Application of a Predictive Model to Detect Long-Term Changes in Nest-Site Selection In

Applicationofapredictivemodeltodetectlong-term changesinnest-siteselectioninthe BeardedVulture Gypaetusbarbatus:conservationinrelation to territoryshrinkage

ANTONIMARGALIDA,1*JOSÉANTONIODONÁZAR,2 JAVIERBUSTAMANTE,2

FRANCISCOJOSÉHERNÁNDEZ3 MARILÓROMERO-PUJANTE4

1BeardedVultureStudyandProtectionGroup,Apdo.43,ElPontdeSuert,E-25520Lleida,Spain

2Departmentof Applied Biology, Estación Biológica de Doñana, C.S.I.C., Avda MaLuisa s/n, E-41013 Sevilla, Spain

3C/LaVega,24.Salteras.E-41909,Sevilla,Spain

4Egmasa,JohanGutenberg,s/n,IsladelaCartuja.E-41092,Sevilla,Spain

In thisstudyweexaminedlong-termvariationintheselectionofnestingcliffsfor therecovering populationoftheBeardedVultureGypaetusbarbatusinhabiting theSpanishPyrenees.We focussedonvariablesindicating ahighprobabilityofcliffoccupancy asdeterminedbya previously publishedmodel.Althoughthebreeding populationincreased from53to93 territoriesbetween1991and2002,thebreedingrangeexpandedonlyslightly.Newandold nestingcliffshadsimilarhabitat features inrelation totopography,altitudeanddegreeof human influence, but the distance betweenoccupied cliffswasreduced (from 11.1 to

8.9km).Thustheprobabilitiesofoccupationpredictedbythemodelwerelowerfornewly colonized locales.Our studyshowsthat territorycompressionmayoccurwithoutserious modificationofnestinghabitat quality.Theseresults mayarisefromthe lackofstrong territorialbehaviourbyBeardedVulturesandthe availability ofhigh-qualitycliffs.The relativelylowqualityofsitesinadjacentmountainsmaypreventtheexpansionofthebreeding range,butconspecificattractionmayalsoplayarole.Our studyconfirmsthat monitoring changesinkeyvariablesimportanttohabitat selection isusefulindetermininglong-term trendsinsettlement patterns inheterogeneousenvironments.Theresultsalsosuggestthat theavailablenest-site selection model mayaccurately predict cliffoccupancy byBearded Vulturesinthoseareaswherethedistancetothenearestneighbourisnotalimitingfactor. Inparticular,themodelmaybeusefulinestablishing priority areasforreintroduction.

Keywords:cliffs,conspecificattraction,despotic competition,habitat quality,Pyrenees.

Explanatoryandpredictivemodelsarepowerful tools inthe study ofspatial distributionsofpopulations andtheiruseis growingexponentiallyinanimal ecology(Guisan Zimmermann2000, Guisan etal.

2002,Rushton etal.2004).Modelsestablishstatistical relationships betweenaresponse andexplanatory variablesthatusuallyquantifyenvironmentalcharacter- isticssuchasclimate,landscape features, anddegree ofhumaninfluence(e.g.BustamanteSeoane2004, GuisanThuiller 2005,Gavashelishvili McGrady

2006). This procedureisincreasingly employedin

*Correspondingauthor.

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wildlifeconservation, mainlytodeterminethe probabilityoffuture siteoccupationforexpanding populations(Mladenoff etal.1995, Buckland etal.

1996, Jerina etal.2003, Hirzel etal.2004) and to examinehabitatsuitabilityfor releasedpopulations within reintroductionprograms(Bustamante1998). Theaccuracyofpredictive modelsis strongly dependentonpopulationequilibrium,biotic inter- actionsandstochastic localevents.Although such complexity frequentlylimitsthegeneralityofthe results (Guisan Zimmermann2000, Guisan etal.

2002),anincreasingnumberofstudiestakethisinto account (e.g.FieldingHaworth1995,Lindenmayer et al.1995, Rodriguez Andrén 1999). Predictive

modelsarenowapotentially valuabletooltodetect long-term trendsinthosekeyvariablescapableof explaining thedistributionoforganisms.

Hereweusea previouslypublished predictive model todeterminelong-termchanges innest-site selectioninanendangeredpopulationoftheBearded Vulture,Gypaetus barbatus.This species isalarge scavenger living in rugged areas where it feeds mainlyon boneremainsfromwildanddomestic ungulates (Margalida etal.2007a).It builds large nests in shelteredcaves and ledges of cliffs (see Hiraldo etal.1979 forreview ofgeneral biology). TheBeardedVulturelived formerlyinallthemountain regionsofthe OldWorld fromsouthernEurope to the Middle Eastandcentral Asia,but atpresent its distributionhasbeenmuch reduced,mainlydueto human persecution (Margalida etal. 2008). In Europe, byfarthe largest populationoccupies the Pyrenean rangebetweenFranceandSpain(Heredia

2005). BecausetheBeardedVulture is considered endangeredinEurope (Annex I, EUWildBirds Directive 79/409/EEC,Appendix IIoftheBern Convention, BonnConventionandCITES) with fewerthan130breeding territories intheEuropean Unionin2005,reintroduction projects havebeen carried out,forexample inAndalucía (Simón etal.

2005)andtheAlps(Terrasse2004),or arein preparation(e.g.Sardinia,theBalkans).

Nestinghabitat selectionbyBeardedVultureswas studied in1991intheSpanishPyreneesbyassessing physiography,landuse,climate, human disturbance and intraspecific density (Donázar etal. 1993). Cliffshavingahighprobabilityofoccupancy were those situatedinruggedareas(i.e.ahighdegreeof topographicirregularity),atanaveragealtitude,far fromvillages andfarfromthenearestconspecific territory(seebelowfordetails).Between 1990 and

2000theBeardedVulturepopulationoftheSpanish Pyrenees grewannually atarate of5%(Heredia& Margalida2002).Thisincreasingtrend isunusual as populationsofthisspeciesaredecreasing overmost oftheir distribution(Del Hoyo etal.1994). How- ever,theareainwhichthePyreneanbirdsarefound hasnotincreased atthesamerate:lessthan 10%of theirformerbreedingrangehasexpandedduringthe lasttwodecades(Heredia2005).

Inthispaper,wehavetheadvantage oftheabove mentioned1991predictivemodeltoassesswhether nest-site selection patternsofthe Bearded Vulture havechangedinparallelwithpopulationgrowth.The resultsmaycontributetothelong-termmanagement ofthe most importantEuropeanpopulationofthis

endangeredspeciesand,moreover, mayhelpto determinethe validityofnest-site selection models as atoolforfuture conservationactions,especially thoseinvolvingreintroductionprograms.

METHODS

Populationtrendsandcliff characterization

Thebasicinformationonthedistributionofterritories and nests ofBearded Vulturesinthe Pyrenees has beenobtained fromtwosources:unpublished databases compiled by R. Heredia from 1977 to

1991(seeDonázaretal.1993) andmonitoringpro- gramsestablishedby regionalgovernments(Navarra, Aragón andCatalunya)from 1991 tothe present. Inallthe regions,the monitoringhasbeen ableto detect theoccupation ofnewterritories thanksto repeatedvisitstolocations with atleast minimum requirements fortheestablishment ofnewpairs (Margalida etal.2003c).Each year, breeding sites known from previous studies, named oldcliffs,and newsiteslocated after1991,named newcliffs, were visitedatleastonceaweekbetweenthemonths of NovemberandAugust.Tolocatethenests,observa- tionsbeganinSeptembercoincidingwiththestartof nestbuilding(MargalidaBertran2000) andended during fledging(June–August).During eachvisit,a pair’s breeding behaviour and whetherthe birds were building nests, incubating,orrearing achick wasrecorded.Thesamplingeffortforthetwoperiods (i.e.1977–91and1991–2002) wassimilar.

Statistical procedures

Comparisonsweredoneonthebasisoffourgroups ofsampling locations (bandccorrespondtothose usedbyDonázar etal.1993,seeTable1):

(a) New(n=36):cliffswithnestsoccupied between

1991and2002.Ifaterritoryhadmorethanonenest, weonlyconsideredtheoneusedthefirsttime.

(b) Old (n=111): allcliffswith nestsoccupied at

leastoncebetween1977and1991.

(c) Random (n=111): unoccupiedcliffsfrom the existingrange,selectedbypseudo-randomgeneration ofco-ordinatesandchoosingthenearest point ona cliffwithout anest.

(d) Peripheral(n=40):cliffswithoutBeardedVulture

nestsselectedatrandomintheformerrangeofthespecies andlocatedin zonesmorethan20kmfromthenearest pair.ThesecliffswereintheEasternPyreneesandthe

Table 1.VariablesusedtocharacterizeBeardedVulturenestingcliffsandrandomcliffs.Inrandomcliffs,distancesweremeasuredfrom a point in the centre of the cliff (modified from Donázaret al.1993).

Topography

RELIEF:Topographicirregularityindex.Totalnumberof20-mcontourlines,cutbyfour1-kmlinesstartingfromthenestindirections

N, S, E and W.

Cliff local characteristics

ALTITUDE: Altitude of the nest above the sea level (m).

CLIFF: Cliff height, measured as the number of 20-m contour cut by a 50-m line perpendicular to the cliff face at nest level. ORIENTATION:Orientationoftheclifffaceatthelevelofthenest.Orientationswerescoredinincreasingshelterfromcoldhumidwinds

from the NW, which are dominant in the area: 1=NW, 2 =N or W, 3 =NE or SW, 4=E or S, 5 =SE.

Environmental characteristics of the surrounding area

FOREST: Extent (%) of forested areas in a 1-km radius around the nest. DISTANCE VILLAGE: Distance to the nearest inhabited village (km). INHABITANTS: Number of inhabitants in the nearest village.

Human disturbance

KILOMETRES ROADS: Kilometres of paved and unpaved roads in a 1-km radius of the nest. DISTANCE PAVED ROAD: Shortest linear distance between the nest and the closest paved road (km). DISTANCE ROAD: Shortest linear distance between the nest and the closest road, paved or unpaved (km).

HEIGHTPAVEDROAD:Altitudinaldifferencebetweenthenestandtheclosestpavedroad,measuredatthepointtheroadiscloserto the nest (m). If the nest is lower than the road, a negative value is obtained.

HEIGHTROAD:Altitudinaldifference(m)betweenthenestandtheclosestroad(pavedorunpaved).Ifthenestislowerthantheroad, a negative value was obtained.

Intraspecific relationships

NEAREST NEIGHBOUR: Linear distance between the nest and the closest nest of the nearest neighbour (km).

Table 2.Descriptivestatistics(mean±sd)andsignificanceofthedifferencesinmeanvaluesbetweensomegroupsobtainedwiththe Mann–Whitneytestofthevariablescharacterizingthenewbreedingcliffs(n =36)occupiedbytheBeardedVultureintheSpanish Pyreneesbetween1991and2002,oldcliffsoccupiedbefore1991(n =111),randomlyselectedcliffs(n =111)andcliffsinperipheral mountains (n =40).

CliffsP (Mann–WhitneyU-test)

Variable

RELIEF77.0 (19.9)83 (18.0)67.8 (15.4)58.8 (13.0)ns0.0030.010

ALTITUDE1424.2 (358.9)1333 (361.2)1316.56 (516.0)1078.7 (955.3)nsns< 0.0001

*Calculated on a sample sizen =19 as consequence of limited data available.

BasqueMountains. They arehabitually visitedby immatureandadultbirdsduringtheirdispersalstage (R.Heredia,D.Campión,A.Margalida,unpubl.data).

We firstused Wilcoxon Mann–Whitneytests to checkif therewerestatisticaldifferencesinenviron-

mental variablescomparing peripheral torandom cliffs.Next,wecomparedthedifferencesinenviron- mental variablesbetweennewandoldnestingcliffs, and between new and random cliffs (Table2). Finally, we compared average probability of cliff

occupancy predictedby the model between old, new and random cliffs.We used generalized linear models(GLMs)to analyzethebinaryresponse variables‘cliff occupation’,assumingabinomial distributionoferrorsandusingalogitlinkfunction (seeDonázaretal.1993).Thefinalmodel included fourvariables:relief,distancetothenearestoccupied nest(log-transformed),altitudeanddistance tothe nearest village(log-transformed):linearpredictor=

–33.9+(0.091*relief)+(1.644*log distance to the neighbour territory)+(0.099*altitude)–(4.024*10–6

*altitude2)+(0.945*log distance to the nearest village). Theresultwasthatin1991theBearded Vultureselected thoseareaswiththemostirregular topographyasnestingcliffs,farfromother breeding pairs,atanaveragealtitude,andawayfromhuman habitation.

Thepredictive abilityofamodeltendstobe optimisticallybiasedwhen evaluated withthesame datausedtobuildit.Becauseofthat,andbecauseof thefactthatoldnestingcliffsandrandom cliffs,rather than newnestingcliffs,havebeenusedtobuildthe model, the probabilityofoccupancy predicted by our model onnew cliffscannot becomparedwith other cliffs. Toavoidthe bias,weestimatedthe probabilityofa cliff beingoccupied byBearded Vulturesbycross-validation.Wedividedeachsample (old, new and random cliffs)into fivegroups with

20%of theobservationsineach.Thefirst groupof observations ineach sample wasused asatest and the remaining fourgroups ofoldcliffsandrandom cliffs(80%oforiginalmodel data) were usedtofit new model parameters.This model was used to predict the probabilityof occupationin the test group ofobservations (20% ofdata). Each ofthe groups ofobservations was droppedin turn from modelconstructionandusedastestdata.Thedataset wasreordered 20timesandthewholeprocedure repeated,sothe probabilityofcliffoccupancy was estimated20timesby 20differentpredictivemodels based on observations before 1991 that did not contain that particular observation.We estimated themean predictedprobability foreachcliffand comparedsamples (old, new and random)with theWilcoxon Mann–Whitney test.Thepredictors included in all models were the same used in the model ofDonázaretal.(1993);we only esti- mated newparametersineachcase. Thewhole procedurewasrepeated,fitting amodel without distancetothenearestneighbour toestimate the effectofthisvariableontheprobability ofcliff occupancy.

RESULTS

TheBeardedVulturepopulation oftheSpanish Pyreneesgrewfrom53territoriesoccupied in1991 to93in2002.Despitethisincrease,thedistribution area changed only slightly during this period: two newterritorieswerelocatedupto40kmwestwards. The restofthe new territorieswere found within theformerbreedingarea, mostlywithinthecentral nucleus ofthemountainrange.Thecliffslocated in peripheralzones,withoutBeardedVultureterritories, showedseveral significantdifferencesfromthose existinginoccupied breeding areas(Table2).They tended tobesmaller(meanheight) andwereusually located inlesssteepandloweraltitude zones.In addition,theywerenearer,indistance andaltitude, toroadsandtheyhadagreaterneighbouringhuman population.

Thenewterritoriesoccupied from1991 to2002 showedsimilarhabitat characteristics tothose occupied before1991(Table2).Theonlyexception wasthevariable‘nearestneighbour’.Newterritories were situatedat asignificantly shorter distance to other occupied territoriesthan they were before (mean:8.9kmvs11.1km).Inrelation torandomly selectedcliffs,newnestsiteswereinareasthatwere morerugged,andincliffs thatwerehigherthan average.Inaddition, newnestingcliffswerenot significantlyfurtherfromthe nearest occupied nest (mean: 8.9km) than were random cliffs (mean:

8.1 km;Table2).These results aresimilar when comparing oldnestswithrandom cliffs(Table2).

The applicationofmodels including the variable

‘nearestneighbour’determinedthatnewlyoccupied cliffshad intermediateprobabilityvalues between oldnestingcliffsandrandom cliffs(Fig.1);thetwo comparisons gavesignificantdifferences(newvsold Z=2.89, P=0.0038; new vs random Z=−3.16, P=0.0016). Previously occupied cliffs had, as expected, ahigher probabilityofoccupancy than random cliffs(Z=8.537, P0.0001).When prob- abilitieswerecalculated onthebasis ofthemodel without‘nearest neighbour’ (Fig.1),new cliffsdid not differ significantly from old cliffs (Z=1.11, P=0.267),but both oldcliffsand new cliffshad significantlyhigheroccupancy probabilities than random cliffs(respectively,Z=−3.592, P=0.0003, Z=6.949, P0.0001).Therefore,during the last decade Bearded Vultures have been selecting a similarkindofcliffaspreviously chosen inrelation totopographyanddistance fromhuman habitation, themainfactorsaffectingcliffselection.Thedistance

Figure 1.Meanprobability(± 95%confidenceintervalsforthe mean)ofacliffbeingusedbyBeardedVulturesfornestinginthe SpanishPyreneesestimated,withmodifications,onthebasisof theGLMmodelfittedbyDonázaret al.(1993).Probabilitiesare shownfornewcliffs(triangle)occupiedafter1991(n =36),old cliffs(square)occupiedbefore1991(n =111)andrandomly selectedcliffs(circle)(n =111).(A)Originalmodel,(B)without the variable‘nearest neighbour’.

betweenneighbouring territoriesdecreased in parallelwiththeincreaseinpopulationdensity(from

4.4 to 2.5 territories/1000km2 between1991 and

2002).

DISCUSSION

Our resultsshowthat theselection ofnestsiteshas notchanged withthepopulation increaseofthe Pyrenean BeardedVulture. Forthose variables determiningtheprobability of cliffoccupancy (ruggedness,altitude anddistance tonearest human habitation),newly establishedterritoriesbetween

1991and2002hadsimilarvaluestothoseoftraditional territories occupied previously.Thesenewpairs, however, occupied cliffsamongtheexistingold territoriessothat the distance betweenneighbours hasreduced byaround 20%,which provesterritory shrinkage (Both Visser2000, Ridleyetal.2004). Inaddition,cliffsremaining unoccupiedbyBearded Vulturesafter1991intheperipheryofthePyrenees hadbothlowervaluesinkey variables(e.g.relief, altitude,distancetovillage)andlowerprobabilityof occupancy than those occupied in the Pyrenean rangeduringthesameperiod.

Thesefindingsseemtocontradictwhat wouldbe expectedfromadistributionbydespotic competition, classically described forbirdsofpreyandother territorialbirds(e.g.FerrerDonázar1996,Newton

1998).Itcouldbearguedthatthereisstillavailability ofgood-qualitybreeding sitesinthe Pyrenees and

that, consequently,the populationhasnot reached thesaturation threshold necessarytoobservethe occupationofmarginalterritoriesby newlyestablished birds.Thisholdstrueifthecomparisonislimited to theexaminationofthequalityofnestingcliffswhere nolong-term changeswereevident.Adifferent picture,however, ariseswhen distance between neighbouringterritories isconsidered.Asthisvariable was significantinthemodelfittedin1991,wecan deduce that saturationistakingplaceandthat there isadecreaseinterritorialqualityviareductioninthe distance betweenbreeding pairs.Inparallel, ithas beendemonstratedthat theproductivity ofthe Pyreneanpopulationhassharplydeclinedduringthe lastdecadeasaconsequenceoftheincreasingbreeding density (Carreteetal.2006a),aclear symptomof populationcrowding,asistheappearanceofunusual mating systems (Carreteetal.2006b).Today, the densityattainedbyBeardedVulturesintheSpanish Pyrenees (226 km2/oneterritory)isthe highest recorded forthespeciesinitsEuropeanbreeding range. Equivalentfiguresare 333km2/territory for the French Pyrenees, 240km2/territoryforCorsica and2065km2/territoryforCrete (Xirouchakis & Nikolakakis2002,Terrasse2004).Tothesenumbers (93pairsin2002),a non-breedingpopulationof around 200 individuals should be added to the SpanishPyrenean population(Heredia2005).

WhydoBeardedVultures tolerateshrinkageof territories?Interritorialbirdsofprey,anincreasein the density ofbreeders usually results inahigher levelofagonisticencounters; largeterritoriesare vigorously defendedagainst conspecifics (Newton

1979, 1998, Ridleyetal.2004). Territorial defence intheBeardedVultureappears,however, tobe restrictedtotheareassurroundingthenest(lessthan

500mradiusaccordingtothemajorityof authors; Hiraldo etal.1979,Brown1988,BertranMargalida

2002,MargalidaBertran2005).Outsidetheselimits, there is habitual tolerancebetweenneighbouring pairs.Tolerance towards conspecificsmaybeevolu- tionarilyfavouredas aconsequenceofthelarge distancesbetweenterritories,whichwouldnotfavour selection for aggressiveness against intruders (see alsoMargalidaetal.2003b).Infact,thestrategyfor findingunpredictable foodmakesitnecessaryto forageoverextensiveareasthatoverlapneighbouring pairs(Brown 1988). Humanmanipulation ofthe availability ofresources (e.g.feeding stations) may alsobeadeterminingfactorexplainingthis‘packing’ of thepopulation.Duringthe1990s,nearly30feeding stations were establishedinthe Spanish Pyrenees.

There, more than 50000kgofbones per yearare left for the Vultures(Regional Governments, unpubl.data). Consequently,it could be that this increaseinthe availabilityofresources hasresulted inthereductionofterritorialbehaviourandfacilitated thecompressionofterritories.Monitoringoffeeding stations reveals a predominant use by immature birds(70%;Heredia 1991), but itisnotpossibleto disregardthefact thatthesefeedingstationsare importantfactorsforadult birdsatspecifictimesof thebreedingcycle. Feedingstationscanstrengthen conspecific attraction,reducing the probabilitythat new breeding birds willoccupy territoriesinareas distant tothecentral zoneofthemountain range (Serrano Tella2003).

Finally,thepackingprocesscouldbealsomotivated bythescarcityofsuitablebreedingsitesinmountain areassurrounding thePyrenees.Asouranalyses demonstrate,potentialnestingcliffsinthoseregions areoflowerquality(intermsofaltitude,topography andhuman influence) thanthoseexistingwithinthe mainmountainrange.Humanpresence isknown to affectstrongly the distributionpatternsofBearded Vulturesandother largeraptors,notonlyinrelation to the safetyofbreeding nest sites(Donázaretal.

2002,Margalidaetal.2007b),butalsoinrelation to foraginggrounds (Bautista etal.2004, Gavashelishvili

McGrady 2006).Previous analyses have shown thatthebreedingsuccessof PyreneanBearded Vulturesis affectedbyhuman activitiesandinfra- structures (Donázar etal. 1993, Arroyo Razin

2006). Therefore,itisreasonable tothink that the lowprobabilityofcliffoccupancyoutsidethePyrenees is determined, at least partially, by the intense human influence ontheseperipheral mountain regions.Inthissense,thePyreneescouldprogressively becomemoreofanecologicalislandfortheBearded Vulturesurroundedbyareasthatareinadequatedue totheincreasinglyintensehumaninfluenceon the environment.Consequently,theriskofextinctionin thispopulationwillremainhighasaconsequenceof stochasticdemographicandenvironmentalphenomena andofthescarcegeneticvariability(Godoyetal.2004).

Theconservation effortsforthepopulationof PyreneanBeardedVultures shouldfacilitatethe geographicexpansion of thespeciestowardsother mountainous zonesoftheIberianPeninsula.Two complementaryactions,thecreationofnewpopulations throughreintroductionplans,andthepromotionof thedispersion ofnon-breeding individualsusing changesintheavailabilityoffood,couldfavourthe maintenanceofametapopulationstructurepermitting

genetic exchange and,fundamentally, determining unequal probability of extinction for different sub-populations.Todeterminethesuitability ofthe areasofreintroduction,where constraintslinkedto territorialitydonotexist,amodelsuchas that determinedin1991,withoutthedistancetonearest neighbourvariable, seems particularlyrelevant. In fact,theaforementioned modelhasbeenusedto predict nesting probabilityinareaswhere the Bearded Vultureisbeingreintroduced,such asthe AlpsandAndalucía (e.g.Bustamante 1996). Ina broader sense,ourstudyshowsthat the probability ofpresencedeterminedbypredictivemodelsmaybe sensitivetosocialbehaviour,inthiscaseflexibilityin territoriality.Thisshowsthenecessityformodelling procedurestotakeinto account variablesquantify- ingintraspecific relationships betweenindividuals (Alexanderetal.2006).

The basic information about the recent distribution (1991–2002) oftheBeardedVulturecomesfromdatabases generatedbytheMinistryof Environment,Organizationof LandandHousing oftheAutonomousRegionofNavarra, theDepartmentofEnvironmentof theGeneralCouncilof AragonandtheDepartmentofEnvironmentandHabitat of the Autonomous Government of Catalonia. Our thankstoall thepeoplewhohavedirectlyorindirectly participatedindifferent phases ofthiswork:I.Afonso, I.Anton,R.Antor,M. Arilla,J.Bertran,J.Bolado,A.Bonada, D.Campión,J.Canut,D.García,D.Gómez,R.Heredia, J. Jové,J. Martín,J.M.MirandaandA.Senosiain.B.E.Arroyo, G.R.Bortolotti,M.Carrete,F.Hiraldo,A.López-Sepulcre andtwoanonymous reviewerscontributedsuggestions which improvedthemanuscript.Thisworkwasfinanced bytheMinistryofEnvironment oftheAutonomous GovernmentofAndalusía, within the Project‘Studiesof viabilityforthe reintroductionofthe BeardedVulturein Andalusía’.Support wasalsoobtainedfromtheBBVA Foundation throughitsawardforscientificresearch in ConservationBiology(2004).

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Received23January2007;revisionaccepted 6September2007.