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: [email protected] 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
ReFeReNCeS
Bensch, S.; Bengt, h.; hasselquist, d. and Nielsen, B. (2000).Partialalbinisminasemi-isolatedpopulationofGreatWarblers.Hereditas,133:167-170.
Bried, J. and Mougeot, F. (1994).Premier casdemélanisme chezunProcellariiforme:LePétrel-tempêteàCroupionGrisGarrodia nereis. Alauda,62:311-312.
Bried, J.; Fraga, h.; Calabuig-Miranda, P. and Neves, v. C. (2005).First two cases of melanism in Cory’s Shearwater Calonectris diomedea. Mar. Ornithol.,33:19-22.
Carlos, C. J. and voisin, J.-F. (2008). Identifying giant petrels,Macronectes giganteusandM. halli,inthefieldandinthehand.Seabird,21:1-15.
Fischer, h. i. (1972). Sympatry of Laysan and Black-footedAlbatrosses.Auk,89:381-402.
garrett, K. (1990). Leucistic Black-vented Shearwaters Puffinus opisthomelasinsouthernCalifornia.Western Birds,21:69-72.
gonçalves-Jr., C. C.; Silva, e. A.; Luca, A. C.; Pongiluppi, T. and Molina, F. B. (2008).RecordofaleucisticRufous-belliedThrushTurdus rufiventris Passeriformes, Turdidae in São Paulo city,SoutheasternBrazil.Rev. Bras. Ornitol.,16:72-75.
Lee, d. S. and grant, g. S. (1986).AnalbinoGreaterShearwater:featherabrasionandflightenergetics.Wilson Bull.,98:488-490.
Lepschi, B. J. (1990).The incidenceof albinismandmelanism inAustralianbirds:areviewoftheliterature.Corella,14:82-85.
Murphy, R. C. (1915). The bird life of Trinidad Islet. Auk,32:332-347.
Murphy, R. C. and Pennoyer, J. M. (1952). Larger petrels of thegenusPterodroma. Amer. Mus. Novit.,1580:1-43.
Nemésio, A. (1999).PlumagensaberrantesemPsittacidaeneotropicais–umarevisão.Melopsittacus,22:51-58.
Nemésio, A. (2001). Plumagens aberrantes em Emberezidaeneotropicais.Tangara,1:39-47.
Onley, d. and Scofield, P. (2007).Albatrosses, petrels and shearwaters of the World.London:ChristopherHelm.
Ristow, d. and Witte, L. (2004).PartialalbinisticcasesinadultandjuvenileCory’sShearwaters.Avocetta,28:31-32.
Sage, B. L. (1963).TheincidenceofalbinismandmelanisminBritishbirds.Brit. Birds,56:409-416.
Shaughnessy, P. d. (1970). The genetics of plumage phasedimorphismof theSouthernGiantPetrelMacronectes giganteus. Heredity,25:501-506.
Shaughnessy, P. d. (1971). Frequency of the white phase of theSouthern Giant Petrel, Macronectes giganteus. Aust. J. Zool.,19:77-83.
Thompson, d.; Murdoch, R. and Page, M. (2000).AnearalbinoCapePigeonDaption capenseoffKaikoura.Notornis,47:235-236.
Tickell, W. L. N. (2000).Albatrosses.Sussex,UK:PicaPress.van grouw, h. (2006). Not every white bird is an albino: sense
andnonsense about colour aberrations in birds.Dutch Birding,28:79-89.
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
