Abnormal iris coloration in the Campo Flicker, Colaptes campestris: pigmentary color production error?

Raphael Igor Dias1, Débora Goedert1 and Regina Helena Macedo2

1 ProgramadePós-GraduaçãoemEcologia,UniversidadedeBrasília,Brazil.2 DepartamentodeZoologia,UniversidadedeBrasília,Brasil.E-mail:rhfmacedo@unb.br

Recebidoem27/02/2009.Aceitoem18/09/2009.

ResuMo: Coloração anormal de íris no pica-pau-do-campo, Colaptes campestris: erro na produção de cor pigmentária?Apesardoamplointeressedospesquisadoresemaspectosenvolvendoacoloraçãodaplumagem,poucosesabeacercadosmecanismosdeproduçãodecorencontradosnasírisdasaves.Nesseestudo,apresentamosdadossobreapossívelvariaçãonacoloraçãodaírisdopica-pau-do-campo,Colaptes campestris,assimcomo,oregistrodeumindivíduocomumacoloraçãonãousualdosolhos.Análisesfotográficasrevelaramquenãoexistevariaçãonacoloraçãodaírisentreossexos.Entretanto,filhotesapresentamumacoloraçãodiferentedeindivíduosjuveniseadultos.Adicionalmente,osdadossugeremqueoregistroencontradopodeserresultadodealgumafalhanaproduçãodacoloraçãopigmentaraolongododesenvolvimento.

PAlAvRAs-CHAve:coloraçãodoolho,pica-pau,pteridinas,dicromatismosexual,írisdasaves.

Key-WoRDs:eyecoloration,woodpecker,pteridines,sexualdicromatism,avianiris.

Birdcolorationisproducedeitherbychemicalpig-mentsorthroughphysicalinteractionsoflightwiththestructureofavianintegumentandtissues.Studiesshowthatbothmechanismsact toproducecoloration in theplumage, skin and eyes of many bird species (Prum2006).However,littleresearchhasfocusedonthemecha-nismsunderlyingproductionandfunctionofthevariablecolorationfoundintheavianiris.

Pteridines are the most common of the pigmentsresponsibleforeyecoloration(Oehme1969).Thewide-spread distribution of pteridines and purines amongavianiriseswasconfirmedbyOliphant(1987),whoalsosuggestedthatcarotenoidsweremuchlesscommonlythebasisforeyecolorationinbirds.Pteridinesareagroupofnitrogenouscompoundsendogenouslysynthesizedfrompurines.Purines, in turn, are responsible for thebrighteyecolorofmanybirds,aswellassilvereyecolorsofbirdssuchasstarlings(McGraw2006).

Iriscolorationoftenvariesintraspecifically,andthisvariationisattributedtodifferencesbetweensexes(Har-dy, 1973; Ervin, 1975) and age classes (Trauger 1974;SweijdandCraig1991;RosenfieldandBielefeldt1997),amongotherpossibilities.Someresearchersusethesedif-ferencesiniriscolorationduringbandingstudiestoclas-sifycapturedindividuals(Yunick1977;Manuwal1978),sinceageandsexmaybeimportantattributesinstudiesofpopulationdynamicsandsocialbehavior,forexample.

Here, we describe an unusual eye coloration doc-umented for an individual Campo Flicker, Colaptes

campestris.CampoFlickersaremedium-sizedwoodpeck-ers(150 g)withavastdistributioninSouthAmerica,oc-curringfromtheBrazilianNortheasttoArgentina.Theyareeasilyrecognizedbytheirshapeandcolor,withyellowcolorationonbothsidesoftheheadandneck,withmalespresentingaredpatchonthemalarregion(Sick1997).

MetHoDs

Wehavebeen capturingCampoFlickers for threeyears(2006-2008)incentralBrazilaspartofastudyonreproductive behavior.The study site is at the FazendaÁguaLimpa (15°57’S, 47°56’W), property of theUni-versityofBrasília.Theareaofapproximately2000 haiscomposed by different vegetation types of Brazilian sa-vanna(Cerrado)andalsobyalteredvegetationduetoag-riculturalusage.However,mostofthestudyisconductedin areas where Campo Flickers are more easily found,composedofopennativevegetationwithsparsetreesandtermitemounds.

We capture individuals with mist nests and bandthemwithacombinationof threecoloredbandsandapermanent metal band from the Brazilian Bird-band-ing Agency (CEMAVE). For each individual we col-lectmorphometricdata,recordeyecoloration,andalsotake a photo. Additionally, during the breeding seasonweactively search fornests.Whenever found,nests aremonitoredandthenestlingsbandedonthe25thdayafter

NotARevista Brasileira de Ornitologia, 17(2):152-154Junho de 2009

hatching, repeating all the procedures carried out withadults.Werepeatthesameprotocolwithrecapturedindi-viduals.Throughtheexaminationofphotoswecancom-pareindividualeyecolorationthroughtimeandexplorevariationslinkedtosexandage.

Results

We have banded 108 Campo Flickers to date, in-cluding56adults,threejuvenilesand49nestlings,con-sideringageonthedayofthefirstcapture.Werecaptured14of thenestlings as juveniles or adults andhave alsomonitoredtheother individuals throughtheyearswithbinoculars, for other purposes. All juveniles and adultshavedarkreddish-brown iriscoloration(Figure 1),andthesexesarenotdichromaticforthistrait(Figures1and2).Nestlingspresentdark-grayeyecolor(Figure 1)thatchanges to the juvenile-adult coloration when they areapproachingfledging.

On14November2007,wecapturedafemalewithapaleiriscoloration(Figure 2).Noothermorphological

orplumageaspectwasdifferentinthisfemalerelativetoothercapturedindividuals.Theabnormaliriscolorationofthisfemaledidnotaffectmateacquisitionandrepro-duction,forshebredinthatyearandproducedfournest-lings,twomalesandtwofemales.Basedonbothrecap-tureandmonitoringdatafortheseyoung,wehavefoundthatnoneofthempresentedthesameeyecolorationofthemotherandnocoloralterationshavebeenperceivedsubsequently.

DIsCussIoN

Although other studies have shown that individu-alsofsomespecieschangeiriscolorationastheyageandthatforotherspeciesthiscolorationissometimessexuallydichromatic(Ervin1975;SweijdandCraig1991;Rosen-field and Bielefeldt 1997), this is not the case for theCampoFlicker.With theexceptionof thedocumentedchange in nestling eye color close to fledging, we havefoundnoiriscolordifferenceinCampoFlickersamongageclassesorbetweensexes.Consideringthatthereisno

FIGuRe 2:FemaleCampoFlicker,Colaptes campestris,withnormaleyecoloration(left)andwithabnormaleyecoloration(right).AllphotosbyR.I.Dias.

FIGuRe 1:MaleCampoFlicker,Colaptes campestris,atdifferentages:nestling,juvenileandadult(lefttoright).AllphotosbyR.I.Dias.

153AbnormaliriscolorationintheCampoFlicker,Colaptes campestris:pigmentarycolorproductionerror?Raphael Igor Dias, Débora Goedert and Regina Helena Macedo

Revista Brasileira de Ornitologia, 17(2), 2009

naturalvariationinadultCampoFlickers’iriscoloration,wepresumethatthisdocumentedcasemayhaveresultedfromsomeontogeneticproblemrelatedwiththemecha-nismofpigmentarycolorproduction.Astudythatevalu-atedpigmentsfromthestromaoftheirisofseveralbirdspecies revealed that for the Northern Flicker (Colaptes auratos),acongenericspecies,theirispigmentswerepri-marilypteridines (Oliphant1977).We speculate that aprobleminpteridinesynthesiscouldhavecausedtheob-servedabnormality.

Some unusual eye colorations are occasionally de-scribedintheliterature(Prescott1972;BoanoandJan-ni 2008), however, no obvious explanations have beensuggestedforthesecases,thuspreventingconclusionsastowhether these colorations arenormally found in thespeciesorwhether theymayresult fromdevelopmentalabnormalities.However,iriscolorationisbasednotonlyonpigmentsbutalsooncomplexcombinationsofpig-ments and other cellular mechanisms of avian integu-ments(Prum2006).Explanationsforthesekindsofab-normalitiesdependupon furtherdocumentationof thephenomenonandstudiesdirectedtowarduncoveringtheunderlying genetic and developmental contexts of birdiriscoloration.

ACKNoWleDGMeNts

This study was supported by the Coordenação deAperfeiçoamento de Pessoal de Nível Superior – CAPES and theConselhoNacionaldeDesenvolvimentoCientífico eTecnológico–CNPqthroughstudentscholarshipstoR.I.D.andthrougharesearchfellowshiptoR.H.M.

ReFeReNCes

Boano, G. e Janni, o. (2008).Rufous-morphBright-rumpedAttila(Attila spadiceus) with white eyes: Photographic evidence fromPeru.Boletín SAO,18:16-19.

ervin, s. (1975).Iriscolorationinyoungbushtits.Condor,77:90-91.Hardy J.W. (1973).Ageandsexdifferencesintheblack-and-bluejays

ofMiddleAmerica.J. Field. Ornithol.,44:81-90.Manuwal, D.A. (1978). Criteria for aging cassin’s auklets. Bird-

Banding,49:157-161.McGraw, K.J. (2006). Mechanics of uncommon colors: Pterins,

porphyrins, and psittacofulvins, p.  354-398. Em: G.E. Hill eK.J. McGraw (eds.). Bird coloration. Volume I: Mechanismsand Measurements. Harvard University Press, Cambridge,Massachusetts.

oehme, H. (1969).VergleichendeUntersuchungenuberdieFarbungderVogeliris.Biol. Zbl.,88:3-35.

oliphant, l.W. (1987).Pteridinesandpurinesasmajorpigmentsoftheavianiris.Pigm. Cell Res.,1:129-131.

Prescott, K.W. (1972).Anadultmockingbirdwithapalewhiteiris.Bird-Banding,43:219-220.

Prum, R.o. (2006).Anatomy,physics, and evolutionof structuralcolors, p.  295-353. Em: G.E. Hill e K.J. McGraw (eds.). Birdcoloration.VolumeI:MechanismsandMeasurements.HarvardUniversityPress,Cambridge,Massachusetts.

Rosenfield, R.N. e Bielefeldt, J. (1997).Reanalysisofrelationshipsamongeyecolor,ageandsexintheCooper’shawk.J. Raptor Res.,31:313-316.

sick, H. (1997).Ornitologia Brasileira.Ed.NovaFronteiraS.A.,RiodeJaneiro,Brasil.

sweijd N. e Craig, A.J. (1991). Histological basis of age relatedchanges in iris color in theAfricanpied starling (Spreo bicolor).Auk,108:53-59.

trauger D.l. (1974).EyecoloroffemaleLesserScaupinrelationtoage.Auk,91:243-254.

yunick, R.P. (1977).EyecolorchangesintheDark-eyedJuncoandWhite-throatedSparrow.N.Amer.Bird Bander,2:155-156

154 AbnormaliriscolorationintheCampoFlicker,Colaptes campestris:pigmentarycolorproductionerror?Raphael Igor Dias, Débora Goedert and Regina Helena Macedo

Revista Brasileira de Ornitologia, 17(2), 2009