RaptorNestDecorationsArea
ReliableThreatAgainstConspecifics
F.Sergio,1*†J.Blas,1†G.Blanco,2A.Tanferna,1L.López,1J.A.Lemus,1F.Hiraldo1
Individualqualityisoftensignaledbyphenotypicflags,suchasbrightplumagepatchesinbirds. Extendedphenotypesignalscansimilarlyshowquality,butinthesecasesthesignalsareexternal totheindividual,oftentakingtheformofobjectsscavengedfromtheenvironment.Through multiplemanipulativeexperiments,weshowedthatobjectsusedfornestdecorationbyaterritorial
abilities(5)andbesubjecttoculturaltransmis- sion(6).Further,our abilityto addressquestions aboutsuchsignalsarefacilitatedbythefactsthat (i)theyareoftenflexibleandlessconstrained thanbodilytraits(4)and(ii)theirconstituent materialsmaybereadilyavailableforexperi- mentalmanipulation(7,8).Despitethebroader appeal,extendedphenotypesignalshavebeen examined inonlyahandfulofpasserinebird andfishspecies,andthesewerealmostexclu- sivelystructuresbuiltsolelyformateattraction
raptor,theblackkite(Milvusmigrans),actasreliablethreatstoconspecifics,revealingthe
viability,territoryquality,andconflict dominanceofthesignaler.Ourresultssuggestthatanimal- builtstructuresmayserveassignalingdevicesmuchmorefrequentlythancurrentlyrecognized.
1DepartmentofConservation Biology,EstaciónBiológicade Doñana,ConsejoSuperiordeInvestigacionesCientíficas(CSIC), C/ AmericoVespucio,41092Seville,Spain.2DepartmentofEvo-
lutionary Ecology,MuseumofNaturalSciences,CSIC,C/José
nimalstransferinformationthroughana- tomical,physical,andbehavioral traits, suchasbrightlycoloredbodypatches,
extravagantornaments,or size-revealingcalls
A
(1–3).Somespeciesgotofurtherextentsbycol- lectingobjectstobuildexternal signalingstruc- turesor“extendedphenotype signals”(4).Such externalsignalsmayinvolvehighercognitive
B
GutiérrezAbascal2, 28006Madrid,Spain.
*To whomcorrespondence shouldbeaddressed. E-mail:
†Theseauthorscontributedequallytothiswork.
Fig.1.Decorationofnestsbyblackkites (Milvusmigrans).(A)Highlydecoratednestand(B) selectionofmaterialsbykitesrelativetotheiravailabilityintheenvironment.Kitesshowapreference forwhite(c2=270.0, P0.0001)plastic(c2=57.0,P0.0001),whereasallothermaterialsand colorsareusedatratesequalto(othermaterialsc2=0.1,P=0.76)orlessthan(paperc2=68.1,P
0.0001;crypticcolorsc2=77.2,P 0.0001;othercolors c2=148.3,P 0.0001)theiravailability inthe environment. [Photocredit:F.Sergio]
andcourtship,suchasthebowersofbower- birds(5–8).However,severalhundredsofspe- cieserectneststructuresinmannersthatcould becompatiblewithextendedphenotypesig- nalingfunctions.Examplesincludetheaddi- tionofman-madeobjects,stones,greenplants, snakeskins,dung,orcarnivorescats bypasser- ines,storks,swans,penguins,corvids,raptors, andfishandthebuildingofmultiplealternative nestsbywrens,weavers,andraptors(4,9–14). Therefore,althoughanimalsarethoughttobuild structuresforcommunicationonlyrarely(12), nestscouldbesignalingdevicesmorefrequently thancurrentlyrecognized.
Wecombinedexperimentalmanipulationsand long-term observations ofalong-livedraptorto showthatnestdecorationcanactasanhonest threattoconspecifics,revealing theviability, ter- ritoryquality, andconflictdominanceofthesig- naler.Ourmodelspecies, theblackkite(Milvus migrans),isamedium-sizedmigratoryraptor.Pairs occupybreedingterritoriesthatmayvarymarkedly inresourcequality(15).Floatingindividualsare preventedfrombreedingthroughsocialdominance but mayattemptviolentterritorytakeovers,which sometimessucceed(16)(fig.S1).Trespassingcan befrequent,especiallyinpre-incubation, andis alsoaimedatstealingfoodresourcesobtainedby
theresidents.Onreturnfrommigrationafterpair formation,bothpartnerscontributeto nestbuild- ing.Oneto2weeksbeforelaying,theymayboth placevariousman-madematerialsinthenest, typically whiteplastic objects(Fig.1A).The objectsseemplacedsoastobehighlyvisibleand arecollectedduringthepeakperiodofterritory trespassing andlongafterpairformation. Thus,we hypothesizedthattheyserveasanextendedphe- notypesignalofthreatagainstintruders(tableS1).
Weusedawell-studied(15, 16)(fig.S2) population ofmarked,known-age(1to25years old)kitesinDoñanaNationalPark.Toinvestigate thesignalingfunctionofnestdecorations(17),we(i) assesseddecoration levelsat127nestsbuiltby individualsofknownageandbodysize,which weresubsequentlyintensivelymonitoredtoesti- matetheirviability(here definedbysubsequent survivalandoffspringproduction);(ii)compared nestdecorations withobjectsavailableinthe environment;(iii)offeredobjectstomarkedindi- vidualstoexamine theirpropensitytousedecora- tions;(iv) estimatedtrespassrates and aggression ofintrudersfor bothnonexperimentalandexper- imental pairs(i.e.,thosewhosenestdecorations hadbeenaugmented); (v)testedwhethernest decorationspredictedtheefficiencyofresource monopolizationmediatedbyaggressionwithin a
Fig.2.Changeinmean(T1SE)nest decoration byblackkites(blackline) withage(n=127).Placementoffreely availableitems(gray)washighestfor birdsinprimeage(7to12yearsold) andlowestforyoungandoldindivid- uals(n=49).
competitivefeedingenvironment awayfromthe nest;and (vi)examinedtheeggpredationratesof experimentaldummykitenestswithand without decorations. Throughthisseriesofexperiments, wespecificallytestedforthe presenceofan hon- estextendedsignalbyaddressingfour hypothe- ses,asproposedbySearcyandNowicki(3):(i)is thesignalreliable;(ii)doreceiversrespondtothe signal inawaythatbenefitssignalers;(iii)isthe signalcostly,andisthecosthigherforlower- qualityindividuals; and(iv)istheredeceit(17) (tableS1)?
Nestdecorations wereobservedin77%ofthe nests(n=127),appearedinthelast20days beforelaying,anddeclinedslightlyduringthe incubationperiodandmarkedlythereafter (fig. S3).Bothsexeswereequallylikely tocarry decorations (males15times,females12;bino- mialtest,P=0.70).Whencomparedtoavail- abilityintransects (Fig.1B),kitesoverselected
plasticmaterials(c2 =57.0,P0.0001)and whitecolor(asassessed byhumanvision;c2 =
270.0,P0.0001).Allothermaterialsandcolors
wereavoidedorusedaccordingtoavailability (Fig.1B).Whenbirdswereofferedasetofex- perimentalobjectsinequalavailability(17),29 of33pairsthatcollected objectsplacedonly whiteplasticitemsintheirnest,twocollected bothwhiteandtransparentitems,andanother twocollectedboth whiteandgreenitems.White
was overselected(c2 =100.7,P0.0001),and theothercolorswereavoided(greenandtrans-
parentc2=24.5,P0.0001).
Isthesignalreliable (hypothesisi)?Nestde- corationincreasedwithterritory quality andbody condition andexhibited aquadratic (parabolic) relationshipwithage(tableS2andFigs.2and3): Thelevelofdecorationincreaseduptoages10to
12anddeclinedthereafter withsenescence(Figs.2
and3).Similarly,37% ofthe pairsrefrainedfrom collecting anyoffereditemdespiteitsprolonged availability. Theseanimalshadlower-qualityter- ritories anddifferedinagefromindividualsthat usedtheoffereditems(tableS3):Individualsthat refrainedfromsignalingwerevery youngorvery old,whereasthosethatusedthedecorationsto signalwerepredominantlyinprimeage(7to12
Fig.3.Changeinlevelofnestdecorationinblackkites.Levelofdecorationwas(A)lowestfor youngbirds,(B)increaseduptoages10to12yearsold,and
(C)declined thereafterwithsenescence.[Photocredit:F.Sergio]
yearsold;Fig.2).Therateandsuccessofattackson trespassersincreasedwithdecoration levels(table S4).Similarly,infeedingobservations,thepercent oftime anindividualspenteating anditssuccess rateinfood-relatedaggressiveinteractionswere relatedtoitsnestdecorationlevel(tableS5).
Doreceivers respondtothesignalanddothey respondinawaythatbenefits signalers(hypothesis ii)?Inpairswithoutexperimentalnestaugmen- tation, territoryintrusionrateswerelowerforhighly decorated nests(tableS4),consistentwiththe hypothesisthattrespassers avoiddecoratednests. However,intruderpressureactuallyincreasedwhen weexperimentally augmentedthedecorations (tableS6).Thissuggeststhatnonterritorialanimals or“floaters”maybestimulatedtoattackpairsthat suddenlyadvertiseahigh-qualityterritory.
Higherlevelsofnestdecoration predicted highersubsequentbreedingsuccessandsurvival (tableS7andFig.4),suggestingthatbirdsmay benefitfromlowerratesofriskyfightsassociated withhigher-qualityadvertisement.
Isthesignalcostly,and isthecosthigherfor
lowerqualityindividuals (hypothesisiii)?Preda- tionratesofexperimentaleggs werehigherfor decorateddummynests(81.3%predated,n=
16)thanfornondecorateddummynests(31.3%,
n=16,c2=8.54,P=0.003), indicatingthatthere
Fig.4.Nestdecorationby blackkitesincreasedwith theviabilityofthesignaler, asestimated bybreeding performance(numberoffledg- lingsproduced,blackcircles, n=127) andsurvivaluntil spring (whitesquares,n=76). DataaremeanT1SE.
Fig.5.Experimentalaugmentation ofnestdecoration.Mean (T1SE) attackratesofblackkitesontres- passerswerehigherinprimeage (7to12yearsold;blackcircles,n=25) individualsandlowerinyoungor old(≤6or≥13yearsold;white squares,n=40)animals.
isacosttoadvertising qualitythroughnest decoration.Similarly,trespassingratesincreased forallindividualsintheaugmentationexperi- ment,butonlythoseinprimeagemanaged to increasetheirattackrateinresponse(tableS6and Fig.5). Veryyoungor senescentindividualsap- pearedincapabletocounteract thecostofsig- naling(Fig.5);thus,itappearsthiscostishigher forlower-qualityindividuals.
Istheredeceit(hypothesisiv)?Intheequal
availabilityexperiment,lower-qualityindividuals almostsystematicallyrefrainedfromsignaling (Fig.2).Oneweekaftertheaugmentation ex- periment,85%oftheindividuals inprimeage hadretained theplasticweplacedintheirnest, whereas 87%intheotherageclasseshad removedit.Ageanditsquadraticeffectwere theonlypredictors ofthelikelihoodthatapair wouldretainorexpeltheexperimentalplastic (tableS8).Deceit,ifpresent,seemsrare.
Ourresultsshowthatnestdecorationisa
graduatedsignalthatconveyscomplexinforma- tiononterritoryquality,individualviability,and dominanceinsocialinteractions. Wefoundno supportforalternativehypotheses(tablesS1and S9).Reliabilityofthesignal wasreinforcedbe- causelower-qualityindividualsrefrainedfrom dishonestsignaling,eventhoughsuchcheating
wouldhavebeenpossible.Theoreticalstudies predictsignalingabstentionbylower-qualityin- dividualsinthepresenceofagonisticretaliatory costsimposedbyreceivers(18).Suchsocialcosts wereevidentinthisstudy:Advertisementofhigh- qualityresourceswasmetwithaggressive chal- lenges.Thecostsofsuchchallengescouldbe disproportionatelyhighforcheatingindividuals, becauseadvertisinghigh-qualityresources may attractstrongcontestants(19)thatareableto displacedishonest signalersthroughaggres- sive,andphysically damaging, conflicts(16) (fig.S1).Consistentwith suchdisproportional costs,onlyindividualsinprimeagewereable torespondtotheincreaseinchallenges stimu- latedbyexperimentalnestaugmentation.Lower- qualityindividualswerenotabletomatchtheir defenserates tothecheatingdecorationlevels thatweimposed.Socialpunishmenthasbeen recurrently shownasamajortheoreticaldeter- minantofcommunicationhonesty,especiallyfor signalsinvolvingminimumproductioncosts [e.g.,(20,21),reviewin(2)],suchasmany extendedphenotypesignals.Thismayexplain whysocialpunishmentandcheatingabsten- tionseemcommoninsuchcommunication sys- tems[e.g.,(7,22–26)].
Extended phenotype signalscanbereliable indicatorsofbothindividualandterritoryqual- ity.Previousanalyseshave shownthatlevelsof externalsignalsmayincreasefromjuvenileto adultageclasses[e.g.,(23,27)]orbeindivid- uallyrepeatablethroughtime[e.g.,(28,29)]. Ourfindings confirmsuchearlier studiesand expandthembyshowingaclearsenescentde- clineinsignalingstrength. Thisreinforcestheidea ofindividuals signaling theirphysicalprowess, whichincreasesandthendeclines withage.Fur- ther,our findingsindicatethatexternalsignalscan beusedinthecontextofresourcedefenseanddo notsolelysignalreproductivequalityinasexual selectioncontext,althoughreinforcementofpair bonding mayhavecontributedtoourresults(10). Inlinewith theseideas,many characteristicstyp- icaloftheobjectsusedtocreateextended phe- notypesignalingstructuresmakethemoptimalas signalsofterritorialdefense:highvisibility,ef- fectiveness intheabsenceofthesignaler,en- codingofsocial dominanceandmotivation,ease ofdeconstruction, andreliabilityenforcedby punishmentofcheaters[reviews in(1–4)].
ReferencesandNotes
1.J.W.Bradbury, S.L.Vehrencamp, PrinciplesofAnimal
Communication(Sinauer,Sunderland,MA,1998).
2.J.MaynardSmith, D.Harper, AnimalSignals
(OxfordUniv.Press,Oxford,2003).
3.W.A.Searcy, S.Nowicki,TheEvolutionofAnimal
Communication(Princeton Univ.Press,Princeton, NJ,2005).
4.F.C.Schaedelin, M.Taborsky,Biol.Rev.Camb.Philos.Soc.
84,293(2009).
5.J.R.Madden, Proc.Biol.Sci. 268,833(2001).
6.J.R.Madden, Anim.Cogn.11,1(2008).
7.J.R.Madden, Proc.Biol.Sci. 269,1347(2002).
8.S.W.Coleman, G.L.Patricelli, G.Borgia, Nature428,
742(2004).
9.P.H.Wimberger, Auk101,615(1984).
10.J.Moreno, M.Soler, A.P.Møller,M.Linden,Anim.Behav.
47,1297(1994).
11.M.Hansell, BirdNestsandConstructionBehaviour
(CambridgeUniv.Press,Cambridge,2000).
12.M.Hansell, AnimalArchitecture(OxfordUniv.Press, Oxford,2005).
13.D.J.Levey,R.S.Duncan,C.F.Levins,Nature431,39(2004).
14.J.G.Schuetz, Behav.Ecol.16,133(2005).
15.F.Sergio etal., Oecologia160,507(2009).
16.F.Sergio, J.Blas,F.Hiraldo, J. Anim. Ecol.78,109(2009).
17.Materialsandmethodsareavailableassupporting materialonScienceOnline.
18.E.S.Adams,M.Mesterton-Gibbons, J.Theor.Biol. 175,
405(1995).
19.A.Berglund, A.Bisazza,A.Pilastro, Biol.J.Linn.Soc.58,
385(1996).
20.R.A.Johnstone, K.Norris,Behav.Ecol.Sociobiol.32,
127(1993).
21.M.Enquist, S.Ghirlanda,P.L.Hurd, Anim.Behav.56,
749(1998).
22.J.Diamond, Proc.Natl.Acad.Sci.U.S.A.83,3042(1986).
23.G.Borgia, Am.Nat.141,729(1993).
24.S.Östlund-Nilsson, M. Holmlund,Behav.Ecol.Sociobiol.
53,214(2003).
25.J.M.Wojcieszek, J.A.Nicholls, A.W.Goldizen, Behav.
Ecol.18,689(2007).
26.N.R.Doerr, Anim.Behav.79,747(2010).
27.E.C.Collias, N.E.Collias, Auk81,42(1964).
28.B.J.Rushbrook, N.J.Dingemanse,I.Barber,Anim.Behav.
75,547(2008).
29.P.T.Walsh, M.Hansell, W.D.Borello,S.D.Healy,
Biol.Lett.6,149(2010).
30.WethankF.J.Chicano, J.Giralt, andF.G.Vilchesfor helpinthefield.S.N.Vignieriandthreeanonymous reviewersgreatlyimprovedapreviousdraftofthe manuscript. Thestudywasfundedbytheresearch projectsCGL2008-01781, JA-58,RNM1790,andRNM
03822grantedbytheJuntadeAndalucía,Ministeriode
CienciaeInnovación,andNaturalResearchLimited.
SupportingOnlineMaterial
MaterialsandMethods
Figs.S1toS3
TablesS1toS9
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1b
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