditorialINSUE–UNTSanMigueldeTucumán,Argentina,pp.407–415.
Lénonide,J.C.,1962.Formationduporerespiratoireetdelapartieproximaledutube respiratoiredelalarvedeSymmictuscostatusLoew(Diptera,Nemestrinidae) selonlesdiversrégionsducorpsdel’hôte.Bull.Zool.Soc.Fr.87,550–558.
Philippi,R.A.,1865.AufzählungderchilenischenDipteren.Verh.Zool.Bot.Ges.Wien 15,595–782(7plates).
Papavero,N.,Bernardi,N.,2009a.Catalogueofneotropicaldiptera.Nemestrinidae. NeotropicalDiptera7,1–16.
Papavero,N.,Bernardi,N.,2009b.ManualofNeotropicalDiptera.Nemestrinidae. NeotropicalDiptera8,1–11.
Prescott, H.W., 1955. Neorhynchocephalus sackenii and Trichopsidea clausa, nemestrinidparasitesofgrasshoppers.Ann.Ent.Soc.Am.48,392–402.
Prescott, H.W., 1960. Suppression of grasshoppers by nemestrinid parasites (Diptera).Ann.Ent.Soc.Am.53,513–521.
Prescott,H.W.,1961.Respiratoryporeconstructioninthehostbythenemestrinid parasiteNeorhynchocephalussackenii(Diptera)withnotesonrespiratorytube characters.Ann.Ent.Soc.Am.54,557–599.
Richter,V.A.,1997.FamilyNemestrinidae.In:Papp,L.,Darvas,B.(Eds.), Contrib-utionstoaManualofPalaearcticDiptera,vol.2.ScienceHeraldBudapest,pp. 459–468.
Stuardo,C.,1930a.UngénerodeNemestrinidaenomencionadoparalafauna chilena.Rev.Chil.Hist.Nat.33(1929),161–162.
Stuardo,C.,1930b.Notasentomológicas.Rev.Chil.Hist.Nat.34,379.
Stuardo,C.,1932.SinopsisdelosnemestrinidoschilenosdelgéneroHirmoneura Meigen(Diptera).Rev.Chil.Hist.Nat.36,61–81.
Stuardo,C.,1934.SinopsisdelosnemestrinidoschilenosdelgéneroTrichophthalma Westwood(Diptera).Rev.Chil.Hist.Nat.38,214–248.
Stuardo,C.,1935.Algunasobservacionessobrelascostumbresymetamorfosisde HirmoneuraarticulataPh.Rev.Chil.Hist.Nat.38,197–202.
Stuardo,C.,1936.NemestrinidosnuevosChilenosyanotacionessobredosespecies conocidas.Rev.Chil.Hist.Nat.40,169–178.
Teskey,H.J.,1969.LarvaeandpupaeofsomeEasternNorthAmericanTabanidae (Diptera).Mem.Entomol.Soc.Can.63,1–147.
Wagenknecht,H.R.,1940.SobrelaHirmoneuraorellanae.Rev.Chil.Hist.Nat.43, 145–147.