(Wyszecki andStiles,1982),horses (0.02–0.08 Philippe Perret and twilight(0.3–10 chicks orconspecificsintheirnests. exploit bothcolourandbrightnesscueswhenviewingtheireggs, Although thisneedsfurtherinvestigation,itispossiblethatbluetits nesters andtheevolutionarysignificanceofeggchickcoloration. light onthelivelydebatequestioningvisualperformanceofcavity exceed thatthreshold,atleastaftersunrise.Theseresultsshednew previously testedbirdspecies.Fortits,nestlightconditionsprobably © 2014.PublishedbyTheCompanyofBiologistsLtd|JournalExperimentalBiology(2014)217,3775-3778doi:10.1242/jeb.107573 Received 2May2014; Accepted31August2014 1 vision, andisknowninfourspecies:humans(~0.02 limit ofconefunctioningsetstheintensitythresholdcolour and bothatmidlightlevels(mesopicrange).Thelowerintensity vision inbrightlight,rodsforbrightnessdetectionverydimlight in KelberandRoth,2006).Mostvertebratesuseconesforcolour and isoftensacrificedforenhancedbrightnesssensitivity(reviewed colour visionislimitedbyphotoncaptureandsignal-to-noiseratio than achromaticvision,becauseofcolourconstancy. Indimlight, of spectralcompositionirrespectivebrightness–ismorestable days. Insucharangeofconditions,colourvision–discrimination Light intensityvarieswidelyfromdimstarlighttobrightsunny experiment, Eggcoloration,BirdCommunication KEY WORDS:Colourvision,Cavity-nestingbird,Conditioning ranging from0.05to0.2 colour cuestofoodrewardsinthreeindividuals,wefindathreshold , thebluetit( parrot species.Here,wefirstexplorethisthresholdinapasserine threshold ofcolourvisionisknownonlyforhumans,horsesandtwo performance indimlightislargelyunknown.Theintensity Many vertebratesusecolourvisionforvitalbehaviourbuttheirvisual Doris Gomez blue (Cyanistescaeruleus The intensitythresholdofcolourvisioninapasserinebird,the SHORT COMMUNICATION *Author ([email protected]) for correspondence 34090 Montpellier, France. 2008), twoparrotspecies(0.1–0.4 which fallbetweenlevelsequivalenttomoonlight(0.01–0.1 (mostlypasserines)showthatparentsadjusttheirbehaviour to al., 2010;Avilés etal.,2011). Manyexperimentsincavity-nesting the intensitylimitoflosscolourvisioninbirds(Holveck et communication.Forexample,thereisadebateconcerning light conditions,whichiscrucialknowledgeforunderstanding dawn, dusk).Nevertheless,littleisknownabouttheirvisionin such can beactiveindimlightenvironments(cavities,denseforestcover, INTRODUCTION ABSTRACT UMR 7179CNRSMNHN, 91800Brunoy, France. Many diurnalvertebratesrelyonvisionforvitalbehaviourand 1,2, Cyanistes caeruleus 2 *, ArnaudGrégoire

and ClaireDoutrelant cd m

cd − 2 ). m − 2 . Resultsarecomparabletothetwo cd ). Usingclassicconditioningof m − 2 2 ) (LindandKelber, 2009), UMR 5175,CNRSCEFE, 2 , MariaDelReyGranado cd 2 m − 2 ) (Rothetal.,

cd cd ) m m − − 2 2 ) ) levels outsidetheirnestshould bebetween0.5and20 and Maziarz,2012).Forbluetitstodetectcoloursintheirnest, light tits) arerecordedas1–10%ofthelightlevelsoutside(Weso nests ofmarshtitsandgreat(withsimilarnestinghabitsto blue evidence (CherryandGosler, 2010).Light levelswithinnatural birds, givenlightlimitationsandthelackofrobustexperimental to malesoffemalequalityisconsideredunlikelyforcavity-nesting suggesting thatitcouldevolvethroughsexualselectionasasignal been consideredtodriveeggshellcoloration,therecenthypothesis egg coloration,althoughcrypsisandbroodparasitismhave long the evolutionofeggorchickcoloration(Reynoldsetal.,2009). For debate concerningvisionperformanceofcavity-nestingbirds and comparable samplesizes.Ourresultsareinterestinginthecurrent Bourke’s parrotsandbudgerigars (LindandKelber, 2009),with caeruleus the intensitythresholdofcolourvisioninbluetit their colourvisionthresholdremainsunknown.Here,wedetermine regularly experiencedimlightconditions(e.g.Thomasetal.,2002), Roth, 2006). vision inmesopicconditionsremainspoorlyunderstood(Kelberand mesopic range.Whichphotoreceptorsmaycontributetocolour Avilés etal., 2011). However, nestlightconditionsmayfallinbirds’ conditions –predictnocolourdiscriminability(Holvecketal.,2010; Osorio, 1998)–usedfordimlightbutunvalidatedsuch (Wesoł argue thatnestlightconditionsmakecoloursunexploitable remains unknown(butseeAntonovetal.,2011). Someauthors Slagsvold, 2009).Whethertheyusecolourand/orachromaticcues 2006; Tanner andRichner, 2008;Dugas,2009;Wiebe and 2011; Avilés etal.,2011) or chicks(Jourdieetal.,2004;Bize Puente etal.,2007;SanzandGarcía-Navas,2009;Antonov colour-manipulated eggs(Morenoetal.,2006;Martínez-dela 0.05 We foundanintensitythresholdofcolourvisionrangingfrom exploit, whichwouldthusbepotentialtargets ofselection. help toidentifywhichvisualcuesareavailableforparents sensitivity invisualmodelling(Antonovetal.,2011). Ourstudywill considered asarepresentativespecieswithhighultraviolet 2010). Itisknownforitsvision(Hartetal.,2000)andoften faces dimlightconditions(Amrheinetal.,2008;Steinmeyer and theyareactive throughouttheday, visiting theirownnestand sunrise (A.G.,R.Guerreiroand M.-J.Holveck,unpublisheddata) daytime. Bluetitscanbeobserved aroundtheirnest1 individual) toexploitcolourand brightnesscuesattheirnest,during Hence, itwouldbepossiblefor bluetits(evenourworst-performing twilight correspondsto1–10 values ofaround0.4 RESULTS ANDDISCUSSION Although passerinesrepresent~60%ofavianspeciesand 2 cd , MarineBassoul owski andMaziarz,2012).Visual models(Vorobyev and m − Linnaeus 1758.Thiscavity-nestingpasserinefrequently 2 to 0.2 cd m cd − 2 m ntretse niiul Fg 1).Similar in threetestedindividuals(Fig. 2 − , DavidDegueldre 2 and 0.1

cd m − cd 2 (Kelber andRoth,2006). m − 2 have beenobtainedin 2 ,

cd m Cyanistes

h before − 2 ł . Civil owski 3775

The Journal of Experimental Biology (two-tailed binomialtest). from randomchoices,determiningtheintensitythresholdofcolourvision binomial test.Belowthe 3776 palustris, cavity nesterssuchas visual performance.Usingtheir dataandresults,wefoundthat larger thanexpectedeyesizestartsingingearlierandhave a greater onset, Thomasetal.(Thomasal.,2002)findthatpasserines with et al.,2008).Relatingeyesizetobodymassandtimeofsinging improve colourvisionmoreefficiently thanmonofocaloptics(Lind have multifocaloptics,whichcorrectforchromaticaberration and dim conditions. variation, isindispensabletodeterminewhetherbirdsusecolours in coloration irrespectiveofbrightness,withinnaturalranges of probably usedbrightness(Antonovetal.,2011). Manipulationof not determinewhichcueswereused,exceptinonecase,where birds Slagsvold, 2009;Antonovetal.,2011). However, thesestudiesdid Avilés etal.,2011) oroverabroadwavelengthrange(Wiebe and the UV range(Jourdieetal.,2004;Bize2006;Dugas,2009; showed achangeinparentalbehaviourmanipulatedreflectanceover altering eggorchickcolorationincavitiestitsandotherspecies, discriminated andusedtoadjustbehaviour. Experimentalstudies remains unknownwhetherrefinedcolourdifferences canbe in dimlight.Evenifcolourvisioncanbeusedatnestlightlevels,it the differences, themoredifficult theinformationcanbe exploited differences betweenthecardsusedinourexperiment.Thesubtler chicks, orbetweennests(orevenwithinnests)aresubtlerthan they candothis.Second,differences incolorationbetweeneggsor to performrapiddarkadaptation.Nodataareavailableonwhether colour vision,bluetitscouldexploitcuesonlyiftheyareable undergoing rapidchangesinlightintensities.Evenifcapableof nestlings (A.G.,R.G.andM.-J.H.,unpublisheddata),hence blue titsvisittheirnestfor10–90secondswhenfeeding adaptation andtheuseofcolourvisioninnaturalconditions.First, in eggsandchicks. 2010). Iftheydousecolourvision,couldselectforcues the nestsoftheirneighbourswheneggsarepresent(Holvecketal., dashed linerepresentstheobtainedfor triangle; Female2,circle;male1,square)atdecreasinglightintensities.The We testedthreedifferent individuals(Female1, from sunrisetomoonlight. Fig. SHORT COMMUNICATION caeruleus visual performance thanaverage[57passerines tested(Thomaset (1.8–2 forCyanistescaeruleus),whichsuggeststheyhaveagreater hypoleuca The bluetitislikelytohaveagoodvisualperformance.Blue tits Further studiesshouldquestiontwocrucialpoints:dark

1. Proportionofgoodchoicesmadebythebluetit(

Proportion of good choices (%) 100 ) inrelationtolightintensity. 40 50 60 70 80 90 have aneyesize1.3-to2-times larger thanexpected Passer domesticus, 10 Moonlight –2 P Light intensitylevel(logcdm =0.05 line,birdchoicesarenotstatisticallydifferent Cyanistes caeruleus 10 –1 ii wlgt Sunrise civil twilight End of Sturnus vulgarisor 10 Values areexpressedaslogcdm 0 P =0.05 obtainedinatwo-tailed , 10 major, 1 –2 ) Cyanistes 10 Ficedula 2 Parus − 2 light intensitylevels,rangingfrom13.25to0.04cdm feeders, andaluminancemeter(LMT 1009).We exploredfivedifferent (if placedvertically, measurementsyieldedsimilarvalues)justbelowthe performed luminancemeasurementsusingawhitepaperplacedhorizontally wall. Thelightlevelwascontrolledbyusingavariableresistor. We bird movementswithaninfraredcamera(SonyHDR-SR7E)intheopposite inawall,1 deep feeders(18×12×7cm) light:dark photoperiodtoensuretheyhadenoughtimeeat.We placedtwo regularly spacedwhiteLEDs,NichiaNSPL515DS)timedona14h:10h andcontrolleddiffuse ceilinglighting(30 walls (H×L×W: 2×2×1m), We placedbirdsindividuallyina light-safetestingroom,withblack-painted CEFE permitB34-172-11). complying withFrenchregulations(researchprogrampermit201267-003; food Kelber, 2009)].Thewild-caughtbirdswerekeptinoutdooraviarieswith 2008); threeintheBourke’s parrotandsixinthebudgerigar(Lind investigating lightthresholdforcolourvision[threeinthehorse(Rothetal., and one6-month-oldmale,asamplesizesimilartopreviousstudies old) We testedcolourvisioninthree blue tits:twoadultfemales(>1year involved inintraspecificcommunicationdimlightconditions. opens newresearchpathstoexperimentallytestwhethercolouris It addsimportantinformationtothecurrentdebateofbirdvisionand tits toexploitcolourandbrightnesscues,atleastduringthedaytime. nesters deservesfurtherinvestigation. al., 2002)].Whetherthisvisualperformanceisspecifictocavity returned toits aviary beforerelease.Female1 enteredthefeeders and wedidnottestthebirdat nextlowestlightlevel.Thebirdwas considered thatthebirddidnotuse colourvisionatthetestedlightlevel, test showedthatchoicewasnot different fromarandom choice, we tested itatthenextlowestlightlevel. Otherwise,ifthetwo-tailedbinomial tailed binomialtest),weconsidered itwasstillabletodetectcoloursandwe than 64.8%correctchoices(35 choicesoutof54, consecutive setsof18presentations (54tests).Whenthebirdmademore After atleast30minutesofacclimatization,wepresentedthebirdwith three to testing,atdecreasingluminancelevels,startingfromthehighest level. corresponding toP choices intwoconsecutivesetsof18cardpairs(77%correctchoices, and usedcolourstochoosethefeeder, whenitmadeatleast14/18correct by usingsetsof18cardpairs.We consideredabirdwasefficiently trained and Kelber, 2009).We firsttrainedthebirdsathighestluminancelevel We followedtheconditioningprotocolestablishedbyLindandKelber(Lind disturbance tothebird. associated withthebluecardfromoutsideroom,minimal outside. Afterachoice,wechangedthepositionofcardsand grid metallic gridjustabovethemealworms,whichwerethusnotviewablefrom food, bluecardassociatedwithfoodmadeinaccessiblebythepresenceofa were associatedwithacolourcard:greencardaccessible for parrots(LindandKelber, 2009).Bothfeederscontainedmealwormsand following thesameprotocolandlearningcriteriaasLindKelberused training ittodiscriminatebluefromgreen,greenbeingtherewardingcolour, access toapple,muesli,mealwormsandseedsonthecagefloor. hperday–ithad from thefeeders.Otherwise–whichrepresentedatleast2 had accessonlytomealwormsinfeedersincreaseitsmotivationfeed could notviewthemfromoutside.Duringconditioningandtesting,thebird perches, andmealwormsplacedinthefeeders,deepenoughsothatbird 2). relevant dimlightconditionsexperiencedbywildbluetits(Fig. 0.11, 0.04),equivalenttolatedaymoonlight,whichareecologically Testing room MATERIALS ANDMETHODS Conditioning andtestingprotocol As soonasabirdstartedtofeedroutinelyfromfeeders,we At alltimes,thebirdcouldaccessawatersupply, anestboxandvarious In summary, ourstudystrongly suggeststhatitispossibleforblue ad libitum The JournalofExperimentalBiology(2014)doi:10.1242/jeb.107573 (mealworms, freshapples,seedsandcake),inconditions =0.05 inatwo-tailedbinomialtest).We thenproceeded

m belowtheceiling,andmonitored − 2 (13.25, 0.60,0.29, P <0.05 inatwo-

The Journal of Experimental Biology Rods Double cones SHORT COMMUNICATION present thequantumcatchvalues(QC) inarbitraryunitsforthesystemresponsiblebrightnessdetection. Finally, contrast(∆ thecolour respectively.example, fordc1,weusedtheproportions: red=0,green=0.8andblue=1forthebluecard;RGBvalueswere therefore0,87and109, We also andmethods.For was 0forthebluecolours,B-channel was0forthegreencolours.TheRGBvaluesfollowedproportions givenintheMaterials We builteightpairsfordoubleconesandfiverods.For eachpair, areshown.TheR-channel RGBvaluesforthechannels thathadnon-nullvalues learning. respectively, toenterthefeedersbutimmediatelyshowedeffective 10days, showing effective learning.Bycontrast,Female2andMale1took22 immediately afterbeingputinthetestroombuttook309testsbefore noise asthe inthesystem. of apair, computedasin Vorobyev andOsorio’s model(Vorobyevwas computed, usingneural andOsorio,1998)initslogformulation(Osorioet al.,2004) Table C B A

5107 6 8 4. 6 65.58 63.69 61.5 58.93 55.11 164 149 133 117 53.71 102 53.23 52.71 52.08 309 50.97 145.6 294 49.66 132.8 278 48.23 120 261 46.06 106.4 245 93.6 229 213 198 108 182 102 166 96 150 133 89 165 117 83 149 77 134 71 118 65 180 102 170 160 149 310 139 72 294 129 66 278 119 60 262 109 54 246 48 230 214 181 152 120 144 110 136 100 128 90 120 80 112 104 87 190 r5 180 r4 170 r3 160 r2 150 r1 140 130 dc8 109 dc7 dc6 dc5 dc4 dc3 dc2 dc1 Reflectance (%) 100 20 40 60 80

1. Visual stimulibuiltforvisiontestinginthebluetit( 0 400 MWS 450 -au nRBGvlei G CGvlei G -au nRBQC R-valueinRGB G-valueinRGB QC G-valueinRGB B-value inRGB Blue card 500 Wavelength (nm) SWS 550 600 LWS 650 Cyanistes caeruleus 700

and 0 0.2 0.4 0.6 0.8 1 presentations wasorganised intwoconsecutiveseriesofninecard a blueandgreencardfromthesamepair(seeFig. We built13pairsofblueandgreencards.Eachtrialconsistedinpresenting Visual stimuli Visual Relative emission Green card (cross symbols)androds(circleareshown. other receptors.Blueandgreenpairsmatchedfordoublecones calculations) becauseitsresponsewasverylowrelativetothatofthe ultraviolet-sensitive conewasignoredontheplot(butnotin hence theyarenotcorrectedforanyadaptivebackground.The computed asinVorobyev andOsorio(Vorobyev andOsorio,1998); wavelength-sensitive (LWS) receptors. Quantumcatchesare sensitive (SWS),middle-wavelength-sensitive(MWS),andlong- normalised tothesumofallquantumcatches)forshort-wavelength- space oftherelativequantumcatches(acatchis (plain blackline).(C)Chromaticitydiagramrepresentingthereceptor Relative emissionspectrumofthewhiteLEDsusedinexperiment green lines)andr3matchedforrods(dashedbluelines). brightness detection,dc4matchedfordoublecones(plainblueand (B) Exampleofreflectancespectrafortwocardpairsmatched (A) Exampleofblueandgreencardsapair(dc4,seeTable 1). Fig. )

.Cardpairsusedforvisionconditionandtesting. 2. The JournalofExperimentalBiology(2014)doi:10.1242/jeb.107573

2A). Eachsetof18card S ) betweenthecards ∆ S 3777

The Journal of Experimental Biology 3778 A.G., C.D.andD.G.developedtheconceptofexperimentwrotearticle. All authorscontributedtocollectionofdataandelaborationexperimentaldesign; The authorsdeclarenocompetingfinancialinterests. measurements andtherefereesfortheircomments. Holveck forpit-tagdata,F. Viénot andF. Génietforhelpwithluminance We thankP. Auryfortechnicalhelp,R.Guerreirobehavioral data,M.-J. presentations. Cardsconsistedofchequeredpatterns(5×5 SHORT COMMUNICATION presented absolutelynobiasincardpresentation. of ninecardpairs.Thisensuredthateachset18pairpresentations series ofninecardpairs,andsideswerealternatedforthefollowing which toplacethegreencard.Thissidewasrandomlychosenforfirst pairs. We alsochosewhichreplicatetotakeforeachpairandthesideon randomly chosethesequenceofpairswithineachseriesninecard Each cardpairwastestedtwice,onceineachseriesofninepairs.We then series ofninecardpairs),werandomlychosethepairstobetested. in thechromaticspaceFig. an exampleofthereflectancespectrainFig. differed intheirpatterns.DatausedforcardsarepresentedTable patterns weregeneratedatrandomforeachcard,allcardswithinapair 25 squaresofdifferent brightnessvaluesaroundtheaveragecomputed.As purpose-built program.Eachcardpresentedaninternalcontrastof0.3and average brightnessvaluestogeneratethechequeredpatternsbyusinga and blue=1)forblue(red=0.8,green=1,blue=0)green.We usedthe For cardsadjustedforrodvision,weusedtheproportions(red=0,green=0.6 green=0.8 andblue=1)forblue(red=0.6,green=1,blue=0)green. were closestinslopetocreatethemaximalnumberofpossiblepairs. the regressionlineforeachcolour, andretainedthebluegreencoloursthat filtering (Govardovskiietal.,2000;HartandVorobyev, 2005).We established Hart andVorobyev, 2005)andtemplatesforphotoreceptorsoildroplet absorbance, oildropletfiltering,ocularmediatransmission(Hartetal.,2000; and doubleconequantumcatchesusingphysiologicaldataonspectrum Avantes spectrometerandadeuteriumhalogenlightsource.We computedrod obtained byagivenRGBproportion.We measuredtheirreflectanceusingan responsible forbrightnessdetection.We firstgeneratedasetofcolours,each a colourpatchand Author contributions Competing interests Acknowledgements where (from 1to5forlevelsfrom13.250.04). level decreased,wetestedanincreasingnumberofcardsadjustedforrods adjusted eightpairsofcardsfordoublecones,andfiverods.Asthelight vision, wehadtoadjustbrightnessforbothtypesofphotoreceptors.We targeted themesopicrangewhereconesand/orrodsmaycontributeto light, androdsinnocturnalconditions(Hartetal.,2000).Becausewe (Table quantum catchforthephotoreceptorresponsiblebrightnessdetection card wouldyieldthesamebrightnessimpressionforabluetit,i.e. each pair, wecomputedtheaveragevaluessothatgreenandblue patterns toavoidbirdsusingbrightnesscuesdiscriminatefeeders.For 1).We usedchequered range ofbrightnessvaluesfortheseaverages(Table of different brightnessvaluesaroundanaveragevalue.We exploredalarge For eachsetof18cardpairpresentations(organised intwoconsecutive For cardsadjustedfordoubleconevision,weusedtheproportions(red=0, We computedquantumcatches

I 1). Inthebluetit,brightnessisdetectedbydoubleconesinbright is theirradiancespectrumofwhiteLEDs, S is theabsorbancespectrumofphotoreceptor QIRS =

∫ 2C. )()() () λλλδλ Q as:

2B andthelocationofallpairs ,(1) R is thereflectanceof

cm) of25squares

1, with hry .I n olr A.G. P.Gosler, and Heeb, M.I. Cherry, and B. Moureau, R., Piault, P., Bize, N. Hart, and J. Soler, J., A., Moksnes, Avilés, J.R., Vikan, V., Spasova, B.G., Stokke, J.M., Aviles, A., Antonov, at .S n ooyv M. Vorobyev, and N.S. Hart, (2011) program. 09-JCJC-0050-01]; andtheLanguedoc-RoussillonregionPromisingResearchers This workreceivedfundingfromtheNationalAgencyforResearch[grantnumber enls .J,Mri,G .adCse,P. H.M. Cassey, and Buchanan-Smith, G.R. Martin, and S.J., Reynolds, M. Vorobyev, A.C., Smith, D., Osorio, Moreno, Lobato, J., Morales, G., Tomás, J., Moreno, S., Merino, J., Martínez-de laPuente, id .E,Kle,A n rgr R.H. Kröger, and A. Kelber, O.E., Lind, A. Kelber, and O. Lind, L.S.V. Roth, and A. Kelber, A.T. D. Bennett, and I.C. Cuthill, J.C., Partridge, N.S., Hart, K. Donner, and D.G. Kuzmin, T., Reuter, N., Fyhrquist, V. I., Govardovskii, M.B. Dugas, ori,V,Mueu . ent,A .D n eb P. Heeb, and A.T. D. Bennett, B., Moureau, Grégoire, V., and Jourdie, D. Gomez, P., Perret, R., Guerreiro, C., Doutrelant, M.-J., Holveck, T. Slagsvold, and L. Kristiansen, L.E., Johannessen, V., Amrhein, References Funding oh .S . aknu,A n ebr A. Kelber, and A. Balkenius, L.S.V., Roth, az .J n acaNvs V. García-Navas, and J. Sanz, timyr . cileh . ule,J .adKmear,B. Kempenaers, and J.C. Mueller, H., Schielzeth, C., Steinmeyer, anr .adRcnr H. Richner, and M. Tanner, Wesoł ooyv .adOoi,D. Osorio, and M. Vorobyev, Frayling, S.E., Newson, D.G.C., Harper, I.C., Cuthill, T., Székely, R.J., Thomas, ib,K .adSasod T. Slagsvold, and K.L. Wiebe, yzci .adSie,W. S. Stiles, and G. Wyszecki, Nat. Detection offruitandtheselectionprimatevisualpigmentsforcolorvision. think. J.Exp.Biol. reflectance bytheskinofnestlings. merula species ofpasserinebird:thebluetit( pigments, oildroplets,ocularmediaandconephotoreceptordistributionintwo spectral sensitivitiesofbirdconephotoreceptors. In searchofthevisualpigmenttemplate. adaptive explanations. 2063-2068. condition mediatescontext-dependentparentalfavouritism. Behav. Ecol.Sociobiol. physiological modelsandeggdiscriminationexperimentsinacavity-nestingbird. E. Roskaft, and W. nesting passerineunderdimlightconditions. Liang, C.C., Yang, Ecol. Sociobiol. Reproductive strategyandsingingactivity:bluetitgreatcompared. functional significanceofeggshellcolorationhypotheses? 560. flycatcher (2006). Morecolourfuleggsinduceahigherrelativepaternalinvestmentinthepied 377-384. J. Martínez, and indicators ofhealthandconditioninbluetits S. García-Fraile, E., pupil dynamicsinbirds. of parrot.J.Exp.Biol. nestlings withmouthcoloursthatappearcarotenoid-rich. visits andmodellingofeggvisualdiscriminationinbluetits. A. vision inthehorse. breeding performanceofbluetits age andenvironment. in sleepbehaviourfree-livingbluetits, offspring communicationinthegreattit( nesting birds? thresholds. Proc. R.Soc.B P. D. Wallis, and T. D. Quantitative DataandFormulae detection orsignallingquality? (2010). Caneggsinacavitybefemalesecondarysexualsignal?Malenest wk,T n air,M. Maziarz, and T. owski, 164 . oae,J,Lbt,E,Mrn,S,Tms .adl une J.M.D. laPuente, and G. Tomas, S., Merino, E., Lobato, J., Morales, J., L.). J.Comp.Physiol.A , 696-708. Ficedula hypoleuca Proc. Biol.Sci. (2009). Housesparrow, Passerdomesticus,parentspreferentiallyfeed The JournalofExperimentalBiology(2014)doi:10.1242/jeb.107573 J. Avian Biol. 62, 1633-1641. 269 209 PLoS ONE , 831-837. 212 , 781-788. Anim. Behav. (2009). Theintensitythresholdofcolourvisionintwospecies Biol. J.Linn.Soc.Lond. 65, 1721-1730. J. Exp.Biol. (2002). Eyesizeinbirdsandthetimingofsongatdawn. , 3693-3699. 265 (2006). Nocturnalcolourvision–notasrarewemight 43, 454-460. (2008). Ultravioletreflectanceofplumageforparent- (2010). Avian eggshellcoloration:newperspectiveson : across-fosteringexperiment. (2005). Modellingoildropletabsorptionspectraand , 351-358. Anim. Behav. (1998). Receptornoiseasadeterminantofcolour 3 (2009). Mouthcolorationinnestlingbirds:increasing 186 . NewYork, NY: Wiley-Blackwell. , e3711. (2009). Eggshellpigmentationpatterninrelationto Cyanistes caeruleus (2012). Darktreecavities–achallengeforhole (1982). (2011). Sexualselectionbasedoneggcolour: , 375-387. Nature 80, 853-864. 211, 2752-2758. Parus caeruleus Parus major (2007). Areeggshellspottinessandcolour Vis. Neurosci. Color Science,ConceptsandMethods, 431 (2008). Theabsolutethresholdofcolour 78, 1413-1420. (2011). Eggdiscriminationinanopen Ethology Cyanistes caeruleus (2008). Multifocalopticalsystemsand (2009). Issexualselectionblurringthe Cyanistes caeruleus , 262-262. 100 J. Comp.Physiol.A (2006). A UVsignalofoffspring , 753-762. ). Behav. Ecol. . J.Anim.Ecol. 117 17, 509-528. L.) andtheblackbird( Anim. Behav. (2004). Ecology:ultraviolet Anim. Behav. , 1128-1137. Biol. Lett. J. Avian Biol. Proc. Biol.Sci. ? : effects ofsex, 19, 369-373. J. Avian Biol. (2010). Variation 6 78, 31-41. 191 (2000). Visual , 453-457. 78, 767-772. 78, 209-215. , 381-392. 37, 555- (2004). (2000). (2008). Behav. Turdus 273 Am. 38, ,

The Journal of Experimental Biology