Immature stages of Hamadryas fornax fornax (Hübner) (Lepidoptera: Nymphalidae: Biblidinae)

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REVISTA

BRASILEIRA

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Entomologia

AJournalonInsectDiversityandEvolution

Systematics,

Morphology

and

Biogeography

Immature

stages

of

Hamadryas

fornax

fornax

(Hübner)

(Lepidoptera:

Nymphalidae:

Biblidinae)

Lucy

Mila

Garcia

Salik

a,∗

,

Luis

Anderson

Ribeiro

Leite

b

_,

_Fernando

_Maia

_Silva

_Dias

a

_,

Mirna

Martins

Casagrande

a

_,

_Olaf

_Hermann

_Hendrik

_Mielke

a a_{DepartamentodeZoologia,UniversidadeFederaldoParaná,Curitiba,PR,Brazil}

b_{LaboratóriodeEntomologia,DepartamentodeBiologia,UniversidadeFederaldeSergipe,SãoCristóvão,SE,Brazil}

a

r

t

i

c

l

e

i

n

f

o

Articlehistory: Received12August2014 Accepted4August2015 Availableonline1October2015 AssociateEditor:LuisParra Keywords: Bionomy Lifecycle Neotropical Papilionoidea

a

b

s

t

r

a

c

t

TheexternalmorphologyandbiologyoftheimmaturestagesofHamadryasfornaxfornax(Hübner,[1823])

(Lepidoptera,Nymphalidae,Biblidinae)recordedonDalechampiatriphylla(Euphorbiaceae)inCuritiba,

Paraná,Brazilaredescribed.Morphologicalcharactersareillustratedanddescribed,asaresultof

obser-vationsinscanningelectron,stereoscopeandopticalmicroscopes,thelasttwoattachedtoacamera

lucida.ResultsarecomparedanddiscussedwithimmaturestagesofotherspeciesofBiblidinae.

©2015SociedadeBrasileiradeEntomologia.PublishedbyElsevierEditoraLtda.Thisisanopen

accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction

HamadryasHübner,[1806](Lepidoptera:Nymphalidae: Biblid-inae)encompasses20speciesand33 subspecies(Lamas,2004); these butterflies are popularly known as crackers, due to the characteristicnoise somespecies producewhileflying(Jenkins, 1983;Otero,1991;Monge-Nájera,1992,1995;Monge-Nájeraand Hernández,1993;Monge-Nájera et al.,1998; Yacket al.,2000; Marini-Filhoand Benson,2010; Murillo-Hiller, 2011).They are restricted to the Americas and occur in tropical and subtropi-cal forests, savannas, arid and semi-arid lands (Jenkins, 1983). Hamadryasfornax(Hübner,[1823])hastworecognizedsubspecies (Lamas, 2004): H. fornax fornax (Hübner, [1823]) with South AmericandistributionfromVenezuelatoArgentinaandH.fornax fornacalia(Fruhstorfer,1907)distributedfromtheSouthofUnited StatestotheNorthernpartofColombiaandVenezuela(DeVries, 1987;Jenkins,1983;Neild,1996;Lamas,2004).

Hamadryas fornax fornax (Hübner, [1823]) usually perches upsidedownontreetrunksonvalleysofriversandclearingsin for-esthabitatsanddespiteitssimilaritywiththeotherspeciesofthe genus,itisdistinguishedbyitsforewingontheventralsurfacewith theproximalareaofthediscalcellpresentingwhiteor grayish-whitecoloration,rarelypale-yellowandthemustardcoloration

∗ Correspondingauthor.

E-mail:lucymilas@gmail.com(L.M.G.Salik).

ontheventralsideofthehindwing(Jenkins,1983).Immatures areassociatedtoplantsofthegenusDalechampia(Euphorbiaceae) (D’Almeida, 1922; Costa Lima, 1936; Armbruster, 1982, 1983; Jenkins,1983;Neild,1996;Canals,2003;Pastrana,2004).Females aresimilartomales,butfrequentlywithlargersizeandforewings withamoreroundedshape(Figs.1–4)(Jenkins,1983).

Despite the largeamount of data on the geographic distri-bution and host plants found in the literature (Jenkins, 1983; DeVries,1987;Neild, 1996;Pastrana, 2004;Contreras Chialchia and Contreras Roqué, 2010), currently there is information on the morphology and biology of immature stages of only eight species:H.feroniaferonia(Linnaeus,1758),(D’Almeida,1922);H. amphinomeamphinome(Linnaeus,1767)(D’Almeida,1922;Müller, 1886;MuyshondtandMuyshondt,1975a);H.fornaxfornax (Hüb-ner, [1823]) (Müller, 1886); H. februa februa (Hübner, [1823]) (ComstockandVasquezGarcia,1961;D’Almeida,1922;Muyshondt andMuyshondt,1975b;Young,1974);H.arete(Doubleday,1847) (Müller,1886);H.guatemalena guatemalena(H.W.Bates,1864) (Muyshondtand Muyshondt, 1975c)and H. epinome (C. Felder &R. Felder,1867) (Müller,1886; D’Almeida, 1922; Leite etal., 2012b).

Itiswidelyknownthatdataontheimmaturestagesare impor-tantfortaxonomicandphylogeneticstudiesofLepidoptera(Freitas etal.,1997;FreitasandBrown,2004);thereforethisstudyaimsto provideinformationandextendtheknowledgeonthesubfamily

http://dx.doi.org/10.1016/j.rbe.2015.08.002

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/).

302 L.M.G.Saliketal./RevistaBrasileiradeEntomologia59(2015)301–306

Figs.1–4.Hamadryasfornaxfornax(Hübner,[1823]).1,2.Male:1,dorsalview;2,ventralview;3,4.Female:3,dorsalview;4,ventralview.Scalebar:1cm.

Biblidinaebydescribingtheexternalmorphologyandthebiology oftheimmaturestagesofH.fornaxfornax.

Materialandmethods

EggswerecollectedintheParqueMunicipalBarigui(25◦25S, 49◦18W, 910m), Curitiba, Paraná, Brazil, along with branches of the host plant Dalechampia triphylla Lam. (Euphorbiaceae) andrearedinlaboratory(LaboratóriodeEstudosdeLepidoptera NeotropicalattheUniversidadeFederaldoParaná).Laboratory pro-cedures,suchasthemaintenanceofthesamplesandthehostplant, preparationandobservationofthestructuresusingstereoscopic microscope,drawings,photographs,scanningelectronmicroscopy andterminologyfollowsLeiteetal.(2012b)andotherrecent stud-iesonimmaturesofBiblidinae(Leiteetal.,2012a,2014).Voucher specimens aredeposited at theColec¸ãoEntomológica Pe. Jesus SantiagoMoure;UniversidadeFederaldoParaná,Curitiba,Paraná, Brazil.

Results

Hamadryasfornaxfornax(Hübner,[1823])(Figs.1–29) Egg(Figs.5–9)

Elliptical,withseveralirregularcarinaeandflattenedonthe bot-tompole.Uniformlypearlywhiteincolor.Micropilarregiononthe upperpoleinthecenterofaroundandslightlyconcavearea.

Ovipositionis normally gregarious;theeggs arelaid onthe uppersideofthehostplantDalechampiatriphylla,oneontopof eachother,thefirstinstarhatchlaterally.

Diameter:1.01mm.Averageduration:8days(n=15). Firstinstar(Figs.10,19–22)

Headrounded,black,andwithoutscoli.Fronsventrally delim-itedbytheclypeus,whichappearsasasclerotizedtransverseband. Labrumbilobed.Mandiblesstronglysclerotizedwithaserrated cut-tingedge.Sixstemmata latero-ventrally,1–4and6arranged in semi-circleand5ventrally,andclosertothebaseoftheantenna.

Pronotalplateblackanddivided,formingtwosub-rectangular plates,withfourpairsofsetaeonchalazae.Thoraciclegswiththe

samecolorofthepronotalplate.Bodytranslucentyellowishochre, withroundedwhitespotsregularlydistributedonthedorsaland lateralareas.Numerousspiniformorclavateblacksetaedistributed alongthebody,mostofthemonchalazae.Basesofallblacksetae formingcircularblackenedareasinterspersedwithwhiterounded areas.SpiraclesofT1andA8ellipticalandsimilar;otherspiracles smallerandrounded.Aftertheeclosion,thelarvaearenot gregar-ious,andfeedindependently.ChaetotaxyisgivenbyFigs.19–21.

Headcapsule:width:0.65mm;height:0.68mm.Averagelength ofthelarvabeforemolting:5mm.Averageduration:3days(n=9).

Secondinstar(Figs.11,23)

Headcapsuleblack.Epicraniumwithapairofshorttruncated dorsalscoli.Setaeonlateralandlateroventralregionsofthe epi-craniumoncream-coloredchalazae.Prothoraxyellowochre,with blackanddistallycreamywhitescoli.Remainingsegmentsolive brownwithanarrowyellowochrelateralbandinA1–A10,atthe levelofthesupraventralsetae.Thoraxandabdomenwith subdor-salblackand distallycreamy whitescolionT2,T3, A7and A8, remainingscolitranslucentyellow.

Headcapsule:width:1.04mm,height:0.95mm.Lengthofthe dorsalprotuberance:0.44mm.Averagelengthofthelarvabefore molting:6mm.Averageduration:3days(n=8).

Thirdinstar(Figs.12,24)

Headcapsuleblack;dorsalscolilongerthanthepreviousinstar, blackenedandwithspiniformsetae.Thoraxandabdomenwiththe samecolorationofthehead,exceptfortheyellowochre supraven-tralandventralareas.Mostofthethoracicandabdominalscoli black,exceptforsomelateraltranslucentyellowscolifromA3to A6.

Headcapsule:width:1.63mm;height:1.66mm.Lengthofthe dorsalprotuberance:2.7mm.Averagelengthofthelarva before molting:13.5mm.Averageduration:4days(n=7).

Fourthinstar(Figs.13,25)

Headcapsulesimilartothepreviousinstar.Prothorax anteri-orlyreddish-brown,withblackpronotalplate.Dorsally,twopairs ofyellowlongitudinalbandsfromT2toA9.Reddish-brownband

Figs.5–18.Hamadryasfornaxfornax(Hübner,[1823]).5–9.Egg:5,SEMlateralview;6,SEMlateralviewoftheegg-laying;7,lateralview;8,dorsalview;9,lateralviewof theegg-laying.10–15.Larvae:10,1stinstar;11,2ndinstar;12,3rdinstar;13,4thinstar;14,5thinstarlateralview;15,5thinstardorsalview.16–18.Pupae:16,ventral view;17,dorsalview;18,lateralview.SEM–ScanningElectronicMicroscopy.ScalebarsFigs.7–8:0.5mm,Fig.9:1mm.

laterallydisposedonT2andT3andontheabdominalsegmentsat thelevelofthesupraventralsetae.

Headcapsule: width:1.8mm,height: 1.7mm.Length ofthe dorsalprotuberance:3.2mm.Averagelengthofthelarva before molting:23mm.Averageduration:4days(n=7).

Fifthinstarlarva(Figs.14,15and26)

Headcapsuledarkbrown.Pronotalplateblack.Spiniformsetae distributed along the body, sometimesgrouped in scoli, some-times individualized, light brown setae,except those fromthe supraventralandventralregionsfromT1toA8,whichhaveyellow coloration.Thoraxandabdomenyellow,withseveralblack

longi-tudinalbandsandanorangelateralbandfromthespiraculartothe ventralarea.Abdominallegsorange.

Headcapsule: width: 3.4mm,height: 3.2mm. Lengthof the dorsalprotuberance:6.38mm.Averagelengthofthelarvabefore molting:33mm.Averageduration:7days,1moredayonprepupa (n=7).

Pupa(Figs.27–29)

Adecticousandobtect,suspendedbythecremaster.Elongated, median-dorsallyprojectedonT2andA2,formingcrests.Freshly formedpupaelight green,darkeningtobrownish darkgreenin aboutoneday.LightgreensemicircularspotdorsolaterallyonT2.

304 L.M.G.Saliketal./RevistaBrasileiradeEntomologia59(2015)301–306 D1 XDI XD2 SD1 SD1 SD2 SD2 SD1 L2 L2 L1 L1 L1 V1 XD2 XD1 D1 D1 D2 D2 SD2 SD1 V1 _V1

20

21

19

SV2 SV1 SV1 SV1 SV1 SV1 SV1 SV2 SV2 D2 D1 D1 D1 D1 L2 L1 L1 L3 D2 D2 D2 D2 T1 T2 T3 A1 A2 SV2 SV3 SV4 SV1 V1 SD1 SV1 SD2 SD1 PP A3 A4 A5 A6 A7 A8 A9+10

Figs.19–21.Hamadryasfornaxfornax(Hübner,[1823]).1stinstarchaetotaxy:19,mapofsetaeofthethoraxandabdomen;20,pronotalplate;21,analplate.

Figs.22–24. Hamadryasfornaxfornax(Hübner,[1823]).Headcapsulefrontalview: 22,1stinstar;23,2ndinstar;24,3rdinstar.ScalebarFigs.22,23:0.25mm;Fig.24: 0.5mm.

Apairoffoliaceousdorsolateralappendicesontheheadvertex. Fronssmooth,subtriangularclypeus;mandibleslateroventrallyto theclypeus; labrumasa smalllozengeshapedstructure inferi-orlytotheclypeusandbetweenthemandibles;darkbrowngaleae

Figs.25–26.Hamadryasfornaxfornax(Hübner,[1823]).Headcapsulefrontalview: 25,4thinstar;26,5thinstar;24.ScalebarFig.25:0.5mm;Fig.26:1mm.

arising inferiorly to the mandibles and lateroinferiorly to the labrumandendingnexttothedistalportionoftheantennae;eyes laterallytothemandibularregion;striatedantennaeextendly, lat-eraltotheeyes, proximalportionat thebaseofthe foliaceous appendicesanddistalportionontheforewingmargins.

Pronotum subrectangular and small, with a median suture. Mesonotumlargeandconvex.Metanotumnarrow,withaconvex marginonitsanteromedianregion.Baseoftheprothoraciclegsat theinferiorportionoftheeye,laterallytothegaleaeandendingon theanteriorhalfoftheselastones;baseofthemesothoraciclegson theanteriorthirdoftheantennaeandendingatitsposteriorthird.

Figs.27–29.Hamadryasfornaxfornax(Hübner,[1823]).Pupa:27,lateralview;28,ventralview;29,dorsalview.Scalebar:0.5cm.

Abdomenwithtensegments,lateralellipticalspiraclesfromA2 toA8.NarrowmediandarkbrownbandventrallyfromA4toA8. Cremasterdarkbrown,withdistalsimplehooksontheapexofA10. Averagelengthofthepupa,fromthevertextothecremaster: 30mm.Averagelengthofthefoliaceousappendices:15mm. Aver-ageduration:7days(n=6).

Discussion

SpeciesofHamadryasfeedonspeciesofDalechampia,and D. tryphillaisrecordedashostplantofH.fornaxand furthereight speciesof thegenus(Beccaloni etal., 2008).Recordsof species ofHamadryasfeedingonothergeneraofhostplantsprovidedby Beccalonietal.(2008)areunlikelyandneedconfirmation.

Biblidinaeusuallypresenteggswithwelldefinedcrests,asin species ofTemenis laothoeliberia (Fabricius,1793) (Muyshondt, 1974), DynamineHübner, [1819](Leiteetal., 2012a,2014)and somespeciesofAgeroniini,PanaceaGodmanandSalvin,1883and BatesiaC.FelderandR.Felder,1862(DeVriesetal.,2000;Daniels etal.,2008).Incontrast,speciesofHamadryas,suchasH.fornax for-naxandH.epinome(Leiteetal.,2012b)presenteggswithirregular ornamentationofthechorion,indicatingthatthischaractermight becharacteristicofthegenus.Inthefirstinstar,theshapeofthe baseofSD1andSD2onT1,T2andT3,andthelocalizationofD2on thepronotalplatedifferfromthosefoundinH.epinome(Leiteetal., 2012b).Inthefifthinstar,similartoH.guatemalena,H.februa,and H.amphinome(MuyshondtandMuyshondt,1975a,b,c),H.fornax fornaxpresentsdorsalscolionlyonA7andA8,withthreeandfive branchesrespectively.InH.epinome(Müller,1886;Jenkins,1983; Leiteetal.,2012b)additionaldorsalscoliarepresentinall abdomi-nalsegments,althoughsimpleandsmallerthanthethoseinA7and A8andthesubdorsalscoli.Hamadryas(MuyshondtandMuyshondt, 1975a,b,c)andEctimaDoubleday,[1848](Janzen, 2010)present longfoliaceousprojectionsonthevertexofthepupa.Pupaeofother

Ageroniini,BatesiaC.FelderandR.Felder,1862andPanacea God-manandSalvin,1883donothavetheseprojections(DeVriesetal., 2000;Danielsetal.,2008).InEpiphilini,speciesofTemenisHübner, [1819](Muyshondt,1974)alsohavetheseextensions,althoughnot aslongasinHamadryas;otherspeciesofBiblidinaeoftenhavea slightlypronouncedvertex(i.e.DeVries,1987),butnevergreatly extendedastheabove-citedtaxa.ThedorsolateralcolorofT2of thepupaedifferentiatesH.fornaxfornaxfromH.epinome(Leite, 2012b),whicharelimegreenintheformerandbrowninthelatter. The current understandingof thephylogenetic relationships ofHamadryas(Garzón-Ordu ˜na,2012;Garzón-Ordu ˜naetal.,2013) lackmorphologicalandbiologicalevidencefromimmaturestages ofpotentialevolutionaryimportance,suchastheabove-mentioned differencesinegggregariousness,chaetotaxy,andscoli distribu-tion,forexample.Unfortunately,mostdescriptionsofimmature stagesofHamadryasarebrief,whichlimitscomparisons.Studies likethisareessentialtoprovideanewarrayofcharactersfor phy-logenyandabetterunderstandingthesystematicofthegenus.

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgments

WewouldliketothanktheCentrodeMicroscopiaEletrônica (CME-UFPR)andtheTAXonline–RedeParanaensedeColec¸ões BiológicasoftheUniversidadeFederaldoParanáforsomeofthe photographs; members of the Laboratório de Estudos em Lep-idoptera Neotropical (LELN-UFPR) for additional help; and the Conselho NacionaldeDesenvolvimento CientíficoeTecnológico (CNPq)forthefellowshipgrantedtotheauthors.

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