Records of leucism in albatrosses and petrels (Procellariiformes) in the South Atlantic Ocean

Patrícia L. Mancini1,2; Sebastián Jiménez3,4; Tatiana Neves1 and Leandro Bugoni5

1 Pós-GraduaçãoemOceanografiaBiológica,UniversidadeFederaldoRioGrande.CaixaPostal474,CEP 96201-900,RioGrande,RS,Brasil.2 ProjetoAlbatroz.AvenidadosBancários,76,sala22,PontadaPraia,CEP 11030-300,Santos,SP,Brasil.E-mail: patmancinibr@yahoo.com.br.3 ProyectoAlbatrosyPetreles,CentrodeInvestigaciónyConservaciónMarina.AvenidaGiannattasio,Km 30.500,ElPinar,Canelones,Uruguay.4 DepartamentodeRecursosPelágicos,DirecciónNacionaldeRecursosAcuáticos(DINARA),Constituyente1497,CaixaPostal11.200,

Montevideo,Uruguay.5 InstitutodeCiênciasBiológicas,FundaçãoUniversidadeFederaldoRioGrande-FURG,CaixaPostal474,CEP 96201-900,RioGrande,RS,

Brasil.

Submetidoem:10/08/2009.Aceitoem:19/09/2009.

ReSuMO: Registros de leucismo em albatrozes e petréis (Procellariiformes) no Oceano Atlântico Sul. Foram registradostrêsalbatrozes-de-sobrancelha-negraThalassarche melanophris (dois juveniseumadulto)e trêspombas-do-caboDaption capenseleucísticosentredezembrode2005ejulho-agostode2008emáguasaolargodosuldoBrasil,UruguaieÁfricadoSul,noOceanoAtlântico Sul. Para ambas as espécies, três indivíduos apresentaram plumagem totalmente branca, mas com patas, bico e íriscaracterísticosdaespécie(doisalbatrozes)oulevementemaisclaradoquenaplumagemnormal(umapomba-do-cabo).Oalbatroz-de-sobrancelha-negrafotografadonaÁfricadoSultinhasomentealgumasdascoberteirassuperioresdasasascomcoloraçãobranca.Aspombas-do-caboregistradasnoUruguaitambémapresentaramapenaspartedascoberteirassuperioresbrancas.Aparentemente,apenasumregistrodeleucismoemProcellariiformeshaviasidoreportadonoBrasil,bemcomoparaoAtlânticoSul.Osregistrosdeleucismoemalbatroz-de-sobrancelha-negraparecemserosprimeirosparaaespécie.

PALAvRAS-ChAve: leucismo, albatroz-de-sobrancelha-negra, Thalassarche melanophris, pomba-do-cabo, Daption capense,OceanoAtlânticoSul.

Key-WORd:leucism,Black-browedAlbatross,Thalassarche melanophris,CapePetrel,Daption capense,SouthAtlanticOcean.

Severalkindsofaberrantcolorationshavebeende-scribedinterrestrialbirdspecies(e.g.Sage1963,Nemésio1999,2001,Gonçalves-Jr.et al.2008),aswellasinpro-cellariform seabirds (Fischer 1972, Garrett 1990, Briedand Mougeot 1994, Tickell 2000, Ristow and Witte2004,Briedet al.2005).Themost importantpigmentsthatdetermineplumagecolorationinbirdsaremelaninesand carotenoids. Carotenoids vary in colour from pale-yellowtoscarlet-redandtheyaretakeninwithfoodandtransformedintocolourpigmentsbyenzymes.Thedepo-sitionofpigmentstakesplacedirectlyatthestartoffeath-er growth. Aberrations in this pigmentation are mostlycausedbynutritionaldeficienciesandusuallydonothaveageneticcause(vanGrouw2006).Therearetwotypesofmelaninpresent inbirds:eumelaninandphaeomelanin.The eumelanin is responsible for black, grey and dark-brownfeathers.Inahighconcentration,phaeomelaninisresponsibleforreddish-brownfeathers.Inlowerconcen-trations,thecolourwillappearsasyellow-browntoalmostwhite.Bothmelanins together can give combinationofcolourssuchasgreyish-brown.Intheskinandeyes,onlyeumelaninispresent.Melaninformationinvolvesaseries

ofbiochemicalreactionsandtheformationprocessisde-terminedgenetically.Anyaberrationintheprocesshasapotentialinfluenceonthecoloursofabird.Amutationintheformationoftheenzymetyrosinasemayinhibittheformationofmelanin(vanGrouw2006).Themostcom-moncolourmutationinalbatrossesandpetrelsarealbi-nismandleucism(Briedet al.2005).Albinismisdefinedasatotallackofbothmelaninsinfeathers,eyesandskinasaresultofaninheritedabsenceoftyrosinase(vanGrouw2006),whileleucismisdefinedasapartialortotallackofeumelaninandphaeomelanininthefeathersasaresultofaninheriteddisorderinthedepositionofthesepigmentsinthefeathers.Incertainforms,onlyfeathersbecomeco-lourlesswhileeyes,skinandhornybarepartsarenormallycolored. Leucistic birds always have colored eyes whichdistinguishthemfromalbinos.Thereasonforthisisthatonlythepigmentsoftheirisaremissingandthepigmentsinthebackoftheeyeballremainpresentandthereforetheeyeslookdark(Nemésio1999,2001,vanGrouw2006).InthisstudywereportedleucisminthreeBlack-browedAlbatrossesThalassarche melanophris and threeCapePe-trelsDaption capensefromtheSouthAtlanticOcean.

NOTA Revista Brasileira de Ornitologia, 18(3):245-248 Setembro de 2010

Onealbatrossandonepetrelshowingaberrantplum-age coloration were photographed by Sandro de MelloTerrosowhileaboardafishingvesseloperatingoffsouth-ernBrazilduring July-August2008. InwatersoffUru-guay,FernandoAreaphotographedoneaberrant-plum-agedalbatross inAugust2007, andS. J.photographedtwo petrels on 15 December 2005 and 16 December2007.On26May2007,TrevorHardakerphotographedone albatrosswith aberrantplumageoffCapeTown inSouthAfrica.

All the three albatrosses with aberrant plumageswereidentifiedastheBlack-browedAlbatrossandthepe-trelsastheCapePetrel.ThealbatrossesfromBrazilandUruguaywerejuveniles,whiletheSouthAfricaonewasanadult.Bothjuvenilespecimenshadcompletelywhiteplumage (Figure  1  and  2), the adult only some white

upper-wing coverts (Figure  2; see also www.hardaker.co.za/blackbrowedalbatross1.htm).The eye and bill co-lourswerenormalinallthesebirds.AmongCapePetrels,individual from Brazil had completely white plumage,butthecolorationofthebillwaslighterthanthenormal(black)pattern for the species (Figure 3).Anotherbird(Figure 4)hadmostlywhitebackandwing-coverts,lack-ingthediagnosticspottedpatternofthespecies.Allthesecharacteristics leadus toconclude the six seabirdswereleucistic.

Adult Black-browed Albatrosses are mostly whitewithblackwingsandgreytailandhaveorangebillwithreddish-tip.Thejuvenilesaresimilar,buttheolive-brownbillsbecome lighterwithage, retainingadark tip (Fig-ure 1).Adults and juvenileshave adark eyepatch andbrown iris (Onley and Scofield 2007). The leucistic

FiguRe 1:LeucisticBlack-browedAlbatross,Thalassarche melanophris,amongtwootherindividualsofthesamespecies(left).Detailpictureaboveshowsthebillcolour,characteristicofjuveniles.Atrightapicturewithbetterresolutionofajuvenileofthesamespecieswithnormalplumage.Photos:SandrodeMelloTerroso(left)andDemétrioCarvalho/ProjetoAlbatroz(right).

FiguRe 2:LeucisticadultBlack-browedAlbatross,Thalassarche melanophris,photographedinMay2007inSouthAfricanwaters(left).OntherightajuvenileofthesamespeciesrecordedinUruguayanwatersinAugust2007.Photos:TrevorHandaker(left)andFernandoArea(right).

246 Recordsofleucisminalbatrossesandpetrels(Procellariiformes)intheSouthAtlanticOceanPatrícia L. Mancini; Sebastián Jiménez; Tatiana Neves and Leandro Bugoni

Revista Brasileira de Ornitologia, 18(3), 2010

Black-browedAlbatrossesfromBrazilandUruguaywerejuveniles,basedonthebrownishbillwithadarktip.Ad-ditionally, it was possible to compare them with birdswithnormalplumage in the samepictures,makingtheidentification easier. In 2008, albatrosses with similarcharacteristicswereobservedoffBrazilian coaston twooccasions observed, but not photographed (S. M.Ter-roso,pers. comm.).

TheCapePetrelisadistinctive-lookingprocellariidduetoitsuniquecheckeredblackandwhitedorsalplum-age. Adult and juveniles have similar plumage patterns(OnleyandScofield2007).BirdssupposedtobeleucisticCape Petrels are likely to be misidentified as the SnowPetrelPagodroma nivea,particularlywhere the two spe-ciesoccurs in simpatry (Thompson et  al. 2000).How-ever,thiswasnotthecaseofthetotallywhiteCapePetrel

observedinthisstudy,becausetheSnowPetrelismainlyrestrictedtoAntarcticwatersupto300kmfromthepackice(OnleyandScofield2007).Moreover,thebillsizeandshapeof thebird inquestiondonotmatch thatof theSnowPetrel,whichhaveashorterandbulkierbill(Onleyand Scofield 2007).The observed individual presentedlightercoloursofthebillthanthedarkcharacteristicofthespeciesandtherewasnodoubtaboutidentification.

Thereareseveralkindsofcolouranomaliesinbirds,whileinprocellariiforms,casesofleucism,albinismandmelanismhavebeenrecorded(Briedet al.2005).Amongthealbatrossestheseanomalieshavebeenreportedinatleastfivespecies:WanderingDiomedea exulans,ShyThal-assarche cauta, Laysan Phoebastria immutabilis, Black-footedPhoebastria nigripesandLight-mantledPhoebetria palpebrataAlbatrosses(Fischer1972,Lepschi1990,Bried

FiguRe 3:LeucisticCapePetrel,Daption capense,withnormaleyecoloration,butlegsandbilllighter(left)thanthetypicalspecies,asshowedintherightpicture.Photos:SandrodeMelloTerroso(left)andLeandroBugoni(right).

FiguRe 4:LeucisticCapePetrels,Daption capense, recordedinUruguay in15December2005(left)and16December2007(right).Photos:SebastiánJiménez.

247Recordsofleucisminalbatrossesandpetrels(Procellariiformes)intheSouthAtlanticOceanPatrícia L. Mancini; Sebastián Jiménez; Tatiana Neves and Leandro Bugoni

Revista Brasileira de Ornitologia, 18(3), 2010

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andMougeot1994,Tickell2000).Amongpetrels,plum-ageaberrationshavebeenrecordedinatleast22species(LeeandGrant1986,Garrett1990,Briedet al.2005).

Some authors have erroneously recorded leucisticbirdsasalbinosor‘partiallyalbinos’(seediscussioninvanGrouw 2006 and Gonçalves-Jr. et  al. 2008). Differentformsofleucismareknownandcanvaryfromonlyafewwhitefeathers(< 25%),asintheBlack-browedAlbatrossobservedinSouthAfricaortheCapePetrelinUruguay,towholewhite-plumaged individuals. Incertain forms,only the feathersbecomecolourlesswhile inothers thebill,skinandhornypartscanbecomecolourlessaswell.Leucisticbirdsrarelyrepresentmorethan1%ofallspeci-mens inanaturalpopulation(Sage1963,Benschet al.2000).

Amongtheprocellariiforms,theSouthernGiantPe-trelMacronectes giganteushasadimorphicplumage,beingdark-brown when juveniles and becoming lighter aftersuccessivemoults.Totallywhiteorwhitebirdswithfew,scattered brown feathers also occur (Carlos and Voisin2008).However,thisdimorphism,whichalsoappearsinmany gadfly petrels (Pterodroma spp.), is controlled bytwoautossomicallelegenes,wherewhitedominatesthedarkones(Shaughnessy1970).Thewhiteplumagerepre-sentsabout15%ofsomeSouthernGiantPetrelpopula-tions(Shaughnessy1971).Nevertheless,thelightcolourinSouthernGiantPetrels isadistinctgeneticphenom-enonanditisnotconsideredaplumageaberration.

Apparently, the only previous record of colouranomaliesinBrazilianprocellariiformswasaspecimenofTrindadePetrelPterodroma arminjonianafromTrindadeIsland,whichwasdescribedasanewspecies (Aestrelata chionophara) by Murphy (1915). Later, Murphy recog-nized it to be a leucistic individual (Murphy and Pen-noyer 1952).This study presents, as long as we know,the first records of leucistic Black-browed Albatrosses,demonstrating that this phenomena also occurs in thisspecies.Furthermore,recordsofleucisticprocellariiformsinwinteringareasoftheSouthAtlanticOceanarescarceorabsent,andsothisstudycontributestoabetterknowl-edgeofplumageaberrationsinthisseabirdgroup.

ACKNOWLedgeMeNTS

We are most grateful to the fisherman and Projeto Albatrozpartner S. M.Terroso for pictures taken in Brazilian waters and toall the data provided, which encouraged us to prepare this paper.Wealso thank theobserver fromUruguay,F.Area, for thepicturesofaberrantplumageofthealbatross,Dr.M.AbreuforcheckingthespeciesidentificationandtoT.HardakerforallowingthepublicationofhisbeautifulpicturetakeninSouthAfricaandfurtherdataonthatindividual.ThanksalsotoV.Barquete,F.I.ColabuonoandF.Molinaforkindlyprovidingliterature,toJ.D.StevensforEnglishreviewandtoProgramaPetrobrasAmbiental,AlbatrossTaskForce/RoyalSocietyfortheProtectionofBirds,andFundaçãoOBoticáriodeProteçãoàNaturezaforfinancialsupport.

248 Recordsofleucisminalbatrossesandpetrels(Procellariiformes)intheSouthAtlanticOceanPatrícia L. Mancini; Sebastián Jiménez; Tatiana Neves and Leandro Bugoni

Revista Brasileira de Ornitologia, 18(3), 2010