Onsilverwings:afragilestructuralmechanismincreasesplumage conspicuousness
IsmaelGalva´n,Juan J. Negro,GaryR.Bortolotti andAntoni Margalida
I. Galva´n (correspondence), Dept. of Evol.Ecol., Museo Nacionalde CienciasNaturales (CSIC), Jose´ Gutie´rrez Abascal2, E-28006Madrid,Spain,E-mail: — J.J.Negro,Dept.of Evol.Ecol.,Estacio´n Biol.deDon˜ana(CSIC),Avda. AmericoVespucios/n,E-41092Sevilla,Spain— G.R.Bortolotti,Dept.ofBiol., Univ.ofSaskatchewan, 112SciencePl,SaskatoonSKS7N
5E2,Canada—A. Margalida, BeardedVultureStud.andProt.Gr.,Apdo.43,E-25520ElPontdeSuert(Lleida),Spain—Presentaddressof
I.G.:Dept.ofEcol., Univ.deAlcala´,EdificiodeCiencias,Ctra.deBarcelonaKm.33,600,E-28871Alcala´deHenares,Spain.
Wereportforthefirsttimetheexistenceofastructuralmechanismoffeathersdifferentfromiridescencethatmakes plumageconspicuous.Byusingelectronandlightmicroscopy,weshowthatthemechanismconsistsofspeciallengthened andtwisteddistalbarbulesthatareverysusceptibletodamage.Thedorsalsideofthesebarbulesistranslucent,which createsadistinctivesheencolourationtofeathersthatotherwisewouldbe dark.Whendistalsheenbarbulesarebroken, theblackproximalbarbulesareexposed,thusgeneratingaconspicuousdifferencebetweenabraded andnon-abraded areas.Totalandultravioletreflectanceofsheen (non-abraded)areasarestrikinglyhigherthaninabradedareas.We proposethatthismechanismrepresents acaseofconvergentevolutioninspeciesthatarelimitedindevelopingcolourful plumagepatches.Futurestudiesshouldexplorethepotentialofthiscolourmechanismtoactasasignalofindividual qualityoridentity.
Highlyreflectivesilverystructures standout fromtheir surroundings, ascanbeseenfromthenighttimeshinefrom theeyesofcatsinthebeamofaflashlightandthebright silvergleamofbaitfishastheytwistandturntoavoida predator. The brightnessof a silvery,reflectivesurface allowsforbothextremeconspicuousnessandvisibilityfrom aconsiderabledistance.Whilewethusmight expectthisto beexploitedbyanimalsforcommunicationorsomeother function,examplesarerelativelyfew.Silverystructureshave beendescribedin theexoskeletonofsomeinvertebrates (e.g.,silverfishinsectsLepismasaccharina) andinthescaly integumentofsomevertebrates(fish;Parker2005).How- ever,therearefewexamples of silvery structuresin terrestrialvertebrates,withtheexceptionofthereflective eyesofanimalswithtapetumlucidum,atissuelayerinthe eyethatreflectsthelightbackthroughtheretina.Here wepropose thatcertainmodifiedandsheen coloured featherspresentinseveralaviantaxahavepropertiesthat are similarto reflectivesurfaces:when illuminatedby sunlight,perceivedbrightnessinthesefeathersisenhanced comparedtomoretypicalfeathers(Fig.1).Thisisanovel typeofstructuralcolourationthatappearstohavebeen overlookedeventhough the production mechanisms of structuralcolourin the integumentofbirdshavebeen extensivelyandintensivelyinvestigatedandreviewedinthe pastcentury(LucasandStettenheim1972,Fox1976),and manyrecentadvancesontheirphysicsandevolutionhave beenpublished(Prum2006).Sheenfeathersdifferfrom
those with iridescence,definedasthe phenomenon of glitteringofdifferentcoloursthatchangeaccordingtothe anglewithwhichtheobjectisseenorilluminated(Lucas andStettenheim1972,Prum2006).Iridescentstructural coloursareproducedbycoherentscatteringfromarraysof melaningranules (Prum2006).Thecolourofsheen feathersalsodiffersfrombrightwhite,whichisproduced bylargeairvacuolesinthebarbulesoffeathers,as described, forinstance,byDyck(1976)forthewinterplumageofthe rock ptarmiganLagopusmuta.
Our aim is to describethe structure and optical propertiesofsheenfeatherstostimulatefutureworkon
the ecologyand evolutionof this overlookedtype of plumagecolouration.Wefocusonthenoticeableexample
ofsheenstructureonthedorsalsurfaceofadultbearded
vultures Gypaetusbarbatus, a species whose plumage characteristicssome of us havethoroughlystudied, as thesebirds applycosmeticsoilstotheirfeathers(Negro
etal.1999,2002)andshowfine-tunedplumageadapta-
tions(Margalidaetal.2008).
Methods
Juvenile beardedvulturessportamattedarkbrown plumagesimilartothatofotherOldWorldvulturesand most other birds of prey (order Falconiformes).The numberofsheenfeathers increasesannuallywithmoult
Figure1.Examplesofbirdsshowingfeatherswithsheenstructures.(a)Adultbeardedvulture, (b)Immature(left),andadult(right) beardedvulturesinflight.Notethebrightappearanceoftheadultbirdcomparedwiththeimmatureevenonasnowy(i.e.dark)day, (c)Adult,whitemorphred-footedboobyinflight.Notehow thesheenstructuresofflightfeathersshinemuchmoreintheleftwing, whichisundersunnylight,thanin therightwing,whichisintheshadow.(d)AdultAndeancondorVulturgryphusshowing conspicuous whitishfeathersonthewing,(e)AdultEgyptianvultureNeophronpercnopterusshowingsheenstructuresonremigesthatgivethema whitishappearance.(f)AdultmarabouLeptoptiloscrumeniferus.Thewhitelinesonsecondarycoverts,whichacquirethatcolourbecause ofsheenstructures,whenfresharevisibleallalongthewing.
(seephotosinAdamsandLlopisDell2003),suchthat adultbeardedvultures oversixyearsoldhaveabright sheenappearanceontheupperparts(Fig.1a),fromheadto tail,andonremigesandrectricesparticularlywhenflying (Fig.1b).
Weusedlight(LM),andscanningelectronmicroscopes
(SEM)todescribethemorphological characteristicsofthe sheenfeathers.Wealsotookphotographsofthesestructures
withtheaimofillustrating themorphologicalcharacter-
isticsoffeathersthatgeneratethesheeneffect.Toobtain SEMimages oftheultrastructureoffeathers,wecut portions offeathers atdifferentpointsthat appearedto theunaidedeyeashavingdifferentlevelsofabrasion.The sampleswereanalysedwithaFEIQUANTA200SEM
operatinginlowvacuummodeand25kVandusinga
wavelengthdispersiveX-raydetector(WDS).Thesamples weremountedonstainless-steelpegs byusingdouble- sidedgraphitetapebeforebeingtransferredtotheSEM chamber.ThelightmicroscopewasanOlympusBX51with
amountedDP70cameraforimagecapture.
Tocharacterizetheopticalpropertiesofsheenfeathers, weusedan OceanOpticsUSB2000spectrophotometer
(range 250—800 nm) with ultraviolet (deuterium) and
visible(tungsten-halogen)lamps and a bifurcated400 micrometerfiber-optic probe(Dunedin,Florida).The fibre-opticprobeprovidedbothilluminationandobtained lightreflectedfromthesample,providingareadingarea ofc.1mm2.Themeasurementsweretakenata908angle to feathersamples.Allmeasurements wererelative to a white‘‘Spectralon’’ tablet(WS-1-SS,Dunedin, Florida). Measurementsweretakenatdifferentpointsoffeathers differinginthelevelofabrasion(seeFig.4),exceptfor
theabrasionexperiment (seebelow)forwhichthree measurementsweretakenat the samepoint, removing theprobeaftereachmeasure.Toconfirmthattheoptical propertiescanbeenvironmentallymodified,weexperi- mentallyremovedthesheenstructurein thedistalarea ofabeardedvulturefeatherbylightlyscrapingthesurface withthebladeofapairofscissors,andthenmeasuredthe reflectancespectrumatthesamepoint afterwards.Asa control,weperformedthesameexperimentalmanipula- tion on thedistalblackareaofaprimaryfeatherofa EuropeanmagpiePicapicaasthisspeciesdoesnotpresent sheenstructuresonitsfeathers.
Inadditiontotheresultsobtainedwiththemethods describedaboveforthebeardedvulture,wealsodescribe
thesheenstructureobservedinotherspecies suchasthe snowgooseAnser caerulescens and thered-footedbooby Sulasula,asthisstructurecan beeasilydetectedwithouta
microscopebecauseat closerangetheyhavea unique
‘dusty’or‘fuzzy’appearance thatisperceivedasgreyishor whitish.
Results
Structure ofsheenfeathers
ObservationsunderLMand SEM(Fig.3) ofsheenfeathers of bearded vulturesrevealedthat distal barbuleswere flattenedand twisted,in asimilarwayasdescribedin someiridescentfeathers(Lucasand Stettenheim1972, BrinkandvanderBerg2004),exceptthatdistalbarbules responsiblefor iridescencecontainedlargeamounts of
Figure2.Detailedviewsofsheenstructuresinfeathers.(a)Primaryfeatherofanadultbeardedvulture.(b)Flightandcovertfeathersof anadultbrownmorphred-footedbooby.Inthisspecies,variationintheregularityofthepatterngeneratedbysheenbarbulesamong feathersisduetowear,whichallowsonetoidentifyfeathersofdifferentages(indicatedbyarrows).
melaninwhereassheenbarbulesweretranslucent.Proximal barbules,however,wereflatand dark,astheycontain melaningranules.
Sheenfeathersofthebeardedvulturewerespeckledwith darkspotsinan apparentlyhaphazardfashion(Fig.2a).All individualsexamined(i.e.,15captiveand20free-ranging
individuals)showedthesespots,andatleastsomeofthe spotswerepresentin growingfeathers.The darkspots dottingsheenfeathersareplaceswheredistalbarbuleswere broken, revealingdark proximalbarbules of the barb
underneath.
The tip ofthedistalbarbule(i.e.thepennulum)insheen feathersis lengthenedwith respectto a ‘conventional’
barbule,sothatitswhitish dorsalsideisexposedalonga greaterdistancefrom the point at whichit istwisted (Fig.3; seeShawkeyet al.2005 for additionalexam-
plesshowing theultrastructureofconventionalfeathers). Sheenfeathersarealsodifferentcomparedtootherfeather typeswithlengthenedbutnottwistedbarbules(e.g.owls;
Bachmannetal.2007).Thislengtheningandtwistingof distalbarbulescausesthem tobreakat thepointwherethey twistbecausetheycannotgetcaughtonthebarbulesofthe adjacentbarbsfromthat point on, indicatingthat this
morphologyprobablyincreasesthelikelihoodoffeather abrasion(Figs.2and3a,b,Fitzpatrick1998).Asforthe darkfeatherspots,theirsizedependsonthenumberof
adjacentdistalbarbulesthatarebroken(Fig.3a).
Opticalpropertiesofsheenfeathers
Whenwemeasuredthereflectance ofabeardedvulture featheratapointwherenobrokenbarbuleswereobserved (i.e.thesheencolourwasuniform),theresultingreflectance spectrumshowedadefinedpeakintheultraviolet(UV) range,followedbyadecreaseandasubsequentincreasein reflectance atlongerwavelengths(Fig.4a).Thespectrum obtainedforthesampletakenatapoint wheresomebroken barbuleswere observedshowedasimilarshapebutaslightly lowerUVpeak. However,thespectrumforapointatthe darkestpartofthefeather,withahighernumber ofbroken barbules,alsoshowedalowerUVpeakbutwithconsider- ablyhigherand increasingreflectancevalues at longer wavelengths, similarto the typicalreflectancespectrum
offeatherswithmelanin-basedcolours (McGraw2006). Similarresults wereobtainedwhenabeardedvulture featherwasexperimentallyabraded(Fig.4c). The fact that differences in UVreflectancebetweenabradedand non-abradedparts of beardedvulturefeathersis more markedafteranexperimentalabrasionthaninanaturally abradedfeather,indicatesthatdifferences betweencurves obtained(fromabradedandnon-abradedpoints)couldbe observedonlyaftertheexperimentalabrasionoffeathers (Fig.4c).
Wear-induceddamagewasalsoevidentintheplumage
oftheotherspecieswithsheenfeathersthatwereexamined (Fig.2b).Indeed,differencesinshapeofspectrabetween abraded and non-abraded parts of featherswereeven moremarkedinthesnowgoosefeather(Fig.4b)thanin thebeardedvulturefeather(Fig.4a).Therefore,itappears
thatforsomespecies, physicalabrasionshavetobevery severe before UVreflectancechangeswiththedisappear- anceof the silverysheen,or, alternatively, the silvery sheen isassociatedwithbutnotfullycoupledtotheUV
reflectanceofthesefeathers.Incontrast,reflectancecurves forabradedandnon-abradedareasofaEuropeanmagpie featheroverlappedalongalargeproportionofthespectral range,and the total reflectanceafterthe experimental
abrasionhadtheoppositeeffectandevenincreasedafter manipulation(Fig.4d).
Speciesthathaveevolvedsheenfeathers
In additionto the speciesusedin thisstudy,wehave observedsheenstructures in severalother species.We confirmedthatthese structureswerethesameasthosein thecaseofthebeardedvulturebyusinglightmicroscopy. Inparticular,wehavenotedthepresenceofthistypeof colourationinpelicans(Pelecaniformes),ducksandgeese (Anseriformes),storksand ibises (Ciconiiformes),New Worldvultures,kites,harriers, Egyptianandbearded vultures (Falconiformes), cranes(Gruiformes)and sand- grouse(Pterocliformes;seeFig.1,videoclips1and2,and Fig.S1—S6insuppl.materials).Eventhoughweexamined numerousbirdsintheorderPasseriformes,wefailedtofind sheenfeathers.
Figure3.Ultrastructureoffeatherscontainingsheen barbules.(a)SEMmicrographofaprimaryfeatherofanadultbeardedvulturewith sheenbarbuleswithdifferentlevelsofwear.Distalbarbules(DBb),whichcovertheproximalbarbules(PBb)oftheadjacentbarbs(b), twistatthemiddleoftheirlength(Tp)followinganapparentlyregularpattern.Aftertwisting,DBbshowa translucentareathatcreates thesheencolourthatcontrastsagainstdarkPBb.NotethatDBbalwaysbreakattheTppoint,notatthepointofinsertioninthebarb, hencenotlosingtheircapacityofbindingadjacentbarbs.(b)SEMimageshowingthedetailofdistalbarbulesasin:(a)atTp.(c)SEM imageofanadultmagpieprimaryfeather.Thepicturewastakenat thejunctionofthe blackandwhiteareasofthe feather,butthereare nomorphologicaldifferencecausingthedifferenthuesasthereisinsheenfeathers.Inthistype of‘conventional’feather,barbulesare almostcompletelystraight.
Discussion
Structuralcharacteristics
Weconsidersheencolourationuniqueinbeingfragile,asit ishighlysusceptibletodamage.Asweshowed(Fig.4b), onecaneasilytakeabladeorabrasivemedium(evena fingernail)and removethe barbules to revealthe dark feather underneath. The loss of feather elementshas
sometimesbeenreportedasamechanismtocreateorna- mentsinbirds,suchastheimpressiveracketedtailofthe turquoise-browedmotmot Eumomota superciliosa,dueto theselectivelossofbarbsintherectrices(Murphy2007), and theblackbibofmalesparrows(e.g.,Boglianiand Brangi1990).
Insomespecieswherethedensityofbarbulesis high,the appearanceofsheencanbepurewhite,asintheflight
feathersoftheAndeancondorVulturgryphus(Fig.1dand
Figure4.Reflectancespectraobtained atanareawithoutbrokenbarbules(squares),atotallyabraded(i.e.black/brown)area(circles) andanareawithanintermediatedegreeofbrokenbarbules(triangles)inabeardedvulture(a)andasnowgoose(b)feather.Asimilar result(c)wasobtainedwhenabeardedvulturefeatherwasexperimentallyabraded(circles:reflectance spectrumfromanareaafter barbuleswere experimentallyabraded;squares:reflectancespectrumatthe sameareabeforebarbuleswere abraded).(d)Theresultofthe sameexperimentalabrasiononaEuropeanmagpiefeatherwithoutsheenstructure.Notehowreflectancecurvesforabraded(circles)and non-abraded(squares)areaslargelyoverlap,and,contrarytotheeffectin(b),thereflectancefortheabradedareaslightlyincreased comparedtothenon-abradedarea.
seevideoclip1insuppl.materials).Thiskindofwhite, however,canbeeasilydistinguishedfrom‘conventional’ whitelikethatdescribedbyDyck(1976),asthesefeathers haveamattewhiteanda‘dusty’ appearance. The particularlystrikingexampleoftheAndeancondorillus- trateshowthismechanismofspecialbarbulescangenerate brightnessinfeathersthatareinfactdark.Thissuggeststhat originallyblackfeathers,mayhaveevolvedassuchbecause ofselectivepressuresactingonmelanization(e.g.environ- mentalwearorneedforcrypsis;LucasandStettenheim
1972,Bortolotti2006,Margalidaetal.2008andreferences therein),andthen amechanismdevelopedtochangecolour byincreasingthe brightness and thus the generalcon- spicuousnessofindividuals.
Whendistalbarbuleswereintact,theUVpeakinthe reflectancespectrumoffeathersalsostoodoutagainstthe
remainingportionofthespectrum.Thistypeofspectral
shapeforsheen-whitefeathers,withaninitialdefinedpeak attheUVrangefollowedbyadecreaseandstabilizationin
reflectance values,hasalsobeenobserveedforthewhite plumage of other species with ‘conventional’ feathers
without the sheenstructure discussedhere (Penteriani etal.2006, McGlothlinetal.2007).Atthisstagewe
cannotdeterminewhethersheenfeathershavetheeffect ofincreasingoverall plumagebrightnessoronlyreflectance
at UV wavelengths, but it isnoticeablethat signalling mechanismstostandoutagainstdarkenvironmentsoften
involvethereflectanceofUVlight.Thishasbeenshown fornestlingskin,mouth and carotenoid-basedplumage
colour(Heebetal.2003,Huntetal.2003,Jourdie etal.
2004,Galva´netal.2008),andforthecolourofblue-green eggsincavitynestingbirds (Avile´setal.2006).Asimilar
signallingdeviceinvolvingthe production of startling
flashesofUVlighthasbeenrecentlydiscoveredinfish livinginhabitatswithlimitedenvironmentallight(Novales
Flamariqueetal.2007).Therefore,itislikelythatsheen feathersincreasetheconspicuousnessofbirdsbyincreasing
theirUVreflectance,asUVlightstronglycontrastsagainst certaindarkbackgrounds (seereferencesabove).Ofcourse,
thiswouldnotnecessarilyexcludethepossibilitythatsheen feathersincreaseconspicuousness byincreasing brightness
atallspectralregions.Furtherstudiesshouldsearchfor associationsbetweenprevalenceof sheen feathersand
detailedhabitatcharacteristics.
Possiblefunctionsofsheenstructures
Afirstpossibilityisthatthebreakagesusceptibilityofthe pennulumofsheenbarbulesmakethemasignallingdevice withoutlosingtheirmechanical functionofbinding adjacentbarbs,asthedarkbasesofthedistalbarbulesare not easilydestroyedby abrasion. Alternatively,inter- individualdifferences inthepatternofabrasionofthese barbules iscausedbybehaviouralattributesofbirdsand thussignals,forexample,dominancestatusifthatpatternis modifiedbyagonisticinteractionswithconspecifics.Lastly, it ispossiblethat sheenstructuresserveassignalsfor individualrecognition,iftheydonotconfersignificantand differentialcostswithrespecttoqualitytobearersandshow high(i.e.multimodal)variation(TibbettsandDale 2007). Futurestudiesshouldaddressthesepossibilities.
Giventheoccurrenceofsheenfeathersindifferentavian orders,the structurecreatingthis typeofplumagehas surprisinglybeenoverlooked.Selectionpressuresarestrong infeathertypesthatarecriticalforflightandforprotecting certainpartsofthebodyfromabrasion,andtheincreased resistancetowearmayfrequentlyhavebeenanimportant factorfavouringmelanizationofthistypeoffeather(Lucas andStettenheim1972,Bortolotti2006,McGraw2006, Schreiberetal.2006).Theplumagesofallspeciesinwhich wehaveobserved sheenfeatherstructures is mostly composedofblack,brown,grey andwhitecolours, suggestingalackofotherpigmentsresponsibleforbright colours,suchascarotenoids. Thus,sheenstructuresmay representanalternative,andperhapsinexpensive,wayto becomemorebrightlycoloured,or at leastto increase
‘achromatic conspicuousness’ byincreasingtotalplumage brightness,inthosespecies thatarelimitedingenerating
brightcoloursthroughthepresenceofotherpigments.
Acknowledgements—Theauthorscontributedequallytothispaper, sotheorderofauthorshipisnot meaningful.The authorsof thephotographsshowninfiguresareJ.J.N.(Fig.1d,Fig.S1, Fig.S2andFig.S5),G.R.B.(Fig.1b,c,f,Fig.2a,bandFig.S1), A.M. (Fig.1a),Jose´JuanHerna´ndez(Fig.1e)andFranc¸ois Mougeot(Fig.S6).WethankRichardO.Prum,BeaArroyoand Franc¸oisMougeotforcommentsonthemanuscript,andJudit Smitsforaccessto,andassistanceoperatinghermicroscope.An editorandtwoanonymousrefereesimprovedpreviousversions ofthemanuscript.FinancialsupportforI.G.wasobtainedfrom theprojectCGL2007-61251andaFPIgrantfromtheSpanish MinistryofScience and Innovation(formerlyMinistryof Education and Science).J. J. N. wassupported by project CGL2006-07481on themechanismsofcolourevolutionand funded by the SpanishMinistryof Scienceand Innovation. G.R.B.wassupportedbyagrantfromtheNaturalSciences andEngineeringResearchCouncilofCanada,andtheStuartand MaryHoustonProf.inOrnithology.A.M.wassupportedby MinisteriodeMedioAmbiente, MedioRuralyMarinoand Departament de Medi Ambient i Habitatge of Generalitat deCatalunya.
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Appendix