protected areas under pressure: decline, redistribution ...giacomo tavecchia2, fernando hiraldo1...
TRANSCRIPT
ENDANGERED SPECIES RESEARCHEndang Species Res
Vol 38 189ndash204 2019httpsdoiorg103354esr00946
Published April 25
1 INTRODUCTION
Protected areas represent one of the pillars of theglobal conservation strategy (Watson et al 2014Beissinger et al 2017) Despite some recent debateover the breadth of their function (Naughton-Treveset al 2005) one of the main objectives of protected
areas is the protection of biodiversity and the con-servation of viable populations of imperiled species(eg IUCN 1994) However mounting pressureswithin and around protected areas often challengesuch goals (Hansen amp DeFries 2007) and after aperiod of necessary focus on reserve establishmentmore and more attention is being devoted to moni-
copy The authors 2019 Open Access under Creative Commons byAttribution Licence Use distribution and reproduction are un -restricted Authors and original publication must be credited
Publisher Inter-Research middot wwwint-rescom
Corresponding author fsergioebdcsices
Protected areas under pressure decline redistribution local eradication and projected extinction of a threatened predator the red kite in Dontildeana National Park Spain
Fabrizio Sergio1 Alessandro Tanferna1 Javier Chicano1 Julio Blas1 Giacomo Tavecchia2 Fernando Hiraldo1
1Department of Conservation Biology Estacioacuten Bioloacutegica de Dontildeana minus CSIC CAmerico Vespucio 26 41092 Seville Spain2Animal Demography and Ecology Unit Institute for Mediterranean Studies (IMEDEA) CSIC-UIB 07190 Esporles Spain
ABSTRACT After a period of overfocus on the establishment of reserves attention is increasinglybeing devoted to the capability of protected areas to maintain viable populations of endangeredspecies Here we examined the trends and reproduction of the red kite Milvus milvus a highlyendangered raptor near-endemic to Europe to illustrate the dual benefits and challenges faced bya national park to protect this iconic species Over the past 4 decades the kite population of south-ern Spain has declined steeply and has become progressively confined to Dontildeana National Parkand its buffering Natural Park areas Population deterioration was also evident within the pro-tected area through (1) spikes of rapid eradication of whole sub-populations from buffer areaslikely propelled by illegal poisoning and (2) more gradual but steady deterioration of numbersand reproduction especially in peripheral buffer areas probably caused by the interplay of sev-eral shocks related to food availability habitat degradation competition predation and chemicalcontamination The result was a 46minus55 decline with progressive confinement to the core Nat -ional Park and an alarming effective population size of lt10 pairs Demographic modelling sug-gested low adult survival and predicted further declines with possible extinction over the next 2decades We outline tentative goals for management but these will need urgent information onranging and mortality to provide more efficient targets These results illustrate how establishmentof a large park can prevent regional extinction but not necessarily guarantee species-safety lead-ing to protracted forms of extinction debt We suspect that similar dynamics will become morewidespread as anthropogenic pressures increase around protected areas and their performancemonitoring becomes more prevalent
KEY WORDS Matrix models middot European estimates middot Farmland intensification middot Protected area performance middot Reserves middot Review middot Population growth rate
OPENPEN ACCESSCCESS
Endang Species Res 38 189ndash204 2019
toring whether protected areas actually deliver bio-diversity benefits ie their performance (Gaston etal 2008) For example some studies have reporteddeclines and extinctions of key species in protectedareas and sometimes steeper declines within pro-tected areas than outside them (eg Brashares et al2001 Parks amp Harcourt 2002 Whitfield et al 2007Craigie et al 2010) This calls for the need to assessthe historical levels trends and viability of threat-ened species within protected areas in order toensure that they are properly preserved that theycan act as sources of colonizers for outside areas orthat potential declines are detected and haltedthrough management
Here we report a representative example of thebenefits and challenges provided and faced by pro-tected areas in attaining their biodiversity mainte-nance function In particular we focus on the long-term population dynamics of a highly endangeredavian predator the red kite Milvus milvus breedingin Dontildeana National Park in southern Spain
Dontildeana is one of the most biodiversity-rich parks inEurope currently listed as a Ramsar Site a WorldHeritage Site and a UNESCOrsquos Man and the Bio-sphere Reserve While it is usually lands of low eco-nomic value that are designated as protected areas(eg Scott et al 2001) Dontildeana is a relatively largepark (gt1000 km2) centered around a seasonal wet-land in prime fertile land along a river estuary Whileproviding clear biodiversity benefits its location onvery productive land has caused an exponentiallygrowing anthropogenic pressure at the park bordersespecially by rapid habitat conversion to intensivefarmland with consequent impacts on the watertable that sustains the reserve wetlands The park isalso famous worldwide for its dense populations ofcharismatic vertebrate predators which represent amajor attraction for over 300 000 annual tourists anda key focus for conservation management (eg Ferreramp Hiraldo 1991 Loacutepez et al 2009)
One component of such a predator assemblage isthe red kite a medium-sized raptor endemic to thewestern Palearctic with 95 of its world populationconfined to Europe (Knott et al 2009) This speciestypical of open landscapes with scattered woodlandhas suffered dramatic declines in recent decades inall its stronghold populations of Germany Franceand Spain which hold about 80 of the world popu-lation (Knott et al 2009) Due to such declines thered kite is currently classed as Near Threatened inthe IUCN Red List and included in Annex I of the EUBirds Directive and in Annex II of the Bern Conven-tion on the Conservation of European Wildlife and
Natural Habitats In Spain which holds the worldrsquosthird largest population the species has been clas -sified as lsquoat risk of extinctionrsquo since 2011 and as lsquoatcritical risk of extinctionrsquo within southern Spain(Andaluciacutea Autonomous Region) where the presentstudy was conducted In Dontildeana the breeding popu-lation is concentrated near the marshes (Sergio et al2005) where its generalist and opportunist diet isdominated by prey species typical of the marshes andof the ecotone between wetland and terrestrial habi-tats (eg rabbits Oryctolagus cuniculus waterbirdscarrion and reptiles Delibes amp Garciacutea 1984 Veiga ampHiraldo 1990) The preservation of this population isparticularly important for 3 main reasons (1) It is thelast reservoir of the species in southern Spain (seeSection 31) and thus a strategic key for avoiding fur-ther range contraction (a major goal of the EuropeanAction Plan for this species Knott et al 2009) (2) Itshigh dependence on a seasonal wetland makes this aunique population (Vintildeuela et al 1999 Seoane et al2003) with special adaptations to an unpredictablenatural disturbance regime of marsh inundationwhich would be lost in case of extinction with theconsequent erosion of functional biodiversity (3)During winter large numbers of red kite migrantsfrom central-northern Europe join the resident breed-ing population which can thus act as a sentinel formortality threats potentially impacting far away pop-ulations through carryover effects
Given all the above we reconstruct the historicalregional distribution of the red kite in southernSpain document its progressive extirpation and con-finement to Dontildeana demonstrate long-term declinesin abundance and performance of the park popula-tion across several decades provide projections offuture extinction risk and identify potential threats inurgent need of investigation and management
2 METHODS
21 Study area
The protected area of Dontildeana (hereafter Dontildeana)is located in southwestern Spain (36deg 56rsquo 51rsquorsquo N 6deg 21rsquo31rsquorsquo E) within the Autonomous Region of AndaluciacuteaIt is composed of 542 km2 of National Park institutedin 1969 and 538 km2 of buffering Natural Park witha less strict protection category instituted in 1989(Fig S1 and Table S1 in the Supplement at www int-res com articles suppl n038 p189 _ supp pdf) The Nat -ional Park is dominated by 5 main habitat types(1) seasonal marshland usually flooded during win-
190
Sergio et al Predator extinction debt in national park
ter and progressively drying during the springminus summer (2) scrubland a mixture of different degra-dation stages of autochthonous Mediterranean scrub -land (3) sparse grassland mainly located along theinterface between Mediterranean scrubland and themarshes (hereafter lsquoverarsquo) (4) mobile sand dunesalong the ocean shore and (5) stone pine (Pinuspinea) plantations Mature trees suitable for nestingkites are mainly present in the latter pinewoods andas isolated or small clumps of cork oaks Quercussuber and Eucalyptus trees The portions of the Nat-ural Park relevant for breeding kites are mainly thenorthern and eastern sectors of extensive pinewoodssurrounded by intensive farmland All farmland inand around Dontildeana has become progressively moreintensive especially with the spread of strawberrycultivation since the 1990s
22 Field procedures
Kite territories were censused by looking at territo-rial displays nest material transfers and presence ofbirds perched multiple times in or near their nest dur-ing pre-incubation in FebruaryminusMarch Wheneverpossible nest contents were checked at least 3 times(1) during incubation to assess clutch size (2) justafter hatching to estimate hatching success andbrood size and (3) when the nestlings were ~45 d oldto record the number of reared young (nestlingsfledge at ~55 d Bustamante 1993) Because kites areextremely vulnerable to poisoned baits (Villafuerte etal 1998 Vintildeuela et al 1999) we collected all avail-able data on kites found poisoned in Dontildeana Theseincluded (1) individuals reported to local authoritiesand confirmed as poisoned by subsequent eco-toxi-cological analysis and (2) individuals found dead inor under the nest Based on post-mortem chemical ana -lyses such cases are extremely likely to be caused bypoisoning (details in Hernaacutendez et al 2001)
23 Historical information
Kites were intensively surveyed until being rea-sonably sure to have detected the territorial pairs ofthe whole park since 2012 in collaboration with thepark authority and the Equipo de Seguimiento deProcesos Naturales of the Estacioacuten Bioloacutegica deDontildeana-CSIC (EBD-CSIC) which together surveyedthe peripheral sectors of Marismillas Sanlucarpinewood and Abalario (Fig S1) Before that inten-sive research on red kites was conducted in Dontildeana
in the 1980s and 1990s by a group led by F Hiraldoand subsequently by a group led by F Sergio and FHiraldo (eg Veiga amp Hiraldo 1990 Sergio et al2005) Work by these research groups focused espe-cially on certain portions of the park and thus inte-grated extensive information provided by (1) theEquipo de Seguimiento de Procesos Naturales of theEBD-CSIC (2) the Grupo de Conservacioacuten of Dontilde -ana National Park and (3) the field diaries of dozensof researchers field workers visitors volunteersgamekeepers park managers and wardens active inDontildeana since the 1960s Integrating all these sourcesespecially old field diaries from the 1960sminus 70srequired 2 yr of careful screening of locational infor-mation For example two different field ob serverssometimes visited the same territory in the same yearbut referred to the site using different local nameswhich often required meticulous diary inspection toreconstruct the route travelled by each observer onthat day In most years the census was not availablefor the whole park and the well surveyed sectors var-ied among years depending on research priorities orthe area of action of specific observers (eg wardensor field technicians deputed to certain sectors insome years and others in subsequent years) Becauseof such fragmented surveys we estimated the totalDontildeana population by decade as follows (1) wedivided the park into 12 sectors (Fig 1b) These weredefined on the basis of major differences in land-scape composition relevant for kite ecology (egextensive pinewoods and farmland in the north of thepark vs marsh ecotone in the park center) and delin-eations of private properties be cause these oftencaused abrupt management- driven differences inlandscape and because field workers were oftenassigned to survey whole properties in differentyears (2) For each well surveyed sector we calcu-lated the mean number of pairs per year for eachdecade (3) For each decade we summed up thesemean values to obtain a cumulative estimate for thatdecade (4) In the few cases in which the first com-plete survey of a sector was carried out late (eg inthe 1990s) we assumed that the population was stable in earlier decades (hereafter lsquostatic back- estimatesrsquo) This was done in order to enable a com-plete estimate of the whole population through alldecades and produced conservative estimates ofdeclines (5) In the few cases when complete surveysof a sector were not available for a given decade butthey were for earlier and later decades these wereinterpolated to estimate the missing value (hereafterlsquointerpolated estimatesrsquo) Finally (6) in a few periph-eral sectors complete surveys were available for cer-
191
Endang Species Res 38 189ndash204 2019
tain portions of a sector in some years and other por-tions in different subsequent years In these cases wecalculated the mean number of pairs yrminus1 decademinus1 foreach subsector when well surveyed and summed upthese means to obtain a cumulative estimate de -cademinus1 for the whole sector (hereafter lsquocross-combinedestimatesrsquo) In all procedures above we ensured thatall alternative nests belonging to the same territorywere included within the same sector or subsector inorder to avoid biases caused by re-counting the sameterritory twice when combining different surveyunits Similarly in all cases of doubt we used the
estimate that minimized the historicalpopulation in order to provide conser-vative estimates of decline
To place declines and the potentialstrategic importance of the parkwithin a wider regional context wereconstructed the distribution andpopulation levels of the kite popula-tion for southern Spain (AndaluciacuteaAutonomous Region 87 268 km2) inthe 1970sminus1980s based on informa-tion found in Otero et al (1978) TorresEsquivias et al (1981) Ceballos ampGuimeraacute (1992) Vintildeuela et al (1999)Vintildeuela (2004) and conversationswith local experts Data for the currentred kite population outside Dontildeanawere provided by the Consejeriacutea deMedio Ambiente of the AndaluciacuteaAutonomous Region
24 Statistical analyses
To investigate how generalized thehistorical population declines acrossdifferent sectors of the park were weestimated whether the subpopulationof each sector increased or declinedbetween the earliest available surveyand the 2010s and then tested whetherdeclines were prevalent over stable orincreasing trends by means of a bino-mial test To explore temporal trendsin breeding rates we fitted general-ized linear models (GLMs) with de -cade sector and their interaction asexplanatory variables and with thelikelihood of laying eggs clutch sizehatching success brood reductionthe likelihood of successfully raising
chicks to fledgling and the number of young fledgedper territorial breeding and successful pair as re -sponse variables (Zuur et al 2009) In the aboveanalyses hatching success was defined as the pro-portion of eggs that hatched brood reduction was theproportion of hatched chicks lost before fledging aterritorial pair was one that held a territory a breed-ing pair one that laid at least 1 egg and a successfulpair one that raised at least 1 nestling to fledging age(gt45 d) In particular the likelihood of laying eggsand raising chicks to fledging were examinedthrough GLMs with binomial errors and a logit link
192
Fig 1 Approximate distribution range of the red kite in southern Spain (An-daluciacutea Autonomous Region) (a) in the 1980s (reconstructed on the basis ofsources cited in Section 23) compared to (b) the distribution as recorded in2017 The red sectors in (a) represent (1) the marshes of Dontildeana and Odiel inthe provinces of Huelva and Sevilla (2) the hills and low mountains of SierraMorena in the provinces of Huelva Sevilla and Cordoba and (3) the mountain
complex of Cazorla in the provinces of Granada and Jaeacuten
Sergio et al Predator extinction debt in national park
function while clutch size and the number of fledgedyoung were modelled through GLMs with Poissonerrors and a log link function Finally hatching suc-cess and brood reduction were modelled by GLMswith Poisson errors and a log link function using thenumber of hatched eggs and the number of disap-peared chicks as response variables and clutch sizeand brood size at hatching as offset variables (Zuur etal 2009)
The current expected growth of the Dontildeana popu-lation was estimated by building an age-structureddemographic model (Caswell 2001) M based on theage-dependent values of survival (see below) and themean fertility recorded over the last 5 yr in Dontildeana(0294 young per territorial pair) The matrix Mdescribes the transition of the population between 2consecutive years t and t+1 The asymptotic popula-tion growth λ is calculated as the dominant eigen-value of M (Caswell 2001) In a stable population λ isequal to 1 while lower values indicate a decliningtrend Because survival estimates were not availablefor the Dontildeana population we applied values pub-lished for other European populations (reviewed inTable 1) In all studies survival has been reported for3 age classes 1 yr 2 yr and adult (ge3 yr) so we main-tained the same age classes in the current assess-ment In particular to explore the whole range of sur-vival scenarios potentially experienced by ourpopulation we built 3 separate deterministic matrixmodels based on the minimum average and maxi-mum survival rates reported for other European pop-ulations respectively (Table 1) These exploratoryanalyses were conducted with deterministic modelsbecause uncertainty on parameter estimates de -pended largely on the population considered Wefurther assumed a 11 sex ratio and that all kites hadentered the breeding population by 3 yr of age
Based on the obtained λ we then projected the pop-ulation over the next 10minus20 yr assuming no densitydependence to explore its potential short-term via-bility or extinction over the coming decades Becauseof the assumptions outlined above and the parame-ters taken from other populations these projectionsshould be taken with caution and recalibrated asmore local data become available
Finally we used perturbation analyses to calcu-late the sensitivity S(θ) and elasticity E(θ) of thepopulation growth rate to a given parameter θ(Caswell 2001) Sensitivity is the change in pop -ulation growth rate in response to an absolutechange of a given parameter θ while elasticity isthe change in the population growth rate in re -sponse to a proportional change of a given param-eter θ Throughout all analyses were implementedwith R version 351 (R Development Core Team2018) using the libraries lsquopopbiorsquo and lsquolme4rsquoResults are given as means plusmn 1SE tests are 2-tailed and statistical significance was set at α le005
3 RESULTS
31 Regional distribution and the strategicimportance of the protected area
Red kites must originally have been common be -low 400minus600 m of elevation throughout Andaluciacuteawhich traditionally hosted a dense and well distrib-uted rabbit population as an important prey base(Loacutepez 1861) By the 1970sminus1980s legal and thenillegal shooting and poisoning had reduced the pop-ulation to 3 main nuclei (Fig 1a) (1) the marshes ofDontildeana and Odiel in the provinces of Huelva and
Sevilla (2) the hills and low moun-tains of Sierra Morena in theprovinces of Huelva Sevilla and Cor-doba and (3) the mountain complexof Cazorla in the provinces ofGranada and Jaeacuten The latter 2 nucleiwere reported as lsquoin steep declinersquo ordocumented as already extinct in the1990s (Vintildeuela et al 1999 Vintildeuela2004) so that the current regionalpopulation is virtually confined toDontildeana with 3 additional relict pairslocated in the Sierra de Huelva(Fig 1b) The nuclei outside the pro-tected area of Dontildeana were estimatedto ıhave suffered a 95 decline since
193
Area Age class Reference1 yr 2 yr ge 3 yr
England Midlands 080 094 093 Evans et al (1999)Scotland 037 072 087 Smart et al (2010)Wales uplands 060 079 094 Newton et al (1989)Switzerland 045 074 084 Schaub (2012)Spain Mallorca 072 082 079 Tavecchia et al (2012)Spain Menorca 054 083 084 Sanz Aguilar et al (2015)
Min European estimates 037 072 079Mean European estimates 058 081 087Max European estimates 080 094 094
Table 1 Published estimates of red kite survival by age class Minimum meanand maximum levels were used to set up different demographic scenarios for
matrix population models
Endang Species Res 38 189ndash204 2019
the 1970sminus1980s (from a conservative estimate of40minus77 pairs to 2minus4 current pairs) Thus Dontildeanahosted 52minus63 of the regional population in the1970sminus80s and 95minus96 after 2010 increasing its rel-ative strategic importance
32 Abundance and trends in Dontildeana
Different sectors of the park showed differenttrends (Fig 2 Fig S2) Numbers appeared (1) stableor in moderate decline in the Reserva Biologica deDontildeana RBD (sectors 1 2 and 3) (2) stable or increas-ing in the sector of Puntal and in the vera of Algaida-Manecorro as well as its interior These areas werecharacterized by the removal of Eucalyptus planta-tions that converted large areas of woodland to opengrassland in the 1990s (sectors 4 and 5) or alwaysmaintained a very open landscape through extensivegrazing by livestock (sector 6) Finally (3) declines ofvarying magnitude were observed in all peripheralsectors to the north east and south While declineswere moderate in the eastern and southern sectorsthat were monitored less continuously dramatic de -clines were evident for all the northern sectors in -cluding portions of the National Park and its buffer-ing Natural Park In these sectors (7 8 9) a populationof 20minus25 pairs was basically eradicated in a few yearsbetween the late 1980s and early 1990s re mainingvirtually extinct to date (Fig 3) This rapid eradica-tion was accompanied by the detection of adultsfound dead by poisoning in or under their nest Over-all there was a significant preponderance of declinesbetween the numbers re corded in the earliest survey
available for each sector and the 2010s (binomial testp lt 0001 Fig 2) Correspondingly the surface of theoverall and core distribution range of the Dontildeanapopulation declined by 53 and 58 respectively(Fig 4)
When summing up all sectors the overall Dontildeanapopulation was conservatively (see Section 23) esti-mated at 69 pairs (max peak of 82) in the 1980s 61(max 86) in the 1990s 53 (max 64) in 2000minus2009and 47 (max 70) in 2010minus2017 (Table 2) In 2017 thepopulation was composed of 37 pairs representing a46minus55 decline compared to the meanminusmaximumlevels of the 1980s ie in less than 40 yr Thus the~50 declining rate within the park was high butwas only almost half of the ~95 decline estimatedfor outside pairs over the same 4 decades (χ2 = 184p lt 00001)
33 Distribution in Dontildeana
Local eradication and differential declines pro-duced a contraction of the overall range and a shiftin the relative importance of some sectors Thusin the 1980s the population was well distributedthrough all sectors but more concentrated in thecore sectors of RBD vera Puntal and in the northernpinewoods of the Natural Park buffer (Fig 5aTable 2) From the 1990s onwards the populationbecame progressively more concentrated within theNational Park in particular in the ecotonal zonebetween the marsh and terrestrial habitats withvery low numbers or local extinctions in all theother sectors (Fig 5b Table 2)
34 Offspring production in Dontildeana
Except for the number of young persuccessful pair all breeding parame-ters deteriorated through time (all χ2 ge1733 all p lt 00017) The probabilityof laying eggs clutch size hatchingsuccess the likelihood of successfullyraising chicks to fledging and thenumber of young per territorialbreeding and successful pair declinedthrough the last 5 decades while theextent of brood reduction progres-sively increased (Fig 6) Deteriorationof reproduction was particularly pro-nounced for the probability of layingfor brood reduction for the probability
194
80 ndash100 ndash80 ndash60 ndash40 ndash20 0 20 40 60 100
10 Marismillas11 Sanlucar pinewood
12 AbalarioCumulative total
1 RBD vera2 RBD interior
3 RBD sand dunes
Change in breeding numbers compared to the 1980s ()
Sector
4 Vera Algaida-Manecorro5 Interior6 Puntal
7 Coto del Rey8 NW pinewoods9 NE pinewoods
Fig 2 Percentage change in breeding numbers of the Dontildeana red kite popu-lation by sector from the 1980s or since the earliest available record (1990s for
Puntal and Abalario) to 2017 RBD Reserva Biologica de Dontildeana
Sergio et al Predator extinction debt in national park
of successful breeding and for the number of fledgedyoung (Fig 7)
On average the whole population was estimated toproduce 103 fledglings per year in the 1980s this al-most halved to 57 in the 1990s 48 in 2000minus2009 andagain declined to more than halved to 19 in 2010minus2017In 2015 2016 and 2017 the population produced 7 7and 15 fledglings respectively Population decline and
breeding deterioration were accompa-nied by a change in the relative impor-tance of some sectors for offspring pro-duction (Fig 5 Table 2) In the 1980smost young were produced in thesector RBD vera and the northernpinewoods and most other sectors stillcontributed gt5 of the annual youngproduction (Fig 5c) In subsequentdecades fledgling production becameconcentrated in the marsh ecotone(Puntal RBD vera vera of Algaida-Manecorro) with additional inputsfrom some interior or peripheral sectorsand a larger portion of sectors with vir-tually zero contribution to future gener-ations (Fig 5d) Fig 3 illustrates howdiffuse successful reproduction was inthe 1980s compared to 2017
35 Comparison with otherEuropean populations
Compared to other areas of Europethe Dontildeana population showed a highdensity in the 1980s (well above theEuropean mean Table S3) This pro-gressively declined and has changedto below-average density since 2010All breeding parameters were wellbelow the mean European estimatesfrom the 1980s onwards (Table S3) Inparticular the percentage of success-ful pairs and the number of youngfledged per breeding pair are cur-rently 2 to 3 times lower than themean European values
36 Population growth andprojections for the Dontildeana
population
Observed declines were well cap-tured by the growth rate predicted by the populationmodel based on the minimum European survivalrates (Fig 8) The other 2 scenarios of maximum andmean survival rates predicted a stable population ordeclines from the year 2000 onwards only (Fig 8)For the 2010s the model estimated λ = 0849 0960and 1066 for the scenario based on minimum meanand maximum survival estimates respectively
195
Fig 3 Distribution of breeding territories in Dontildeana (a) in the 1980s and (b) in2017 Pairs that bred successfully (black points) were much more frequent andmore widely distributed especially in the northern sectors and in the NaturalPark in the 1980s than in 2017 when most pairs failed to raise chicks to fledg-ing (white points) Territory locations have been moved slightly for conserva-tion reasons and locations from the 1980s could only be approximate for some
territories especially those in the northern pinewoods
Endang Species Res 38 189ndash204 2019
Based on the model with minimum survival rateswhich gave the best fit to past declines the popula-tion of 37 pairs censused in 2017 would be reduced to7 pairs within 10 yr and virtually extinct (le2 pairs) in17 yr The less supported scenario of mean Europeansurvival estimates projected a population of 25 pairsin 10 yr while the most optimistic scenario of maxi-mum survival predicted a full recovery to the 1980spopulation level of 70 pairs in 10 yr
Despite the current extremely lowbreeding success under all 3 scenar-ios of survival the population growthrate was least sensitive to changes infledglings production [E(F) = 0048minus0079 S(F) = 0137minus 0277] and mostsensitive to variations in adult survivalprobability [E(θ) = 0843minus 0904 S(θ) =0929minus 0955] In Fig 9 we plot thecombination of fledgling productionand adult survival that produce differ-ent levels of population growth Atcurrent levels of reproduction adultsurvival would have to be around090minus095 to attain a stable or slightlyincreasing population while restoringbreeding success to the levels of the1980s of 13 young per pair wouldimply a stable population even with arelatively low adult survival of ~077ie below the minimum ever recordedfor the species (Fig 9)
4 DISCUSSION
Our results showed that the currentdeteriorated condition of the Dontildeanared kite population was not a recentphenomenon but the tip of the ice-berg of decades of regional and localdegradation Although the protectedarea slowed the background levels ofregional decline and likely saved thespecies from local extinction its via-bility maintenance performance wasfar from satisfactory In a way the ob -served long-term deterioration actedas a protracted diluted form of extinc-tion debt (Tilman et al 1994) paidover a time-frame of several decadesWe suspect that similar conditionsmay be common in other protectedareas making this a classical example
of gradual underlying pressures diluted over such along time-frame that their severity becomes evidentonly through a large-scale long-term asses sment oronce population degradation has reached its extremeconsequences Note that for many parameters dete-rioration was not especially alarming from onedecade to the next making it difficult for the succes-sion of local field observers to appreciate the overallseverity of the long-term trends This difficulty in
196
Fig 4 Distribution range of red kites in Dontildeana (a) in the 1980s and (b) in2017 The pink outer polygon represents a 95 kernel constructed aroundthe territory locations while the red polygon is a 50 kernel showing the corearea of distribution The overall and core distribution range contracted by 534and 581 respectively Territory locations have been moved slightly for
conservation reasons
Sergio et al Predator extinction debt in national park 197
12
3 R
BD
4 V
era
56
7 C
oto
8 N
W9
NE
10
11
12
Tot
al
RB
DR
BD
san
dA
lgai
da
Inte
rior
Pu
nta
ld
elp
ine-
pin
e-M
aris
-S
anlu
car
Ab
alar
iod
ecli
ne
vera
inte
rior
du
nes
Man
ecor
roR
eyw
ood
sw
ood
sm
illa
sp
inew
ood
a) M
ean
no
of
pai
rs19
80minus
1989
141
52
33
40a
20a
80b
50
107
44
50
30
40b
687
1990
minus19
9915
35
11
37
74
08
03
34
40
74
5e2
5c4
0a60
8minus
115
2000
minus20
0916
05
21
47
05
06
31
01
00
14
5e2
03
1a52
5minus
236
2010
minus20
1713
03
42
56
63
98
41
90
50
13
01
72
147
1minus
315
2017
100
35
211
00
03
12
37minus
462
b)
No
of
you
ng
pro
du
ced
an
nu
ally
1980
minus19
8916
14
25
66
43
09
610
020
311
06
04
56
010
26
1990
minus19
999
82
60
68
44
06
92
46
60
95
13
86
056
9minus
445
2000
minus20
0913
21
61
27
25
83
71
21
60
24
53
04
647
7minus
535
2010
minus20
172
60
61
11
82
33
50
90
30
01
62
91
919
4minus
811
2017
10
03
07
00
00
22
150
minus85
4
c)
of
the
tota
l p
op
ula
tio
n i
n e
ach
sec
tor
1980
minus19
8920
57
64
85
82
911
67
315
56
47
34
45
819
90minus
1999
251
84
21
126
66
131
55
73
12
74
41
66
2000
minus20
0929
49
62
612
99
211
51
81
80
28
33
79
120
10minus
2017
276
72
53
141
82
178
40
11
03
64
36
45
2017
270
00
81
135
54
297
00
00
00
81
27
54
d)
c
on
trib
uti
on
of
each
sec
tor
to t
ota
l an
nu
al y
ou
ng
pro
du
ctio
n19
80minus
1989
157
41
54
94
62
29
97
198
107
58
44
58
1990
minus19
9917
24
61
112
114
77
04
211
61
68
96
610
520
00minus
2009
277
33
24
78
151
121
24
34
04
94
63
96
2010
minus20
1713
43
35
418
19
411
74
81
30
08
215
09
620
176
70
00
046
720
00
00
00
00
00
013
313
3
a Cro
ss-c
omb
ined
est
imat
e b
Sta
tic
bac
k-e
stim
ate
c In
terp
olat
ed e
stim
ate
See
Sec
tion
23
for
det
ails
Tab
le 2
(a
) M
ean
nu
mb
er o
f p
airs
an
d (
b)
cum
ula
tive
nu
mb
er o
f of
fsp
rin
g p
rod
uce
d a
nn
ual
ly b
y th
e D
ontildean
a re
d k
ite
pop
ula
tion
wit
hin
eac
h s
ecto
r an
d i
n t
he
wh
ole
par
k o
ver
the
pas
t d
ecad
es a
nd
in 2
017
Per
cen
tag
e of
(c)
pai
rs a
nd
(d
) yo
un
g c
ontr
ibu
ted
by
each
sec
tor
to t
he
over
all p
opu
lati
on S
ecto
rs c
ontr
ibu
tin
g m
ore
than
10
ar
e h
igh
lig
hte
d i
n b
old
T
otal
ref
ers
to t
he
sum
of
all
sect
ors
d
ecli
ne
is t
he
dec
lin
e co
mp
ared
to
the
1980
s P
rop
orti
onal
con
trib
uti
ons
are
also
ill
ust
rate
d i
n F
ig
5
RB
D R
eser
va B
iolo
gic
a d
e D
ontildean
a
Endang Species Res 38 189ndash204 2019
detecting the problem was likely exacerbated by thefollowing factors that could be defined as lsquoperceptionobstaclesrsquo (1) The fact that a population becomesmore and more restricted to a park is often used toillustrate the positive role of protected areas byfocusing their performance assessments on range
coverage ie the capability of protected areas tocover a large portion of a species range (eg Czech2005 Godet et al 2007) This diverts attention fromthe wider problems of range contraction and from theactual performance of the park in terms of viabilitymaintenance (Gaston et al 2008) (2) Confinement to
198
of nests in each sector
of annual young generated by each sector
1980s 2010s
1980s 2010s
a) b)
c) d)
Fig 5 Percentage of the total red kite population in each of 12 sectors of Dontildeana (a) in the 1980s and (b) in the 2010s percent-age of the annual young production generated by each sector (c) in the 1980s and (d) in the 2010s (a) In the 1980s the bulk ofthe population was concentrated in northern sectors (7 and 8) and in the southern shores of the marshes (sectors 1 6 and 10)(b) In the 2010s the population virtually disappeared from the northern sectors and became essentially confined to the na-tional park where it concentrated along the marshes (c) In the 1980s the population generated more than 100 young eachyear most of them produced by the northern sectors (7 8 9) and by the northern shores of the marshes (sectors 1 and 4) (d) Inthe 2010s the population generated less than 10 young mostly generated close to wetlands (sectors 1 4 11) with homo -geneously low numbers elsewhere Colors (yellow rarr orange rarr red) classify sectors by tertiles of the range of percentage
contribution
Sergio et al Predator extinction debt in national park
a protected area is usually accompanied by the auto-matic presumption that this will act as a source areawith limited anthropogenic impacts an assumptionthat is increasingly disproved (Hansen amp DeFries2007 Gaston et al 2008 Watson et al 2014) (3) Long-term assessments such as ours required the lengthy
collation of fragmented informationfrom a large number of sequentialfield workers and administrationseach of which had a very limited per-ception of the overall situation (4)Much monitoring was conducted inthe core areas of the park like theRBD where the species has alwaysbeen most abundant and relativelystable (eg Sergio et al 2005) con-fusing the perception of broaderdeclines (5) Finally large numbersof wintering migrants boost the pop-ulation in the winter and earlyspring often producing an optimisticimpression of apparent abundance
even in relatively expert members of the public or oflocal administrations as we frequently noted in pub-lic talks and private conversations
Overall the decline occurred at multiple levels redkites were originally widespread throughout south-ern Spain (Loacutepez 1861) but became progressively
199
2030405060708090
100110
Bree
ding
su
cces
sful
()
a breeding pairs successful pairs
202122232425262728
Clut
ch si
ze
b
25
35
45
55
65
75
85
1970-79 1980-89 1990-99 2000-09 2010-17
Hatc
hing
succ
ess
broo
d re
duct
ion
()
Decade
c Hatching successBrood reduction
03
06
09
12
15
18
21
1970-79 1980-89 1990-99 2000-09 2010-17
Youn
g fle
dged
Decade
d Young breeding pairYoung successful pair
Fig 6 Reproductive parameters of the red kite population of Dontildeana (a) percentage of pairs laying eggs (black dots n = 804)and successfully raising fledglings (white dots n = 1185) (b) mean clutch size (n = 469) (c) hatching success (percentage ofeggs that hatched black dots n = 353) and brood reduction (percentage of chicks that disappeared during the nestling periodwhite dots n = 240) (d) mean number of young fledged per territorial pair (black dots n = 1145) and per successful pair (white
dots n = 576)
0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75
Young fledgedsuccessful pairYoung fledgedbreeding pairYoung fledgedterritorial pair
Probability of successful breedingBrood reduction
Hatching successClutch size
Probability of laying
Deterioration ()
Breeding parameter
Fig 7 Percentage deterioration of breeding parameters of the red kite popu-lation of Dontildeana between the 1980s and the 2010s
Endang Species Res 38 189ndash204 2019
confined to the protected area of Dontildeana in recentdecades However the park did not confer automaticsafety and declines and range contraction also con-tinued within the protected area suggesting perva-sive pressures and range erosion at multiple spatialscales In particular almost one third of the Dontildeana
population was virtually eradicatedfrom the northern pinewoods of thebuffering Natural Park in 5 to 7 yrbetween the late 1980s and early1990s Several lines of evidence sug-gest that illegal poisoning was themain cause of this eradication (1) Sev-eral adults were found poisoned undertheir nest in those sectors and years(2) Large-scale poisoning campaignsof raptors were reported throughoutSpain in those exact same years asa consequence of huntersrsquo illegalattempts to control predator popula-tions to increase the rapidly deterio-rating numbers of small game (rabbitsand partridges Villafuerte et al 1998Vintildeuela amp Villafuerte 2003 Cano et al2008) In this sense the National Parksuffered much wider national-level
pressures (3) The northern sectors of the parkwhere the eradication took place included or wereclose to private small-game reserves and predatorcontrol was well known to occur in some of them (4)Finally the rapidity of the eradication of such a long-lived species (maximum longevity of 29 yr in Dontilde -ana) implied a causative agent that directly affectedadult mortality (Saether amp Bakke 2000) such as poi-soning The marked impact of poisoning on adult sur-vival and population growth are well recognized forthis species whose facultative scavenging habits andforaging method of meticulous low and slow quar-tering of the ground make it particularly sensitive tothis threat (Smart et al 2010 Tavecchia et al 2012Tenan et al 2012 Sanz-Aguilar et al 2015)
Spikes of rapid local eradication were superim-posed on more gradual but steady deterioration ofoffspring production Gradual and continuous ratherthan sudden degradation of performance suggestedthat poisoning was not the only threat in effect Inthis context several factors may have contributed togradually deteriorate ecological conditions for kitesin recent decades (1) Rabbit epidemics have causedprogressive declines in the availability of this keyprey (Vintildeuela amp Villafuerte 2003) (2) Lower preyavailability may have exacerbated competition withthe dense populations of other raptors with similardiets such as the ecologically similar and in creasingblack kite (3) Predation rates on adults and nestlingsmay have increased with the expansion of the popu-lations of potential predators such as eagle owls Bubobubo and goshawks Accipiter gentilis (4) Recentassessments have detected alarming levels of toxic
200
00
02
04
06
08
10
12
1980sndash1990s 1990sndash2000s 2000sndash2010s
Popu
latio
n gr
owth
rate
Period
Observed populationgrowth
Scenario 1 minimumEuropean survival
Scenario 2 meanEuropean survival
Scenario 3 maximumEuropean survival
Fig 8 Population growth of the Dontildeana red kite population during the past 4decades as predicted by matrix demographic models based on 3 scenarioswhich assumed that survival was equal to minimum mean or maximum sur-vival rates reported for other European populations (reviewed in Table 1)Predicted values are compared with observed declines from one decade to
the next
Fig 9 Population growth rate of red kites in relation to adultsurvival and breeding performance (mean number of youngfledged per territorial pair) based on a matrix populationmodel Note that the graph could be applied to any Euro-pean population The 3 points at the base of the graph repre-sent the minimum (black) mean (grey) and maximum (blue)survival published for European populations (reviewed in
Table 1)
Sergio et al Predator extinction debt in national park
chemicals in red kite eggs from Dontildeana (Goacutemara etal 2008) (5) Climate change and agricultural man-agement have lowered the water table with likelyimpacts on marsh inundation levels and aquatic prey(Garciacutea Novo amp Mariacuten Cabrera 2005 Diacuteaz-Paniaguaamp Aragoneacutes 2015 Schmidt et al 2017) (6) Conver-sion to intensive farmland in surrounding lands haseroded habitat and prey availability outside the pro-tected area which may have buffered kites fromperiods of low prey availability within the park (egduring droughts in the marshes) Some of the pat-terns of observed reproductive deterioration lendsupport to some of these impacts For exampledeclining clutch sizes and increasing rates of broodreduction suggest that food was not sufficient to sus-tain earlier reproductive levels while lowered hatch-ing success is often the result of chemical contamina-tion in raptors (review in Newton 1979) While eachof these threats will be quantitatively investigated indetail in the immediate future in the present contextthey illustrate the frequent and complex challengesfaced by (1) protected areas in maintaining biodiver-sity and viable populations of imperiled species and(2) conservation biologists in identifying causes ofdecline for subsequent management interventioneven in lsquoprivilegedrsquo sites such as reserves
Redistribution declining numbers and perform-ance had important repercussions for future viability(1) The population passed from producing gt100annual young to lt10minus20 which will make mainte-nance and recovery difficult (2) These young wereincreasingly produced in the core sectors of themarsh-ecotone within the National Park which prob-ably increased the dependence of the population onmarsh inundation in turn affected by problems oper-ating outside the park (Garciacutea Novo amp Mariacuten Cabrera2005 Diacuteaz-Paniagua amp Aragoneacutes 2015 Schmidt et al2017) (3) Steep declines in the percentage of suc-cessful pairs implied that future generations wereproduced by a progressively more restricted numberof pairs which will make the population more sub-ject to inbreeding and stochastic events For exam-ple in the last 3 yr all the annual young were pro-duced by 6 8 and 9 pairs respectively suggesting aneffective population size 4 to 9 times lower than theoverall abundance
Given all the above it is no surprise that demo-graphic models suggested a negative growth and apopulation incapable of self-sustenance In particu-lar the model that gave the best fit to past observeddeclines was the one based on minimum Europeansurvival estimates followed by the scenario based onmean European survival estimates Given the above-
mentioned threats declines and performance deteri-oration we would expect survival to be closer to min-imum than mean European levels as supported bythe observed fit to past and recent declines Theseresults have 2 main implications (1) If survival is aslow as we suspect demographic models predict vir-tual extinction within a few years demanding anurgent need for identification and management ofmortality threats as well as quantification of actualsurvival to refine predictions Note that virtual ex -tinction could be even earlier when taking intoaccount effective rather than total population sizeand a stochastic rather than deterministic populationmodel (2) Should actual survival be confirmed lowbut further declines not observed the populationwould be a sink sustained by external sources whichwould make it even more at risk from anthropogenicthreats outside the park and thus more challengingto manage (eg Hansen amp DeFries 2007 Blanco et al2017)
5 Conclusions and implications for conservation
The decades-long degradation that we depictedwas likely generated by a combination of factorsboth internal to the park (eg rabbit availabilitymarsh inundation rates predation and competitionwith other species) and external (eg illegal poi-soning contamination farmland intensification)Some of them will be amenable to managementand others less so but the first priority will be tofind rapid ways to identify the key factors thatdrive population growth so as to optimize conserva-tion action before it is too late For example focus-ing conservation lsquoblindlyrsquo on supplementary feedingcould be useless if the problem is chemical contam-ination The quickest way to obtain such informa-tion would be a satelliteGSM (Global System forMobile communication) tagging program that wouldallow to (1) obtain rapid estimates of health andsurvival for young and adults (eg Sergio et al2019) so as to recalibrate future projections andgoals (2) assess the relative contribution of mainmortality causes which is an essential first step inany recovery program (eg Gonzaacutelez et al 2007Margalida et al 2008 Smart et al 2010) and (3)identify the areas used by breeding and non-breed-ing individuals inside and outside of the park toassess their risk-exposure and intervene before orafter death (eg to prosecute perpetrators of illegalpoisoning or re trofit dangerous electricity pylons inareas of high use by kites)
201
Endang Species Res 38 189ndash204 2019
Until this information becomes available below welist some tentative figures and priorities for conserva-tion First of all restoring the current population toformer levels would undoubtedly be challenging andprobably unrealistic given the profound changesincurred by the wider Dontildeana ecosystem in recentdecades Thus we propose an initial target of 60pairs as a long-term restoration goal Elasticity analy-sis suggested that optimal management should focuson improving adult survival which had the largestimpact on population growth as in other long-livedspecies (Saether amp Bakke 2000 Whitfield et al 2004Kruumlger et al 2010) This could be attempted by in -creasing food availability especially of key prey suchas rabbits and by curtailing mortality threats such asillegal poisoning which still continues despite mucheffort to eradicate it by the local administration Thetelemetry program outlined above could help toidentify local perpetrators as occurred in other pop-ulations (Smart et al 2010 Tavecchia et al 2012) Onthe other hand despite their low elasticities repro-ductive rates are currently so low that it would befundamental to increase them eg by increasingfood availability and ensuring proper inundation ofthe marshes Based on Fig 5 we propose as initialtargets for restoration (1) survival rates equal orhigher than the European mean (adult survivalge087) and (2) a number of young fledged per territo-rial pair above 10 which would produce an increas-ing population provided that adult survival is equalto or above the European mean Note that Fig 5could be applied to any European population as atool to check its potential viability Given the highlythreatened status of red kites the speciesrsquo limitedrange confined to Europe and its ongoing declinesviability assessments such as ours may sadly becomemore important for the management and recovery ofmany populations
In conclusion red kites would probably be extinctin southern Spain without the institution of a largenational park In this sense this example well illus-trates how protected areas will continue to be corner-stones of global conservation of threatened taxaHowever their safety is not ensured by park institu-tion per se and performance monitoring and focusedaction will be needed to avoid potential extinctiondebts which may be more protracted than previouslyappreciated In our exemplary case despite the pres-ence of a large national park on prime fertile landwithin a developed country with adequate institu-tional and financial support a key threatened speciessuffered latent but steady declines for decadesobscured by problems of perception lack and frag-
mentation of information and likely caused by acomplex array of within-park threats and growingexternal pressures Viability maintenance and recov-ery will probably require concerted actions withinand outside of the park but only after detailed infor-mation on crucial aspects becomes available whichis probably the most urgent current priority We sus-pect that dynamics like the ones illustrated here aremore common than currently appreciated and willbecome more widespread as anthropogenic pres-sures increase around protected areas and as theirperformance monitoring becomes more prevalent
Acknowledgements We thank all the (too many to mention)researchers field workers visitors volunteers gamekeep-ers park managers and wardens that have provided datasince the 1960s In particular we thank F G Vilches L Gar-ciacutea and the Equipo de Seguimiento de Procesos Naturales ofthe Estacioacuten Bioloacutegica de Dontildeana-CSIC for help in the fieldSpecial thanks to F G Vilches for the priceless help with thecollation and organization of historical information Wethank J P Castellano I Redondo and all the lsquoArea de Con-servacioacutenrsquo of Dontildeana National Park for constant interest andsupport We thank R Cadenas J Madrid R Arenas J RBenitez and all the pertinent personnel of the Consejeriacutea deMedio Ambiente of the Junta de Andaluciacutea for informationon current nest locations in the Sierra de Huelva and fortheir constant attentive support We are grateful to Dr NBunnefeld and 2 anonymous reviewers for constructivecomments that improved the manuscript This study wasfunded by the Foundation Jaime Gonzaacutelez-Gordon and bythe research project 16022015 of the Spanish Ministry ofAgriculture Food and the Environment (National ParksAutonomous Agency)
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Brashares JS Arcese P Sam MK (2001) Human demographyand reserve size predict wildlife extinction in WestAfrica Proc Biol Sci 268 2473minus2478
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Caswell H (2001) Matrix population models Sinauer Sun-derland MA
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Diacuteaz-Paniagua C Aragoneacutes D (2015) Permanent and tempo-rary ponds in Dontildeana National Park (SW Spain) arethreatened by desiccation Limnetica 34 407minus424
Evans IM Summers RW OrsquoToole L Orr-Ewing DC Snell NSmith J (1999) Evaluating the success of translocatingred kites Milvus milvus to the UK Bird Study 46 129minus144
Ferrer M Hiraldo F (1991) Evaluation of management tech-niques for the Spanish imperial eagle Wildl Soc Bull 19 436minus442
Garciacutea Novo F Mariacuten Cabrera C (2005) Dontildeana water andbiosphere Dontildeana 2005 Project Spanish Ministry of theEnvironment Madrid
Gaston KJ Jackson SF Cantuacute-Salazar L Cruz-Pintildeoacuten G(2008) The ecological performance of protected areasAnnu Rev Ecol Evol Syst 39 93minus113
Godet L Devictor V Jiguet F (2007) Estimating relative pop-ulation size included within protected areas BiodiversConserv 16 2587minus2598
Goacutemara B Gonzaacutelez MJ Baos R Hiraldo F Abad E RiveraJ Jimeacutenez B (2008) Unexpected high PCB and total DDTlevels in the breeding population of red kite (Milvus mil-vus) from Dontildeana National Park south-western SpainEnviron Int 34 73minus78
Gonzaacutelez LM Margalida A Mantildeosa S Saacutenchez R and oth-ers (2007) Causes and spatio-temporal variations of non-natural mortality in the vulnerable Spanish imperialeagle Aquila adalberti during a recovery period Oryx41 495minus502
Hansen AJ DeFries R (2007) Ecological mechanisms linkingprotected areas to surrounding lands Ecol Appl 17 974minus988
Hernaacutendez FJ Donaacutezar JA Hiraldo F (2001) Evaluacioacuten deluso de venenos para el control de predadores en laComunidad Autoacutenoma Andaluza y su impacto en la con-servacioacuten de especies amenazadas de vertebrados Con-sejeria de Medio Ambiente and Estacioacuten Bioloacutegica deDontildeana Sevilla
IUCN (The World Conservation Union) (1994) Guidelines forprotected area management categories IUCN Gland
Knott J Newbery P Barov B (2009) Action plan for the redkite Milvus milvus in the European Union EuropeanCommission Brussels
Kruumlger O Gruumlnkorn T Struwe-Juhl B (2010) The return ofthe white-tailed eagle (Haliaeetus albicilla) to northernGermany modelling the past to predict the future BiolConserv 143 710minus721
Loacutepez V (1861) Cataacutelogo de las aves observadas enAndaluciacutea Madrid
Loacutepez G and others (2009) Management measures to controla feline leukemia virus outbreak in the endangered Iber-ian lynx Anim Conserv 12 173minus182
Margalida A Heredia R Razin M Hernaacutendez M (2008)Sources of variation in mortality of the bearded vultureGypaetus barbatus in Europe Bird Conserv Int 18 1minus10
Naughton-Treves L Holland MB Brandon K (2005) The roleof protected areas in conserving biodiversity and sustain-
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Newton I (1979) Population ecology of raptors T amp AD PoyserBerkhamsted
Newton I Davis PE Davis JE (1989) Age of first breedingdispersal and survival of red kites Milvus milvus inWales Ibis 131 16minus21
Otero C Castieacuten E Senosiaiacuten R Portillo F (1978) Fauna deCazorla vertebrados Publicaciones del Ministerio deAgricultura Madrid
Parks SA Harcourt AH (2002) Reserve size local humandensity and mammalian extinctions in US protectedareas Conserv Biol 16 800minus808
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Saeligther BE Bakke Oslash (2000) Avian life history variation andcontribution of demographic traits to the populationgrowth rate Ecology 81 642minus653
Sanz-Aguilar A De Pablo F Donaacutezar JA (2015) Age-depen-dent survival of island vs mainland populations of twoavian scavengers delving into migration costs Oecolo-gia 179 405minus414
Schaub M (2012) Spatial distribution of wind turbines is cru-cial for the survival of red kite populations Biol Conserv155 111minus118
Schmidt G Saacutenchez Navarro R Hernaacutendez E Carmona JJFuentelsaz F Seiz R (2017) The state of water in Dontildeana an evaluation of the state of the water and of the ecosys-tems of the protected space WWFAdena Madrid
Scott JM Davis FW McGhie RG Wright RG Groves CEstes J (2001) Nature reserves Do they capture the fullrange of Americarsquos biological diversity Ecol Appl 11 999minus1007
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Sergio F Tanferna A Blas J Blanco G Hiraldo F (2019) Reli-able methods for identifying animal deaths in GPS- andsatellite-tracking data review testing and calibrationJ Appl Ecol 56562ndash572
Smart J Amar A Sim IMW Etheridge B Cameron DChristie G Wilson JD (2010) Illegal killing slows popula-tion recovery of a re-introduced raptor of high conserva-tion concern mdash the red kite Milvus milvus Biol Conserv143 1278minus1286
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Tenan S Adrover J Muntildeoz Navarro A Sergio F TavecchiaG (2012) Demographic consequences of poison-relatedmortality in a threatened bird of prey PLOS ONE 7 e49187
Tilman D May RM Lehman CL Nowak MA (1994) Habitatdestruction and the extinction debt Nature 371 65minus66
Torres Esquivias JA Jordano P Leoacuten A (1981) Aves de presadiurnas de la provincia de Coacuterdoba Publicaciones CA yMP Coacuterdoba
Veiga JP Hiraldo F (1990) Food habits and the survival andgrowth of nestlings in two sympatric kites (Milvus milvus
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tor persecution caused by population crash in a gamespecies the case of red kites and rabbits in Spain BiolConserv 84 181minus188
Vintildeuela J (2004) Milano real Milvus milvus In Madrontildeo AGonzaacutelez C Atienza JC (eds) Libro rojo de las aves deEspantildea Direccioacuten General para la BiodiversidadminusSEOBirdLife Madrid p 120minus125
Vintildeuela J Villafuerte R (2003) Predators and rabbits (Oryc-tolagus cuniculus) in Spain a key conflict for Europeanraptor conservation In Thompson DBA Redpath SMFielding AH Marquiss M Galbraith CA (eds) Birds ofprey in a changing environment The Stationery OfficeEdinburgh p 511minus526
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Watson JEM Dudley N Segan DB Hockings M (2014) Theperformance and potential of protected areas Nature515 67minus73
Whitfield SM Bell KE Philippi T Sasa M and others (2007)Amphibian and reptile declines over 35 years at La SelvaCosta Rica Proc Natl Acad Sci USA 104 8352minus8356
Whitfield DP Fielding AH McLeod DRA Haworth PF(2004) Modelling the effects of persecution on the popu-lation dynamics of golden eagles in Scotland Biol Con-serv 119 319minus333
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204
Editorial responsibility Nils BunnefeldStirling UK
Submitted October 8 2018 Accepted January 28 2019Proofs received from author(s) April 7 2019
Endang Species Res 38 189ndash204 2019
toring whether protected areas actually deliver bio-diversity benefits ie their performance (Gaston etal 2008) For example some studies have reporteddeclines and extinctions of key species in protectedareas and sometimes steeper declines within pro-tected areas than outside them (eg Brashares et al2001 Parks amp Harcourt 2002 Whitfield et al 2007Craigie et al 2010) This calls for the need to assessthe historical levels trends and viability of threat-ened species within protected areas in order toensure that they are properly preserved that theycan act as sources of colonizers for outside areas orthat potential declines are detected and haltedthrough management
Here we report a representative example of thebenefits and challenges provided and faced by pro-tected areas in attaining their biodiversity mainte-nance function In particular we focus on the long-term population dynamics of a highly endangeredavian predator the red kite Milvus milvus breedingin Dontildeana National Park in southern Spain
Dontildeana is one of the most biodiversity-rich parks inEurope currently listed as a Ramsar Site a WorldHeritage Site and a UNESCOrsquos Man and the Bio-sphere Reserve While it is usually lands of low eco-nomic value that are designated as protected areas(eg Scott et al 2001) Dontildeana is a relatively largepark (gt1000 km2) centered around a seasonal wet-land in prime fertile land along a river estuary Whileproviding clear biodiversity benefits its location onvery productive land has caused an exponentiallygrowing anthropogenic pressure at the park bordersespecially by rapid habitat conversion to intensivefarmland with consequent impacts on the watertable that sustains the reserve wetlands The park isalso famous worldwide for its dense populations ofcharismatic vertebrate predators which represent amajor attraction for over 300 000 annual tourists anda key focus for conservation management (eg Ferreramp Hiraldo 1991 Loacutepez et al 2009)
One component of such a predator assemblage isthe red kite a medium-sized raptor endemic to thewestern Palearctic with 95 of its world populationconfined to Europe (Knott et al 2009) This speciestypical of open landscapes with scattered woodlandhas suffered dramatic declines in recent decades inall its stronghold populations of Germany Franceand Spain which hold about 80 of the world popu-lation (Knott et al 2009) Due to such declines thered kite is currently classed as Near Threatened inthe IUCN Red List and included in Annex I of the EUBirds Directive and in Annex II of the Bern Conven-tion on the Conservation of European Wildlife and
Natural Habitats In Spain which holds the worldrsquosthird largest population the species has been clas -sified as lsquoat risk of extinctionrsquo since 2011 and as lsquoatcritical risk of extinctionrsquo within southern Spain(Andaluciacutea Autonomous Region) where the presentstudy was conducted In Dontildeana the breeding popu-lation is concentrated near the marshes (Sergio et al2005) where its generalist and opportunist diet isdominated by prey species typical of the marshes andof the ecotone between wetland and terrestrial habi-tats (eg rabbits Oryctolagus cuniculus waterbirdscarrion and reptiles Delibes amp Garciacutea 1984 Veiga ampHiraldo 1990) The preservation of this population isparticularly important for 3 main reasons (1) It is thelast reservoir of the species in southern Spain (seeSection 31) and thus a strategic key for avoiding fur-ther range contraction (a major goal of the EuropeanAction Plan for this species Knott et al 2009) (2) Itshigh dependence on a seasonal wetland makes this aunique population (Vintildeuela et al 1999 Seoane et al2003) with special adaptations to an unpredictablenatural disturbance regime of marsh inundationwhich would be lost in case of extinction with theconsequent erosion of functional biodiversity (3)During winter large numbers of red kite migrantsfrom central-northern Europe join the resident breed-ing population which can thus act as a sentinel formortality threats potentially impacting far away pop-ulations through carryover effects
Given all the above we reconstruct the historicalregional distribution of the red kite in southernSpain document its progressive extirpation and con-finement to Dontildeana demonstrate long-term declinesin abundance and performance of the park popula-tion across several decades provide projections offuture extinction risk and identify potential threats inurgent need of investigation and management
2 METHODS
21 Study area
The protected area of Dontildeana (hereafter Dontildeana)is located in southwestern Spain (36deg 56rsquo 51rsquorsquo N 6deg 21rsquo31rsquorsquo E) within the Autonomous Region of AndaluciacuteaIt is composed of 542 km2 of National Park institutedin 1969 and 538 km2 of buffering Natural Park witha less strict protection category instituted in 1989(Fig S1 and Table S1 in the Supplement at www int-res com articles suppl n038 p189 _ supp pdf) The Nat -ional Park is dominated by 5 main habitat types(1) seasonal marshland usually flooded during win-
190
Sergio et al Predator extinction debt in national park
ter and progressively drying during the springminus summer (2) scrubland a mixture of different degra-dation stages of autochthonous Mediterranean scrub -land (3) sparse grassland mainly located along theinterface between Mediterranean scrubland and themarshes (hereafter lsquoverarsquo) (4) mobile sand dunesalong the ocean shore and (5) stone pine (Pinuspinea) plantations Mature trees suitable for nestingkites are mainly present in the latter pinewoods andas isolated or small clumps of cork oaks Quercussuber and Eucalyptus trees The portions of the Nat-ural Park relevant for breeding kites are mainly thenorthern and eastern sectors of extensive pinewoodssurrounded by intensive farmland All farmland inand around Dontildeana has become progressively moreintensive especially with the spread of strawberrycultivation since the 1990s
22 Field procedures
Kite territories were censused by looking at territo-rial displays nest material transfers and presence ofbirds perched multiple times in or near their nest dur-ing pre-incubation in FebruaryminusMarch Wheneverpossible nest contents were checked at least 3 times(1) during incubation to assess clutch size (2) justafter hatching to estimate hatching success andbrood size and (3) when the nestlings were ~45 d oldto record the number of reared young (nestlingsfledge at ~55 d Bustamante 1993) Because kites areextremely vulnerable to poisoned baits (Villafuerte etal 1998 Vintildeuela et al 1999) we collected all avail-able data on kites found poisoned in Dontildeana Theseincluded (1) individuals reported to local authoritiesand confirmed as poisoned by subsequent eco-toxi-cological analysis and (2) individuals found dead inor under the nest Based on post-mortem chemical ana -lyses such cases are extremely likely to be caused bypoisoning (details in Hernaacutendez et al 2001)
23 Historical information
Kites were intensively surveyed until being rea-sonably sure to have detected the territorial pairs ofthe whole park since 2012 in collaboration with thepark authority and the Equipo de Seguimiento deProcesos Naturales of the Estacioacuten Bioloacutegica deDontildeana-CSIC (EBD-CSIC) which together surveyedthe peripheral sectors of Marismillas Sanlucarpinewood and Abalario (Fig S1) Before that inten-sive research on red kites was conducted in Dontildeana
in the 1980s and 1990s by a group led by F Hiraldoand subsequently by a group led by F Sergio and FHiraldo (eg Veiga amp Hiraldo 1990 Sergio et al2005) Work by these research groups focused espe-cially on certain portions of the park and thus inte-grated extensive information provided by (1) theEquipo de Seguimiento de Procesos Naturales of theEBD-CSIC (2) the Grupo de Conservacioacuten of Dontilde -ana National Park and (3) the field diaries of dozensof researchers field workers visitors volunteersgamekeepers park managers and wardens active inDontildeana since the 1960s Integrating all these sourcesespecially old field diaries from the 1960sminus 70srequired 2 yr of careful screening of locational infor-mation For example two different field ob serverssometimes visited the same territory in the same yearbut referred to the site using different local nameswhich often required meticulous diary inspection toreconstruct the route travelled by each observer onthat day In most years the census was not availablefor the whole park and the well surveyed sectors var-ied among years depending on research priorities orthe area of action of specific observers (eg wardensor field technicians deputed to certain sectors insome years and others in subsequent years) Becauseof such fragmented surveys we estimated the totalDontildeana population by decade as follows (1) wedivided the park into 12 sectors (Fig 1b) These weredefined on the basis of major differences in land-scape composition relevant for kite ecology (egextensive pinewoods and farmland in the north of thepark vs marsh ecotone in the park center) and delin-eations of private properties be cause these oftencaused abrupt management- driven differences inlandscape and because field workers were oftenassigned to survey whole properties in differentyears (2) For each well surveyed sector we calcu-lated the mean number of pairs per year for eachdecade (3) For each decade we summed up thesemean values to obtain a cumulative estimate for thatdecade (4) In the few cases in which the first com-plete survey of a sector was carried out late (eg inthe 1990s) we assumed that the population was stable in earlier decades (hereafter lsquostatic back- estimatesrsquo) This was done in order to enable a com-plete estimate of the whole population through alldecades and produced conservative estimates ofdeclines (5) In the few cases when complete surveysof a sector were not available for a given decade butthey were for earlier and later decades these wereinterpolated to estimate the missing value (hereafterlsquointerpolated estimatesrsquo) Finally (6) in a few periph-eral sectors complete surveys were available for cer-
191
Endang Species Res 38 189ndash204 2019
tain portions of a sector in some years and other por-tions in different subsequent years In these cases wecalculated the mean number of pairs yrminus1 decademinus1 foreach subsector when well surveyed and summed upthese means to obtain a cumulative estimate de -cademinus1 for the whole sector (hereafter lsquocross-combinedestimatesrsquo) In all procedures above we ensured thatall alternative nests belonging to the same territorywere included within the same sector or subsector inorder to avoid biases caused by re-counting the sameterritory twice when combining different surveyunits Similarly in all cases of doubt we used the
estimate that minimized the historicalpopulation in order to provide conser-vative estimates of decline
To place declines and the potentialstrategic importance of the parkwithin a wider regional context wereconstructed the distribution andpopulation levels of the kite popula-tion for southern Spain (AndaluciacuteaAutonomous Region 87 268 km2) inthe 1970sminus1980s based on informa-tion found in Otero et al (1978) TorresEsquivias et al (1981) Ceballos ampGuimeraacute (1992) Vintildeuela et al (1999)Vintildeuela (2004) and conversationswith local experts Data for the currentred kite population outside Dontildeanawere provided by the Consejeriacutea deMedio Ambiente of the AndaluciacuteaAutonomous Region
24 Statistical analyses
To investigate how generalized thehistorical population declines acrossdifferent sectors of the park were weestimated whether the subpopulationof each sector increased or declinedbetween the earliest available surveyand the 2010s and then tested whetherdeclines were prevalent over stable orincreasing trends by means of a bino-mial test To explore temporal trendsin breeding rates we fitted general-ized linear models (GLMs) with de -cade sector and their interaction asexplanatory variables and with thelikelihood of laying eggs clutch sizehatching success brood reductionthe likelihood of successfully raising
chicks to fledgling and the number of young fledgedper territorial breeding and successful pair as re -sponse variables (Zuur et al 2009) In the aboveanalyses hatching success was defined as the pro-portion of eggs that hatched brood reduction was theproportion of hatched chicks lost before fledging aterritorial pair was one that held a territory a breed-ing pair one that laid at least 1 egg and a successfulpair one that raised at least 1 nestling to fledging age(gt45 d) In particular the likelihood of laying eggsand raising chicks to fledging were examinedthrough GLMs with binomial errors and a logit link
192
Fig 1 Approximate distribution range of the red kite in southern Spain (An-daluciacutea Autonomous Region) (a) in the 1980s (reconstructed on the basis ofsources cited in Section 23) compared to (b) the distribution as recorded in2017 The red sectors in (a) represent (1) the marshes of Dontildeana and Odiel inthe provinces of Huelva and Sevilla (2) the hills and low mountains of SierraMorena in the provinces of Huelva Sevilla and Cordoba and (3) the mountain
complex of Cazorla in the provinces of Granada and Jaeacuten
Sergio et al Predator extinction debt in national park
function while clutch size and the number of fledgedyoung were modelled through GLMs with Poissonerrors and a log link function Finally hatching suc-cess and brood reduction were modelled by GLMswith Poisson errors and a log link function using thenumber of hatched eggs and the number of disap-peared chicks as response variables and clutch sizeand brood size at hatching as offset variables (Zuur etal 2009)
The current expected growth of the Dontildeana popu-lation was estimated by building an age-structureddemographic model (Caswell 2001) M based on theage-dependent values of survival (see below) and themean fertility recorded over the last 5 yr in Dontildeana(0294 young per territorial pair) The matrix Mdescribes the transition of the population between 2consecutive years t and t+1 The asymptotic popula-tion growth λ is calculated as the dominant eigen-value of M (Caswell 2001) In a stable population λ isequal to 1 while lower values indicate a decliningtrend Because survival estimates were not availablefor the Dontildeana population we applied values pub-lished for other European populations (reviewed inTable 1) In all studies survival has been reported for3 age classes 1 yr 2 yr and adult (ge3 yr) so we main-tained the same age classes in the current assess-ment In particular to explore the whole range of sur-vival scenarios potentially experienced by ourpopulation we built 3 separate deterministic matrixmodels based on the minimum average and maxi-mum survival rates reported for other European pop-ulations respectively (Table 1) These exploratoryanalyses were conducted with deterministic modelsbecause uncertainty on parameter estimates de -pended largely on the population considered Wefurther assumed a 11 sex ratio and that all kites hadentered the breeding population by 3 yr of age
Based on the obtained λ we then projected the pop-ulation over the next 10minus20 yr assuming no densitydependence to explore its potential short-term via-bility or extinction over the coming decades Becauseof the assumptions outlined above and the parame-ters taken from other populations these projectionsshould be taken with caution and recalibrated asmore local data become available
Finally we used perturbation analyses to calcu-late the sensitivity S(θ) and elasticity E(θ) of thepopulation growth rate to a given parameter θ(Caswell 2001) Sensitivity is the change in pop -ulation growth rate in response to an absolutechange of a given parameter θ while elasticity isthe change in the population growth rate in re -sponse to a proportional change of a given param-eter θ Throughout all analyses were implementedwith R version 351 (R Development Core Team2018) using the libraries lsquopopbiorsquo and lsquolme4rsquoResults are given as means plusmn 1SE tests are 2-tailed and statistical significance was set at α le005
3 RESULTS
31 Regional distribution and the strategicimportance of the protected area
Red kites must originally have been common be -low 400minus600 m of elevation throughout Andaluciacuteawhich traditionally hosted a dense and well distrib-uted rabbit population as an important prey base(Loacutepez 1861) By the 1970sminus1980s legal and thenillegal shooting and poisoning had reduced the pop-ulation to 3 main nuclei (Fig 1a) (1) the marshes ofDontildeana and Odiel in the provinces of Huelva and
Sevilla (2) the hills and low moun-tains of Sierra Morena in theprovinces of Huelva Sevilla and Cor-doba and (3) the mountain complexof Cazorla in the provinces ofGranada and Jaeacuten The latter 2 nucleiwere reported as lsquoin steep declinersquo ordocumented as already extinct in the1990s (Vintildeuela et al 1999 Vintildeuela2004) so that the current regionalpopulation is virtually confined toDontildeana with 3 additional relict pairslocated in the Sierra de Huelva(Fig 1b) The nuclei outside the pro-tected area of Dontildeana were estimatedto ıhave suffered a 95 decline since
193
Area Age class Reference1 yr 2 yr ge 3 yr
England Midlands 080 094 093 Evans et al (1999)Scotland 037 072 087 Smart et al (2010)Wales uplands 060 079 094 Newton et al (1989)Switzerland 045 074 084 Schaub (2012)Spain Mallorca 072 082 079 Tavecchia et al (2012)Spain Menorca 054 083 084 Sanz Aguilar et al (2015)
Min European estimates 037 072 079Mean European estimates 058 081 087Max European estimates 080 094 094
Table 1 Published estimates of red kite survival by age class Minimum meanand maximum levels were used to set up different demographic scenarios for
matrix population models
Endang Species Res 38 189ndash204 2019
the 1970sminus1980s (from a conservative estimate of40minus77 pairs to 2minus4 current pairs) Thus Dontildeanahosted 52minus63 of the regional population in the1970sminus80s and 95minus96 after 2010 increasing its rel-ative strategic importance
32 Abundance and trends in Dontildeana
Different sectors of the park showed differenttrends (Fig 2 Fig S2) Numbers appeared (1) stableor in moderate decline in the Reserva Biologica deDontildeana RBD (sectors 1 2 and 3) (2) stable or increas-ing in the sector of Puntal and in the vera of Algaida-Manecorro as well as its interior These areas werecharacterized by the removal of Eucalyptus planta-tions that converted large areas of woodland to opengrassland in the 1990s (sectors 4 and 5) or alwaysmaintained a very open landscape through extensivegrazing by livestock (sector 6) Finally (3) declines ofvarying magnitude were observed in all peripheralsectors to the north east and south While declineswere moderate in the eastern and southern sectorsthat were monitored less continuously dramatic de -clines were evident for all the northern sectors in -cluding portions of the National Park and its buffer-ing Natural Park In these sectors (7 8 9) a populationof 20minus25 pairs was basically eradicated in a few yearsbetween the late 1980s and early 1990s re mainingvirtually extinct to date (Fig 3) This rapid eradica-tion was accompanied by the detection of adultsfound dead by poisoning in or under their nest Over-all there was a significant preponderance of declinesbetween the numbers re corded in the earliest survey
available for each sector and the 2010s (binomial testp lt 0001 Fig 2) Correspondingly the surface of theoverall and core distribution range of the Dontildeanapopulation declined by 53 and 58 respectively(Fig 4)
When summing up all sectors the overall Dontildeanapopulation was conservatively (see Section 23) esti-mated at 69 pairs (max peak of 82) in the 1980s 61(max 86) in the 1990s 53 (max 64) in 2000minus2009and 47 (max 70) in 2010minus2017 (Table 2) In 2017 thepopulation was composed of 37 pairs representing a46minus55 decline compared to the meanminusmaximumlevels of the 1980s ie in less than 40 yr Thus the~50 declining rate within the park was high butwas only almost half of the ~95 decline estimatedfor outside pairs over the same 4 decades (χ2 = 184p lt 00001)
33 Distribution in Dontildeana
Local eradication and differential declines pro-duced a contraction of the overall range and a shiftin the relative importance of some sectors Thusin the 1980s the population was well distributedthrough all sectors but more concentrated in thecore sectors of RBD vera Puntal and in the northernpinewoods of the Natural Park buffer (Fig 5aTable 2) From the 1990s onwards the populationbecame progressively more concentrated within theNational Park in particular in the ecotonal zonebetween the marsh and terrestrial habitats withvery low numbers or local extinctions in all theother sectors (Fig 5b Table 2)
34 Offspring production in Dontildeana
Except for the number of young persuccessful pair all breeding parame-ters deteriorated through time (all χ2 ge1733 all p lt 00017) The probabilityof laying eggs clutch size hatchingsuccess the likelihood of successfullyraising chicks to fledging and thenumber of young per territorialbreeding and successful pair declinedthrough the last 5 decades while theextent of brood reduction progres-sively increased (Fig 6) Deteriorationof reproduction was particularly pro-nounced for the probability of layingfor brood reduction for the probability
194
80 ndash100 ndash80 ndash60 ndash40 ndash20 0 20 40 60 100
10 Marismillas11 Sanlucar pinewood
12 AbalarioCumulative total
1 RBD vera2 RBD interior
3 RBD sand dunes
Change in breeding numbers compared to the 1980s ()
Sector
4 Vera Algaida-Manecorro5 Interior6 Puntal
7 Coto del Rey8 NW pinewoods9 NE pinewoods
Fig 2 Percentage change in breeding numbers of the Dontildeana red kite popu-lation by sector from the 1980s or since the earliest available record (1990s for
Puntal and Abalario) to 2017 RBD Reserva Biologica de Dontildeana
Sergio et al Predator extinction debt in national park
of successful breeding and for the number of fledgedyoung (Fig 7)
On average the whole population was estimated toproduce 103 fledglings per year in the 1980s this al-most halved to 57 in the 1990s 48 in 2000minus2009 andagain declined to more than halved to 19 in 2010minus2017In 2015 2016 and 2017 the population produced 7 7and 15 fledglings respectively Population decline and
breeding deterioration were accompa-nied by a change in the relative impor-tance of some sectors for offspring pro-duction (Fig 5 Table 2) In the 1980smost young were produced in thesector RBD vera and the northernpinewoods and most other sectors stillcontributed gt5 of the annual youngproduction (Fig 5c) In subsequentdecades fledgling production becameconcentrated in the marsh ecotone(Puntal RBD vera vera of Algaida-Manecorro) with additional inputsfrom some interior or peripheral sectorsand a larger portion of sectors with vir-tually zero contribution to future gener-ations (Fig 5d) Fig 3 illustrates howdiffuse successful reproduction was inthe 1980s compared to 2017
35 Comparison with otherEuropean populations
Compared to other areas of Europethe Dontildeana population showed a highdensity in the 1980s (well above theEuropean mean Table S3) This pro-gressively declined and has changedto below-average density since 2010All breeding parameters were wellbelow the mean European estimatesfrom the 1980s onwards (Table S3) Inparticular the percentage of success-ful pairs and the number of youngfledged per breeding pair are cur-rently 2 to 3 times lower than themean European values
36 Population growth andprojections for the Dontildeana
population
Observed declines were well cap-tured by the growth rate predicted by the populationmodel based on the minimum European survivalrates (Fig 8) The other 2 scenarios of maximum andmean survival rates predicted a stable population ordeclines from the year 2000 onwards only (Fig 8)For the 2010s the model estimated λ = 0849 0960and 1066 for the scenario based on minimum meanand maximum survival estimates respectively
195
Fig 3 Distribution of breeding territories in Dontildeana (a) in the 1980s and (b) in2017 Pairs that bred successfully (black points) were much more frequent andmore widely distributed especially in the northern sectors and in the NaturalPark in the 1980s than in 2017 when most pairs failed to raise chicks to fledg-ing (white points) Territory locations have been moved slightly for conserva-tion reasons and locations from the 1980s could only be approximate for some
territories especially those in the northern pinewoods
Endang Species Res 38 189ndash204 2019
Based on the model with minimum survival rateswhich gave the best fit to past declines the popula-tion of 37 pairs censused in 2017 would be reduced to7 pairs within 10 yr and virtually extinct (le2 pairs) in17 yr The less supported scenario of mean Europeansurvival estimates projected a population of 25 pairsin 10 yr while the most optimistic scenario of maxi-mum survival predicted a full recovery to the 1980spopulation level of 70 pairs in 10 yr
Despite the current extremely lowbreeding success under all 3 scenar-ios of survival the population growthrate was least sensitive to changes infledglings production [E(F) = 0048minus0079 S(F) = 0137minus 0277] and mostsensitive to variations in adult survivalprobability [E(θ) = 0843minus 0904 S(θ) =0929minus 0955] In Fig 9 we plot thecombination of fledgling productionand adult survival that produce differ-ent levels of population growth Atcurrent levels of reproduction adultsurvival would have to be around090minus095 to attain a stable or slightlyincreasing population while restoringbreeding success to the levels of the1980s of 13 young per pair wouldimply a stable population even with arelatively low adult survival of ~077ie below the minimum ever recordedfor the species (Fig 9)
4 DISCUSSION
Our results showed that the currentdeteriorated condition of the Dontildeanared kite population was not a recentphenomenon but the tip of the ice-berg of decades of regional and localdegradation Although the protectedarea slowed the background levels ofregional decline and likely saved thespecies from local extinction its via-bility maintenance performance wasfar from satisfactory In a way the ob -served long-term deterioration actedas a protracted diluted form of extinc-tion debt (Tilman et al 1994) paidover a time-frame of several decadesWe suspect that similar conditionsmay be common in other protectedareas making this a classical example
of gradual underlying pressures diluted over such along time-frame that their severity becomes evidentonly through a large-scale long-term asses sment oronce population degradation has reached its extremeconsequences Note that for many parameters dete-rioration was not especially alarming from onedecade to the next making it difficult for the succes-sion of local field observers to appreciate the overallseverity of the long-term trends This difficulty in
196
Fig 4 Distribution range of red kites in Dontildeana (a) in the 1980s and (b) in2017 The pink outer polygon represents a 95 kernel constructed aroundthe territory locations while the red polygon is a 50 kernel showing the corearea of distribution The overall and core distribution range contracted by 534and 581 respectively Territory locations have been moved slightly for
conservation reasons
Sergio et al Predator extinction debt in national park 197
12
3 R
BD
4 V
era
56
7 C
oto
8 N
W9
NE
10
11
12
Tot
al
RB
DR
BD
san
dA
lgai
da
Inte
rior
Pu
nta
ld
elp
ine-
pin
e-M
aris
-S
anlu
car
Ab
alar
iod
ecli
ne
vera
inte
rior
du
nes
Man
ecor
roR
eyw
ood
sw
ood
sm
illa
sp
inew
ood
a) M
ean
no
of
pai
rs19
80minus
1989
141
52
33
40a
20a
80b
50
107
44
50
30
40b
687
1990
minus19
9915
35
11
37
74
08
03
34
40
74
5e2
5c4
0a60
8minus
115
2000
minus20
0916
05
21
47
05
06
31
01
00
14
5e2
03
1a52
5minus
236
2010
minus20
1713
03
42
56
63
98
41
90
50
13
01
72
147
1minus
315
2017
100
35
211
00
03
12
37minus
462
b)
No
of
you
ng
pro
du
ced
an
nu
ally
1980
minus19
8916
14
25
66
43
09
610
020
311
06
04
56
010
26
1990
minus19
999
82
60
68
44
06
92
46
60
95
13
86
056
9minus
445
2000
minus20
0913
21
61
27
25
83
71
21
60
24
53
04
647
7minus
535
2010
minus20
172
60
61
11
82
33
50
90
30
01
62
91
919
4minus
811
2017
10
03
07
00
00
22
150
minus85
4
c)
of
the
tota
l p
op
ula
tio
n i
n e
ach
sec
tor
1980
minus19
8920
57
64
85
82
911
67
315
56
47
34
45
819
90minus
1999
251
84
21
126
66
131
55
73
12
74
41
66
2000
minus20
0929
49
62
612
99
211
51
81
80
28
33
79
120
10minus
2017
276
72
53
141
82
178
40
11
03
64
36
45
2017
270
00
81
135
54
297
00
00
00
81
27
54
d)
c
on
trib
uti
on
of
each
sec
tor
to t
ota
l an
nu
al y
ou
ng
pro
du
ctio
n19
80minus
1989
157
41
54
94
62
29
97
198
107
58
44
58
1990
minus19
9917
24
61
112
114
77
04
211
61
68
96
610
520
00minus
2009
277
33
24
78
151
121
24
34
04
94
63
96
2010
minus20
1713
43
35
418
19
411
74
81
30
08
215
09
620
176
70
00
046
720
00
00
00
00
00
013
313
3
a Cro
ss-c
omb
ined
est
imat
e b
Sta
tic
bac
k-e
stim
ate
c In
terp
olat
ed e
stim
ate
See
Sec
tion
23
for
det
ails
Tab
le 2
(a
) M
ean
nu
mb
er o
f p
airs
an
d (
b)
cum
ula
tive
nu
mb
er o
f of
fsp
rin
g p
rod
uce
d a
nn
ual
ly b
y th
e D
ontildean
a re
d k
ite
pop
ula
tion
wit
hin
eac
h s
ecto
r an
d i
n t
he
wh
ole
par
k o
ver
the
pas
t d
ecad
es a
nd
in 2
017
Per
cen
tag
e of
(c)
pai
rs a
nd
(d
) yo
un
g c
ontr
ibu
ted
by
each
sec
tor
to t
he
over
all p
opu
lati
on S
ecto
rs c
ontr
ibu
tin
g m
ore
than
10
ar
e h
igh
lig
hte
d i
n b
old
T
otal
ref
ers
to t
he
sum
of
all
sect
ors
d
ecli
ne
is t
he
dec
lin
e co
mp
ared
to
the
1980
s P
rop
orti
onal
con
trib
uti
ons
are
also
ill
ust
rate
d i
n F
ig
5
RB
D R
eser
va B
iolo
gic
a d
e D
ontildean
a
Endang Species Res 38 189ndash204 2019
detecting the problem was likely exacerbated by thefollowing factors that could be defined as lsquoperceptionobstaclesrsquo (1) The fact that a population becomesmore and more restricted to a park is often used toillustrate the positive role of protected areas byfocusing their performance assessments on range
coverage ie the capability of protected areas tocover a large portion of a species range (eg Czech2005 Godet et al 2007) This diverts attention fromthe wider problems of range contraction and from theactual performance of the park in terms of viabilitymaintenance (Gaston et al 2008) (2) Confinement to
198
of nests in each sector
of annual young generated by each sector
1980s 2010s
1980s 2010s
a) b)
c) d)
Fig 5 Percentage of the total red kite population in each of 12 sectors of Dontildeana (a) in the 1980s and (b) in the 2010s percent-age of the annual young production generated by each sector (c) in the 1980s and (d) in the 2010s (a) In the 1980s the bulk ofthe population was concentrated in northern sectors (7 and 8) and in the southern shores of the marshes (sectors 1 6 and 10)(b) In the 2010s the population virtually disappeared from the northern sectors and became essentially confined to the na-tional park where it concentrated along the marshes (c) In the 1980s the population generated more than 100 young eachyear most of them produced by the northern sectors (7 8 9) and by the northern shores of the marshes (sectors 1 and 4) (d) Inthe 2010s the population generated less than 10 young mostly generated close to wetlands (sectors 1 4 11) with homo -geneously low numbers elsewhere Colors (yellow rarr orange rarr red) classify sectors by tertiles of the range of percentage
contribution
Sergio et al Predator extinction debt in national park
a protected area is usually accompanied by the auto-matic presumption that this will act as a source areawith limited anthropogenic impacts an assumptionthat is increasingly disproved (Hansen amp DeFries2007 Gaston et al 2008 Watson et al 2014) (3) Long-term assessments such as ours required the lengthy
collation of fragmented informationfrom a large number of sequentialfield workers and administrationseach of which had a very limited per-ception of the overall situation (4)Much monitoring was conducted inthe core areas of the park like theRBD where the species has alwaysbeen most abundant and relativelystable (eg Sergio et al 2005) con-fusing the perception of broaderdeclines (5) Finally large numbersof wintering migrants boost the pop-ulation in the winter and earlyspring often producing an optimisticimpression of apparent abundance
even in relatively expert members of the public or oflocal administrations as we frequently noted in pub-lic talks and private conversations
Overall the decline occurred at multiple levels redkites were originally widespread throughout south-ern Spain (Loacutepez 1861) but became progressively
199
2030405060708090
100110
Bree
ding
su
cces
sful
()
a breeding pairs successful pairs
202122232425262728
Clut
ch si
ze
b
25
35
45
55
65
75
85
1970-79 1980-89 1990-99 2000-09 2010-17
Hatc
hing
succ
ess
broo
d re
duct
ion
()
Decade
c Hatching successBrood reduction
03
06
09
12
15
18
21
1970-79 1980-89 1990-99 2000-09 2010-17
Youn
g fle
dged
Decade
d Young breeding pairYoung successful pair
Fig 6 Reproductive parameters of the red kite population of Dontildeana (a) percentage of pairs laying eggs (black dots n = 804)and successfully raising fledglings (white dots n = 1185) (b) mean clutch size (n = 469) (c) hatching success (percentage ofeggs that hatched black dots n = 353) and brood reduction (percentage of chicks that disappeared during the nestling periodwhite dots n = 240) (d) mean number of young fledged per territorial pair (black dots n = 1145) and per successful pair (white
dots n = 576)
0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75
Young fledgedsuccessful pairYoung fledgedbreeding pairYoung fledgedterritorial pair
Probability of successful breedingBrood reduction
Hatching successClutch size
Probability of laying
Deterioration ()
Breeding parameter
Fig 7 Percentage deterioration of breeding parameters of the red kite popu-lation of Dontildeana between the 1980s and the 2010s
Endang Species Res 38 189ndash204 2019
confined to the protected area of Dontildeana in recentdecades However the park did not confer automaticsafety and declines and range contraction also con-tinued within the protected area suggesting perva-sive pressures and range erosion at multiple spatialscales In particular almost one third of the Dontildeana
population was virtually eradicatedfrom the northern pinewoods of thebuffering Natural Park in 5 to 7 yrbetween the late 1980s and early1990s Several lines of evidence sug-gest that illegal poisoning was themain cause of this eradication (1) Sev-eral adults were found poisoned undertheir nest in those sectors and years(2) Large-scale poisoning campaignsof raptors were reported throughoutSpain in those exact same years asa consequence of huntersrsquo illegalattempts to control predator popula-tions to increase the rapidly deterio-rating numbers of small game (rabbitsand partridges Villafuerte et al 1998Vintildeuela amp Villafuerte 2003 Cano et al2008) In this sense the National Parksuffered much wider national-level
pressures (3) The northern sectors of the parkwhere the eradication took place included or wereclose to private small-game reserves and predatorcontrol was well known to occur in some of them (4)Finally the rapidity of the eradication of such a long-lived species (maximum longevity of 29 yr in Dontilde -ana) implied a causative agent that directly affectedadult mortality (Saether amp Bakke 2000) such as poi-soning The marked impact of poisoning on adult sur-vival and population growth are well recognized forthis species whose facultative scavenging habits andforaging method of meticulous low and slow quar-tering of the ground make it particularly sensitive tothis threat (Smart et al 2010 Tavecchia et al 2012Tenan et al 2012 Sanz-Aguilar et al 2015)
Spikes of rapid local eradication were superim-posed on more gradual but steady deterioration ofoffspring production Gradual and continuous ratherthan sudden degradation of performance suggestedthat poisoning was not the only threat in effect Inthis context several factors may have contributed togradually deteriorate ecological conditions for kitesin recent decades (1) Rabbit epidemics have causedprogressive declines in the availability of this keyprey (Vintildeuela amp Villafuerte 2003) (2) Lower preyavailability may have exacerbated competition withthe dense populations of other raptors with similardiets such as the ecologically similar and in creasingblack kite (3) Predation rates on adults and nestlingsmay have increased with the expansion of the popu-lations of potential predators such as eagle owls Bubobubo and goshawks Accipiter gentilis (4) Recentassessments have detected alarming levels of toxic
200
00
02
04
06
08
10
12
1980sndash1990s 1990sndash2000s 2000sndash2010s
Popu
latio
n gr
owth
rate
Period
Observed populationgrowth
Scenario 1 minimumEuropean survival
Scenario 2 meanEuropean survival
Scenario 3 maximumEuropean survival
Fig 8 Population growth of the Dontildeana red kite population during the past 4decades as predicted by matrix demographic models based on 3 scenarioswhich assumed that survival was equal to minimum mean or maximum sur-vival rates reported for other European populations (reviewed in Table 1)Predicted values are compared with observed declines from one decade to
the next
Fig 9 Population growth rate of red kites in relation to adultsurvival and breeding performance (mean number of youngfledged per territorial pair) based on a matrix populationmodel Note that the graph could be applied to any Euro-pean population The 3 points at the base of the graph repre-sent the minimum (black) mean (grey) and maximum (blue)survival published for European populations (reviewed in
Table 1)
Sergio et al Predator extinction debt in national park
chemicals in red kite eggs from Dontildeana (Goacutemara etal 2008) (5) Climate change and agricultural man-agement have lowered the water table with likelyimpacts on marsh inundation levels and aquatic prey(Garciacutea Novo amp Mariacuten Cabrera 2005 Diacuteaz-Paniaguaamp Aragoneacutes 2015 Schmidt et al 2017) (6) Conver-sion to intensive farmland in surrounding lands haseroded habitat and prey availability outside the pro-tected area which may have buffered kites fromperiods of low prey availability within the park (egduring droughts in the marshes) Some of the pat-terns of observed reproductive deterioration lendsupport to some of these impacts For exampledeclining clutch sizes and increasing rates of broodreduction suggest that food was not sufficient to sus-tain earlier reproductive levels while lowered hatch-ing success is often the result of chemical contamina-tion in raptors (review in Newton 1979) While eachof these threats will be quantitatively investigated indetail in the immediate future in the present contextthey illustrate the frequent and complex challengesfaced by (1) protected areas in maintaining biodiver-sity and viable populations of imperiled species and(2) conservation biologists in identifying causes ofdecline for subsequent management interventioneven in lsquoprivilegedrsquo sites such as reserves
Redistribution declining numbers and perform-ance had important repercussions for future viability(1) The population passed from producing gt100annual young to lt10minus20 which will make mainte-nance and recovery difficult (2) These young wereincreasingly produced in the core sectors of themarsh-ecotone within the National Park which prob-ably increased the dependence of the population onmarsh inundation in turn affected by problems oper-ating outside the park (Garciacutea Novo amp Mariacuten Cabrera2005 Diacuteaz-Paniagua amp Aragoneacutes 2015 Schmidt et al2017) (3) Steep declines in the percentage of suc-cessful pairs implied that future generations wereproduced by a progressively more restricted numberof pairs which will make the population more sub-ject to inbreeding and stochastic events For exam-ple in the last 3 yr all the annual young were pro-duced by 6 8 and 9 pairs respectively suggesting aneffective population size 4 to 9 times lower than theoverall abundance
Given all the above it is no surprise that demo-graphic models suggested a negative growth and apopulation incapable of self-sustenance In particu-lar the model that gave the best fit to past observeddeclines was the one based on minimum Europeansurvival estimates followed by the scenario based onmean European survival estimates Given the above-
mentioned threats declines and performance deteri-oration we would expect survival to be closer to min-imum than mean European levels as supported bythe observed fit to past and recent declines Theseresults have 2 main implications (1) If survival is aslow as we suspect demographic models predict vir-tual extinction within a few years demanding anurgent need for identification and management ofmortality threats as well as quantification of actualsurvival to refine predictions Note that virtual ex -tinction could be even earlier when taking intoaccount effective rather than total population sizeand a stochastic rather than deterministic populationmodel (2) Should actual survival be confirmed lowbut further declines not observed the populationwould be a sink sustained by external sources whichwould make it even more at risk from anthropogenicthreats outside the park and thus more challengingto manage (eg Hansen amp DeFries 2007 Blanco et al2017)
5 Conclusions and implications for conservation
The decades-long degradation that we depictedwas likely generated by a combination of factorsboth internal to the park (eg rabbit availabilitymarsh inundation rates predation and competitionwith other species) and external (eg illegal poi-soning contamination farmland intensification)Some of them will be amenable to managementand others less so but the first priority will be tofind rapid ways to identify the key factors thatdrive population growth so as to optimize conserva-tion action before it is too late For example focus-ing conservation lsquoblindlyrsquo on supplementary feedingcould be useless if the problem is chemical contam-ination The quickest way to obtain such informa-tion would be a satelliteGSM (Global System forMobile communication) tagging program that wouldallow to (1) obtain rapid estimates of health andsurvival for young and adults (eg Sergio et al2019) so as to recalibrate future projections andgoals (2) assess the relative contribution of mainmortality causes which is an essential first step inany recovery program (eg Gonzaacutelez et al 2007Margalida et al 2008 Smart et al 2010) and (3)identify the areas used by breeding and non-breed-ing individuals inside and outside of the park toassess their risk-exposure and intervene before orafter death (eg to prosecute perpetrators of illegalpoisoning or re trofit dangerous electricity pylons inareas of high use by kites)
201
Endang Species Res 38 189ndash204 2019
Until this information becomes available below welist some tentative figures and priorities for conserva-tion First of all restoring the current population toformer levels would undoubtedly be challenging andprobably unrealistic given the profound changesincurred by the wider Dontildeana ecosystem in recentdecades Thus we propose an initial target of 60pairs as a long-term restoration goal Elasticity analy-sis suggested that optimal management should focuson improving adult survival which had the largestimpact on population growth as in other long-livedspecies (Saether amp Bakke 2000 Whitfield et al 2004Kruumlger et al 2010) This could be attempted by in -creasing food availability especially of key prey suchas rabbits and by curtailing mortality threats such asillegal poisoning which still continues despite mucheffort to eradicate it by the local administration Thetelemetry program outlined above could help toidentify local perpetrators as occurred in other pop-ulations (Smart et al 2010 Tavecchia et al 2012) Onthe other hand despite their low elasticities repro-ductive rates are currently so low that it would befundamental to increase them eg by increasingfood availability and ensuring proper inundation ofthe marshes Based on Fig 5 we propose as initialtargets for restoration (1) survival rates equal orhigher than the European mean (adult survivalge087) and (2) a number of young fledged per territo-rial pair above 10 which would produce an increas-ing population provided that adult survival is equalto or above the European mean Note that Fig 5could be applied to any European population as atool to check its potential viability Given the highlythreatened status of red kites the speciesrsquo limitedrange confined to Europe and its ongoing declinesviability assessments such as ours may sadly becomemore important for the management and recovery ofmany populations
In conclusion red kites would probably be extinctin southern Spain without the institution of a largenational park In this sense this example well illus-trates how protected areas will continue to be corner-stones of global conservation of threatened taxaHowever their safety is not ensured by park institu-tion per se and performance monitoring and focusedaction will be needed to avoid potential extinctiondebts which may be more protracted than previouslyappreciated In our exemplary case despite the pres-ence of a large national park on prime fertile landwithin a developed country with adequate institu-tional and financial support a key threatened speciessuffered latent but steady declines for decadesobscured by problems of perception lack and frag-
mentation of information and likely caused by acomplex array of within-park threats and growingexternal pressures Viability maintenance and recov-ery will probably require concerted actions withinand outside of the park but only after detailed infor-mation on crucial aspects becomes available whichis probably the most urgent current priority We sus-pect that dynamics like the ones illustrated here aremore common than currently appreciated and willbecome more widespread as anthropogenic pres-sures increase around protected areas and as theirperformance monitoring becomes more prevalent
Acknowledgements We thank all the (too many to mention)researchers field workers visitors volunteers gamekeep-ers park managers and wardens that have provided datasince the 1960s In particular we thank F G Vilches L Gar-ciacutea and the Equipo de Seguimiento de Procesos Naturales ofthe Estacioacuten Bioloacutegica de Dontildeana-CSIC for help in the fieldSpecial thanks to F G Vilches for the priceless help with thecollation and organization of historical information Wethank J P Castellano I Redondo and all the lsquoArea de Con-servacioacutenrsquo of Dontildeana National Park for constant interest andsupport We thank R Cadenas J Madrid R Arenas J RBenitez and all the pertinent personnel of the Consejeriacutea deMedio Ambiente of the Junta de Andaluciacutea for informationon current nest locations in the Sierra de Huelva and fortheir constant attentive support We are grateful to Dr NBunnefeld and 2 anonymous reviewers for constructivecomments that improved the manuscript This study wasfunded by the Foundation Jaime Gonzaacutelez-Gordon and bythe research project 16022015 of the Spanish Ministry ofAgriculture Food and the Environment (National ParksAutonomous Agency)
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Brashares JS Arcese P Sam MK (2001) Human demographyand reserve size predict wildlife extinction in WestAfrica Proc Biol Sci 268 2473minus2478
Bustamante J (1993) Post-fledging dependence period anddevelopment of flight and hunting behaviour in the redkite Milvus milvus Bird Study 40 181minus188
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Caswell H (2001) Matrix population models Sinauer Sun-derland MA
Ceballos JJ Guimeraacute VM (1992) Guiacutea de las aves de Jerez yde la Provincia de Caacutediz atlas ornitoloacutegico de lasespecies nidificantes Ayuntamiento de Jerez Jerez
Craigie ID Baillie JEM Balmford A Carbone C Collen BGreen RE Hutton JM (2010) Large mammal population
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declines in Africarsquos protected areas Biol Conserv 143 2221minus2228
Czech B (2005) The capacity of the National WildlifeRefuge System to conserve threatened and endangeredanimal species in the United States Conserv Biol 19 1246minus1253
Delibes M Garciacutea L (1984) Haacutebitos alimenticios del milanoreal en Dontildeana durante el periodo de criacutea Ardeola 31 115minus121
Diacuteaz-Paniagua C Aragoneacutes D (2015) Permanent and tempo-rary ponds in Dontildeana National Park (SW Spain) arethreatened by desiccation Limnetica 34 407minus424
Evans IM Summers RW OrsquoToole L Orr-Ewing DC Snell NSmith J (1999) Evaluating the success of translocatingred kites Milvus milvus to the UK Bird Study 46 129minus144
Ferrer M Hiraldo F (1991) Evaluation of management tech-niques for the Spanish imperial eagle Wildl Soc Bull 19 436minus442
Garciacutea Novo F Mariacuten Cabrera C (2005) Dontildeana water andbiosphere Dontildeana 2005 Project Spanish Ministry of theEnvironment Madrid
Gaston KJ Jackson SF Cantuacute-Salazar L Cruz-Pintildeoacuten G(2008) The ecological performance of protected areasAnnu Rev Ecol Evol Syst 39 93minus113
Godet L Devictor V Jiguet F (2007) Estimating relative pop-ulation size included within protected areas BiodiversConserv 16 2587minus2598
Goacutemara B Gonzaacutelez MJ Baos R Hiraldo F Abad E RiveraJ Jimeacutenez B (2008) Unexpected high PCB and total DDTlevels in the breeding population of red kite (Milvus mil-vus) from Dontildeana National Park south-western SpainEnviron Int 34 73minus78
Gonzaacutelez LM Margalida A Mantildeosa S Saacutenchez R and oth-ers (2007) Causes and spatio-temporal variations of non-natural mortality in the vulnerable Spanish imperialeagle Aquila adalberti during a recovery period Oryx41 495minus502
Hansen AJ DeFries R (2007) Ecological mechanisms linkingprotected areas to surrounding lands Ecol Appl 17 974minus988
Hernaacutendez FJ Donaacutezar JA Hiraldo F (2001) Evaluacioacuten deluso de venenos para el control de predadores en laComunidad Autoacutenoma Andaluza y su impacto en la con-servacioacuten de especies amenazadas de vertebrados Con-sejeria de Medio Ambiente and Estacioacuten Bioloacutegica deDontildeana Sevilla
IUCN (The World Conservation Union) (1994) Guidelines forprotected area management categories IUCN Gland
Knott J Newbery P Barov B (2009) Action plan for the redkite Milvus milvus in the European Union EuropeanCommission Brussels
Kruumlger O Gruumlnkorn T Struwe-Juhl B (2010) The return ofthe white-tailed eagle (Haliaeetus albicilla) to northernGermany modelling the past to predict the future BiolConserv 143 710minus721
Loacutepez V (1861) Cataacutelogo de las aves observadas enAndaluciacutea Madrid
Loacutepez G and others (2009) Management measures to controla feline leukemia virus outbreak in the endangered Iber-ian lynx Anim Conserv 12 173minus182
Margalida A Heredia R Razin M Hernaacutendez M (2008)Sources of variation in mortality of the bearded vultureGypaetus barbatus in Europe Bird Conserv Int 18 1minus10
Naughton-Treves L Holland MB Brandon K (2005) The roleof protected areas in conserving biodiversity and sustain-
ing local livelihoods Annu Rev Environ Resour 30 219minus252
Newton I (1979) Population ecology of raptors T amp AD PoyserBerkhamsted
Newton I Davis PE Davis JE (1989) Age of first breedingdispersal and survival of red kites Milvus milvus inWales Ibis 131 16minus21
Otero C Castieacuten E Senosiaiacuten R Portillo F (1978) Fauna deCazorla vertebrados Publicaciones del Ministerio deAgricultura Madrid
Parks SA Harcourt AH (2002) Reserve size local humandensity and mammalian extinctions in US protectedareas Conserv Biol 16 800minus808
R Development Core Team (2018) R a language and envi-ronment for statistical computing R Foundation for Sta-tistical Computing Vienna wwwr-projectorg
Saeligther BE Bakke Oslash (2000) Avian life history variation andcontribution of demographic traits to the populationgrowth rate Ecology 81 642minus653
Sanz-Aguilar A De Pablo F Donaacutezar JA (2015) Age-depen-dent survival of island vs mainland populations of twoavian scavengers delving into migration costs Oecolo-gia 179 405minus414
Schaub M (2012) Spatial distribution of wind turbines is cru-cial for the survival of red kite populations Biol Conserv155 111minus118
Schmidt G Saacutenchez Navarro R Hernaacutendez E Carmona JJFuentelsaz F Seiz R (2017) The state of water in Dontildeana an evaluation of the state of the water and of the ecosys-tems of the protected space WWFAdena Madrid
Scott JM Davis FW McGhie RG Wright RG Groves CEstes J (2001) Nature reserves Do they capture the fullrange of Americarsquos biological diversity Ecol Appl 11 999minus1007
Seoane J Vintildeuela J Diacuteaz-Delgado R Bustamante J (2003)The effects of land use and climate on red kite distribu-tion in the Iberian peninsula Biol Conserv 111 401minus414
Sergio F Blas J Feroro M Fernaacutendez N Donaacutezar JAHiraldo F (2005) Preservation of wide-ranging top pred-ators by site-protection black and red kites in DontildeanaNational Park Biol Conserv 125 11minus21
Sergio F Tanferna A Blas J Blanco G Hiraldo F (2019) Reli-able methods for identifying animal deaths in GPS- andsatellite-tracking data review testing and calibrationJ Appl Ecol 56562ndash572
Smart J Amar A Sim IMW Etheridge B Cameron DChristie G Wilson JD (2010) Illegal killing slows popula-tion recovery of a re-introduced raptor of high conserva-tion concern mdash the red kite Milvus milvus Biol Conserv143 1278minus1286
Tavecchia G Adrover J Muntildeoz Navarro A Pradel R (2012)Modelling mortality causes in longitudinal data in thepresence of tag loss application to raptor poisoning andelectrocution J Appl Ecol 49 297minus305
Tenan S Adrover J Muntildeoz Navarro A Sergio F TavecchiaG (2012) Demographic consequences of poison-relatedmortality in a threatened bird of prey PLOS ONE 7 e49187
Tilman D May RM Lehman CL Nowak MA (1994) Habitatdestruction and the extinction debt Nature 371 65minus66
Torres Esquivias JA Jordano P Leoacuten A (1981) Aves de presadiurnas de la provincia de Coacuterdoba Publicaciones CA yMP Coacuterdoba
Veiga JP Hiraldo F (1990) Food habits and the survival andgrowth of nestlings in two sympatric kites (Milvus milvus
203
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and Milvus migrans) Holarct Ecol 13 62minus71 Villafuerte R Vintildeuela J Blanco JC (1998) Extensive preda-
tor persecution caused by population crash in a gamespecies the case of red kites and rabbits in Spain BiolConserv 84 181minus188
Vintildeuela J (2004) Milano real Milvus milvus In Madrontildeo AGonzaacutelez C Atienza JC (eds) Libro rojo de las aves deEspantildea Direccioacuten General para la BiodiversidadminusSEOBirdLife Madrid p 120minus125
Vintildeuela J Villafuerte R (2003) Predators and rabbits (Oryc-tolagus cuniculus) in Spain a key conflict for Europeanraptor conservation In Thompson DBA Redpath SMFielding AH Marquiss M Galbraith CA (eds) Birds ofprey in a changing environment The Stationery OfficeEdinburgh p 511minus526
Vintildeuela J Martiacute R Ruiz A (eds) (1999) El milano real enEspantildea SEOBirdlife Madrid
Watson JEM Dudley N Segan DB Hockings M (2014) Theperformance and potential of protected areas Nature515 67minus73
Whitfield SM Bell KE Philippi T Sasa M and others (2007)Amphibian and reptile declines over 35 years at La SelvaCosta Rica Proc Natl Acad Sci USA 104 8352minus8356
Whitfield DP Fielding AH McLeod DRA Haworth PF(2004) Modelling the effects of persecution on the popu-lation dynamics of golden eagles in Scotland Biol Con-serv 119 319minus333
Zuur A Ieno EN Walker N Saveliev AA Smith GM (2009)Mixed effects models and extensions in ecology with RSpringer New York NY
204
Editorial responsibility Nils BunnefeldStirling UK
Submitted October 8 2018 Accepted January 28 2019Proofs received from author(s) April 7 2019
Sergio et al Predator extinction debt in national park
ter and progressively drying during the springminus summer (2) scrubland a mixture of different degra-dation stages of autochthonous Mediterranean scrub -land (3) sparse grassland mainly located along theinterface between Mediterranean scrubland and themarshes (hereafter lsquoverarsquo) (4) mobile sand dunesalong the ocean shore and (5) stone pine (Pinuspinea) plantations Mature trees suitable for nestingkites are mainly present in the latter pinewoods andas isolated or small clumps of cork oaks Quercussuber and Eucalyptus trees The portions of the Nat-ural Park relevant for breeding kites are mainly thenorthern and eastern sectors of extensive pinewoodssurrounded by intensive farmland All farmland inand around Dontildeana has become progressively moreintensive especially with the spread of strawberrycultivation since the 1990s
22 Field procedures
Kite territories were censused by looking at territo-rial displays nest material transfers and presence ofbirds perched multiple times in or near their nest dur-ing pre-incubation in FebruaryminusMarch Wheneverpossible nest contents were checked at least 3 times(1) during incubation to assess clutch size (2) justafter hatching to estimate hatching success andbrood size and (3) when the nestlings were ~45 d oldto record the number of reared young (nestlingsfledge at ~55 d Bustamante 1993) Because kites areextremely vulnerable to poisoned baits (Villafuerte etal 1998 Vintildeuela et al 1999) we collected all avail-able data on kites found poisoned in Dontildeana Theseincluded (1) individuals reported to local authoritiesand confirmed as poisoned by subsequent eco-toxi-cological analysis and (2) individuals found dead inor under the nest Based on post-mortem chemical ana -lyses such cases are extremely likely to be caused bypoisoning (details in Hernaacutendez et al 2001)
23 Historical information
Kites were intensively surveyed until being rea-sonably sure to have detected the territorial pairs ofthe whole park since 2012 in collaboration with thepark authority and the Equipo de Seguimiento deProcesos Naturales of the Estacioacuten Bioloacutegica deDontildeana-CSIC (EBD-CSIC) which together surveyedthe peripheral sectors of Marismillas Sanlucarpinewood and Abalario (Fig S1) Before that inten-sive research on red kites was conducted in Dontildeana
in the 1980s and 1990s by a group led by F Hiraldoand subsequently by a group led by F Sergio and FHiraldo (eg Veiga amp Hiraldo 1990 Sergio et al2005) Work by these research groups focused espe-cially on certain portions of the park and thus inte-grated extensive information provided by (1) theEquipo de Seguimiento de Procesos Naturales of theEBD-CSIC (2) the Grupo de Conservacioacuten of Dontilde -ana National Park and (3) the field diaries of dozensof researchers field workers visitors volunteersgamekeepers park managers and wardens active inDontildeana since the 1960s Integrating all these sourcesespecially old field diaries from the 1960sminus 70srequired 2 yr of careful screening of locational infor-mation For example two different field ob serverssometimes visited the same territory in the same yearbut referred to the site using different local nameswhich often required meticulous diary inspection toreconstruct the route travelled by each observer onthat day In most years the census was not availablefor the whole park and the well surveyed sectors var-ied among years depending on research priorities orthe area of action of specific observers (eg wardensor field technicians deputed to certain sectors insome years and others in subsequent years) Becauseof such fragmented surveys we estimated the totalDontildeana population by decade as follows (1) wedivided the park into 12 sectors (Fig 1b) These weredefined on the basis of major differences in land-scape composition relevant for kite ecology (egextensive pinewoods and farmland in the north of thepark vs marsh ecotone in the park center) and delin-eations of private properties be cause these oftencaused abrupt management- driven differences inlandscape and because field workers were oftenassigned to survey whole properties in differentyears (2) For each well surveyed sector we calcu-lated the mean number of pairs per year for eachdecade (3) For each decade we summed up thesemean values to obtain a cumulative estimate for thatdecade (4) In the few cases in which the first com-plete survey of a sector was carried out late (eg inthe 1990s) we assumed that the population was stable in earlier decades (hereafter lsquostatic back- estimatesrsquo) This was done in order to enable a com-plete estimate of the whole population through alldecades and produced conservative estimates ofdeclines (5) In the few cases when complete surveysof a sector were not available for a given decade butthey were for earlier and later decades these wereinterpolated to estimate the missing value (hereafterlsquointerpolated estimatesrsquo) Finally (6) in a few periph-eral sectors complete surveys were available for cer-
191
Endang Species Res 38 189ndash204 2019
tain portions of a sector in some years and other por-tions in different subsequent years In these cases wecalculated the mean number of pairs yrminus1 decademinus1 foreach subsector when well surveyed and summed upthese means to obtain a cumulative estimate de -cademinus1 for the whole sector (hereafter lsquocross-combinedestimatesrsquo) In all procedures above we ensured thatall alternative nests belonging to the same territorywere included within the same sector or subsector inorder to avoid biases caused by re-counting the sameterritory twice when combining different surveyunits Similarly in all cases of doubt we used the
estimate that minimized the historicalpopulation in order to provide conser-vative estimates of decline
To place declines and the potentialstrategic importance of the parkwithin a wider regional context wereconstructed the distribution andpopulation levels of the kite popula-tion for southern Spain (AndaluciacuteaAutonomous Region 87 268 km2) inthe 1970sminus1980s based on informa-tion found in Otero et al (1978) TorresEsquivias et al (1981) Ceballos ampGuimeraacute (1992) Vintildeuela et al (1999)Vintildeuela (2004) and conversationswith local experts Data for the currentred kite population outside Dontildeanawere provided by the Consejeriacutea deMedio Ambiente of the AndaluciacuteaAutonomous Region
24 Statistical analyses
To investigate how generalized thehistorical population declines acrossdifferent sectors of the park were weestimated whether the subpopulationof each sector increased or declinedbetween the earliest available surveyand the 2010s and then tested whetherdeclines were prevalent over stable orincreasing trends by means of a bino-mial test To explore temporal trendsin breeding rates we fitted general-ized linear models (GLMs) with de -cade sector and their interaction asexplanatory variables and with thelikelihood of laying eggs clutch sizehatching success brood reductionthe likelihood of successfully raising
chicks to fledgling and the number of young fledgedper territorial breeding and successful pair as re -sponse variables (Zuur et al 2009) In the aboveanalyses hatching success was defined as the pro-portion of eggs that hatched brood reduction was theproportion of hatched chicks lost before fledging aterritorial pair was one that held a territory a breed-ing pair one that laid at least 1 egg and a successfulpair one that raised at least 1 nestling to fledging age(gt45 d) In particular the likelihood of laying eggsand raising chicks to fledging were examinedthrough GLMs with binomial errors and a logit link
192
Fig 1 Approximate distribution range of the red kite in southern Spain (An-daluciacutea Autonomous Region) (a) in the 1980s (reconstructed on the basis ofsources cited in Section 23) compared to (b) the distribution as recorded in2017 The red sectors in (a) represent (1) the marshes of Dontildeana and Odiel inthe provinces of Huelva and Sevilla (2) the hills and low mountains of SierraMorena in the provinces of Huelva Sevilla and Cordoba and (3) the mountain
complex of Cazorla in the provinces of Granada and Jaeacuten
Sergio et al Predator extinction debt in national park
function while clutch size and the number of fledgedyoung were modelled through GLMs with Poissonerrors and a log link function Finally hatching suc-cess and brood reduction were modelled by GLMswith Poisson errors and a log link function using thenumber of hatched eggs and the number of disap-peared chicks as response variables and clutch sizeand brood size at hatching as offset variables (Zuur etal 2009)
The current expected growth of the Dontildeana popu-lation was estimated by building an age-structureddemographic model (Caswell 2001) M based on theage-dependent values of survival (see below) and themean fertility recorded over the last 5 yr in Dontildeana(0294 young per territorial pair) The matrix Mdescribes the transition of the population between 2consecutive years t and t+1 The asymptotic popula-tion growth λ is calculated as the dominant eigen-value of M (Caswell 2001) In a stable population λ isequal to 1 while lower values indicate a decliningtrend Because survival estimates were not availablefor the Dontildeana population we applied values pub-lished for other European populations (reviewed inTable 1) In all studies survival has been reported for3 age classes 1 yr 2 yr and adult (ge3 yr) so we main-tained the same age classes in the current assess-ment In particular to explore the whole range of sur-vival scenarios potentially experienced by ourpopulation we built 3 separate deterministic matrixmodels based on the minimum average and maxi-mum survival rates reported for other European pop-ulations respectively (Table 1) These exploratoryanalyses were conducted with deterministic modelsbecause uncertainty on parameter estimates de -pended largely on the population considered Wefurther assumed a 11 sex ratio and that all kites hadentered the breeding population by 3 yr of age
Based on the obtained λ we then projected the pop-ulation over the next 10minus20 yr assuming no densitydependence to explore its potential short-term via-bility or extinction over the coming decades Becauseof the assumptions outlined above and the parame-ters taken from other populations these projectionsshould be taken with caution and recalibrated asmore local data become available
Finally we used perturbation analyses to calcu-late the sensitivity S(θ) and elasticity E(θ) of thepopulation growth rate to a given parameter θ(Caswell 2001) Sensitivity is the change in pop -ulation growth rate in response to an absolutechange of a given parameter θ while elasticity isthe change in the population growth rate in re -sponse to a proportional change of a given param-eter θ Throughout all analyses were implementedwith R version 351 (R Development Core Team2018) using the libraries lsquopopbiorsquo and lsquolme4rsquoResults are given as means plusmn 1SE tests are 2-tailed and statistical significance was set at α le005
3 RESULTS
31 Regional distribution and the strategicimportance of the protected area
Red kites must originally have been common be -low 400minus600 m of elevation throughout Andaluciacuteawhich traditionally hosted a dense and well distrib-uted rabbit population as an important prey base(Loacutepez 1861) By the 1970sminus1980s legal and thenillegal shooting and poisoning had reduced the pop-ulation to 3 main nuclei (Fig 1a) (1) the marshes ofDontildeana and Odiel in the provinces of Huelva and
Sevilla (2) the hills and low moun-tains of Sierra Morena in theprovinces of Huelva Sevilla and Cor-doba and (3) the mountain complexof Cazorla in the provinces ofGranada and Jaeacuten The latter 2 nucleiwere reported as lsquoin steep declinersquo ordocumented as already extinct in the1990s (Vintildeuela et al 1999 Vintildeuela2004) so that the current regionalpopulation is virtually confined toDontildeana with 3 additional relict pairslocated in the Sierra de Huelva(Fig 1b) The nuclei outside the pro-tected area of Dontildeana were estimatedto ıhave suffered a 95 decline since
193
Area Age class Reference1 yr 2 yr ge 3 yr
England Midlands 080 094 093 Evans et al (1999)Scotland 037 072 087 Smart et al (2010)Wales uplands 060 079 094 Newton et al (1989)Switzerland 045 074 084 Schaub (2012)Spain Mallorca 072 082 079 Tavecchia et al (2012)Spain Menorca 054 083 084 Sanz Aguilar et al (2015)
Min European estimates 037 072 079Mean European estimates 058 081 087Max European estimates 080 094 094
Table 1 Published estimates of red kite survival by age class Minimum meanand maximum levels were used to set up different demographic scenarios for
matrix population models
Endang Species Res 38 189ndash204 2019
the 1970sminus1980s (from a conservative estimate of40minus77 pairs to 2minus4 current pairs) Thus Dontildeanahosted 52minus63 of the regional population in the1970sminus80s and 95minus96 after 2010 increasing its rel-ative strategic importance
32 Abundance and trends in Dontildeana
Different sectors of the park showed differenttrends (Fig 2 Fig S2) Numbers appeared (1) stableor in moderate decline in the Reserva Biologica deDontildeana RBD (sectors 1 2 and 3) (2) stable or increas-ing in the sector of Puntal and in the vera of Algaida-Manecorro as well as its interior These areas werecharacterized by the removal of Eucalyptus planta-tions that converted large areas of woodland to opengrassland in the 1990s (sectors 4 and 5) or alwaysmaintained a very open landscape through extensivegrazing by livestock (sector 6) Finally (3) declines ofvarying magnitude were observed in all peripheralsectors to the north east and south While declineswere moderate in the eastern and southern sectorsthat were monitored less continuously dramatic de -clines were evident for all the northern sectors in -cluding portions of the National Park and its buffer-ing Natural Park In these sectors (7 8 9) a populationof 20minus25 pairs was basically eradicated in a few yearsbetween the late 1980s and early 1990s re mainingvirtually extinct to date (Fig 3) This rapid eradica-tion was accompanied by the detection of adultsfound dead by poisoning in or under their nest Over-all there was a significant preponderance of declinesbetween the numbers re corded in the earliest survey
available for each sector and the 2010s (binomial testp lt 0001 Fig 2) Correspondingly the surface of theoverall and core distribution range of the Dontildeanapopulation declined by 53 and 58 respectively(Fig 4)
When summing up all sectors the overall Dontildeanapopulation was conservatively (see Section 23) esti-mated at 69 pairs (max peak of 82) in the 1980s 61(max 86) in the 1990s 53 (max 64) in 2000minus2009and 47 (max 70) in 2010minus2017 (Table 2) In 2017 thepopulation was composed of 37 pairs representing a46minus55 decline compared to the meanminusmaximumlevels of the 1980s ie in less than 40 yr Thus the~50 declining rate within the park was high butwas only almost half of the ~95 decline estimatedfor outside pairs over the same 4 decades (χ2 = 184p lt 00001)
33 Distribution in Dontildeana
Local eradication and differential declines pro-duced a contraction of the overall range and a shiftin the relative importance of some sectors Thusin the 1980s the population was well distributedthrough all sectors but more concentrated in thecore sectors of RBD vera Puntal and in the northernpinewoods of the Natural Park buffer (Fig 5aTable 2) From the 1990s onwards the populationbecame progressively more concentrated within theNational Park in particular in the ecotonal zonebetween the marsh and terrestrial habitats withvery low numbers or local extinctions in all theother sectors (Fig 5b Table 2)
34 Offspring production in Dontildeana
Except for the number of young persuccessful pair all breeding parame-ters deteriorated through time (all χ2 ge1733 all p lt 00017) The probabilityof laying eggs clutch size hatchingsuccess the likelihood of successfullyraising chicks to fledging and thenumber of young per territorialbreeding and successful pair declinedthrough the last 5 decades while theextent of brood reduction progres-sively increased (Fig 6) Deteriorationof reproduction was particularly pro-nounced for the probability of layingfor brood reduction for the probability
194
80 ndash100 ndash80 ndash60 ndash40 ndash20 0 20 40 60 100
10 Marismillas11 Sanlucar pinewood
12 AbalarioCumulative total
1 RBD vera2 RBD interior
3 RBD sand dunes
Change in breeding numbers compared to the 1980s ()
Sector
4 Vera Algaida-Manecorro5 Interior6 Puntal
7 Coto del Rey8 NW pinewoods9 NE pinewoods
Fig 2 Percentage change in breeding numbers of the Dontildeana red kite popu-lation by sector from the 1980s or since the earliest available record (1990s for
Puntal and Abalario) to 2017 RBD Reserva Biologica de Dontildeana
Sergio et al Predator extinction debt in national park
of successful breeding and for the number of fledgedyoung (Fig 7)
On average the whole population was estimated toproduce 103 fledglings per year in the 1980s this al-most halved to 57 in the 1990s 48 in 2000minus2009 andagain declined to more than halved to 19 in 2010minus2017In 2015 2016 and 2017 the population produced 7 7and 15 fledglings respectively Population decline and
breeding deterioration were accompa-nied by a change in the relative impor-tance of some sectors for offspring pro-duction (Fig 5 Table 2) In the 1980smost young were produced in thesector RBD vera and the northernpinewoods and most other sectors stillcontributed gt5 of the annual youngproduction (Fig 5c) In subsequentdecades fledgling production becameconcentrated in the marsh ecotone(Puntal RBD vera vera of Algaida-Manecorro) with additional inputsfrom some interior or peripheral sectorsand a larger portion of sectors with vir-tually zero contribution to future gener-ations (Fig 5d) Fig 3 illustrates howdiffuse successful reproduction was inthe 1980s compared to 2017
35 Comparison with otherEuropean populations
Compared to other areas of Europethe Dontildeana population showed a highdensity in the 1980s (well above theEuropean mean Table S3) This pro-gressively declined and has changedto below-average density since 2010All breeding parameters were wellbelow the mean European estimatesfrom the 1980s onwards (Table S3) Inparticular the percentage of success-ful pairs and the number of youngfledged per breeding pair are cur-rently 2 to 3 times lower than themean European values
36 Population growth andprojections for the Dontildeana
population
Observed declines were well cap-tured by the growth rate predicted by the populationmodel based on the minimum European survivalrates (Fig 8) The other 2 scenarios of maximum andmean survival rates predicted a stable population ordeclines from the year 2000 onwards only (Fig 8)For the 2010s the model estimated λ = 0849 0960and 1066 for the scenario based on minimum meanand maximum survival estimates respectively
195
Fig 3 Distribution of breeding territories in Dontildeana (a) in the 1980s and (b) in2017 Pairs that bred successfully (black points) were much more frequent andmore widely distributed especially in the northern sectors and in the NaturalPark in the 1980s than in 2017 when most pairs failed to raise chicks to fledg-ing (white points) Territory locations have been moved slightly for conserva-tion reasons and locations from the 1980s could only be approximate for some
territories especially those in the northern pinewoods
Endang Species Res 38 189ndash204 2019
Based on the model with minimum survival rateswhich gave the best fit to past declines the popula-tion of 37 pairs censused in 2017 would be reduced to7 pairs within 10 yr and virtually extinct (le2 pairs) in17 yr The less supported scenario of mean Europeansurvival estimates projected a population of 25 pairsin 10 yr while the most optimistic scenario of maxi-mum survival predicted a full recovery to the 1980spopulation level of 70 pairs in 10 yr
Despite the current extremely lowbreeding success under all 3 scenar-ios of survival the population growthrate was least sensitive to changes infledglings production [E(F) = 0048minus0079 S(F) = 0137minus 0277] and mostsensitive to variations in adult survivalprobability [E(θ) = 0843minus 0904 S(θ) =0929minus 0955] In Fig 9 we plot thecombination of fledgling productionand adult survival that produce differ-ent levels of population growth Atcurrent levels of reproduction adultsurvival would have to be around090minus095 to attain a stable or slightlyincreasing population while restoringbreeding success to the levels of the1980s of 13 young per pair wouldimply a stable population even with arelatively low adult survival of ~077ie below the minimum ever recordedfor the species (Fig 9)
4 DISCUSSION
Our results showed that the currentdeteriorated condition of the Dontildeanared kite population was not a recentphenomenon but the tip of the ice-berg of decades of regional and localdegradation Although the protectedarea slowed the background levels ofregional decline and likely saved thespecies from local extinction its via-bility maintenance performance wasfar from satisfactory In a way the ob -served long-term deterioration actedas a protracted diluted form of extinc-tion debt (Tilman et al 1994) paidover a time-frame of several decadesWe suspect that similar conditionsmay be common in other protectedareas making this a classical example
of gradual underlying pressures diluted over such along time-frame that their severity becomes evidentonly through a large-scale long-term asses sment oronce population degradation has reached its extremeconsequences Note that for many parameters dete-rioration was not especially alarming from onedecade to the next making it difficult for the succes-sion of local field observers to appreciate the overallseverity of the long-term trends This difficulty in
196
Fig 4 Distribution range of red kites in Dontildeana (a) in the 1980s and (b) in2017 The pink outer polygon represents a 95 kernel constructed aroundthe territory locations while the red polygon is a 50 kernel showing the corearea of distribution The overall and core distribution range contracted by 534and 581 respectively Territory locations have been moved slightly for
conservation reasons
Sergio et al Predator extinction debt in national park 197
12
3 R
BD
4 V
era
56
7 C
oto
8 N
W9
NE
10
11
12
Tot
al
RB
DR
BD
san
dA
lgai
da
Inte
rior
Pu
nta
ld
elp
ine-
pin
e-M
aris
-S
anlu
car
Ab
alar
iod
ecli
ne
vera
inte
rior
du
nes
Man
ecor
roR
eyw
ood
sw
ood
sm
illa
sp
inew
ood
a) M
ean
no
of
pai
rs19
80minus
1989
141
52
33
40a
20a
80b
50
107
44
50
30
40b
687
1990
minus19
9915
35
11
37
74
08
03
34
40
74
5e2
5c4
0a60
8minus
115
2000
minus20
0916
05
21
47
05
06
31
01
00
14
5e2
03
1a52
5minus
236
2010
minus20
1713
03
42
56
63
98
41
90
50
13
01
72
147
1minus
315
2017
100
35
211
00
03
12
37minus
462
b)
No
of
you
ng
pro
du
ced
an
nu
ally
1980
minus19
8916
14
25
66
43
09
610
020
311
06
04
56
010
26
1990
minus19
999
82
60
68
44
06
92
46
60
95
13
86
056
9minus
445
2000
minus20
0913
21
61
27
25
83
71
21
60
24
53
04
647
7minus
535
2010
minus20
172
60
61
11
82
33
50
90
30
01
62
91
919
4minus
811
2017
10
03
07
00
00
22
150
minus85
4
c)
of
the
tota
l p
op
ula
tio
n i
n e
ach
sec
tor
1980
minus19
8920
57
64
85
82
911
67
315
56
47
34
45
819
90minus
1999
251
84
21
126
66
131
55
73
12
74
41
66
2000
minus20
0929
49
62
612
99
211
51
81
80
28
33
79
120
10minus
2017
276
72
53
141
82
178
40
11
03
64
36
45
2017
270
00
81
135
54
297
00
00
00
81
27
54
d)
c
on
trib
uti
on
of
each
sec
tor
to t
ota
l an
nu
al y
ou
ng
pro
du
ctio
n19
80minus
1989
157
41
54
94
62
29
97
198
107
58
44
58
1990
minus19
9917
24
61
112
114
77
04
211
61
68
96
610
520
00minus
2009
277
33
24
78
151
121
24
34
04
94
63
96
2010
minus20
1713
43
35
418
19
411
74
81
30
08
215
09
620
176
70
00
046
720
00
00
00
00
00
013
313
3
a Cro
ss-c
omb
ined
est
imat
e b
Sta
tic
bac
k-e
stim
ate
c In
terp
olat
ed e
stim
ate
See
Sec
tion
23
for
det
ails
Tab
le 2
(a
) M
ean
nu
mb
er o
f p
airs
an
d (
b)
cum
ula
tive
nu
mb
er o
f of
fsp
rin
g p
rod
uce
d a
nn
ual
ly b
y th
e D
ontildean
a re
d k
ite
pop
ula
tion
wit
hin
eac
h s
ecto
r an
d i
n t
he
wh
ole
par
k o
ver
the
pas
t d
ecad
es a
nd
in 2
017
Per
cen
tag
e of
(c)
pai
rs a
nd
(d
) yo
un
g c
ontr
ibu
ted
by
each
sec
tor
to t
he
over
all p
opu
lati
on S
ecto
rs c
ontr
ibu
tin
g m
ore
than
10
ar
e h
igh
lig
hte
d i
n b
old
T
otal
ref
ers
to t
he
sum
of
all
sect
ors
d
ecli
ne
is t
he
dec
lin
e co
mp
ared
to
the
1980
s P
rop
orti
onal
con
trib
uti
ons
are
also
ill
ust
rate
d i
n F
ig
5
RB
D R
eser
va B
iolo
gic
a d
e D
ontildean
a
Endang Species Res 38 189ndash204 2019
detecting the problem was likely exacerbated by thefollowing factors that could be defined as lsquoperceptionobstaclesrsquo (1) The fact that a population becomesmore and more restricted to a park is often used toillustrate the positive role of protected areas byfocusing their performance assessments on range
coverage ie the capability of protected areas tocover a large portion of a species range (eg Czech2005 Godet et al 2007) This diverts attention fromthe wider problems of range contraction and from theactual performance of the park in terms of viabilitymaintenance (Gaston et al 2008) (2) Confinement to
198
of nests in each sector
of annual young generated by each sector
1980s 2010s
1980s 2010s
a) b)
c) d)
Fig 5 Percentage of the total red kite population in each of 12 sectors of Dontildeana (a) in the 1980s and (b) in the 2010s percent-age of the annual young production generated by each sector (c) in the 1980s and (d) in the 2010s (a) In the 1980s the bulk ofthe population was concentrated in northern sectors (7 and 8) and in the southern shores of the marshes (sectors 1 6 and 10)(b) In the 2010s the population virtually disappeared from the northern sectors and became essentially confined to the na-tional park where it concentrated along the marshes (c) In the 1980s the population generated more than 100 young eachyear most of them produced by the northern sectors (7 8 9) and by the northern shores of the marshes (sectors 1 and 4) (d) Inthe 2010s the population generated less than 10 young mostly generated close to wetlands (sectors 1 4 11) with homo -geneously low numbers elsewhere Colors (yellow rarr orange rarr red) classify sectors by tertiles of the range of percentage
contribution
Sergio et al Predator extinction debt in national park
a protected area is usually accompanied by the auto-matic presumption that this will act as a source areawith limited anthropogenic impacts an assumptionthat is increasingly disproved (Hansen amp DeFries2007 Gaston et al 2008 Watson et al 2014) (3) Long-term assessments such as ours required the lengthy
collation of fragmented informationfrom a large number of sequentialfield workers and administrationseach of which had a very limited per-ception of the overall situation (4)Much monitoring was conducted inthe core areas of the park like theRBD where the species has alwaysbeen most abundant and relativelystable (eg Sergio et al 2005) con-fusing the perception of broaderdeclines (5) Finally large numbersof wintering migrants boost the pop-ulation in the winter and earlyspring often producing an optimisticimpression of apparent abundance
even in relatively expert members of the public or oflocal administrations as we frequently noted in pub-lic talks and private conversations
Overall the decline occurred at multiple levels redkites were originally widespread throughout south-ern Spain (Loacutepez 1861) but became progressively
199
2030405060708090
100110
Bree
ding
su
cces
sful
()
a breeding pairs successful pairs
202122232425262728
Clut
ch si
ze
b
25
35
45
55
65
75
85
1970-79 1980-89 1990-99 2000-09 2010-17
Hatc
hing
succ
ess
broo
d re
duct
ion
()
Decade
c Hatching successBrood reduction
03
06
09
12
15
18
21
1970-79 1980-89 1990-99 2000-09 2010-17
Youn
g fle
dged
Decade
d Young breeding pairYoung successful pair
Fig 6 Reproductive parameters of the red kite population of Dontildeana (a) percentage of pairs laying eggs (black dots n = 804)and successfully raising fledglings (white dots n = 1185) (b) mean clutch size (n = 469) (c) hatching success (percentage ofeggs that hatched black dots n = 353) and brood reduction (percentage of chicks that disappeared during the nestling periodwhite dots n = 240) (d) mean number of young fledged per territorial pair (black dots n = 1145) and per successful pair (white
dots n = 576)
0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75
Young fledgedsuccessful pairYoung fledgedbreeding pairYoung fledgedterritorial pair
Probability of successful breedingBrood reduction
Hatching successClutch size
Probability of laying
Deterioration ()
Breeding parameter
Fig 7 Percentage deterioration of breeding parameters of the red kite popu-lation of Dontildeana between the 1980s and the 2010s
Endang Species Res 38 189ndash204 2019
confined to the protected area of Dontildeana in recentdecades However the park did not confer automaticsafety and declines and range contraction also con-tinued within the protected area suggesting perva-sive pressures and range erosion at multiple spatialscales In particular almost one third of the Dontildeana
population was virtually eradicatedfrom the northern pinewoods of thebuffering Natural Park in 5 to 7 yrbetween the late 1980s and early1990s Several lines of evidence sug-gest that illegal poisoning was themain cause of this eradication (1) Sev-eral adults were found poisoned undertheir nest in those sectors and years(2) Large-scale poisoning campaignsof raptors were reported throughoutSpain in those exact same years asa consequence of huntersrsquo illegalattempts to control predator popula-tions to increase the rapidly deterio-rating numbers of small game (rabbitsand partridges Villafuerte et al 1998Vintildeuela amp Villafuerte 2003 Cano et al2008) In this sense the National Parksuffered much wider national-level
pressures (3) The northern sectors of the parkwhere the eradication took place included or wereclose to private small-game reserves and predatorcontrol was well known to occur in some of them (4)Finally the rapidity of the eradication of such a long-lived species (maximum longevity of 29 yr in Dontilde -ana) implied a causative agent that directly affectedadult mortality (Saether amp Bakke 2000) such as poi-soning The marked impact of poisoning on adult sur-vival and population growth are well recognized forthis species whose facultative scavenging habits andforaging method of meticulous low and slow quar-tering of the ground make it particularly sensitive tothis threat (Smart et al 2010 Tavecchia et al 2012Tenan et al 2012 Sanz-Aguilar et al 2015)
Spikes of rapid local eradication were superim-posed on more gradual but steady deterioration ofoffspring production Gradual and continuous ratherthan sudden degradation of performance suggestedthat poisoning was not the only threat in effect Inthis context several factors may have contributed togradually deteriorate ecological conditions for kitesin recent decades (1) Rabbit epidemics have causedprogressive declines in the availability of this keyprey (Vintildeuela amp Villafuerte 2003) (2) Lower preyavailability may have exacerbated competition withthe dense populations of other raptors with similardiets such as the ecologically similar and in creasingblack kite (3) Predation rates on adults and nestlingsmay have increased with the expansion of the popu-lations of potential predators such as eagle owls Bubobubo and goshawks Accipiter gentilis (4) Recentassessments have detected alarming levels of toxic
200
00
02
04
06
08
10
12
1980sndash1990s 1990sndash2000s 2000sndash2010s
Popu
latio
n gr
owth
rate
Period
Observed populationgrowth
Scenario 1 minimumEuropean survival
Scenario 2 meanEuropean survival
Scenario 3 maximumEuropean survival
Fig 8 Population growth of the Dontildeana red kite population during the past 4decades as predicted by matrix demographic models based on 3 scenarioswhich assumed that survival was equal to minimum mean or maximum sur-vival rates reported for other European populations (reviewed in Table 1)Predicted values are compared with observed declines from one decade to
the next
Fig 9 Population growth rate of red kites in relation to adultsurvival and breeding performance (mean number of youngfledged per territorial pair) based on a matrix populationmodel Note that the graph could be applied to any Euro-pean population The 3 points at the base of the graph repre-sent the minimum (black) mean (grey) and maximum (blue)survival published for European populations (reviewed in
Table 1)
Sergio et al Predator extinction debt in national park
chemicals in red kite eggs from Dontildeana (Goacutemara etal 2008) (5) Climate change and agricultural man-agement have lowered the water table with likelyimpacts on marsh inundation levels and aquatic prey(Garciacutea Novo amp Mariacuten Cabrera 2005 Diacuteaz-Paniaguaamp Aragoneacutes 2015 Schmidt et al 2017) (6) Conver-sion to intensive farmland in surrounding lands haseroded habitat and prey availability outside the pro-tected area which may have buffered kites fromperiods of low prey availability within the park (egduring droughts in the marshes) Some of the pat-terns of observed reproductive deterioration lendsupport to some of these impacts For exampledeclining clutch sizes and increasing rates of broodreduction suggest that food was not sufficient to sus-tain earlier reproductive levels while lowered hatch-ing success is often the result of chemical contamina-tion in raptors (review in Newton 1979) While eachof these threats will be quantitatively investigated indetail in the immediate future in the present contextthey illustrate the frequent and complex challengesfaced by (1) protected areas in maintaining biodiver-sity and viable populations of imperiled species and(2) conservation biologists in identifying causes ofdecline for subsequent management interventioneven in lsquoprivilegedrsquo sites such as reserves
Redistribution declining numbers and perform-ance had important repercussions for future viability(1) The population passed from producing gt100annual young to lt10minus20 which will make mainte-nance and recovery difficult (2) These young wereincreasingly produced in the core sectors of themarsh-ecotone within the National Park which prob-ably increased the dependence of the population onmarsh inundation in turn affected by problems oper-ating outside the park (Garciacutea Novo amp Mariacuten Cabrera2005 Diacuteaz-Paniagua amp Aragoneacutes 2015 Schmidt et al2017) (3) Steep declines in the percentage of suc-cessful pairs implied that future generations wereproduced by a progressively more restricted numberof pairs which will make the population more sub-ject to inbreeding and stochastic events For exam-ple in the last 3 yr all the annual young were pro-duced by 6 8 and 9 pairs respectively suggesting aneffective population size 4 to 9 times lower than theoverall abundance
Given all the above it is no surprise that demo-graphic models suggested a negative growth and apopulation incapable of self-sustenance In particu-lar the model that gave the best fit to past observeddeclines was the one based on minimum Europeansurvival estimates followed by the scenario based onmean European survival estimates Given the above-
mentioned threats declines and performance deteri-oration we would expect survival to be closer to min-imum than mean European levels as supported bythe observed fit to past and recent declines Theseresults have 2 main implications (1) If survival is aslow as we suspect demographic models predict vir-tual extinction within a few years demanding anurgent need for identification and management ofmortality threats as well as quantification of actualsurvival to refine predictions Note that virtual ex -tinction could be even earlier when taking intoaccount effective rather than total population sizeand a stochastic rather than deterministic populationmodel (2) Should actual survival be confirmed lowbut further declines not observed the populationwould be a sink sustained by external sources whichwould make it even more at risk from anthropogenicthreats outside the park and thus more challengingto manage (eg Hansen amp DeFries 2007 Blanco et al2017)
5 Conclusions and implications for conservation
The decades-long degradation that we depictedwas likely generated by a combination of factorsboth internal to the park (eg rabbit availabilitymarsh inundation rates predation and competitionwith other species) and external (eg illegal poi-soning contamination farmland intensification)Some of them will be amenable to managementand others less so but the first priority will be tofind rapid ways to identify the key factors thatdrive population growth so as to optimize conserva-tion action before it is too late For example focus-ing conservation lsquoblindlyrsquo on supplementary feedingcould be useless if the problem is chemical contam-ination The quickest way to obtain such informa-tion would be a satelliteGSM (Global System forMobile communication) tagging program that wouldallow to (1) obtain rapid estimates of health andsurvival for young and adults (eg Sergio et al2019) so as to recalibrate future projections andgoals (2) assess the relative contribution of mainmortality causes which is an essential first step inany recovery program (eg Gonzaacutelez et al 2007Margalida et al 2008 Smart et al 2010) and (3)identify the areas used by breeding and non-breed-ing individuals inside and outside of the park toassess their risk-exposure and intervene before orafter death (eg to prosecute perpetrators of illegalpoisoning or re trofit dangerous electricity pylons inareas of high use by kites)
201
Endang Species Res 38 189ndash204 2019
Until this information becomes available below welist some tentative figures and priorities for conserva-tion First of all restoring the current population toformer levels would undoubtedly be challenging andprobably unrealistic given the profound changesincurred by the wider Dontildeana ecosystem in recentdecades Thus we propose an initial target of 60pairs as a long-term restoration goal Elasticity analy-sis suggested that optimal management should focuson improving adult survival which had the largestimpact on population growth as in other long-livedspecies (Saether amp Bakke 2000 Whitfield et al 2004Kruumlger et al 2010) This could be attempted by in -creasing food availability especially of key prey suchas rabbits and by curtailing mortality threats such asillegal poisoning which still continues despite mucheffort to eradicate it by the local administration Thetelemetry program outlined above could help toidentify local perpetrators as occurred in other pop-ulations (Smart et al 2010 Tavecchia et al 2012) Onthe other hand despite their low elasticities repro-ductive rates are currently so low that it would befundamental to increase them eg by increasingfood availability and ensuring proper inundation ofthe marshes Based on Fig 5 we propose as initialtargets for restoration (1) survival rates equal orhigher than the European mean (adult survivalge087) and (2) a number of young fledged per territo-rial pair above 10 which would produce an increas-ing population provided that adult survival is equalto or above the European mean Note that Fig 5could be applied to any European population as atool to check its potential viability Given the highlythreatened status of red kites the speciesrsquo limitedrange confined to Europe and its ongoing declinesviability assessments such as ours may sadly becomemore important for the management and recovery ofmany populations
In conclusion red kites would probably be extinctin southern Spain without the institution of a largenational park In this sense this example well illus-trates how protected areas will continue to be corner-stones of global conservation of threatened taxaHowever their safety is not ensured by park institu-tion per se and performance monitoring and focusedaction will be needed to avoid potential extinctiondebts which may be more protracted than previouslyappreciated In our exemplary case despite the pres-ence of a large national park on prime fertile landwithin a developed country with adequate institu-tional and financial support a key threatened speciessuffered latent but steady declines for decadesobscured by problems of perception lack and frag-
mentation of information and likely caused by acomplex array of within-park threats and growingexternal pressures Viability maintenance and recov-ery will probably require concerted actions withinand outside of the park but only after detailed infor-mation on crucial aspects becomes available whichis probably the most urgent current priority We sus-pect that dynamics like the ones illustrated here aremore common than currently appreciated and willbecome more widespread as anthropogenic pres-sures increase around protected areas and as theirperformance monitoring becomes more prevalent
Acknowledgements We thank all the (too many to mention)researchers field workers visitors volunteers gamekeep-ers park managers and wardens that have provided datasince the 1960s In particular we thank F G Vilches L Gar-ciacutea and the Equipo de Seguimiento de Procesos Naturales ofthe Estacioacuten Bioloacutegica de Dontildeana-CSIC for help in the fieldSpecial thanks to F G Vilches for the priceless help with thecollation and organization of historical information Wethank J P Castellano I Redondo and all the lsquoArea de Con-servacioacutenrsquo of Dontildeana National Park for constant interest andsupport We thank R Cadenas J Madrid R Arenas J RBenitez and all the pertinent personnel of the Consejeriacutea deMedio Ambiente of the Junta de Andaluciacutea for informationon current nest locations in the Sierra de Huelva and fortheir constant attentive support We are grateful to Dr NBunnefeld and 2 anonymous reviewers for constructivecomments that improved the manuscript This study wasfunded by the Foundation Jaime Gonzaacutelez-Gordon and bythe research project 16022015 of the Spanish Ministry ofAgriculture Food and the Environment (National ParksAutonomous Agency)
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Blanco G Cardells J Garijo-Toledo MM (2017) Supplemen-tary feeding and endoparasites in threatened avian scav-engers coprologic evidence from red kites in their win-tering stronghold Environ Res 155 22minus30
Brashares JS Arcese P Sam MK (2001) Human demographyand reserve size predict wildlife extinction in WestAfrica Proc Biol Sci 268 2473minus2478
Bustamante J (1993) Post-fledging dependence period anddevelopment of flight and hunting behaviour in the redkite Milvus milvus Bird Study 40 181minus188
Cano C Ayerza P Fernaacutendez J (2008) Poisoning in Spain(1990minus2005) analysis of the problem incidence andcauses WWFAdena Madrid (in Spanish)
Caswell H (2001) Matrix population models Sinauer Sun-derland MA
Ceballos JJ Guimeraacute VM (1992) Guiacutea de las aves de Jerez yde la Provincia de Caacutediz atlas ornitoloacutegico de lasespecies nidificantes Ayuntamiento de Jerez Jerez
Craigie ID Baillie JEM Balmford A Carbone C Collen BGreen RE Hutton JM (2010) Large mammal population
202
Sergio et al Predator extinction debt in national park
declines in Africarsquos protected areas Biol Conserv 143 2221minus2228
Czech B (2005) The capacity of the National WildlifeRefuge System to conserve threatened and endangeredanimal species in the United States Conserv Biol 19 1246minus1253
Delibes M Garciacutea L (1984) Haacutebitos alimenticios del milanoreal en Dontildeana durante el periodo de criacutea Ardeola 31 115minus121
Diacuteaz-Paniagua C Aragoneacutes D (2015) Permanent and tempo-rary ponds in Dontildeana National Park (SW Spain) arethreatened by desiccation Limnetica 34 407minus424
Evans IM Summers RW OrsquoToole L Orr-Ewing DC Snell NSmith J (1999) Evaluating the success of translocatingred kites Milvus milvus to the UK Bird Study 46 129minus144
Ferrer M Hiraldo F (1991) Evaluation of management tech-niques for the Spanish imperial eagle Wildl Soc Bull 19 436minus442
Garciacutea Novo F Mariacuten Cabrera C (2005) Dontildeana water andbiosphere Dontildeana 2005 Project Spanish Ministry of theEnvironment Madrid
Gaston KJ Jackson SF Cantuacute-Salazar L Cruz-Pintildeoacuten G(2008) The ecological performance of protected areasAnnu Rev Ecol Evol Syst 39 93minus113
Godet L Devictor V Jiguet F (2007) Estimating relative pop-ulation size included within protected areas BiodiversConserv 16 2587minus2598
Goacutemara B Gonzaacutelez MJ Baos R Hiraldo F Abad E RiveraJ Jimeacutenez B (2008) Unexpected high PCB and total DDTlevels in the breeding population of red kite (Milvus mil-vus) from Dontildeana National Park south-western SpainEnviron Int 34 73minus78
Gonzaacutelez LM Margalida A Mantildeosa S Saacutenchez R and oth-ers (2007) Causes and spatio-temporal variations of non-natural mortality in the vulnerable Spanish imperialeagle Aquila adalberti during a recovery period Oryx41 495minus502
Hansen AJ DeFries R (2007) Ecological mechanisms linkingprotected areas to surrounding lands Ecol Appl 17 974minus988
Hernaacutendez FJ Donaacutezar JA Hiraldo F (2001) Evaluacioacuten deluso de venenos para el control de predadores en laComunidad Autoacutenoma Andaluza y su impacto en la con-servacioacuten de especies amenazadas de vertebrados Con-sejeria de Medio Ambiente and Estacioacuten Bioloacutegica deDontildeana Sevilla
IUCN (The World Conservation Union) (1994) Guidelines forprotected area management categories IUCN Gland
Knott J Newbery P Barov B (2009) Action plan for the redkite Milvus milvus in the European Union EuropeanCommission Brussels
Kruumlger O Gruumlnkorn T Struwe-Juhl B (2010) The return ofthe white-tailed eagle (Haliaeetus albicilla) to northernGermany modelling the past to predict the future BiolConserv 143 710minus721
Loacutepez V (1861) Cataacutelogo de las aves observadas enAndaluciacutea Madrid
Loacutepez G and others (2009) Management measures to controla feline leukemia virus outbreak in the endangered Iber-ian lynx Anim Conserv 12 173minus182
Margalida A Heredia R Razin M Hernaacutendez M (2008)Sources of variation in mortality of the bearded vultureGypaetus barbatus in Europe Bird Conserv Int 18 1minus10
Naughton-Treves L Holland MB Brandon K (2005) The roleof protected areas in conserving biodiversity and sustain-
ing local livelihoods Annu Rev Environ Resour 30 219minus252
Newton I (1979) Population ecology of raptors T amp AD PoyserBerkhamsted
Newton I Davis PE Davis JE (1989) Age of first breedingdispersal and survival of red kites Milvus milvus inWales Ibis 131 16minus21
Otero C Castieacuten E Senosiaiacuten R Portillo F (1978) Fauna deCazorla vertebrados Publicaciones del Ministerio deAgricultura Madrid
Parks SA Harcourt AH (2002) Reserve size local humandensity and mammalian extinctions in US protectedareas Conserv Biol 16 800minus808
R Development Core Team (2018) R a language and envi-ronment for statistical computing R Foundation for Sta-tistical Computing Vienna wwwr-projectorg
Saeligther BE Bakke Oslash (2000) Avian life history variation andcontribution of demographic traits to the populationgrowth rate Ecology 81 642minus653
Sanz-Aguilar A De Pablo F Donaacutezar JA (2015) Age-depen-dent survival of island vs mainland populations of twoavian scavengers delving into migration costs Oecolo-gia 179 405minus414
Schaub M (2012) Spatial distribution of wind turbines is cru-cial for the survival of red kite populations Biol Conserv155 111minus118
Schmidt G Saacutenchez Navarro R Hernaacutendez E Carmona JJFuentelsaz F Seiz R (2017) The state of water in Dontildeana an evaluation of the state of the water and of the ecosys-tems of the protected space WWFAdena Madrid
Scott JM Davis FW McGhie RG Wright RG Groves CEstes J (2001) Nature reserves Do they capture the fullrange of Americarsquos biological diversity Ecol Appl 11 999minus1007
Seoane J Vintildeuela J Diacuteaz-Delgado R Bustamante J (2003)The effects of land use and climate on red kite distribu-tion in the Iberian peninsula Biol Conserv 111 401minus414
Sergio F Blas J Feroro M Fernaacutendez N Donaacutezar JAHiraldo F (2005) Preservation of wide-ranging top pred-ators by site-protection black and red kites in DontildeanaNational Park Biol Conserv 125 11minus21
Sergio F Tanferna A Blas J Blanco G Hiraldo F (2019) Reli-able methods for identifying animal deaths in GPS- andsatellite-tracking data review testing and calibrationJ Appl Ecol 56562ndash572
Smart J Amar A Sim IMW Etheridge B Cameron DChristie G Wilson JD (2010) Illegal killing slows popula-tion recovery of a re-introduced raptor of high conserva-tion concern mdash the red kite Milvus milvus Biol Conserv143 1278minus1286
Tavecchia G Adrover J Muntildeoz Navarro A Pradel R (2012)Modelling mortality causes in longitudinal data in thepresence of tag loss application to raptor poisoning andelectrocution J Appl Ecol 49 297minus305
Tenan S Adrover J Muntildeoz Navarro A Sergio F TavecchiaG (2012) Demographic consequences of poison-relatedmortality in a threatened bird of prey PLOS ONE 7 e49187
Tilman D May RM Lehman CL Nowak MA (1994) Habitatdestruction and the extinction debt Nature 371 65minus66
Torres Esquivias JA Jordano P Leoacuten A (1981) Aves de presadiurnas de la provincia de Coacuterdoba Publicaciones CA yMP Coacuterdoba
Veiga JP Hiraldo F (1990) Food habits and the survival andgrowth of nestlings in two sympatric kites (Milvus milvus
203
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and Milvus migrans) Holarct Ecol 13 62minus71 Villafuerte R Vintildeuela J Blanco JC (1998) Extensive preda-
tor persecution caused by population crash in a gamespecies the case of red kites and rabbits in Spain BiolConserv 84 181minus188
Vintildeuela J (2004) Milano real Milvus milvus In Madrontildeo AGonzaacutelez C Atienza JC (eds) Libro rojo de las aves deEspantildea Direccioacuten General para la BiodiversidadminusSEOBirdLife Madrid p 120minus125
Vintildeuela J Villafuerte R (2003) Predators and rabbits (Oryc-tolagus cuniculus) in Spain a key conflict for Europeanraptor conservation In Thompson DBA Redpath SMFielding AH Marquiss M Galbraith CA (eds) Birds ofprey in a changing environment The Stationery OfficeEdinburgh p 511minus526
Vintildeuela J Martiacute R Ruiz A (eds) (1999) El milano real enEspantildea SEOBirdlife Madrid
Watson JEM Dudley N Segan DB Hockings M (2014) Theperformance and potential of protected areas Nature515 67minus73
Whitfield SM Bell KE Philippi T Sasa M and others (2007)Amphibian and reptile declines over 35 years at La SelvaCosta Rica Proc Natl Acad Sci USA 104 8352minus8356
Whitfield DP Fielding AH McLeod DRA Haworth PF(2004) Modelling the effects of persecution on the popu-lation dynamics of golden eagles in Scotland Biol Con-serv 119 319minus333
Zuur A Ieno EN Walker N Saveliev AA Smith GM (2009)Mixed effects models and extensions in ecology with RSpringer New York NY
204
Editorial responsibility Nils BunnefeldStirling UK
Submitted October 8 2018 Accepted January 28 2019Proofs received from author(s) April 7 2019
Endang Species Res 38 189ndash204 2019
tain portions of a sector in some years and other por-tions in different subsequent years In these cases wecalculated the mean number of pairs yrminus1 decademinus1 foreach subsector when well surveyed and summed upthese means to obtain a cumulative estimate de -cademinus1 for the whole sector (hereafter lsquocross-combinedestimatesrsquo) In all procedures above we ensured thatall alternative nests belonging to the same territorywere included within the same sector or subsector inorder to avoid biases caused by re-counting the sameterritory twice when combining different surveyunits Similarly in all cases of doubt we used the
estimate that minimized the historicalpopulation in order to provide conser-vative estimates of decline
To place declines and the potentialstrategic importance of the parkwithin a wider regional context wereconstructed the distribution andpopulation levels of the kite popula-tion for southern Spain (AndaluciacuteaAutonomous Region 87 268 km2) inthe 1970sminus1980s based on informa-tion found in Otero et al (1978) TorresEsquivias et al (1981) Ceballos ampGuimeraacute (1992) Vintildeuela et al (1999)Vintildeuela (2004) and conversationswith local experts Data for the currentred kite population outside Dontildeanawere provided by the Consejeriacutea deMedio Ambiente of the AndaluciacuteaAutonomous Region
24 Statistical analyses
To investigate how generalized thehistorical population declines acrossdifferent sectors of the park were weestimated whether the subpopulationof each sector increased or declinedbetween the earliest available surveyand the 2010s and then tested whetherdeclines were prevalent over stable orincreasing trends by means of a bino-mial test To explore temporal trendsin breeding rates we fitted general-ized linear models (GLMs) with de -cade sector and their interaction asexplanatory variables and with thelikelihood of laying eggs clutch sizehatching success brood reductionthe likelihood of successfully raising
chicks to fledgling and the number of young fledgedper territorial breeding and successful pair as re -sponse variables (Zuur et al 2009) In the aboveanalyses hatching success was defined as the pro-portion of eggs that hatched brood reduction was theproportion of hatched chicks lost before fledging aterritorial pair was one that held a territory a breed-ing pair one that laid at least 1 egg and a successfulpair one that raised at least 1 nestling to fledging age(gt45 d) In particular the likelihood of laying eggsand raising chicks to fledging were examinedthrough GLMs with binomial errors and a logit link
192
Fig 1 Approximate distribution range of the red kite in southern Spain (An-daluciacutea Autonomous Region) (a) in the 1980s (reconstructed on the basis ofsources cited in Section 23) compared to (b) the distribution as recorded in2017 The red sectors in (a) represent (1) the marshes of Dontildeana and Odiel inthe provinces of Huelva and Sevilla (2) the hills and low mountains of SierraMorena in the provinces of Huelva Sevilla and Cordoba and (3) the mountain
complex of Cazorla in the provinces of Granada and Jaeacuten
Sergio et al Predator extinction debt in national park
function while clutch size and the number of fledgedyoung were modelled through GLMs with Poissonerrors and a log link function Finally hatching suc-cess and brood reduction were modelled by GLMswith Poisson errors and a log link function using thenumber of hatched eggs and the number of disap-peared chicks as response variables and clutch sizeand brood size at hatching as offset variables (Zuur etal 2009)
The current expected growth of the Dontildeana popu-lation was estimated by building an age-structureddemographic model (Caswell 2001) M based on theage-dependent values of survival (see below) and themean fertility recorded over the last 5 yr in Dontildeana(0294 young per territorial pair) The matrix Mdescribes the transition of the population between 2consecutive years t and t+1 The asymptotic popula-tion growth λ is calculated as the dominant eigen-value of M (Caswell 2001) In a stable population λ isequal to 1 while lower values indicate a decliningtrend Because survival estimates were not availablefor the Dontildeana population we applied values pub-lished for other European populations (reviewed inTable 1) In all studies survival has been reported for3 age classes 1 yr 2 yr and adult (ge3 yr) so we main-tained the same age classes in the current assess-ment In particular to explore the whole range of sur-vival scenarios potentially experienced by ourpopulation we built 3 separate deterministic matrixmodels based on the minimum average and maxi-mum survival rates reported for other European pop-ulations respectively (Table 1) These exploratoryanalyses were conducted with deterministic modelsbecause uncertainty on parameter estimates de -pended largely on the population considered Wefurther assumed a 11 sex ratio and that all kites hadentered the breeding population by 3 yr of age
Based on the obtained λ we then projected the pop-ulation over the next 10minus20 yr assuming no densitydependence to explore its potential short-term via-bility or extinction over the coming decades Becauseof the assumptions outlined above and the parame-ters taken from other populations these projectionsshould be taken with caution and recalibrated asmore local data become available
Finally we used perturbation analyses to calcu-late the sensitivity S(θ) and elasticity E(θ) of thepopulation growth rate to a given parameter θ(Caswell 2001) Sensitivity is the change in pop -ulation growth rate in response to an absolutechange of a given parameter θ while elasticity isthe change in the population growth rate in re -sponse to a proportional change of a given param-eter θ Throughout all analyses were implementedwith R version 351 (R Development Core Team2018) using the libraries lsquopopbiorsquo and lsquolme4rsquoResults are given as means plusmn 1SE tests are 2-tailed and statistical significance was set at α le005
3 RESULTS
31 Regional distribution and the strategicimportance of the protected area
Red kites must originally have been common be -low 400minus600 m of elevation throughout Andaluciacuteawhich traditionally hosted a dense and well distrib-uted rabbit population as an important prey base(Loacutepez 1861) By the 1970sminus1980s legal and thenillegal shooting and poisoning had reduced the pop-ulation to 3 main nuclei (Fig 1a) (1) the marshes ofDontildeana and Odiel in the provinces of Huelva and
Sevilla (2) the hills and low moun-tains of Sierra Morena in theprovinces of Huelva Sevilla and Cor-doba and (3) the mountain complexof Cazorla in the provinces ofGranada and Jaeacuten The latter 2 nucleiwere reported as lsquoin steep declinersquo ordocumented as already extinct in the1990s (Vintildeuela et al 1999 Vintildeuela2004) so that the current regionalpopulation is virtually confined toDontildeana with 3 additional relict pairslocated in the Sierra de Huelva(Fig 1b) The nuclei outside the pro-tected area of Dontildeana were estimatedto ıhave suffered a 95 decline since
193
Area Age class Reference1 yr 2 yr ge 3 yr
England Midlands 080 094 093 Evans et al (1999)Scotland 037 072 087 Smart et al (2010)Wales uplands 060 079 094 Newton et al (1989)Switzerland 045 074 084 Schaub (2012)Spain Mallorca 072 082 079 Tavecchia et al (2012)Spain Menorca 054 083 084 Sanz Aguilar et al (2015)
Min European estimates 037 072 079Mean European estimates 058 081 087Max European estimates 080 094 094
Table 1 Published estimates of red kite survival by age class Minimum meanand maximum levels were used to set up different demographic scenarios for
matrix population models
Endang Species Res 38 189ndash204 2019
the 1970sminus1980s (from a conservative estimate of40minus77 pairs to 2minus4 current pairs) Thus Dontildeanahosted 52minus63 of the regional population in the1970sminus80s and 95minus96 after 2010 increasing its rel-ative strategic importance
32 Abundance and trends in Dontildeana
Different sectors of the park showed differenttrends (Fig 2 Fig S2) Numbers appeared (1) stableor in moderate decline in the Reserva Biologica deDontildeana RBD (sectors 1 2 and 3) (2) stable or increas-ing in the sector of Puntal and in the vera of Algaida-Manecorro as well as its interior These areas werecharacterized by the removal of Eucalyptus planta-tions that converted large areas of woodland to opengrassland in the 1990s (sectors 4 and 5) or alwaysmaintained a very open landscape through extensivegrazing by livestock (sector 6) Finally (3) declines ofvarying magnitude were observed in all peripheralsectors to the north east and south While declineswere moderate in the eastern and southern sectorsthat were monitored less continuously dramatic de -clines were evident for all the northern sectors in -cluding portions of the National Park and its buffer-ing Natural Park In these sectors (7 8 9) a populationof 20minus25 pairs was basically eradicated in a few yearsbetween the late 1980s and early 1990s re mainingvirtually extinct to date (Fig 3) This rapid eradica-tion was accompanied by the detection of adultsfound dead by poisoning in or under their nest Over-all there was a significant preponderance of declinesbetween the numbers re corded in the earliest survey
available for each sector and the 2010s (binomial testp lt 0001 Fig 2) Correspondingly the surface of theoverall and core distribution range of the Dontildeanapopulation declined by 53 and 58 respectively(Fig 4)
When summing up all sectors the overall Dontildeanapopulation was conservatively (see Section 23) esti-mated at 69 pairs (max peak of 82) in the 1980s 61(max 86) in the 1990s 53 (max 64) in 2000minus2009and 47 (max 70) in 2010minus2017 (Table 2) In 2017 thepopulation was composed of 37 pairs representing a46minus55 decline compared to the meanminusmaximumlevels of the 1980s ie in less than 40 yr Thus the~50 declining rate within the park was high butwas only almost half of the ~95 decline estimatedfor outside pairs over the same 4 decades (χ2 = 184p lt 00001)
33 Distribution in Dontildeana
Local eradication and differential declines pro-duced a contraction of the overall range and a shiftin the relative importance of some sectors Thusin the 1980s the population was well distributedthrough all sectors but more concentrated in thecore sectors of RBD vera Puntal and in the northernpinewoods of the Natural Park buffer (Fig 5aTable 2) From the 1990s onwards the populationbecame progressively more concentrated within theNational Park in particular in the ecotonal zonebetween the marsh and terrestrial habitats withvery low numbers or local extinctions in all theother sectors (Fig 5b Table 2)
34 Offspring production in Dontildeana
Except for the number of young persuccessful pair all breeding parame-ters deteriorated through time (all χ2 ge1733 all p lt 00017) The probabilityof laying eggs clutch size hatchingsuccess the likelihood of successfullyraising chicks to fledging and thenumber of young per territorialbreeding and successful pair declinedthrough the last 5 decades while theextent of brood reduction progres-sively increased (Fig 6) Deteriorationof reproduction was particularly pro-nounced for the probability of layingfor brood reduction for the probability
194
80 ndash100 ndash80 ndash60 ndash40 ndash20 0 20 40 60 100
10 Marismillas11 Sanlucar pinewood
12 AbalarioCumulative total
1 RBD vera2 RBD interior
3 RBD sand dunes
Change in breeding numbers compared to the 1980s ()
Sector
4 Vera Algaida-Manecorro5 Interior6 Puntal
7 Coto del Rey8 NW pinewoods9 NE pinewoods
Fig 2 Percentage change in breeding numbers of the Dontildeana red kite popu-lation by sector from the 1980s or since the earliest available record (1990s for
Puntal and Abalario) to 2017 RBD Reserva Biologica de Dontildeana
Sergio et al Predator extinction debt in national park
of successful breeding and for the number of fledgedyoung (Fig 7)
On average the whole population was estimated toproduce 103 fledglings per year in the 1980s this al-most halved to 57 in the 1990s 48 in 2000minus2009 andagain declined to more than halved to 19 in 2010minus2017In 2015 2016 and 2017 the population produced 7 7and 15 fledglings respectively Population decline and
breeding deterioration were accompa-nied by a change in the relative impor-tance of some sectors for offspring pro-duction (Fig 5 Table 2) In the 1980smost young were produced in thesector RBD vera and the northernpinewoods and most other sectors stillcontributed gt5 of the annual youngproduction (Fig 5c) In subsequentdecades fledgling production becameconcentrated in the marsh ecotone(Puntal RBD vera vera of Algaida-Manecorro) with additional inputsfrom some interior or peripheral sectorsand a larger portion of sectors with vir-tually zero contribution to future gener-ations (Fig 5d) Fig 3 illustrates howdiffuse successful reproduction was inthe 1980s compared to 2017
35 Comparison with otherEuropean populations
Compared to other areas of Europethe Dontildeana population showed a highdensity in the 1980s (well above theEuropean mean Table S3) This pro-gressively declined and has changedto below-average density since 2010All breeding parameters were wellbelow the mean European estimatesfrom the 1980s onwards (Table S3) Inparticular the percentage of success-ful pairs and the number of youngfledged per breeding pair are cur-rently 2 to 3 times lower than themean European values
36 Population growth andprojections for the Dontildeana
population
Observed declines were well cap-tured by the growth rate predicted by the populationmodel based on the minimum European survivalrates (Fig 8) The other 2 scenarios of maximum andmean survival rates predicted a stable population ordeclines from the year 2000 onwards only (Fig 8)For the 2010s the model estimated λ = 0849 0960and 1066 for the scenario based on minimum meanand maximum survival estimates respectively
195
Fig 3 Distribution of breeding territories in Dontildeana (a) in the 1980s and (b) in2017 Pairs that bred successfully (black points) were much more frequent andmore widely distributed especially in the northern sectors and in the NaturalPark in the 1980s than in 2017 when most pairs failed to raise chicks to fledg-ing (white points) Territory locations have been moved slightly for conserva-tion reasons and locations from the 1980s could only be approximate for some
territories especially those in the northern pinewoods
Endang Species Res 38 189ndash204 2019
Based on the model with minimum survival rateswhich gave the best fit to past declines the popula-tion of 37 pairs censused in 2017 would be reduced to7 pairs within 10 yr and virtually extinct (le2 pairs) in17 yr The less supported scenario of mean Europeansurvival estimates projected a population of 25 pairsin 10 yr while the most optimistic scenario of maxi-mum survival predicted a full recovery to the 1980spopulation level of 70 pairs in 10 yr
Despite the current extremely lowbreeding success under all 3 scenar-ios of survival the population growthrate was least sensitive to changes infledglings production [E(F) = 0048minus0079 S(F) = 0137minus 0277] and mostsensitive to variations in adult survivalprobability [E(θ) = 0843minus 0904 S(θ) =0929minus 0955] In Fig 9 we plot thecombination of fledgling productionand adult survival that produce differ-ent levels of population growth Atcurrent levels of reproduction adultsurvival would have to be around090minus095 to attain a stable or slightlyincreasing population while restoringbreeding success to the levels of the1980s of 13 young per pair wouldimply a stable population even with arelatively low adult survival of ~077ie below the minimum ever recordedfor the species (Fig 9)
4 DISCUSSION
Our results showed that the currentdeteriorated condition of the Dontildeanared kite population was not a recentphenomenon but the tip of the ice-berg of decades of regional and localdegradation Although the protectedarea slowed the background levels ofregional decline and likely saved thespecies from local extinction its via-bility maintenance performance wasfar from satisfactory In a way the ob -served long-term deterioration actedas a protracted diluted form of extinc-tion debt (Tilman et al 1994) paidover a time-frame of several decadesWe suspect that similar conditionsmay be common in other protectedareas making this a classical example
of gradual underlying pressures diluted over such along time-frame that their severity becomes evidentonly through a large-scale long-term asses sment oronce population degradation has reached its extremeconsequences Note that for many parameters dete-rioration was not especially alarming from onedecade to the next making it difficult for the succes-sion of local field observers to appreciate the overallseverity of the long-term trends This difficulty in
196
Fig 4 Distribution range of red kites in Dontildeana (a) in the 1980s and (b) in2017 The pink outer polygon represents a 95 kernel constructed aroundthe territory locations while the red polygon is a 50 kernel showing the corearea of distribution The overall and core distribution range contracted by 534and 581 respectively Territory locations have been moved slightly for
conservation reasons
Sergio et al Predator extinction debt in national park 197
12
3 R
BD
4 V
era
56
7 C
oto
8 N
W9
NE
10
11
12
Tot
al
RB
DR
BD
san
dA
lgai
da
Inte
rior
Pu
nta
ld
elp
ine-
pin
e-M
aris
-S
anlu
car
Ab
alar
iod
ecli
ne
vera
inte
rior
du
nes
Man
ecor
roR
eyw
ood
sw
ood
sm
illa
sp
inew
ood
a) M
ean
no
of
pai
rs19
80minus
1989
141
52
33
40a
20a
80b
50
107
44
50
30
40b
687
1990
minus19
9915
35
11
37
74
08
03
34
40
74
5e2
5c4
0a60
8minus
115
2000
minus20
0916
05
21
47
05
06
31
01
00
14
5e2
03
1a52
5minus
236
2010
minus20
1713
03
42
56
63
98
41
90
50
13
01
72
147
1minus
315
2017
100
35
211
00
03
12
37minus
462
b)
No
of
you
ng
pro
du
ced
an
nu
ally
1980
minus19
8916
14
25
66
43
09
610
020
311
06
04
56
010
26
1990
minus19
999
82
60
68
44
06
92
46
60
95
13
86
056
9minus
445
2000
minus20
0913
21
61
27
25
83
71
21
60
24
53
04
647
7minus
535
2010
minus20
172
60
61
11
82
33
50
90
30
01
62
91
919
4minus
811
2017
10
03
07
00
00
22
150
minus85
4
c)
of
the
tota
l p
op
ula
tio
n i
n e
ach
sec
tor
1980
minus19
8920
57
64
85
82
911
67
315
56
47
34
45
819
90minus
1999
251
84
21
126
66
131
55
73
12
74
41
66
2000
minus20
0929
49
62
612
99
211
51
81
80
28
33
79
120
10minus
2017
276
72
53
141
82
178
40
11
03
64
36
45
2017
270
00
81
135
54
297
00
00
00
81
27
54
d)
c
on
trib
uti
on
of
each
sec
tor
to t
ota
l an
nu
al y
ou
ng
pro
du
ctio
n19
80minus
1989
157
41
54
94
62
29
97
198
107
58
44
58
1990
minus19
9917
24
61
112
114
77
04
211
61
68
96
610
520
00minus
2009
277
33
24
78
151
121
24
34
04
94
63
96
2010
minus20
1713
43
35
418
19
411
74
81
30
08
215
09
620
176
70
00
046
720
00
00
00
00
00
013
313
3
a Cro
ss-c
omb
ined
est
imat
e b
Sta
tic
bac
k-e
stim
ate
c In
terp
olat
ed e
stim
ate
See
Sec
tion
23
for
det
ails
Tab
le 2
(a
) M
ean
nu
mb
er o
f p
airs
an
d (
b)
cum
ula
tive
nu
mb
er o
f of
fsp
rin
g p
rod
uce
d a
nn
ual
ly b
y th
e D
ontildean
a re
d k
ite
pop
ula
tion
wit
hin
eac
h s
ecto
r an
d i
n t
he
wh
ole
par
k o
ver
the
pas
t d
ecad
es a
nd
in 2
017
Per
cen
tag
e of
(c)
pai
rs a
nd
(d
) yo
un
g c
ontr
ibu
ted
by
each
sec
tor
to t
he
over
all p
opu
lati
on S
ecto
rs c
ontr
ibu
tin
g m
ore
than
10
ar
e h
igh
lig
hte
d i
n b
old
T
otal
ref
ers
to t
he
sum
of
all
sect
ors
d
ecli
ne
is t
he
dec
lin
e co
mp
ared
to
the
1980
s P
rop
orti
onal
con
trib
uti
ons
are
also
ill
ust
rate
d i
n F
ig
5
RB
D R
eser
va B
iolo
gic
a d
e D
ontildean
a
Endang Species Res 38 189ndash204 2019
detecting the problem was likely exacerbated by thefollowing factors that could be defined as lsquoperceptionobstaclesrsquo (1) The fact that a population becomesmore and more restricted to a park is often used toillustrate the positive role of protected areas byfocusing their performance assessments on range
coverage ie the capability of protected areas tocover a large portion of a species range (eg Czech2005 Godet et al 2007) This diverts attention fromthe wider problems of range contraction and from theactual performance of the park in terms of viabilitymaintenance (Gaston et al 2008) (2) Confinement to
198
of nests in each sector
of annual young generated by each sector
1980s 2010s
1980s 2010s
a) b)
c) d)
Fig 5 Percentage of the total red kite population in each of 12 sectors of Dontildeana (a) in the 1980s and (b) in the 2010s percent-age of the annual young production generated by each sector (c) in the 1980s and (d) in the 2010s (a) In the 1980s the bulk ofthe population was concentrated in northern sectors (7 and 8) and in the southern shores of the marshes (sectors 1 6 and 10)(b) In the 2010s the population virtually disappeared from the northern sectors and became essentially confined to the na-tional park where it concentrated along the marshes (c) In the 1980s the population generated more than 100 young eachyear most of them produced by the northern sectors (7 8 9) and by the northern shores of the marshes (sectors 1 and 4) (d) Inthe 2010s the population generated less than 10 young mostly generated close to wetlands (sectors 1 4 11) with homo -geneously low numbers elsewhere Colors (yellow rarr orange rarr red) classify sectors by tertiles of the range of percentage
contribution
Sergio et al Predator extinction debt in national park
a protected area is usually accompanied by the auto-matic presumption that this will act as a source areawith limited anthropogenic impacts an assumptionthat is increasingly disproved (Hansen amp DeFries2007 Gaston et al 2008 Watson et al 2014) (3) Long-term assessments such as ours required the lengthy
collation of fragmented informationfrom a large number of sequentialfield workers and administrationseach of which had a very limited per-ception of the overall situation (4)Much monitoring was conducted inthe core areas of the park like theRBD where the species has alwaysbeen most abundant and relativelystable (eg Sergio et al 2005) con-fusing the perception of broaderdeclines (5) Finally large numbersof wintering migrants boost the pop-ulation in the winter and earlyspring often producing an optimisticimpression of apparent abundance
even in relatively expert members of the public or oflocal administrations as we frequently noted in pub-lic talks and private conversations
Overall the decline occurred at multiple levels redkites were originally widespread throughout south-ern Spain (Loacutepez 1861) but became progressively
199
2030405060708090
100110
Bree
ding
su
cces
sful
()
a breeding pairs successful pairs
202122232425262728
Clut
ch si
ze
b
25
35
45
55
65
75
85
1970-79 1980-89 1990-99 2000-09 2010-17
Hatc
hing
succ
ess
broo
d re
duct
ion
()
Decade
c Hatching successBrood reduction
03
06
09
12
15
18
21
1970-79 1980-89 1990-99 2000-09 2010-17
Youn
g fle
dged
Decade
d Young breeding pairYoung successful pair
Fig 6 Reproductive parameters of the red kite population of Dontildeana (a) percentage of pairs laying eggs (black dots n = 804)and successfully raising fledglings (white dots n = 1185) (b) mean clutch size (n = 469) (c) hatching success (percentage ofeggs that hatched black dots n = 353) and brood reduction (percentage of chicks that disappeared during the nestling periodwhite dots n = 240) (d) mean number of young fledged per territorial pair (black dots n = 1145) and per successful pair (white
dots n = 576)
0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75
Young fledgedsuccessful pairYoung fledgedbreeding pairYoung fledgedterritorial pair
Probability of successful breedingBrood reduction
Hatching successClutch size
Probability of laying
Deterioration ()
Breeding parameter
Fig 7 Percentage deterioration of breeding parameters of the red kite popu-lation of Dontildeana between the 1980s and the 2010s
Endang Species Res 38 189ndash204 2019
confined to the protected area of Dontildeana in recentdecades However the park did not confer automaticsafety and declines and range contraction also con-tinued within the protected area suggesting perva-sive pressures and range erosion at multiple spatialscales In particular almost one third of the Dontildeana
population was virtually eradicatedfrom the northern pinewoods of thebuffering Natural Park in 5 to 7 yrbetween the late 1980s and early1990s Several lines of evidence sug-gest that illegal poisoning was themain cause of this eradication (1) Sev-eral adults were found poisoned undertheir nest in those sectors and years(2) Large-scale poisoning campaignsof raptors were reported throughoutSpain in those exact same years asa consequence of huntersrsquo illegalattempts to control predator popula-tions to increase the rapidly deterio-rating numbers of small game (rabbitsand partridges Villafuerte et al 1998Vintildeuela amp Villafuerte 2003 Cano et al2008) In this sense the National Parksuffered much wider national-level
pressures (3) The northern sectors of the parkwhere the eradication took place included or wereclose to private small-game reserves and predatorcontrol was well known to occur in some of them (4)Finally the rapidity of the eradication of such a long-lived species (maximum longevity of 29 yr in Dontilde -ana) implied a causative agent that directly affectedadult mortality (Saether amp Bakke 2000) such as poi-soning The marked impact of poisoning on adult sur-vival and population growth are well recognized forthis species whose facultative scavenging habits andforaging method of meticulous low and slow quar-tering of the ground make it particularly sensitive tothis threat (Smart et al 2010 Tavecchia et al 2012Tenan et al 2012 Sanz-Aguilar et al 2015)
Spikes of rapid local eradication were superim-posed on more gradual but steady deterioration ofoffspring production Gradual and continuous ratherthan sudden degradation of performance suggestedthat poisoning was not the only threat in effect Inthis context several factors may have contributed togradually deteriorate ecological conditions for kitesin recent decades (1) Rabbit epidemics have causedprogressive declines in the availability of this keyprey (Vintildeuela amp Villafuerte 2003) (2) Lower preyavailability may have exacerbated competition withthe dense populations of other raptors with similardiets such as the ecologically similar and in creasingblack kite (3) Predation rates on adults and nestlingsmay have increased with the expansion of the popu-lations of potential predators such as eagle owls Bubobubo and goshawks Accipiter gentilis (4) Recentassessments have detected alarming levels of toxic
200
00
02
04
06
08
10
12
1980sndash1990s 1990sndash2000s 2000sndash2010s
Popu
latio
n gr
owth
rate
Period
Observed populationgrowth
Scenario 1 minimumEuropean survival
Scenario 2 meanEuropean survival
Scenario 3 maximumEuropean survival
Fig 8 Population growth of the Dontildeana red kite population during the past 4decades as predicted by matrix demographic models based on 3 scenarioswhich assumed that survival was equal to minimum mean or maximum sur-vival rates reported for other European populations (reviewed in Table 1)Predicted values are compared with observed declines from one decade to
the next
Fig 9 Population growth rate of red kites in relation to adultsurvival and breeding performance (mean number of youngfledged per territorial pair) based on a matrix populationmodel Note that the graph could be applied to any Euro-pean population The 3 points at the base of the graph repre-sent the minimum (black) mean (grey) and maximum (blue)survival published for European populations (reviewed in
Table 1)
Sergio et al Predator extinction debt in national park
chemicals in red kite eggs from Dontildeana (Goacutemara etal 2008) (5) Climate change and agricultural man-agement have lowered the water table with likelyimpacts on marsh inundation levels and aquatic prey(Garciacutea Novo amp Mariacuten Cabrera 2005 Diacuteaz-Paniaguaamp Aragoneacutes 2015 Schmidt et al 2017) (6) Conver-sion to intensive farmland in surrounding lands haseroded habitat and prey availability outside the pro-tected area which may have buffered kites fromperiods of low prey availability within the park (egduring droughts in the marshes) Some of the pat-terns of observed reproductive deterioration lendsupport to some of these impacts For exampledeclining clutch sizes and increasing rates of broodreduction suggest that food was not sufficient to sus-tain earlier reproductive levels while lowered hatch-ing success is often the result of chemical contamina-tion in raptors (review in Newton 1979) While eachof these threats will be quantitatively investigated indetail in the immediate future in the present contextthey illustrate the frequent and complex challengesfaced by (1) protected areas in maintaining biodiver-sity and viable populations of imperiled species and(2) conservation biologists in identifying causes ofdecline for subsequent management interventioneven in lsquoprivilegedrsquo sites such as reserves
Redistribution declining numbers and perform-ance had important repercussions for future viability(1) The population passed from producing gt100annual young to lt10minus20 which will make mainte-nance and recovery difficult (2) These young wereincreasingly produced in the core sectors of themarsh-ecotone within the National Park which prob-ably increased the dependence of the population onmarsh inundation in turn affected by problems oper-ating outside the park (Garciacutea Novo amp Mariacuten Cabrera2005 Diacuteaz-Paniagua amp Aragoneacutes 2015 Schmidt et al2017) (3) Steep declines in the percentage of suc-cessful pairs implied that future generations wereproduced by a progressively more restricted numberof pairs which will make the population more sub-ject to inbreeding and stochastic events For exam-ple in the last 3 yr all the annual young were pro-duced by 6 8 and 9 pairs respectively suggesting aneffective population size 4 to 9 times lower than theoverall abundance
Given all the above it is no surprise that demo-graphic models suggested a negative growth and apopulation incapable of self-sustenance In particu-lar the model that gave the best fit to past observeddeclines was the one based on minimum Europeansurvival estimates followed by the scenario based onmean European survival estimates Given the above-
mentioned threats declines and performance deteri-oration we would expect survival to be closer to min-imum than mean European levels as supported bythe observed fit to past and recent declines Theseresults have 2 main implications (1) If survival is aslow as we suspect demographic models predict vir-tual extinction within a few years demanding anurgent need for identification and management ofmortality threats as well as quantification of actualsurvival to refine predictions Note that virtual ex -tinction could be even earlier when taking intoaccount effective rather than total population sizeand a stochastic rather than deterministic populationmodel (2) Should actual survival be confirmed lowbut further declines not observed the populationwould be a sink sustained by external sources whichwould make it even more at risk from anthropogenicthreats outside the park and thus more challengingto manage (eg Hansen amp DeFries 2007 Blanco et al2017)
5 Conclusions and implications for conservation
The decades-long degradation that we depictedwas likely generated by a combination of factorsboth internal to the park (eg rabbit availabilitymarsh inundation rates predation and competitionwith other species) and external (eg illegal poi-soning contamination farmland intensification)Some of them will be amenable to managementand others less so but the first priority will be tofind rapid ways to identify the key factors thatdrive population growth so as to optimize conserva-tion action before it is too late For example focus-ing conservation lsquoblindlyrsquo on supplementary feedingcould be useless if the problem is chemical contam-ination The quickest way to obtain such informa-tion would be a satelliteGSM (Global System forMobile communication) tagging program that wouldallow to (1) obtain rapid estimates of health andsurvival for young and adults (eg Sergio et al2019) so as to recalibrate future projections andgoals (2) assess the relative contribution of mainmortality causes which is an essential first step inany recovery program (eg Gonzaacutelez et al 2007Margalida et al 2008 Smart et al 2010) and (3)identify the areas used by breeding and non-breed-ing individuals inside and outside of the park toassess their risk-exposure and intervene before orafter death (eg to prosecute perpetrators of illegalpoisoning or re trofit dangerous electricity pylons inareas of high use by kites)
201
Endang Species Res 38 189ndash204 2019
Until this information becomes available below welist some tentative figures and priorities for conserva-tion First of all restoring the current population toformer levels would undoubtedly be challenging andprobably unrealistic given the profound changesincurred by the wider Dontildeana ecosystem in recentdecades Thus we propose an initial target of 60pairs as a long-term restoration goal Elasticity analy-sis suggested that optimal management should focuson improving adult survival which had the largestimpact on population growth as in other long-livedspecies (Saether amp Bakke 2000 Whitfield et al 2004Kruumlger et al 2010) This could be attempted by in -creasing food availability especially of key prey suchas rabbits and by curtailing mortality threats such asillegal poisoning which still continues despite mucheffort to eradicate it by the local administration Thetelemetry program outlined above could help toidentify local perpetrators as occurred in other pop-ulations (Smart et al 2010 Tavecchia et al 2012) Onthe other hand despite their low elasticities repro-ductive rates are currently so low that it would befundamental to increase them eg by increasingfood availability and ensuring proper inundation ofthe marshes Based on Fig 5 we propose as initialtargets for restoration (1) survival rates equal orhigher than the European mean (adult survivalge087) and (2) a number of young fledged per territo-rial pair above 10 which would produce an increas-ing population provided that adult survival is equalto or above the European mean Note that Fig 5could be applied to any European population as atool to check its potential viability Given the highlythreatened status of red kites the speciesrsquo limitedrange confined to Europe and its ongoing declinesviability assessments such as ours may sadly becomemore important for the management and recovery ofmany populations
In conclusion red kites would probably be extinctin southern Spain without the institution of a largenational park In this sense this example well illus-trates how protected areas will continue to be corner-stones of global conservation of threatened taxaHowever their safety is not ensured by park institu-tion per se and performance monitoring and focusedaction will be needed to avoid potential extinctiondebts which may be more protracted than previouslyappreciated In our exemplary case despite the pres-ence of a large national park on prime fertile landwithin a developed country with adequate institu-tional and financial support a key threatened speciessuffered latent but steady declines for decadesobscured by problems of perception lack and frag-
mentation of information and likely caused by acomplex array of within-park threats and growingexternal pressures Viability maintenance and recov-ery will probably require concerted actions withinand outside of the park but only after detailed infor-mation on crucial aspects becomes available whichis probably the most urgent current priority We sus-pect that dynamics like the ones illustrated here aremore common than currently appreciated and willbecome more widespread as anthropogenic pres-sures increase around protected areas and as theirperformance monitoring becomes more prevalent
Acknowledgements We thank all the (too many to mention)researchers field workers visitors volunteers gamekeep-ers park managers and wardens that have provided datasince the 1960s In particular we thank F G Vilches L Gar-ciacutea and the Equipo de Seguimiento de Procesos Naturales ofthe Estacioacuten Bioloacutegica de Dontildeana-CSIC for help in the fieldSpecial thanks to F G Vilches for the priceless help with thecollation and organization of historical information Wethank J P Castellano I Redondo and all the lsquoArea de Con-servacioacutenrsquo of Dontildeana National Park for constant interest andsupport We thank R Cadenas J Madrid R Arenas J RBenitez and all the pertinent personnel of the Consejeriacutea deMedio Ambiente of the Junta de Andaluciacutea for informationon current nest locations in the Sierra de Huelva and fortheir constant attentive support We are grateful to Dr NBunnefeld and 2 anonymous reviewers for constructivecomments that improved the manuscript This study wasfunded by the Foundation Jaime Gonzaacutelez-Gordon and bythe research project 16022015 of the Spanish Ministry ofAgriculture Food and the Environment (National ParksAutonomous Agency)
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Sergio F Tanferna A Blas J Blanco G Hiraldo F (2019) Reli-able methods for identifying animal deaths in GPS- andsatellite-tracking data review testing and calibrationJ Appl Ecol 56562ndash572
Smart J Amar A Sim IMW Etheridge B Cameron DChristie G Wilson JD (2010) Illegal killing slows popula-tion recovery of a re-introduced raptor of high conserva-tion concern mdash the red kite Milvus milvus Biol Conserv143 1278minus1286
Tavecchia G Adrover J Muntildeoz Navarro A Pradel R (2012)Modelling mortality causes in longitudinal data in thepresence of tag loss application to raptor poisoning andelectrocution J Appl Ecol 49 297minus305
Tenan S Adrover J Muntildeoz Navarro A Sergio F TavecchiaG (2012) Demographic consequences of poison-relatedmortality in a threatened bird of prey PLOS ONE 7 e49187
Tilman D May RM Lehman CL Nowak MA (1994) Habitatdestruction and the extinction debt Nature 371 65minus66
Torres Esquivias JA Jordano P Leoacuten A (1981) Aves de presadiurnas de la provincia de Coacuterdoba Publicaciones CA yMP Coacuterdoba
Veiga JP Hiraldo F (1990) Food habits and the survival andgrowth of nestlings in two sympatric kites (Milvus milvus
203
Endang Species Res 38 189ndash204 2019
and Milvus migrans) Holarct Ecol 13 62minus71 Villafuerte R Vintildeuela J Blanco JC (1998) Extensive preda-
tor persecution caused by population crash in a gamespecies the case of red kites and rabbits in Spain BiolConserv 84 181minus188
Vintildeuela J (2004) Milano real Milvus milvus In Madrontildeo AGonzaacutelez C Atienza JC (eds) Libro rojo de las aves deEspantildea Direccioacuten General para la BiodiversidadminusSEOBirdLife Madrid p 120minus125
Vintildeuela J Villafuerte R (2003) Predators and rabbits (Oryc-tolagus cuniculus) in Spain a key conflict for Europeanraptor conservation In Thompson DBA Redpath SMFielding AH Marquiss M Galbraith CA (eds) Birds ofprey in a changing environment The Stationery OfficeEdinburgh p 511minus526
Vintildeuela J Martiacute R Ruiz A (eds) (1999) El milano real enEspantildea SEOBirdlife Madrid
Watson JEM Dudley N Segan DB Hockings M (2014) Theperformance and potential of protected areas Nature515 67minus73
Whitfield SM Bell KE Philippi T Sasa M and others (2007)Amphibian and reptile declines over 35 years at La SelvaCosta Rica Proc Natl Acad Sci USA 104 8352minus8356
Whitfield DP Fielding AH McLeod DRA Haworth PF(2004) Modelling the effects of persecution on the popu-lation dynamics of golden eagles in Scotland Biol Con-serv 119 319minus333
Zuur A Ieno EN Walker N Saveliev AA Smith GM (2009)Mixed effects models and extensions in ecology with RSpringer New York NY
204
Editorial responsibility Nils BunnefeldStirling UK
Submitted October 8 2018 Accepted January 28 2019Proofs received from author(s) April 7 2019
Sergio et al Predator extinction debt in national park
function while clutch size and the number of fledgedyoung were modelled through GLMs with Poissonerrors and a log link function Finally hatching suc-cess and brood reduction were modelled by GLMswith Poisson errors and a log link function using thenumber of hatched eggs and the number of disap-peared chicks as response variables and clutch sizeand brood size at hatching as offset variables (Zuur etal 2009)
The current expected growth of the Dontildeana popu-lation was estimated by building an age-structureddemographic model (Caswell 2001) M based on theage-dependent values of survival (see below) and themean fertility recorded over the last 5 yr in Dontildeana(0294 young per territorial pair) The matrix Mdescribes the transition of the population between 2consecutive years t and t+1 The asymptotic popula-tion growth λ is calculated as the dominant eigen-value of M (Caswell 2001) In a stable population λ isequal to 1 while lower values indicate a decliningtrend Because survival estimates were not availablefor the Dontildeana population we applied values pub-lished for other European populations (reviewed inTable 1) In all studies survival has been reported for3 age classes 1 yr 2 yr and adult (ge3 yr) so we main-tained the same age classes in the current assess-ment In particular to explore the whole range of sur-vival scenarios potentially experienced by ourpopulation we built 3 separate deterministic matrixmodels based on the minimum average and maxi-mum survival rates reported for other European pop-ulations respectively (Table 1) These exploratoryanalyses were conducted with deterministic modelsbecause uncertainty on parameter estimates de -pended largely on the population considered Wefurther assumed a 11 sex ratio and that all kites hadentered the breeding population by 3 yr of age
Based on the obtained λ we then projected the pop-ulation over the next 10minus20 yr assuming no densitydependence to explore its potential short-term via-bility or extinction over the coming decades Becauseof the assumptions outlined above and the parame-ters taken from other populations these projectionsshould be taken with caution and recalibrated asmore local data become available
Finally we used perturbation analyses to calcu-late the sensitivity S(θ) and elasticity E(θ) of thepopulation growth rate to a given parameter θ(Caswell 2001) Sensitivity is the change in pop -ulation growth rate in response to an absolutechange of a given parameter θ while elasticity isthe change in the population growth rate in re -sponse to a proportional change of a given param-eter θ Throughout all analyses were implementedwith R version 351 (R Development Core Team2018) using the libraries lsquopopbiorsquo and lsquolme4rsquoResults are given as means plusmn 1SE tests are 2-tailed and statistical significance was set at α le005
3 RESULTS
31 Regional distribution and the strategicimportance of the protected area
Red kites must originally have been common be -low 400minus600 m of elevation throughout Andaluciacuteawhich traditionally hosted a dense and well distrib-uted rabbit population as an important prey base(Loacutepez 1861) By the 1970sminus1980s legal and thenillegal shooting and poisoning had reduced the pop-ulation to 3 main nuclei (Fig 1a) (1) the marshes ofDontildeana and Odiel in the provinces of Huelva and
Sevilla (2) the hills and low moun-tains of Sierra Morena in theprovinces of Huelva Sevilla and Cor-doba and (3) the mountain complexof Cazorla in the provinces ofGranada and Jaeacuten The latter 2 nucleiwere reported as lsquoin steep declinersquo ordocumented as already extinct in the1990s (Vintildeuela et al 1999 Vintildeuela2004) so that the current regionalpopulation is virtually confined toDontildeana with 3 additional relict pairslocated in the Sierra de Huelva(Fig 1b) The nuclei outside the pro-tected area of Dontildeana were estimatedto ıhave suffered a 95 decline since
193
Area Age class Reference1 yr 2 yr ge 3 yr
England Midlands 080 094 093 Evans et al (1999)Scotland 037 072 087 Smart et al (2010)Wales uplands 060 079 094 Newton et al (1989)Switzerland 045 074 084 Schaub (2012)Spain Mallorca 072 082 079 Tavecchia et al (2012)Spain Menorca 054 083 084 Sanz Aguilar et al (2015)
Min European estimates 037 072 079Mean European estimates 058 081 087Max European estimates 080 094 094
Table 1 Published estimates of red kite survival by age class Minimum meanand maximum levels were used to set up different demographic scenarios for
matrix population models
Endang Species Res 38 189ndash204 2019
the 1970sminus1980s (from a conservative estimate of40minus77 pairs to 2minus4 current pairs) Thus Dontildeanahosted 52minus63 of the regional population in the1970sminus80s and 95minus96 after 2010 increasing its rel-ative strategic importance
32 Abundance and trends in Dontildeana
Different sectors of the park showed differenttrends (Fig 2 Fig S2) Numbers appeared (1) stableor in moderate decline in the Reserva Biologica deDontildeana RBD (sectors 1 2 and 3) (2) stable or increas-ing in the sector of Puntal and in the vera of Algaida-Manecorro as well as its interior These areas werecharacterized by the removal of Eucalyptus planta-tions that converted large areas of woodland to opengrassland in the 1990s (sectors 4 and 5) or alwaysmaintained a very open landscape through extensivegrazing by livestock (sector 6) Finally (3) declines ofvarying magnitude were observed in all peripheralsectors to the north east and south While declineswere moderate in the eastern and southern sectorsthat were monitored less continuously dramatic de -clines were evident for all the northern sectors in -cluding portions of the National Park and its buffer-ing Natural Park In these sectors (7 8 9) a populationof 20minus25 pairs was basically eradicated in a few yearsbetween the late 1980s and early 1990s re mainingvirtually extinct to date (Fig 3) This rapid eradica-tion was accompanied by the detection of adultsfound dead by poisoning in or under their nest Over-all there was a significant preponderance of declinesbetween the numbers re corded in the earliest survey
available for each sector and the 2010s (binomial testp lt 0001 Fig 2) Correspondingly the surface of theoverall and core distribution range of the Dontildeanapopulation declined by 53 and 58 respectively(Fig 4)
When summing up all sectors the overall Dontildeanapopulation was conservatively (see Section 23) esti-mated at 69 pairs (max peak of 82) in the 1980s 61(max 86) in the 1990s 53 (max 64) in 2000minus2009and 47 (max 70) in 2010minus2017 (Table 2) In 2017 thepopulation was composed of 37 pairs representing a46minus55 decline compared to the meanminusmaximumlevels of the 1980s ie in less than 40 yr Thus the~50 declining rate within the park was high butwas only almost half of the ~95 decline estimatedfor outside pairs over the same 4 decades (χ2 = 184p lt 00001)
33 Distribution in Dontildeana
Local eradication and differential declines pro-duced a contraction of the overall range and a shiftin the relative importance of some sectors Thusin the 1980s the population was well distributedthrough all sectors but more concentrated in thecore sectors of RBD vera Puntal and in the northernpinewoods of the Natural Park buffer (Fig 5aTable 2) From the 1990s onwards the populationbecame progressively more concentrated within theNational Park in particular in the ecotonal zonebetween the marsh and terrestrial habitats withvery low numbers or local extinctions in all theother sectors (Fig 5b Table 2)
34 Offspring production in Dontildeana
Except for the number of young persuccessful pair all breeding parame-ters deteriorated through time (all χ2 ge1733 all p lt 00017) The probabilityof laying eggs clutch size hatchingsuccess the likelihood of successfullyraising chicks to fledging and thenumber of young per territorialbreeding and successful pair declinedthrough the last 5 decades while theextent of brood reduction progres-sively increased (Fig 6) Deteriorationof reproduction was particularly pro-nounced for the probability of layingfor brood reduction for the probability
194
80 ndash100 ndash80 ndash60 ndash40 ndash20 0 20 40 60 100
10 Marismillas11 Sanlucar pinewood
12 AbalarioCumulative total
1 RBD vera2 RBD interior
3 RBD sand dunes
Change in breeding numbers compared to the 1980s ()
Sector
4 Vera Algaida-Manecorro5 Interior6 Puntal
7 Coto del Rey8 NW pinewoods9 NE pinewoods
Fig 2 Percentage change in breeding numbers of the Dontildeana red kite popu-lation by sector from the 1980s or since the earliest available record (1990s for
Puntal and Abalario) to 2017 RBD Reserva Biologica de Dontildeana
Sergio et al Predator extinction debt in national park
of successful breeding and for the number of fledgedyoung (Fig 7)
On average the whole population was estimated toproduce 103 fledglings per year in the 1980s this al-most halved to 57 in the 1990s 48 in 2000minus2009 andagain declined to more than halved to 19 in 2010minus2017In 2015 2016 and 2017 the population produced 7 7and 15 fledglings respectively Population decline and
breeding deterioration were accompa-nied by a change in the relative impor-tance of some sectors for offspring pro-duction (Fig 5 Table 2) In the 1980smost young were produced in thesector RBD vera and the northernpinewoods and most other sectors stillcontributed gt5 of the annual youngproduction (Fig 5c) In subsequentdecades fledgling production becameconcentrated in the marsh ecotone(Puntal RBD vera vera of Algaida-Manecorro) with additional inputsfrom some interior or peripheral sectorsand a larger portion of sectors with vir-tually zero contribution to future gener-ations (Fig 5d) Fig 3 illustrates howdiffuse successful reproduction was inthe 1980s compared to 2017
35 Comparison with otherEuropean populations
Compared to other areas of Europethe Dontildeana population showed a highdensity in the 1980s (well above theEuropean mean Table S3) This pro-gressively declined and has changedto below-average density since 2010All breeding parameters were wellbelow the mean European estimatesfrom the 1980s onwards (Table S3) Inparticular the percentage of success-ful pairs and the number of youngfledged per breeding pair are cur-rently 2 to 3 times lower than themean European values
36 Population growth andprojections for the Dontildeana
population
Observed declines were well cap-tured by the growth rate predicted by the populationmodel based on the minimum European survivalrates (Fig 8) The other 2 scenarios of maximum andmean survival rates predicted a stable population ordeclines from the year 2000 onwards only (Fig 8)For the 2010s the model estimated λ = 0849 0960and 1066 for the scenario based on minimum meanand maximum survival estimates respectively
195
Fig 3 Distribution of breeding territories in Dontildeana (a) in the 1980s and (b) in2017 Pairs that bred successfully (black points) were much more frequent andmore widely distributed especially in the northern sectors and in the NaturalPark in the 1980s than in 2017 when most pairs failed to raise chicks to fledg-ing (white points) Territory locations have been moved slightly for conserva-tion reasons and locations from the 1980s could only be approximate for some
territories especially those in the northern pinewoods
Endang Species Res 38 189ndash204 2019
Based on the model with minimum survival rateswhich gave the best fit to past declines the popula-tion of 37 pairs censused in 2017 would be reduced to7 pairs within 10 yr and virtually extinct (le2 pairs) in17 yr The less supported scenario of mean Europeansurvival estimates projected a population of 25 pairsin 10 yr while the most optimistic scenario of maxi-mum survival predicted a full recovery to the 1980spopulation level of 70 pairs in 10 yr
Despite the current extremely lowbreeding success under all 3 scenar-ios of survival the population growthrate was least sensitive to changes infledglings production [E(F) = 0048minus0079 S(F) = 0137minus 0277] and mostsensitive to variations in adult survivalprobability [E(θ) = 0843minus 0904 S(θ) =0929minus 0955] In Fig 9 we plot thecombination of fledgling productionand adult survival that produce differ-ent levels of population growth Atcurrent levels of reproduction adultsurvival would have to be around090minus095 to attain a stable or slightlyincreasing population while restoringbreeding success to the levels of the1980s of 13 young per pair wouldimply a stable population even with arelatively low adult survival of ~077ie below the minimum ever recordedfor the species (Fig 9)
4 DISCUSSION
Our results showed that the currentdeteriorated condition of the Dontildeanared kite population was not a recentphenomenon but the tip of the ice-berg of decades of regional and localdegradation Although the protectedarea slowed the background levels ofregional decline and likely saved thespecies from local extinction its via-bility maintenance performance wasfar from satisfactory In a way the ob -served long-term deterioration actedas a protracted diluted form of extinc-tion debt (Tilman et al 1994) paidover a time-frame of several decadesWe suspect that similar conditionsmay be common in other protectedareas making this a classical example
of gradual underlying pressures diluted over such along time-frame that their severity becomes evidentonly through a large-scale long-term asses sment oronce population degradation has reached its extremeconsequences Note that for many parameters dete-rioration was not especially alarming from onedecade to the next making it difficult for the succes-sion of local field observers to appreciate the overallseverity of the long-term trends This difficulty in
196
Fig 4 Distribution range of red kites in Dontildeana (a) in the 1980s and (b) in2017 The pink outer polygon represents a 95 kernel constructed aroundthe territory locations while the red polygon is a 50 kernel showing the corearea of distribution The overall and core distribution range contracted by 534and 581 respectively Territory locations have been moved slightly for
conservation reasons
Sergio et al Predator extinction debt in national park 197
12
3 R
BD
4 V
era
56
7 C
oto
8 N
W9
NE
10
11
12
Tot
al
RB
DR
BD
san
dA
lgai
da
Inte
rior
Pu
nta
ld
elp
ine-
pin
e-M
aris
-S
anlu
car
Ab
alar
iod
ecli
ne
vera
inte
rior
du
nes
Man
ecor
roR
eyw
ood
sw
ood
sm
illa
sp
inew
ood
a) M
ean
no
of
pai
rs19
80minus
1989
141
52
33
40a
20a
80b
50
107
44
50
30
40b
687
1990
minus19
9915
35
11
37
74
08
03
34
40
74
5e2
5c4
0a60
8minus
115
2000
minus20
0916
05
21
47
05
06
31
01
00
14
5e2
03
1a52
5minus
236
2010
minus20
1713
03
42
56
63
98
41
90
50
13
01
72
147
1minus
315
2017
100
35
211
00
03
12
37minus
462
b)
No
of
you
ng
pro
du
ced
an
nu
ally
1980
minus19
8916
14
25
66
43
09
610
020
311
06
04
56
010
26
1990
minus19
999
82
60
68
44
06
92
46
60
95
13
86
056
9minus
445
2000
minus20
0913
21
61
27
25
83
71
21
60
24
53
04
647
7minus
535
2010
minus20
172
60
61
11
82
33
50
90
30
01
62
91
919
4minus
811
2017
10
03
07
00
00
22
150
minus85
4
c)
of
the
tota
l p
op
ula
tio
n i
n e
ach
sec
tor
1980
minus19
8920
57
64
85
82
911
67
315
56
47
34
45
819
90minus
1999
251
84
21
126
66
131
55
73
12
74
41
66
2000
minus20
0929
49
62
612
99
211
51
81
80
28
33
79
120
10minus
2017
276
72
53
141
82
178
40
11
03
64
36
45
2017
270
00
81
135
54
297
00
00
00
81
27
54
d)
c
on
trib
uti
on
of
each
sec
tor
to t
ota
l an
nu
al y
ou
ng
pro
du
ctio
n19
80minus
1989
157
41
54
94
62
29
97
198
107
58
44
58
1990
minus19
9917
24
61
112
114
77
04
211
61
68
96
610
520
00minus
2009
277
33
24
78
151
121
24
34
04
94
63
96
2010
minus20
1713
43
35
418
19
411
74
81
30
08
215
09
620
176
70
00
046
720
00
00
00
00
00
013
313
3
a Cro
ss-c
omb
ined
est
imat
e b
Sta
tic
bac
k-e
stim
ate
c In
terp
olat
ed e
stim
ate
See
Sec
tion
23
for
det
ails
Tab
le 2
(a
) M
ean
nu
mb
er o
f p
airs
an
d (
b)
cum
ula
tive
nu
mb
er o
f of
fsp
rin
g p
rod
uce
d a
nn
ual
ly b
y th
e D
ontildean
a re
d k
ite
pop
ula
tion
wit
hin
eac
h s
ecto
r an
d i
n t
he
wh
ole
par
k o
ver
the
pas
t d
ecad
es a
nd
in 2
017
Per
cen
tag
e of
(c)
pai
rs a
nd
(d
) yo
un
g c
ontr
ibu
ted
by
each
sec
tor
to t
he
over
all p
opu
lati
on S
ecto
rs c
ontr
ibu
tin
g m
ore
than
10
ar
e h
igh
lig
hte
d i
n b
old
T
otal
ref
ers
to t
he
sum
of
all
sect
ors
d
ecli
ne
is t
he
dec
lin
e co
mp
ared
to
the
1980
s P
rop
orti
onal
con
trib
uti
ons
are
also
ill
ust
rate
d i
n F
ig
5
RB
D R
eser
va B
iolo
gic
a d
e D
ontildean
a
Endang Species Res 38 189ndash204 2019
detecting the problem was likely exacerbated by thefollowing factors that could be defined as lsquoperceptionobstaclesrsquo (1) The fact that a population becomesmore and more restricted to a park is often used toillustrate the positive role of protected areas byfocusing their performance assessments on range
coverage ie the capability of protected areas tocover a large portion of a species range (eg Czech2005 Godet et al 2007) This diverts attention fromthe wider problems of range contraction and from theactual performance of the park in terms of viabilitymaintenance (Gaston et al 2008) (2) Confinement to
198
of nests in each sector
of annual young generated by each sector
1980s 2010s
1980s 2010s
a) b)
c) d)
Fig 5 Percentage of the total red kite population in each of 12 sectors of Dontildeana (a) in the 1980s and (b) in the 2010s percent-age of the annual young production generated by each sector (c) in the 1980s and (d) in the 2010s (a) In the 1980s the bulk ofthe population was concentrated in northern sectors (7 and 8) and in the southern shores of the marshes (sectors 1 6 and 10)(b) In the 2010s the population virtually disappeared from the northern sectors and became essentially confined to the na-tional park where it concentrated along the marshes (c) In the 1980s the population generated more than 100 young eachyear most of them produced by the northern sectors (7 8 9) and by the northern shores of the marshes (sectors 1 and 4) (d) Inthe 2010s the population generated less than 10 young mostly generated close to wetlands (sectors 1 4 11) with homo -geneously low numbers elsewhere Colors (yellow rarr orange rarr red) classify sectors by tertiles of the range of percentage
contribution
Sergio et al Predator extinction debt in national park
a protected area is usually accompanied by the auto-matic presumption that this will act as a source areawith limited anthropogenic impacts an assumptionthat is increasingly disproved (Hansen amp DeFries2007 Gaston et al 2008 Watson et al 2014) (3) Long-term assessments such as ours required the lengthy
collation of fragmented informationfrom a large number of sequentialfield workers and administrationseach of which had a very limited per-ception of the overall situation (4)Much monitoring was conducted inthe core areas of the park like theRBD where the species has alwaysbeen most abundant and relativelystable (eg Sergio et al 2005) con-fusing the perception of broaderdeclines (5) Finally large numbersof wintering migrants boost the pop-ulation in the winter and earlyspring often producing an optimisticimpression of apparent abundance
even in relatively expert members of the public or oflocal administrations as we frequently noted in pub-lic talks and private conversations
Overall the decline occurred at multiple levels redkites were originally widespread throughout south-ern Spain (Loacutepez 1861) but became progressively
199
2030405060708090
100110
Bree
ding
su
cces
sful
()
a breeding pairs successful pairs
202122232425262728
Clut
ch si
ze
b
25
35
45
55
65
75
85
1970-79 1980-89 1990-99 2000-09 2010-17
Hatc
hing
succ
ess
broo
d re
duct
ion
()
Decade
c Hatching successBrood reduction
03
06
09
12
15
18
21
1970-79 1980-89 1990-99 2000-09 2010-17
Youn
g fle
dged
Decade
d Young breeding pairYoung successful pair
Fig 6 Reproductive parameters of the red kite population of Dontildeana (a) percentage of pairs laying eggs (black dots n = 804)and successfully raising fledglings (white dots n = 1185) (b) mean clutch size (n = 469) (c) hatching success (percentage ofeggs that hatched black dots n = 353) and brood reduction (percentage of chicks that disappeared during the nestling periodwhite dots n = 240) (d) mean number of young fledged per territorial pair (black dots n = 1145) and per successful pair (white
dots n = 576)
0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75
Young fledgedsuccessful pairYoung fledgedbreeding pairYoung fledgedterritorial pair
Probability of successful breedingBrood reduction
Hatching successClutch size
Probability of laying
Deterioration ()
Breeding parameter
Fig 7 Percentage deterioration of breeding parameters of the red kite popu-lation of Dontildeana between the 1980s and the 2010s
Endang Species Res 38 189ndash204 2019
confined to the protected area of Dontildeana in recentdecades However the park did not confer automaticsafety and declines and range contraction also con-tinued within the protected area suggesting perva-sive pressures and range erosion at multiple spatialscales In particular almost one third of the Dontildeana
population was virtually eradicatedfrom the northern pinewoods of thebuffering Natural Park in 5 to 7 yrbetween the late 1980s and early1990s Several lines of evidence sug-gest that illegal poisoning was themain cause of this eradication (1) Sev-eral adults were found poisoned undertheir nest in those sectors and years(2) Large-scale poisoning campaignsof raptors were reported throughoutSpain in those exact same years asa consequence of huntersrsquo illegalattempts to control predator popula-tions to increase the rapidly deterio-rating numbers of small game (rabbitsand partridges Villafuerte et al 1998Vintildeuela amp Villafuerte 2003 Cano et al2008) In this sense the National Parksuffered much wider national-level
pressures (3) The northern sectors of the parkwhere the eradication took place included or wereclose to private small-game reserves and predatorcontrol was well known to occur in some of them (4)Finally the rapidity of the eradication of such a long-lived species (maximum longevity of 29 yr in Dontilde -ana) implied a causative agent that directly affectedadult mortality (Saether amp Bakke 2000) such as poi-soning The marked impact of poisoning on adult sur-vival and population growth are well recognized forthis species whose facultative scavenging habits andforaging method of meticulous low and slow quar-tering of the ground make it particularly sensitive tothis threat (Smart et al 2010 Tavecchia et al 2012Tenan et al 2012 Sanz-Aguilar et al 2015)
Spikes of rapid local eradication were superim-posed on more gradual but steady deterioration ofoffspring production Gradual and continuous ratherthan sudden degradation of performance suggestedthat poisoning was not the only threat in effect Inthis context several factors may have contributed togradually deteriorate ecological conditions for kitesin recent decades (1) Rabbit epidemics have causedprogressive declines in the availability of this keyprey (Vintildeuela amp Villafuerte 2003) (2) Lower preyavailability may have exacerbated competition withthe dense populations of other raptors with similardiets such as the ecologically similar and in creasingblack kite (3) Predation rates on adults and nestlingsmay have increased with the expansion of the popu-lations of potential predators such as eagle owls Bubobubo and goshawks Accipiter gentilis (4) Recentassessments have detected alarming levels of toxic
200
00
02
04
06
08
10
12
1980sndash1990s 1990sndash2000s 2000sndash2010s
Popu
latio
n gr
owth
rate
Period
Observed populationgrowth
Scenario 1 minimumEuropean survival
Scenario 2 meanEuropean survival
Scenario 3 maximumEuropean survival
Fig 8 Population growth of the Dontildeana red kite population during the past 4decades as predicted by matrix demographic models based on 3 scenarioswhich assumed that survival was equal to minimum mean or maximum sur-vival rates reported for other European populations (reviewed in Table 1)Predicted values are compared with observed declines from one decade to
the next
Fig 9 Population growth rate of red kites in relation to adultsurvival and breeding performance (mean number of youngfledged per territorial pair) based on a matrix populationmodel Note that the graph could be applied to any Euro-pean population The 3 points at the base of the graph repre-sent the minimum (black) mean (grey) and maximum (blue)survival published for European populations (reviewed in
Table 1)
Sergio et al Predator extinction debt in national park
chemicals in red kite eggs from Dontildeana (Goacutemara etal 2008) (5) Climate change and agricultural man-agement have lowered the water table with likelyimpacts on marsh inundation levels and aquatic prey(Garciacutea Novo amp Mariacuten Cabrera 2005 Diacuteaz-Paniaguaamp Aragoneacutes 2015 Schmidt et al 2017) (6) Conver-sion to intensive farmland in surrounding lands haseroded habitat and prey availability outside the pro-tected area which may have buffered kites fromperiods of low prey availability within the park (egduring droughts in the marshes) Some of the pat-terns of observed reproductive deterioration lendsupport to some of these impacts For exampledeclining clutch sizes and increasing rates of broodreduction suggest that food was not sufficient to sus-tain earlier reproductive levels while lowered hatch-ing success is often the result of chemical contamina-tion in raptors (review in Newton 1979) While eachof these threats will be quantitatively investigated indetail in the immediate future in the present contextthey illustrate the frequent and complex challengesfaced by (1) protected areas in maintaining biodiver-sity and viable populations of imperiled species and(2) conservation biologists in identifying causes ofdecline for subsequent management interventioneven in lsquoprivilegedrsquo sites such as reserves
Redistribution declining numbers and perform-ance had important repercussions for future viability(1) The population passed from producing gt100annual young to lt10minus20 which will make mainte-nance and recovery difficult (2) These young wereincreasingly produced in the core sectors of themarsh-ecotone within the National Park which prob-ably increased the dependence of the population onmarsh inundation in turn affected by problems oper-ating outside the park (Garciacutea Novo amp Mariacuten Cabrera2005 Diacuteaz-Paniagua amp Aragoneacutes 2015 Schmidt et al2017) (3) Steep declines in the percentage of suc-cessful pairs implied that future generations wereproduced by a progressively more restricted numberof pairs which will make the population more sub-ject to inbreeding and stochastic events For exam-ple in the last 3 yr all the annual young were pro-duced by 6 8 and 9 pairs respectively suggesting aneffective population size 4 to 9 times lower than theoverall abundance
Given all the above it is no surprise that demo-graphic models suggested a negative growth and apopulation incapable of self-sustenance In particu-lar the model that gave the best fit to past observeddeclines was the one based on minimum Europeansurvival estimates followed by the scenario based onmean European survival estimates Given the above-
mentioned threats declines and performance deteri-oration we would expect survival to be closer to min-imum than mean European levels as supported bythe observed fit to past and recent declines Theseresults have 2 main implications (1) If survival is aslow as we suspect demographic models predict vir-tual extinction within a few years demanding anurgent need for identification and management ofmortality threats as well as quantification of actualsurvival to refine predictions Note that virtual ex -tinction could be even earlier when taking intoaccount effective rather than total population sizeand a stochastic rather than deterministic populationmodel (2) Should actual survival be confirmed lowbut further declines not observed the populationwould be a sink sustained by external sources whichwould make it even more at risk from anthropogenicthreats outside the park and thus more challengingto manage (eg Hansen amp DeFries 2007 Blanco et al2017)
5 Conclusions and implications for conservation
The decades-long degradation that we depictedwas likely generated by a combination of factorsboth internal to the park (eg rabbit availabilitymarsh inundation rates predation and competitionwith other species) and external (eg illegal poi-soning contamination farmland intensification)Some of them will be amenable to managementand others less so but the first priority will be tofind rapid ways to identify the key factors thatdrive population growth so as to optimize conserva-tion action before it is too late For example focus-ing conservation lsquoblindlyrsquo on supplementary feedingcould be useless if the problem is chemical contam-ination The quickest way to obtain such informa-tion would be a satelliteGSM (Global System forMobile communication) tagging program that wouldallow to (1) obtain rapid estimates of health andsurvival for young and adults (eg Sergio et al2019) so as to recalibrate future projections andgoals (2) assess the relative contribution of mainmortality causes which is an essential first step inany recovery program (eg Gonzaacutelez et al 2007Margalida et al 2008 Smart et al 2010) and (3)identify the areas used by breeding and non-breed-ing individuals inside and outside of the park toassess their risk-exposure and intervene before orafter death (eg to prosecute perpetrators of illegalpoisoning or re trofit dangerous electricity pylons inareas of high use by kites)
201
Endang Species Res 38 189ndash204 2019
Until this information becomes available below welist some tentative figures and priorities for conserva-tion First of all restoring the current population toformer levels would undoubtedly be challenging andprobably unrealistic given the profound changesincurred by the wider Dontildeana ecosystem in recentdecades Thus we propose an initial target of 60pairs as a long-term restoration goal Elasticity analy-sis suggested that optimal management should focuson improving adult survival which had the largestimpact on population growth as in other long-livedspecies (Saether amp Bakke 2000 Whitfield et al 2004Kruumlger et al 2010) This could be attempted by in -creasing food availability especially of key prey suchas rabbits and by curtailing mortality threats such asillegal poisoning which still continues despite mucheffort to eradicate it by the local administration Thetelemetry program outlined above could help toidentify local perpetrators as occurred in other pop-ulations (Smart et al 2010 Tavecchia et al 2012) Onthe other hand despite their low elasticities repro-ductive rates are currently so low that it would befundamental to increase them eg by increasingfood availability and ensuring proper inundation ofthe marshes Based on Fig 5 we propose as initialtargets for restoration (1) survival rates equal orhigher than the European mean (adult survivalge087) and (2) a number of young fledged per territo-rial pair above 10 which would produce an increas-ing population provided that adult survival is equalto or above the European mean Note that Fig 5could be applied to any European population as atool to check its potential viability Given the highlythreatened status of red kites the speciesrsquo limitedrange confined to Europe and its ongoing declinesviability assessments such as ours may sadly becomemore important for the management and recovery ofmany populations
In conclusion red kites would probably be extinctin southern Spain without the institution of a largenational park In this sense this example well illus-trates how protected areas will continue to be corner-stones of global conservation of threatened taxaHowever their safety is not ensured by park institu-tion per se and performance monitoring and focusedaction will be needed to avoid potential extinctiondebts which may be more protracted than previouslyappreciated In our exemplary case despite the pres-ence of a large national park on prime fertile landwithin a developed country with adequate institu-tional and financial support a key threatened speciessuffered latent but steady declines for decadesobscured by problems of perception lack and frag-
mentation of information and likely caused by acomplex array of within-park threats and growingexternal pressures Viability maintenance and recov-ery will probably require concerted actions withinand outside of the park but only after detailed infor-mation on crucial aspects becomes available whichis probably the most urgent current priority We sus-pect that dynamics like the ones illustrated here aremore common than currently appreciated and willbecome more widespread as anthropogenic pres-sures increase around protected areas and as theirperformance monitoring becomes more prevalent
Acknowledgements We thank all the (too many to mention)researchers field workers visitors volunteers gamekeep-ers park managers and wardens that have provided datasince the 1960s In particular we thank F G Vilches L Gar-ciacutea and the Equipo de Seguimiento de Procesos Naturales ofthe Estacioacuten Bioloacutegica de Dontildeana-CSIC for help in the fieldSpecial thanks to F G Vilches for the priceless help with thecollation and organization of historical information Wethank J P Castellano I Redondo and all the lsquoArea de Con-servacioacutenrsquo of Dontildeana National Park for constant interest andsupport We thank R Cadenas J Madrid R Arenas J RBenitez and all the pertinent personnel of the Consejeriacutea deMedio Ambiente of the Junta de Andaluciacutea for informationon current nest locations in the Sierra de Huelva and fortheir constant attentive support We are grateful to Dr NBunnefeld and 2 anonymous reviewers for constructivecomments that improved the manuscript This study wasfunded by the Foundation Jaime Gonzaacutelez-Gordon and bythe research project 16022015 of the Spanish Ministry ofAgriculture Food and the Environment (National ParksAutonomous Agency)
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Blanco G Cardells J Garijo-Toledo MM (2017) Supplemen-tary feeding and endoparasites in threatened avian scav-engers coprologic evidence from red kites in their win-tering stronghold Environ Res 155 22minus30
Brashares JS Arcese P Sam MK (2001) Human demographyand reserve size predict wildlife extinction in WestAfrica Proc Biol Sci 268 2473minus2478
Bustamante J (1993) Post-fledging dependence period anddevelopment of flight and hunting behaviour in the redkite Milvus milvus Bird Study 40 181minus188
Cano C Ayerza P Fernaacutendez J (2008) Poisoning in Spain(1990minus2005) analysis of the problem incidence andcauses WWFAdena Madrid (in Spanish)
Caswell H (2001) Matrix population models Sinauer Sun-derland MA
Ceballos JJ Guimeraacute VM (1992) Guiacutea de las aves de Jerez yde la Provincia de Caacutediz atlas ornitoloacutegico de lasespecies nidificantes Ayuntamiento de Jerez Jerez
Craigie ID Baillie JEM Balmford A Carbone C Collen BGreen RE Hutton JM (2010) Large mammal population
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declines in Africarsquos protected areas Biol Conserv 143 2221minus2228
Czech B (2005) The capacity of the National WildlifeRefuge System to conserve threatened and endangeredanimal species in the United States Conserv Biol 19 1246minus1253
Delibes M Garciacutea L (1984) Haacutebitos alimenticios del milanoreal en Dontildeana durante el periodo de criacutea Ardeola 31 115minus121
Diacuteaz-Paniagua C Aragoneacutes D (2015) Permanent and tempo-rary ponds in Dontildeana National Park (SW Spain) arethreatened by desiccation Limnetica 34 407minus424
Evans IM Summers RW OrsquoToole L Orr-Ewing DC Snell NSmith J (1999) Evaluating the success of translocatingred kites Milvus milvus to the UK Bird Study 46 129minus144
Ferrer M Hiraldo F (1991) Evaluation of management tech-niques for the Spanish imperial eagle Wildl Soc Bull 19 436minus442
Garciacutea Novo F Mariacuten Cabrera C (2005) Dontildeana water andbiosphere Dontildeana 2005 Project Spanish Ministry of theEnvironment Madrid
Gaston KJ Jackson SF Cantuacute-Salazar L Cruz-Pintildeoacuten G(2008) The ecological performance of protected areasAnnu Rev Ecol Evol Syst 39 93minus113
Godet L Devictor V Jiguet F (2007) Estimating relative pop-ulation size included within protected areas BiodiversConserv 16 2587minus2598
Goacutemara B Gonzaacutelez MJ Baos R Hiraldo F Abad E RiveraJ Jimeacutenez B (2008) Unexpected high PCB and total DDTlevels in the breeding population of red kite (Milvus mil-vus) from Dontildeana National Park south-western SpainEnviron Int 34 73minus78
Gonzaacutelez LM Margalida A Mantildeosa S Saacutenchez R and oth-ers (2007) Causes and spatio-temporal variations of non-natural mortality in the vulnerable Spanish imperialeagle Aquila adalberti during a recovery period Oryx41 495minus502
Hansen AJ DeFries R (2007) Ecological mechanisms linkingprotected areas to surrounding lands Ecol Appl 17 974minus988
Hernaacutendez FJ Donaacutezar JA Hiraldo F (2001) Evaluacioacuten deluso de venenos para el control de predadores en laComunidad Autoacutenoma Andaluza y su impacto en la con-servacioacuten de especies amenazadas de vertebrados Con-sejeria de Medio Ambiente and Estacioacuten Bioloacutegica deDontildeana Sevilla
IUCN (The World Conservation Union) (1994) Guidelines forprotected area management categories IUCN Gland
Knott J Newbery P Barov B (2009) Action plan for the redkite Milvus milvus in the European Union EuropeanCommission Brussels
Kruumlger O Gruumlnkorn T Struwe-Juhl B (2010) The return ofthe white-tailed eagle (Haliaeetus albicilla) to northernGermany modelling the past to predict the future BiolConserv 143 710minus721
Loacutepez V (1861) Cataacutelogo de las aves observadas enAndaluciacutea Madrid
Loacutepez G and others (2009) Management measures to controla feline leukemia virus outbreak in the endangered Iber-ian lynx Anim Conserv 12 173minus182
Margalida A Heredia R Razin M Hernaacutendez M (2008)Sources of variation in mortality of the bearded vultureGypaetus barbatus in Europe Bird Conserv Int 18 1minus10
Naughton-Treves L Holland MB Brandon K (2005) The roleof protected areas in conserving biodiversity and sustain-
ing local livelihoods Annu Rev Environ Resour 30 219minus252
Newton I (1979) Population ecology of raptors T amp AD PoyserBerkhamsted
Newton I Davis PE Davis JE (1989) Age of first breedingdispersal and survival of red kites Milvus milvus inWales Ibis 131 16minus21
Otero C Castieacuten E Senosiaiacuten R Portillo F (1978) Fauna deCazorla vertebrados Publicaciones del Ministerio deAgricultura Madrid
Parks SA Harcourt AH (2002) Reserve size local humandensity and mammalian extinctions in US protectedareas Conserv Biol 16 800minus808
R Development Core Team (2018) R a language and envi-ronment for statistical computing R Foundation for Sta-tistical Computing Vienna wwwr-projectorg
Saeligther BE Bakke Oslash (2000) Avian life history variation andcontribution of demographic traits to the populationgrowth rate Ecology 81 642minus653
Sanz-Aguilar A De Pablo F Donaacutezar JA (2015) Age-depen-dent survival of island vs mainland populations of twoavian scavengers delving into migration costs Oecolo-gia 179 405minus414
Schaub M (2012) Spatial distribution of wind turbines is cru-cial for the survival of red kite populations Biol Conserv155 111minus118
Schmidt G Saacutenchez Navarro R Hernaacutendez E Carmona JJFuentelsaz F Seiz R (2017) The state of water in Dontildeana an evaluation of the state of the water and of the ecosys-tems of the protected space WWFAdena Madrid
Scott JM Davis FW McGhie RG Wright RG Groves CEstes J (2001) Nature reserves Do they capture the fullrange of Americarsquos biological diversity Ecol Appl 11 999minus1007
Seoane J Vintildeuela J Diacuteaz-Delgado R Bustamante J (2003)The effects of land use and climate on red kite distribu-tion in the Iberian peninsula Biol Conserv 111 401minus414
Sergio F Blas J Feroro M Fernaacutendez N Donaacutezar JAHiraldo F (2005) Preservation of wide-ranging top pred-ators by site-protection black and red kites in DontildeanaNational Park Biol Conserv 125 11minus21
Sergio F Tanferna A Blas J Blanco G Hiraldo F (2019) Reli-able methods for identifying animal deaths in GPS- andsatellite-tracking data review testing and calibrationJ Appl Ecol 56562ndash572
Smart J Amar A Sim IMW Etheridge B Cameron DChristie G Wilson JD (2010) Illegal killing slows popula-tion recovery of a re-introduced raptor of high conserva-tion concern mdash the red kite Milvus milvus Biol Conserv143 1278minus1286
Tavecchia G Adrover J Muntildeoz Navarro A Pradel R (2012)Modelling mortality causes in longitudinal data in thepresence of tag loss application to raptor poisoning andelectrocution J Appl Ecol 49 297minus305
Tenan S Adrover J Muntildeoz Navarro A Sergio F TavecchiaG (2012) Demographic consequences of poison-relatedmortality in a threatened bird of prey PLOS ONE 7 e49187
Tilman D May RM Lehman CL Nowak MA (1994) Habitatdestruction and the extinction debt Nature 371 65minus66
Torres Esquivias JA Jordano P Leoacuten A (1981) Aves de presadiurnas de la provincia de Coacuterdoba Publicaciones CA yMP Coacuterdoba
Veiga JP Hiraldo F (1990) Food habits and the survival andgrowth of nestlings in two sympatric kites (Milvus milvus
203
Endang Species Res 38 189ndash204 2019
and Milvus migrans) Holarct Ecol 13 62minus71 Villafuerte R Vintildeuela J Blanco JC (1998) Extensive preda-
tor persecution caused by population crash in a gamespecies the case of red kites and rabbits in Spain BiolConserv 84 181minus188
Vintildeuela J (2004) Milano real Milvus milvus In Madrontildeo AGonzaacutelez C Atienza JC (eds) Libro rojo de las aves deEspantildea Direccioacuten General para la BiodiversidadminusSEOBirdLife Madrid p 120minus125
Vintildeuela J Villafuerte R (2003) Predators and rabbits (Oryc-tolagus cuniculus) in Spain a key conflict for Europeanraptor conservation In Thompson DBA Redpath SMFielding AH Marquiss M Galbraith CA (eds) Birds ofprey in a changing environment The Stationery OfficeEdinburgh p 511minus526
Vintildeuela J Martiacute R Ruiz A (eds) (1999) El milano real enEspantildea SEOBirdlife Madrid
Watson JEM Dudley N Segan DB Hockings M (2014) Theperformance and potential of protected areas Nature515 67minus73
Whitfield SM Bell KE Philippi T Sasa M and others (2007)Amphibian and reptile declines over 35 years at La SelvaCosta Rica Proc Natl Acad Sci USA 104 8352minus8356
Whitfield DP Fielding AH McLeod DRA Haworth PF(2004) Modelling the effects of persecution on the popu-lation dynamics of golden eagles in Scotland Biol Con-serv 119 319minus333
Zuur A Ieno EN Walker N Saveliev AA Smith GM (2009)Mixed effects models and extensions in ecology with RSpringer New York NY
204
Editorial responsibility Nils BunnefeldStirling UK
Submitted October 8 2018 Accepted January 28 2019Proofs received from author(s) April 7 2019
Endang Species Res 38 189ndash204 2019
the 1970sminus1980s (from a conservative estimate of40minus77 pairs to 2minus4 current pairs) Thus Dontildeanahosted 52minus63 of the regional population in the1970sminus80s and 95minus96 after 2010 increasing its rel-ative strategic importance
32 Abundance and trends in Dontildeana
Different sectors of the park showed differenttrends (Fig 2 Fig S2) Numbers appeared (1) stableor in moderate decline in the Reserva Biologica deDontildeana RBD (sectors 1 2 and 3) (2) stable or increas-ing in the sector of Puntal and in the vera of Algaida-Manecorro as well as its interior These areas werecharacterized by the removal of Eucalyptus planta-tions that converted large areas of woodland to opengrassland in the 1990s (sectors 4 and 5) or alwaysmaintained a very open landscape through extensivegrazing by livestock (sector 6) Finally (3) declines ofvarying magnitude were observed in all peripheralsectors to the north east and south While declineswere moderate in the eastern and southern sectorsthat were monitored less continuously dramatic de -clines were evident for all the northern sectors in -cluding portions of the National Park and its buffer-ing Natural Park In these sectors (7 8 9) a populationof 20minus25 pairs was basically eradicated in a few yearsbetween the late 1980s and early 1990s re mainingvirtually extinct to date (Fig 3) This rapid eradica-tion was accompanied by the detection of adultsfound dead by poisoning in or under their nest Over-all there was a significant preponderance of declinesbetween the numbers re corded in the earliest survey
available for each sector and the 2010s (binomial testp lt 0001 Fig 2) Correspondingly the surface of theoverall and core distribution range of the Dontildeanapopulation declined by 53 and 58 respectively(Fig 4)
When summing up all sectors the overall Dontildeanapopulation was conservatively (see Section 23) esti-mated at 69 pairs (max peak of 82) in the 1980s 61(max 86) in the 1990s 53 (max 64) in 2000minus2009and 47 (max 70) in 2010minus2017 (Table 2) In 2017 thepopulation was composed of 37 pairs representing a46minus55 decline compared to the meanminusmaximumlevels of the 1980s ie in less than 40 yr Thus the~50 declining rate within the park was high butwas only almost half of the ~95 decline estimatedfor outside pairs over the same 4 decades (χ2 = 184p lt 00001)
33 Distribution in Dontildeana
Local eradication and differential declines pro-duced a contraction of the overall range and a shiftin the relative importance of some sectors Thusin the 1980s the population was well distributedthrough all sectors but more concentrated in thecore sectors of RBD vera Puntal and in the northernpinewoods of the Natural Park buffer (Fig 5aTable 2) From the 1990s onwards the populationbecame progressively more concentrated within theNational Park in particular in the ecotonal zonebetween the marsh and terrestrial habitats withvery low numbers or local extinctions in all theother sectors (Fig 5b Table 2)
34 Offspring production in Dontildeana
Except for the number of young persuccessful pair all breeding parame-ters deteriorated through time (all χ2 ge1733 all p lt 00017) The probabilityof laying eggs clutch size hatchingsuccess the likelihood of successfullyraising chicks to fledging and thenumber of young per territorialbreeding and successful pair declinedthrough the last 5 decades while theextent of brood reduction progres-sively increased (Fig 6) Deteriorationof reproduction was particularly pro-nounced for the probability of layingfor brood reduction for the probability
194
80 ndash100 ndash80 ndash60 ndash40 ndash20 0 20 40 60 100
10 Marismillas11 Sanlucar pinewood
12 AbalarioCumulative total
1 RBD vera2 RBD interior
3 RBD sand dunes
Change in breeding numbers compared to the 1980s ()
Sector
4 Vera Algaida-Manecorro5 Interior6 Puntal
7 Coto del Rey8 NW pinewoods9 NE pinewoods
Fig 2 Percentage change in breeding numbers of the Dontildeana red kite popu-lation by sector from the 1980s or since the earliest available record (1990s for
Puntal and Abalario) to 2017 RBD Reserva Biologica de Dontildeana
Sergio et al Predator extinction debt in national park
of successful breeding and for the number of fledgedyoung (Fig 7)
On average the whole population was estimated toproduce 103 fledglings per year in the 1980s this al-most halved to 57 in the 1990s 48 in 2000minus2009 andagain declined to more than halved to 19 in 2010minus2017In 2015 2016 and 2017 the population produced 7 7and 15 fledglings respectively Population decline and
breeding deterioration were accompa-nied by a change in the relative impor-tance of some sectors for offspring pro-duction (Fig 5 Table 2) In the 1980smost young were produced in thesector RBD vera and the northernpinewoods and most other sectors stillcontributed gt5 of the annual youngproduction (Fig 5c) In subsequentdecades fledgling production becameconcentrated in the marsh ecotone(Puntal RBD vera vera of Algaida-Manecorro) with additional inputsfrom some interior or peripheral sectorsand a larger portion of sectors with vir-tually zero contribution to future gener-ations (Fig 5d) Fig 3 illustrates howdiffuse successful reproduction was inthe 1980s compared to 2017
35 Comparison with otherEuropean populations
Compared to other areas of Europethe Dontildeana population showed a highdensity in the 1980s (well above theEuropean mean Table S3) This pro-gressively declined and has changedto below-average density since 2010All breeding parameters were wellbelow the mean European estimatesfrom the 1980s onwards (Table S3) Inparticular the percentage of success-ful pairs and the number of youngfledged per breeding pair are cur-rently 2 to 3 times lower than themean European values
36 Population growth andprojections for the Dontildeana
population
Observed declines were well cap-tured by the growth rate predicted by the populationmodel based on the minimum European survivalrates (Fig 8) The other 2 scenarios of maximum andmean survival rates predicted a stable population ordeclines from the year 2000 onwards only (Fig 8)For the 2010s the model estimated λ = 0849 0960and 1066 for the scenario based on minimum meanand maximum survival estimates respectively
195
Fig 3 Distribution of breeding territories in Dontildeana (a) in the 1980s and (b) in2017 Pairs that bred successfully (black points) were much more frequent andmore widely distributed especially in the northern sectors and in the NaturalPark in the 1980s than in 2017 when most pairs failed to raise chicks to fledg-ing (white points) Territory locations have been moved slightly for conserva-tion reasons and locations from the 1980s could only be approximate for some
territories especially those in the northern pinewoods
Endang Species Res 38 189ndash204 2019
Based on the model with minimum survival rateswhich gave the best fit to past declines the popula-tion of 37 pairs censused in 2017 would be reduced to7 pairs within 10 yr and virtually extinct (le2 pairs) in17 yr The less supported scenario of mean Europeansurvival estimates projected a population of 25 pairsin 10 yr while the most optimistic scenario of maxi-mum survival predicted a full recovery to the 1980spopulation level of 70 pairs in 10 yr
Despite the current extremely lowbreeding success under all 3 scenar-ios of survival the population growthrate was least sensitive to changes infledglings production [E(F) = 0048minus0079 S(F) = 0137minus 0277] and mostsensitive to variations in adult survivalprobability [E(θ) = 0843minus 0904 S(θ) =0929minus 0955] In Fig 9 we plot thecombination of fledgling productionand adult survival that produce differ-ent levels of population growth Atcurrent levels of reproduction adultsurvival would have to be around090minus095 to attain a stable or slightlyincreasing population while restoringbreeding success to the levels of the1980s of 13 young per pair wouldimply a stable population even with arelatively low adult survival of ~077ie below the minimum ever recordedfor the species (Fig 9)
4 DISCUSSION
Our results showed that the currentdeteriorated condition of the Dontildeanared kite population was not a recentphenomenon but the tip of the ice-berg of decades of regional and localdegradation Although the protectedarea slowed the background levels ofregional decline and likely saved thespecies from local extinction its via-bility maintenance performance wasfar from satisfactory In a way the ob -served long-term deterioration actedas a protracted diluted form of extinc-tion debt (Tilman et al 1994) paidover a time-frame of several decadesWe suspect that similar conditionsmay be common in other protectedareas making this a classical example
of gradual underlying pressures diluted over such along time-frame that their severity becomes evidentonly through a large-scale long-term asses sment oronce population degradation has reached its extremeconsequences Note that for many parameters dete-rioration was not especially alarming from onedecade to the next making it difficult for the succes-sion of local field observers to appreciate the overallseverity of the long-term trends This difficulty in
196
Fig 4 Distribution range of red kites in Dontildeana (a) in the 1980s and (b) in2017 The pink outer polygon represents a 95 kernel constructed aroundthe territory locations while the red polygon is a 50 kernel showing the corearea of distribution The overall and core distribution range contracted by 534and 581 respectively Territory locations have been moved slightly for
conservation reasons
Sergio et al Predator extinction debt in national park 197
12
3 R
BD
4 V
era
56
7 C
oto
8 N
W9
NE
10
11
12
Tot
al
RB
DR
BD
san
dA
lgai
da
Inte
rior
Pu
nta
ld
elp
ine-
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aris
-S
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Ab
alar
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ne
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Man
ecor
roR
eyw
ood
sw
ood
sm
illa
sp
inew
ood
a) M
ean
no
of
pai
rs19
80minus
1989
141
52
33
40a
20a
80b
50
107
44
50
30
40b
687
1990
minus19
9915
35
11
37
74
08
03
34
40
74
5e2
5c4
0a60
8minus
115
2000
minus20
0916
05
21
47
05
06
31
01
00
14
5e2
03
1a52
5minus
236
2010
minus20
1713
03
42
56
63
98
41
90
50
13
01
72
147
1minus
315
2017
100
35
211
00
03
12
37minus
462
b)
No
of
you
ng
pro
du
ced
an
nu
ally
1980
minus19
8916
14
25
66
43
09
610
020
311
06
04
56
010
26
1990
minus19
999
82
60
68
44
06
92
46
60
95
13
86
056
9minus
445
2000
minus20
0913
21
61
27
25
83
71
21
60
24
53
04
647
7minus
535
2010
minus20
172
60
61
11
82
33
50
90
30
01
62
91
919
4minus
811
2017
10
03
07
00
00
22
150
minus85
4
c)
of
the
tota
l p
op
ula
tio
n i
n e
ach
sec
tor
1980
minus19
8920
57
64
85
82
911
67
315
56
47
34
45
819
90minus
1999
251
84
21
126
66
131
55
73
12
74
41
66
2000
minus20
0929
49
62
612
99
211
51
81
80
28
33
79
120
10minus
2017
276
72
53
141
82
178
40
11
03
64
36
45
2017
270
00
81
135
54
297
00
00
00
81
27
54
d)
c
on
trib
uti
on
of
each
sec
tor
to t
ota
l an
nu
al y
ou
ng
pro
du
ctio
n19
80minus
1989
157
41
54
94
62
29
97
198
107
58
44
58
1990
minus19
9917
24
61
112
114
77
04
211
61
68
96
610
520
00minus
2009
277
33
24
78
151
121
24
34
04
94
63
96
2010
minus20
1713
43
35
418
19
411
74
81
30
08
215
09
620
176
70
00
046
720
00
00
00
00
00
013
313
3
a Cro
ss-c
omb
ined
est
imat
e b
Sta
tic
bac
k-e
stim
ate
c In
terp
olat
ed e
stim
ate
See
Sec
tion
23
for
det
ails
Tab
le 2
(a
) M
ean
nu
mb
er o
f p
airs
an
d (
b)
cum
ula
tive
nu
mb
er o
f of
fsp
rin
g p
rod
uce
d a
nn
ual
ly b
y th
e D
ontildean
a re
d k
ite
pop
ula
tion
wit
hin
eac
h s
ecto
r an
d i
n t
he
wh
ole
par
k o
ver
the
pas
t d
ecad
es a
nd
in 2
017
Per
cen
tag
e of
(c)
pai
rs a
nd
(d
) yo
un
g c
ontr
ibu
ted
by
each
sec
tor
to t
he
over
all p
opu
lati
on S
ecto
rs c
ontr
ibu
tin
g m
ore
than
10
ar
e h
igh
lig
hte
d i
n b
old
T
otal
ref
ers
to t
he
sum
of
all
sect
ors
d
ecli
ne
is t
he
dec
lin
e co
mp
ared
to
the
1980
s P
rop
orti
onal
con
trib
uti
ons
are
also
ill
ust
rate
d i
n F
ig
5
RB
D R
eser
va B
iolo
gic
a d
e D
ontildean
a
Endang Species Res 38 189ndash204 2019
detecting the problem was likely exacerbated by thefollowing factors that could be defined as lsquoperceptionobstaclesrsquo (1) The fact that a population becomesmore and more restricted to a park is often used toillustrate the positive role of protected areas byfocusing their performance assessments on range
coverage ie the capability of protected areas tocover a large portion of a species range (eg Czech2005 Godet et al 2007) This diverts attention fromthe wider problems of range contraction and from theactual performance of the park in terms of viabilitymaintenance (Gaston et al 2008) (2) Confinement to
198
of nests in each sector
of annual young generated by each sector
1980s 2010s
1980s 2010s
a) b)
c) d)
Fig 5 Percentage of the total red kite population in each of 12 sectors of Dontildeana (a) in the 1980s and (b) in the 2010s percent-age of the annual young production generated by each sector (c) in the 1980s and (d) in the 2010s (a) In the 1980s the bulk ofthe population was concentrated in northern sectors (7 and 8) and in the southern shores of the marshes (sectors 1 6 and 10)(b) In the 2010s the population virtually disappeared from the northern sectors and became essentially confined to the na-tional park where it concentrated along the marshes (c) In the 1980s the population generated more than 100 young eachyear most of them produced by the northern sectors (7 8 9) and by the northern shores of the marshes (sectors 1 and 4) (d) Inthe 2010s the population generated less than 10 young mostly generated close to wetlands (sectors 1 4 11) with homo -geneously low numbers elsewhere Colors (yellow rarr orange rarr red) classify sectors by tertiles of the range of percentage
contribution
Sergio et al Predator extinction debt in national park
a protected area is usually accompanied by the auto-matic presumption that this will act as a source areawith limited anthropogenic impacts an assumptionthat is increasingly disproved (Hansen amp DeFries2007 Gaston et al 2008 Watson et al 2014) (3) Long-term assessments such as ours required the lengthy
collation of fragmented informationfrom a large number of sequentialfield workers and administrationseach of which had a very limited per-ception of the overall situation (4)Much monitoring was conducted inthe core areas of the park like theRBD where the species has alwaysbeen most abundant and relativelystable (eg Sergio et al 2005) con-fusing the perception of broaderdeclines (5) Finally large numbersof wintering migrants boost the pop-ulation in the winter and earlyspring often producing an optimisticimpression of apparent abundance
even in relatively expert members of the public or oflocal administrations as we frequently noted in pub-lic talks and private conversations
Overall the decline occurred at multiple levels redkites were originally widespread throughout south-ern Spain (Loacutepez 1861) but became progressively
199
2030405060708090
100110
Bree
ding
su
cces
sful
()
a breeding pairs successful pairs
202122232425262728
Clut
ch si
ze
b
25
35
45
55
65
75
85
1970-79 1980-89 1990-99 2000-09 2010-17
Hatc
hing
succ
ess
broo
d re
duct
ion
()
Decade
c Hatching successBrood reduction
03
06
09
12
15
18
21
1970-79 1980-89 1990-99 2000-09 2010-17
Youn
g fle
dged
Decade
d Young breeding pairYoung successful pair
Fig 6 Reproductive parameters of the red kite population of Dontildeana (a) percentage of pairs laying eggs (black dots n = 804)and successfully raising fledglings (white dots n = 1185) (b) mean clutch size (n = 469) (c) hatching success (percentage ofeggs that hatched black dots n = 353) and brood reduction (percentage of chicks that disappeared during the nestling periodwhite dots n = 240) (d) mean number of young fledged per territorial pair (black dots n = 1145) and per successful pair (white
dots n = 576)
0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75
Young fledgedsuccessful pairYoung fledgedbreeding pairYoung fledgedterritorial pair
Probability of successful breedingBrood reduction
Hatching successClutch size
Probability of laying
Deterioration ()
Breeding parameter
Fig 7 Percentage deterioration of breeding parameters of the red kite popu-lation of Dontildeana between the 1980s and the 2010s
Endang Species Res 38 189ndash204 2019
confined to the protected area of Dontildeana in recentdecades However the park did not confer automaticsafety and declines and range contraction also con-tinued within the protected area suggesting perva-sive pressures and range erosion at multiple spatialscales In particular almost one third of the Dontildeana
population was virtually eradicatedfrom the northern pinewoods of thebuffering Natural Park in 5 to 7 yrbetween the late 1980s and early1990s Several lines of evidence sug-gest that illegal poisoning was themain cause of this eradication (1) Sev-eral adults were found poisoned undertheir nest in those sectors and years(2) Large-scale poisoning campaignsof raptors were reported throughoutSpain in those exact same years asa consequence of huntersrsquo illegalattempts to control predator popula-tions to increase the rapidly deterio-rating numbers of small game (rabbitsand partridges Villafuerte et al 1998Vintildeuela amp Villafuerte 2003 Cano et al2008) In this sense the National Parksuffered much wider national-level
pressures (3) The northern sectors of the parkwhere the eradication took place included or wereclose to private small-game reserves and predatorcontrol was well known to occur in some of them (4)Finally the rapidity of the eradication of such a long-lived species (maximum longevity of 29 yr in Dontilde -ana) implied a causative agent that directly affectedadult mortality (Saether amp Bakke 2000) such as poi-soning The marked impact of poisoning on adult sur-vival and population growth are well recognized forthis species whose facultative scavenging habits andforaging method of meticulous low and slow quar-tering of the ground make it particularly sensitive tothis threat (Smart et al 2010 Tavecchia et al 2012Tenan et al 2012 Sanz-Aguilar et al 2015)
Spikes of rapid local eradication were superim-posed on more gradual but steady deterioration ofoffspring production Gradual and continuous ratherthan sudden degradation of performance suggestedthat poisoning was not the only threat in effect Inthis context several factors may have contributed togradually deteriorate ecological conditions for kitesin recent decades (1) Rabbit epidemics have causedprogressive declines in the availability of this keyprey (Vintildeuela amp Villafuerte 2003) (2) Lower preyavailability may have exacerbated competition withthe dense populations of other raptors with similardiets such as the ecologically similar and in creasingblack kite (3) Predation rates on adults and nestlingsmay have increased with the expansion of the popu-lations of potential predators such as eagle owls Bubobubo and goshawks Accipiter gentilis (4) Recentassessments have detected alarming levels of toxic
200
00
02
04
06
08
10
12
1980sndash1990s 1990sndash2000s 2000sndash2010s
Popu
latio
n gr
owth
rate
Period
Observed populationgrowth
Scenario 1 minimumEuropean survival
Scenario 2 meanEuropean survival
Scenario 3 maximumEuropean survival
Fig 8 Population growth of the Dontildeana red kite population during the past 4decades as predicted by matrix demographic models based on 3 scenarioswhich assumed that survival was equal to minimum mean or maximum sur-vival rates reported for other European populations (reviewed in Table 1)Predicted values are compared with observed declines from one decade to
the next
Fig 9 Population growth rate of red kites in relation to adultsurvival and breeding performance (mean number of youngfledged per territorial pair) based on a matrix populationmodel Note that the graph could be applied to any Euro-pean population The 3 points at the base of the graph repre-sent the minimum (black) mean (grey) and maximum (blue)survival published for European populations (reviewed in
Table 1)
Sergio et al Predator extinction debt in national park
chemicals in red kite eggs from Dontildeana (Goacutemara etal 2008) (5) Climate change and agricultural man-agement have lowered the water table with likelyimpacts on marsh inundation levels and aquatic prey(Garciacutea Novo amp Mariacuten Cabrera 2005 Diacuteaz-Paniaguaamp Aragoneacutes 2015 Schmidt et al 2017) (6) Conver-sion to intensive farmland in surrounding lands haseroded habitat and prey availability outside the pro-tected area which may have buffered kites fromperiods of low prey availability within the park (egduring droughts in the marshes) Some of the pat-terns of observed reproductive deterioration lendsupport to some of these impacts For exampledeclining clutch sizes and increasing rates of broodreduction suggest that food was not sufficient to sus-tain earlier reproductive levels while lowered hatch-ing success is often the result of chemical contamina-tion in raptors (review in Newton 1979) While eachof these threats will be quantitatively investigated indetail in the immediate future in the present contextthey illustrate the frequent and complex challengesfaced by (1) protected areas in maintaining biodiver-sity and viable populations of imperiled species and(2) conservation biologists in identifying causes ofdecline for subsequent management interventioneven in lsquoprivilegedrsquo sites such as reserves
Redistribution declining numbers and perform-ance had important repercussions for future viability(1) The population passed from producing gt100annual young to lt10minus20 which will make mainte-nance and recovery difficult (2) These young wereincreasingly produced in the core sectors of themarsh-ecotone within the National Park which prob-ably increased the dependence of the population onmarsh inundation in turn affected by problems oper-ating outside the park (Garciacutea Novo amp Mariacuten Cabrera2005 Diacuteaz-Paniagua amp Aragoneacutes 2015 Schmidt et al2017) (3) Steep declines in the percentage of suc-cessful pairs implied that future generations wereproduced by a progressively more restricted numberof pairs which will make the population more sub-ject to inbreeding and stochastic events For exam-ple in the last 3 yr all the annual young were pro-duced by 6 8 and 9 pairs respectively suggesting aneffective population size 4 to 9 times lower than theoverall abundance
Given all the above it is no surprise that demo-graphic models suggested a negative growth and apopulation incapable of self-sustenance In particu-lar the model that gave the best fit to past observeddeclines was the one based on minimum Europeansurvival estimates followed by the scenario based onmean European survival estimates Given the above-
mentioned threats declines and performance deteri-oration we would expect survival to be closer to min-imum than mean European levels as supported bythe observed fit to past and recent declines Theseresults have 2 main implications (1) If survival is aslow as we suspect demographic models predict vir-tual extinction within a few years demanding anurgent need for identification and management ofmortality threats as well as quantification of actualsurvival to refine predictions Note that virtual ex -tinction could be even earlier when taking intoaccount effective rather than total population sizeand a stochastic rather than deterministic populationmodel (2) Should actual survival be confirmed lowbut further declines not observed the populationwould be a sink sustained by external sources whichwould make it even more at risk from anthropogenicthreats outside the park and thus more challengingto manage (eg Hansen amp DeFries 2007 Blanco et al2017)
5 Conclusions and implications for conservation
The decades-long degradation that we depictedwas likely generated by a combination of factorsboth internal to the park (eg rabbit availabilitymarsh inundation rates predation and competitionwith other species) and external (eg illegal poi-soning contamination farmland intensification)Some of them will be amenable to managementand others less so but the first priority will be tofind rapid ways to identify the key factors thatdrive population growth so as to optimize conserva-tion action before it is too late For example focus-ing conservation lsquoblindlyrsquo on supplementary feedingcould be useless if the problem is chemical contam-ination The quickest way to obtain such informa-tion would be a satelliteGSM (Global System forMobile communication) tagging program that wouldallow to (1) obtain rapid estimates of health andsurvival for young and adults (eg Sergio et al2019) so as to recalibrate future projections andgoals (2) assess the relative contribution of mainmortality causes which is an essential first step inany recovery program (eg Gonzaacutelez et al 2007Margalida et al 2008 Smart et al 2010) and (3)identify the areas used by breeding and non-breed-ing individuals inside and outside of the park toassess their risk-exposure and intervene before orafter death (eg to prosecute perpetrators of illegalpoisoning or re trofit dangerous electricity pylons inareas of high use by kites)
201
Endang Species Res 38 189ndash204 2019
Until this information becomes available below welist some tentative figures and priorities for conserva-tion First of all restoring the current population toformer levels would undoubtedly be challenging andprobably unrealistic given the profound changesincurred by the wider Dontildeana ecosystem in recentdecades Thus we propose an initial target of 60pairs as a long-term restoration goal Elasticity analy-sis suggested that optimal management should focuson improving adult survival which had the largestimpact on population growth as in other long-livedspecies (Saether amp Bakke 2000 Whitfield et al 2004Kruumlger et al 2010) This could be attempted by in -creasing food availability especially of key prey suchas rabbits and by curtailing mortality threats such asillegal poisoning which still continues despite mucheffort to eradicate it by the local administration Thetelemetry program outlined above could help toidentify local perpetrators as occurred in other pop-ulations (Smart et al 2010 Tavecchia et al 2012) Onthe other hand despite their low elasticities repro-ductive rates are currently so low that it would befundamental to increase them eg by increasingfood availability and ensuring proper inundation ofthe marshes Based on Fig 5 we propose as initialtargets for restoration (1) survival rates equal orhigher than the European mean (adult survivalge087) and (2) a number of young fledged per territo-rial pair above 10 which would produce an increas-ing population provided that adult survival is equalto or above the European mean Note that Fig 5could be applied to any European population as atool to check its potential viability Given the highlythreatened status of red kites the speciesrsquo limitedrange confined to Europe and its ongoing declinesviability assessments such as ours may sadly becomemore important for the management and recovery ofmany populations
In conclusion red kites would probably be extinctin southern Spain without the institution of a largenational park In this sense this example well illus-trates how protected areas will continue to be corner-stones of global conservation of threatened taxaHowever their safety is not ensured by park institu-tion per se and performance monitoring and focusedaction will be needed to avoid potential extinctiondebts which may be more protracted than previouslyappreciated In our exemplary case despite the pres-ence of a large national park on prime fertile landwithin a developed country with adequate institu-tional and financial support a key threatened speciessuffered latent but steady declines for decadesobscured by problems of perception lack and frag-
mentation of information and likely caused by acomplex array of within-park threats and growingexternal pressures Viability maintenance and recov-ery will probably require concerted actions withinand outside of the park but only after detailed infor-mation on crucial aspects becomes available whichis probably the most urgent current priority We sus-pect that dynamics like the ones illustrated here aremore common than currently appreciated and willbecome more widespread as anthropogenic pres-sures increase around protected areas and as theirperformance monitoring becomes more prevalent
Acknowledgements We thank all the (too many to mention)researchers field workers visitors volunteers gamekeep-ers park managers and wardens that have provided datasince the 1960s In particular we thank F G Vilches L Gar-ciacutea and the Equipo de Seguimiento de Procesos Naturales ofthe Estacioacuten Bioloacutegica de Dontildeana-CSIC for help in the fieldSpecial thanks to F G Vilches for the priceless help with thecollation and organization of historical information Wethank J P Castellano I Redondo and all the lsquoArea de Con-servacioacutenrsquo of Dontildeana National Park for constant interest andsupport We thank R Cadenas J Madrid R Arenas J RBenitez and all the pertinent personnel of the Consejeriacutea deMedio Ambiente of the Junta de Andaluciacutea for informationon current nest locations in the Sierra de Huelva and fortheir constant attentive support We are grateful to Dr NBunnefeld and 2 anonymous reviewers for constructivecomments that improved the manuscript This study wasfunded by the Foundation Jaime Gonzaacutelez-Gordon and bythe research project 16022015 of the Spanish Ministry ofAgriculture Food and the Environment (National ParksAutonomous Agency)
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Blanco G Cardells J Garijo-Toledo MM (2017) Supplemen-tary feeding and endoparasites in threatened avian scav-engers coprologic evidence from red kites in their win-tering stronghold Environ Res 155 22minus30
Brashares JS Arcese P Sam MK (2001) Human demographyand reserve size predict wildlife extinction in WestAfrica Proc Biol Sci 268 2473minus2478
Bustamante J (1993) Post-fledging dependence period anddevelopment of flight and hunting behaviour in the redkite Milvus milvus Bird Study 40 181minus188
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Caswell H (2001) Matrix population models Sinauer Sun-derland MA
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Craigie ID Baillie JEM Balmford A Carbone C Collen BGreen RE Hutton JM (2010) Large mammal population
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declines in Africarsquos protected areas Biol Conserv 143 2221minus2228
Czech B (2005) The capacity of the National WildlifeRefuge System to conserve threatened and endangeredanimal species in the United States Conserv Biol 19 1246minus1253
Delibes M Garciacutea L (1984) Haacutebitos alimenticios del milanoreal en Dontildeana durante el periodo de criacutea Ardeola 31 115minus121
Diacuteaz-Paniagua C Aragoneacutes D (2015) Permanent and tempo-rary ponds in Dontildeana National Park (SW Spain) arethreatened by desiccation Limnetica 34 407minus424
Evans IM Summers RW OrsquoToole L Orr-Ewing DC Snell NSmith J (1999) Evaluating the success of translocatingred kites Milvus milvus to the UK Bird Study 46 129minus144
Ferrer M Hiraldo F (1991) Evaluation of management tech-niques for the Spanish imperial eagle Wildl Soc Bull 19 436minus442
Garciacutea Novo F Mariacuten Cabrera C (2005) Dontildeana water andbiosphere Dontildeana 2005 Project Spanish Ministry of theEnvironment Madrid
Gaston KJ Jackson SF Cantuacute-Salazar L Cruz-Pintildeoacuten G(2008) The ecological performance of protected areasAnnu Rev Ecol Evol Syst 39 93minus113
Godet L Devictor V Jiguet F (2007) Estimating relative pop-ulation size included within protected areas BiodiversConserv 16 2587minus2598
Goacutemara B Gonzaacutelez MJ Baos R Hiraldo F Abad E RiveraJ Jimeacutenez B (2008) Unexpected high PCB and total DDTlevels in the breeding population of red kite (Milvus mil-vus) from Dontildeana National Park south-western SpainEnviron Int 34 73minus78
Gonzaacutelez LM Margalida A Mantildeosa S Saacutenchez R and oth-ers (2007) Causes and spatio-temporal variations of non-natural mortality in the vulnerable Spanish imperialeagle Aquila adalberti during a recovery period Oryx41 495minus502
Hansen AJ DeFries R (2007) Ecological mechanisms linkingprotected areas to surrounding lands Ecol Appl 17 974minus988
Hernaacutendez FJ Donaacutezar JA Hiraldo F (2001) Evaluacioacuten deluso de venenos para el control de predadores en laComunidad Autoacutenoma Andaluza y su impacto en la con-servacioacuten de especies amenazadas de vertebrados Con-sejeria de Medio Ambiente and Estacioacuten Bioloacutegica deDontildeana Sevilla
IUCN (The World Conservation Union) (1994) Guidelines forprotected area management categories IUCN Gland
Knott J Newbery P Barov B (2009) Action plan for the redkite Milvus milvus in the European Union EuropeanCommission Brussels
Kruumlger O Gruumlnkorn T Struwe-Juhl B (2010) The return ofthe white-tailed eagle (Haliaeetus albicilla) to northernGermany modelling the past to predict the future BiolConserv 143 710minus721
Loacutepez V (1861) Cataacutelogo de las aves observadas enAndaluciacutea Madrid
Loacutepez G and others (2009) Management measures to controla feline leukemia virus outbreak in the endangered Iber-ian lynx Anim Conserv 12 173minus182
Margalida A Heredia R Razin M Hernaacutendez M (2008)Sources of variation in mortality of the bearded vultureGypaetus barbatus in Europe Bird Conserv Int 18 1minus10
Naughton-Treves L Holland MB Brandon K (2005) The roleof protected areas in conserving biodiversity and sustain-
ing local livelihoods Annu Rev Environ Resour 30 219minus252
Newton I (1979) Population ecology of raptors T amp AD PoyserBerkhamsted
Newton I Davis PE Davis JE (1989) Age of first breedingdispersal and survival of red kites Milvus milvus inWales Ibis 131 16minus21
Otero C Castieacuten E Senosiaiacuten R Portillo F (1978) Fauna deCazorla vertebrados Publicaciones del Ministerio deAgricultura Madrid
Parks SA Harcourt AH (2002) Reserve size local humandensity and mammalian extinctions in US protectedareas Conserv Biol 16 800minus808
R Development Core Team (2018) R a language and envi-ronment for statistical computing R Foundation for Sta-tistical Computing Vienna wwwr-projectorg
Saeligther BE Bakke Oslash (2000) Avian life history variation andcontribution of demographic traits to the populationgrowth rate Ecology 81 642minus653
Sanz-Aguilar A De Pablo F Donaacutezar JA (2015) Age-depen-dent survival of island vs mainland populations of twoavian scavengers delving into migration costs Oecolo-gia 179 405minus414
Schaub M (2012) Spatial distribution of wind turbines is cru-cial for the survival of red kite populations Biol Conserv155 111minus118
Schmidt G Saacutenchez Navarro R Hernaacutendez E Carmona JJFuentelsaz F Seiz R (2017) The state of water in Dontildeana an evaluation of the state of the water and of the ecosys-tems of the protected space WWFAdena Madrid
Scott JM Davis FW McGhie RG Wright RG Groves CEstes J (2001) Nature reserves Do they capture the fullrange of Americarsquos biological diversity Ecol Appl 11 999minus1007
Seoane J Vintildeuela J Diacuteaz-Delgado R Bustamante J (2003)The effects of land use and climate on red kite distribu-tion in the Iberian peninsula Biol Conserv 111 401minus414
Sergio F Blas J Feroro M Fernaacutendez N Donaacutezar JAHiraldo F (2005) Preservation of wide-ranging top pred-ators by site-protection black and red kites in DontildeanaNational Park Biol Conserv 125 11minus21
Sergio F Tanferna A Blas J Blanco G Hiraldo F (2019) Reli-able methods for identifying animal deaths in GPS- andsatellite-tracking data review testing and calibrationJ Appl Ecol 56562ndash572
Smart J Amar A Sim IMW Etheridge B Cameron DChristie G Wilson JD (2010) Illegal killing slows popula-tion recovery of a re-introduced raptor of high conserva-tion concern mdash the red kite Milvus milvus Biol Conserv143 1278minus1286
Tavecchia G Adrover J Muntildeoz Navarro A Pradel R (2012)Modelling mortality causes in longitudinal data in thepresence of tag loss application to raptor poisoning andelectrocution J Appl Ecol 49 297minus305
Tenan S Adrover J Muntildeoz Navarro A Sergio F TavecchiaG (2012) Demographic consequences of poison-relatedmortality in a threatened bird of prey PLOS ONE 7 e49187
Tilman D May RM Lehman CL Nowak MA (1994) Habitatdestruction and the extinction debt Nature 371 65minus66
Torres Esquivias JA Jordano P Leoacuten A (1981) Aves de presadiurnas de la provincia de Coacuterdoba Publicaciones CA yMP Coacuterdoba
Veiga JP Hiraldo F (1990) Food habits and the survival andgrowth of nestlings in two sympatric kites (Milvus milvus
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and Milvus migrans) Holarct Ecol 13 62minus71 Villafuerte R Vintildeuela J Blanco JC (1998) Extensive preda-
tor persecution caused by population crash in a gamespecies the case of red kites and rabbits in Spain BiolConserv 84 181minus188
Vintildeuela J (2004) Milano real Milvus milvus In Madrontildeo AGonzaacutelez C Atienza JC (eds) Libro rojo de las aves deEspantildea Direccioacuten General para la BiodiversidadminusSEOBirdLife Madrid p 120minus125
Vintildeuela J Villafuerte R (2003) Predators and rabbits (Oryc-tolagus cuniculus) in Spain a key conflict for Europeanraptor conservation In Thompson DBA Redpath SMFielding AH Marquiss M Galbraith CA (eds) Birds ofprey in a changing environment The Stationery OfficeEdinburgh p 511minus526
Vintildeuela J Martiacute R Ruiz A (eds) (1999) El milano real enEspantildea SEOBirdlife Madrid
Watson JEM Dudley N Segan DB Hockings M (2014) Theperformance and potential of protected areas Nature515 67minus73
Whitfield SM Bell KE Philippi T Sasa M and others (2007)Amphibian and reptile declines over 35 years at La SelvaCosta Rica Proc Natl Acad Sci USA 104 8352minus8356
Whitfield DP Fielding AH McLeod DRA Haworth PF(2004) Modelling the effects of persecution on the popu-lation dynamics of golden eagles in Scotland Biol Con-serv 119 319minus333
Zuur A Ieno EN Walker N Saveliev AA Smith GM (2009)Mixed effects models and extensions in ecology with RSpringer New York NY
204
Editorial responsibility Nils BunnefeldStirling UK
Submitted October 8 2018 Accepted January 28 2019Proofs received from author(s) April 7 2019
Sergio et al Predator extinction debt in national park
of successful breeding and for the number of fledgedyoung (Fig 7)
On average the whole population was estimated toproduce 103 fledglings per year in the 1980s this al-most halved to 57 in the 1990s 48 in 2000minus2009 andagain declined to more than halved to 19 in 2010minus2017In 2015 2016 and 2017 the population produced 7 7and 15 fledglings respectively Population decline and
breeding deterioration were accompa-nied by a change in the relative impor-tance of some sectors for offspring pro-duction (Fig 5 Table 2) In the 1980smost young were produced in thesector RBD vera and the northernpinewoods and most other sectors stillcontributed gt5 of the annual youngproduction (Fig 5c) In subsequentdecades fledgling production becameconcentrated in the marsh ecotone(Puntal RBD vera vera of Algaida-Manecorro) with additional inputsfrom some interior or peripheral sectorsand a larger portion of sectors with vir-tually zero contribution to future gener-ations (Fig 5d) Fig 3 illustrates howdiffuse successful reproduction was inthe 1980s compared to 2017
35 Comparison with otherEuropean populations
Compared to other areas of Europethe Dontildeana population showed a highdensity in the 1980s (well above theEuropean mean Table S3) This pro-gressively declined and has changedto below-average density since 2010All breeding parameters were wellbelow the mean European estimatesfrom the 1980s onwards (Table S3) Inparticular the percentage of success-ful pairs and the number of youngfledged per breeding pair are cur-rently 2 to 3 times lower than themean European values
36 Population growth andprojections for the Dontildeana
population
Observed declines were well cap-tured by the growth rate predicted by the populationmodel based on the minimum European survivalrates (Fig 8) The other 2 scenarios of maximum andmean survival rates predicted a stable population ordeclines from the year 2000 onwards only (Fig 8)For the 2010s the model estimated λ = 0849 0960and 1066 for the scenario based on minimum meanand maximum survival estimates respectively
195
Fig 3 Distribution of breeding territories in Dontildeana (a) in the 1980s and (b) in2017 Pairs that bred successfully (black points) were much more frequent andmore widely distributed especially in the northern sectors and in the NaturalPark in the 1980s than in 2017 when most pairs failed to raise chicks to fledg-ing (white points) Territory locations have been moved slightly for conserva-tion reasons and locations from the 1980s could only be approximate for some
territories especially those in the northern pinewoods
Endang Species Res 38 189ndash204 2019
Based on the model with minimum survival rateswhich gave the best fit to past declines the popula-tion of 37 pairs censused in 2017 would be reduced to7 pairs within 10 yr and virtually extinct (le2 pairs) in17 yr The less supported scenario of mean Europeansurvival estimates projected a population of 25 pairsin 10 yr while the most optimistic scenario of maxi-mum survival predicted a full recovery to the 1980spopulation level of 70 pairs in 10 yr
Despite the current extremely lowbreeding success under all 3 scenar-ios of survival the population growthrate was least sensitive to changes infledglings production [E(F) = 0048minus0079 S(F) = 0137minus 0277] and mostsensitive to variations in adult survivalprobability [E(θ) = 0843minus 0904 S(θ) =0929minus 0955] In Fig 9 we plot thecombination of fledgling productionand adult survival that produce differ-ent levels of population growth Atcurrent levels of reproduction adultsurvival would have to be around090minus095 to attain a stable or slightlyincreasing population while restoringbreeding success to the levels of the1980s of 13 young per pair wouldimply a stable population even with arelatively low adult survival of ~077ie below the minimum ever recordedfor the species (Fig 9)
4 DISCUSSION
Our results showed that the currentdeteriorated condition of the Dontildeanared kite population was not a recentphenomenon but the tip of the ice-berg of decades of regional and localdegradation Although the protectedarea slowed the background levels ofregional decline and likely saved thespecies from local extinction its via-bility maintenance performance wasfar from satisfactory In a way the ob -served long-term deterioration actedas a protracted diluted form of extinc-tion debt (Tilman et al 1994) paidover a time-frame of several decadesWe suspect that similar conditionsmay be common in other protectedareas making this a classical example
of gradual underlying pressures diluted over such along time-frame that their severity becomes evidentonly through a large-scale long-term asses sment oronce population degradation has reached its extremeconsequences Note that for many parameters dete-rioration was not especially alarming from onedecade to the next making it difficult for the succes-sion of local field observers to appreciate the overallseverity of the long-term trends This difficulty in
196
Fig 4 Distribution range of red kites in Dontildeana (a) in the 1980s and (b) in2017 The pink outer polygon represents a 95 kernel constructed aroundthe territory locations while the red polygon is a 50 kernel showing the corearea of distribution The overall and core distribution range contracted by 534and 581 respectively Territory locations have been moved slightly for
conservation reasons
Sergio et al Predator extinction debt in national park 197
12
3 R
BD
4 V
era
56
7 C
oto
8 N
W9
NE
10
11
12
Tot
al
RB
DR
BD
san
dA
lgai
da
Inte
rior
Pu
nta
ld
elp
ine-
pin
e-M
aris
-S
anlu
car
Ab
alar
iod
ecli
ne
vera
inte
rior
du
nes
Man
ecor
roR
eyw
ood
sw
ood
sm
illa
sp
inew
ood
a) M
ean
no
of
pai
rs19
80minus
1989
141
52
33
40a
20a
80b
50
107
44
50
30
40b
687
1990
minus19
9915
35
11
37
74
08
03
34
40
74
5e2
5c4
0a60
8minus
115
2000
minus20
0916
05
21
47
05
06
31
01
00
14
5e2
03
1a52
5minus
236
2010
minus20
1713
03
42
56
63
98
41
90
50
13
01
72
147
1minus
315
2017
100
35
211
00
03
12
37minus
462
b)
No
of
you
ng
pro
du
ced
an
nu
ally
1980
minus19
8916
14
25
66
43
09
610
020
311
06
04
56
010
26
1990
minus19
999
82
60
68
44
06
92
46
60
95
13
86
056
9minus
445
2000
minus20
0913
21
61
27
25
83
71
21
60
24
53
04
647
7minus
535
2010
minus20
172
60
61
11
82
33
50
90
30
01
62
91
919
4minus
811
2017
10
03
07
00
00
22
150
minus85
4
c)
of
the
tota
l p
op
ula
tio
n i
n e
ach
sec
tor
1980
minus19
8920
57
64
85
82
911
67
315
56
47
34
45
819
90minus
1999
251
84
21
126
66
131
55
73
12
74
41
66
2000
minus20
0929
49
62
612
99
211
51
81
80
28
33
79
120
10minus
2017
276
72
53
141
82
178
40
11
03
64
36
45
2017
270
00
81
135
54
297
00
00
00
81
27
54
d)
c
on
trib
uti
on
of
each
sec
tor
to t
ota
l an
nu
al y
ou
ng
pro
du
ctio
n19
80minus
1989
157
41
54
94
62
29
97
198
107
58
44
58
1990
minus19
9917
24
61
112
114
77
04
211
61
68
96
610
520
00minus
2009
277
33
24
78
151
121
24
34
04
94
63
96
2010
minus20
1713
43
35
418
19
411
74
81
30
08
215
09
620
176
70
00
046
720
00
00
00
00
00
013
313
3
a Cro
ss-c
omb
ined
est
imat
e b
Sta
tic
bac
k-e
stim
ate
c In
terp
olat
ed e
stim
ate
See
Sec
tion
23
for
det
ails
Tab
le 2
(a
) M
ean
nu
mb
er o
f p
airs
an
d (
b)
cum
ula
tive
nu
mb
er o
f of
fsp
rin
g p
rod
uce
d a
nn
ual
ly b
y th
e D
ontildean
a re
d k
ite
pop
ula
tion
wit
hin
eac
h s
ecto
r an
d i
n t
he
wh
ole
par
k o
ver
the
pas
t d
ecad
es a
nd
in 2
017
Per
cen
tag
e of
(c)
pai
rs a
nd
(d
) yo
un
g c
ontr
ibu
ted
by
each
sec
tor
to t
he
over
all p
opu
lati
on S
ecto
rs c
ontr
ibu
tin
g m
ore
than
10
ar
e h
igh
lig
hte
d i
n b
old
T
otal
ref
ers
to t
he
sum
of
all
sect
ors
d
ecli
ne
is t
he
dec
lin
e co
mp
ared
to
the
1980
s P
rop
orti
onal
con
trib
uti
ons
are
also
ill
ust
rate
d i
n F
ig
5
RB
D R
eser
va B
iolo
gic
a d
e D
ontildean
a
Endang Species Res 38 189ndash204 2019
detecting the problem was likely exacerbated by thefollowing factors that could be defined as lsquoperceptionobstaclesrsquo (1) The fact that a population becomesmore and more restricted to a park is often used toillustrate the positive role of protected areas byfocusing their performance assessments on range
coverage ie the capability of protected areas tocover a large portion of a species range (eg Czech2005 Godet et al 2007) This diverts attention fromthe wider problems of range contraction and from theactual performance of the park in terms of viabilitymaintenance (Gaston et al 2008) (2) Confinement to
198
of nests in each sector
of annual young generated by each sector
1980s 2010s
1980s 2010s
a) b)
c) d)
Fig 5 Percentage of the total red kite population in each of 12 sectors of Dontildeana (a) in the 1980s and (b) in the 2010s percent-age of the annual young production generated by each sector (c) in the 1980s and (d) in the 2010s (a) In the 1980s the bulk ofthe population was concentrated in northern sectors (7 and 8) and in the southern shores of the marshes (sectors 1 6 and 10)(b) In the 2010s the population virtually disappeared from the northern sectors and became essentially confined to the na-tional park where it concentrated along the marshes (c) In the 1980s the population generated more than 100 young eachyear most of them produced by the northern sectors (7 8 9) and by the northern shores of the marshes (sectors 1 and 4) (d) Inthe 2010s the population generated less than 10 young mostly generated close to wetlands (sectors 1 4 11) with homo -geneously low numbers elsewhere Colors (yellow rarr orange rarr red) classify sectors by tertiles of the range of percentage
contribution
Sergio et al Predator extinction debt in national park
a protected area is usually accompanied by the auto-matic presumption that this will act as a source areawith limited anthropogenic impacts an assumptionthat is increasingly disproved (Hansen amp DeFries2007 Gaston et al 2008 Watson et al 2014) (3) Long-term assessments such as ours required the lengthy
collation of fragmented informationfrom a large number of sequentialfield workers and administrationseach of which had a very limited per-ception of the overall situation (4)Much monitoring was conducted inthe core areas of the park like theRBD where the species has alwaysbeen most abundant and relativelystable (eg Sergio et al 2005) con-fusing the perception of broaderdeclines (5) Finally large numbersof wintering migrants boost the pop-ulation in the winter and earlyspring often producing an optimisticimpression of apparent abundance
even in relatively expert members of the public or oflocal administrations as we frequently noted in pub-lic talks and private conversations
Overall the decline occurred at multiple levels redkites were originally widespread throughout south-ern Spain (Loacutepez 1861) but became progressively
199
2030405060708090
100110
Bree
ding
su
cces
sful
()
a breeding pairs successful pairs
202122232425262728
Clut
ch si
ze
b
25
35
45
55
65
75
85
1970-79 1980-89 1990-99 2000-09 2010-17
Hatc
hing
succ
ess
broo
d re
duct
ion
()
Decade
c Hatching successBrood reduction
03
06
09
12
15
18
21
1970-79 1980-89 1990-99 2000-09 2010-17
Youn
g fle
dged
Decade
d Young breeding pairYoung successful pair
Fig 6 Reproductive parameters of the red kite population of Dontildeana (a) percentage of pairs laying eggs (black dots n = 804)and successfully raising fledglings (white dots n = 1185) (b) mean clutch size (n = 469) (c) hatching success (percentage ofeggs that hatched black dots n = 353) and brood reduction (percentage of chicks that disappeared during the nestling periodwhite dots n = 240) (d) mean number of young fledged per territorial pair (black dots n = 1145) and per successful pair (white
dots n = 576)
0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75
Young fledgedsuccessful pairYoung fledgedbreeding pairYoung fledgedterritorial pair
Probability of successful breedingBrood reduction
Hatching successClutch size
Probability of laying
Deterioration ()
Breeding parameter
Fig 7 Percentage deterioration of breeding parameters of the red kite popu-lation of Dontildeana between the 1980s and the 2010s
Endang Species Res 38 189ndash204 2019
confined to the protected area of Dontildeana in recentdecades However the park did not confer automaticsafety and declines and range contraction also con-tinued within the protected area suggesting perva-sive pressures and range erosion at multiple spatialscales In particular almost one third of the Dontildeana
population was virtually eradicatedfrom the northern pinewoods of thebuffering Natural Park in 5 to 7 yrbetween the late 1980s and early1990s Several lines of evidence sug-gest that illegal poisoning was themain cause of this eradication (1) Sev-eral adults were found poisoned undertheir nest in those sectors and years(2) Large-scale poisoning campaignsof raptors were reported throughoutSpain in those exact same years asa consequence of huntersrsquo illegalattempts to control predator popula-tions to increase the rapidly deterio-rating numbers of small game (rabbitsand partridges Villafuerte et al 1998Vintildeuela amp Villafuerte 2003 Cano et al2008) In this sense the National Parksuffered much wider national-level
pressures (3) The northern sectors of the parkwhere the eradication took place included or wereclose to private small-game reserves and predatorcontrol was well known to occur in some of them (4)Finally the rapidity of the eradication of such a long-lived species (maximum longevity of 29 yr in Dontilde -ana) implied a causative agent that directly affectedadult mortality (Saether amp Bakke 2000) such as poi-soning The marked impact of poisoning on adult sur-vival and population growth are well recognized forthis species whose facultative scavenging habits andforaging method of meticulous low and slow quar-tering of the ground make it particularly sensitive tothis threat (Smart et al 2010 Tavecchia et al 2012Tenan et al 2012 Sanz-Aguilar et al 2015)
Spikes of rapid local eradication were superim-posed on more gradual but steady deterioration ofoffspring production Gradual and continuous ratherthan sudden degradation of performance suggestedthat poisoning was not the only threat in effect Inthis context several factors may have contributed togradually deteriorate ecological conditions for kitesin recent decades (1) Rabbit epidemics have causedprogressive declines in the availability of this keyprey (Vintildeuela amp Villafuerte 2003) (2) Lower preyavailability may have exacerbated competition withthe dense populations of other raptors with similardiets such as the ecologically similar and in creasingblack kite (3) Predation rates on adults and nestlingsmay have increased with the expansion of the popu-lations of potential predators such as eagle owls Bubobubo and goshawks Accipiter gentilis (4) Recentassessments have detected alarming levels of toxic
200
00
02
04
06
08
10
12
1980sndash1990s 1990sndash2000s 2000sndash2010s
Popu
latio
n gr
owth
rate
Period
Observed populationgrowth
Scenario 1 minimumEuropean survival
Scenario 2 meanEuropean survival
Scenario 3 maximumEuropean survival
Fig 8 Population growth of the Dontildeana red kite population during the past 4decades as predicted by matrix demographic models based on 3 scenarioswhich assumed that survival was equal to minimum mean or maximum sur-vival rates reported for other European populations (reviewed in Table 1)Predicted values are compared with observed declines from one decade to
the next
Fig 9 Population growth rate of red kites in relation to adultsurvival and breeding performance (mean number of youngfledged per territorial pair) based on a matrix populationmodel Note that the graph could be applied to any Euro-pean population The 3 points at the base of the graph repre-sent the minimum (black) mean (grey) and maximum (blue)survival published for European populations (reviewed in
Table 1)
Sergio et al Predator extinction debt in national park
chemicals in red kite eggs from Dontildeana (Goacutemara etal 2008) (5) Climate change and agricultural man-agement have lowered the water table with likelyimpacts on marsh inundation levels and aquatic prey(Garciacutea Novo amp Mariacuten Cabrera 2005 Diacuteaz-Paniaguaamp Aragoneacutes 2015 Schmidt et al 2017) (6) Conver-sion to intensive farmland in surrounding lands haseroded habitat and prey availability outside the pro-tected area which may have buffered kites fromperiods of low prey availability within the park (egduring droughts in the marshes) Some of the pat-terns of observed reproductive deterioration lendsupport to some of these impacts For exampledeclining clutch sizes and increasing rates of broodreduction suggest that food was not sufficient to sus-tain earlier reproductive levels while lowered hatch-ing success is often the result of chemical contamina-tion in raptors (review in Newton 1979) While eachof these threats will be quantitatively investigated indetail in the immediate future in the present contextthey illustrate the frequent and complex challengesfaced by (1) protected areas in maintaining biodiver-sity and viable populations of imperiled species and(2) conservation biologists in identifying causes ofdecline for subsequent management interventioneven in lsquoprivilegedrsquo sites such as reserves
Redistribution declining numbers and perform-ance had important repercussions for future viability(1) The population passed from producing gt100annual young to lt10minus20 which will make mainte-nance and recovery difficult (2) These young wereincreasingly produced in the core sectors of themarsh-ecotone within the National Park which prob-ably increased the dependence of the population onmarsh inundation in turn affected by problems oper-ating outside the park (Garciacutea Novo amp Mariacuten Cabrera2005 Diacuteaz-Paniagua amp Aragoneacutes 2015 Schmidt et al2017) (3) Steep declines in the percentage of suc-cessful pairs implied that future generations wereproduced by a progressively more restricted numberof pairs which will make the population more sub-ject to inbreeding and stochastic events For exam-ple in the last 3 yr all the annual young were pro-duced by 6 8 and 9 pairs respectively suggesting aneffective population size 4 to 9 times lower than theoverall abundance
Given all the above it is no surprise that demo-graphic models suggested a negative growth and apopulation incapable of self-sustenance In particu-lar the model that gave the best fit to past observeddeclines was the one based on minimum Europeansurvival estimates followed by the scenario based onmean European survival estimates Given the above-
mentioned threats declines and performance deteri-oration we would expect survival to be closer to min-imum than mean European levels as supported bythe observed fit to past and recent declines Theseresults have 2 main implications (1) If survival is aslow as we suspect demographic models predict vir-tual extinction within a few years demanding anurgent need for identification and management ofmortality threats as well as quantification of actualsurvival to refine predictions Note that virtual ex -tinction could be even earlier when taking intoaccount effective rather than total population sizeand a stochastic rather than deterministic populationmodel (2) Should actual survival be confirmed lowbut further declines not observed the populationwould be a sink sustained by external sources whichwould make it even more at risk from anthropogenicthreats outside the park and thus more challengingto manage (eg Hansen amp DeFries 2007 Blanco et al2017)
5 Conclusions and implications for conservation
The decades-long degradation that we depictedwas likely generated by a combination of factorsboth internal to the park (eg rabbit availabilitymarsh inundation rates predation and competitionwith other species) and external (eg illegal poi-soning contamination farmland intensification)Some of them will be amenable to managementand others less so but the first priority will be tofind rapid ways to identify the key factors thatdrive population growth so as to optimize conserva-tion action before it is too late For example focus-ing conservation lsquoblindlyrsquo on supplementary feedingcould be useless if the problem is chemical contam-ination The quickest way to obtain such informa-tion would be a satelliteGSM (Global System forMobile communication) tagging program that wouldallow to (1) obtain rapid estimates of health andsurvival for young and adults (eg Sergio et al2019) so as to recalibrate future projections andgoals (2) assess the relative contribution of mainmortality causes which is an essential first step inany recovery program (eg Gonzaacutelez et al 2007Margalida et al 2008 Smart et al 2010) and (3)identify the areas used by breeding and non-breed-ing individuals inside and outside of the park toassess their risk-exposure and intervene before orafter death (eg to prosecute perpetrators of illegalpoisoning or re trofit dangerous electricity pylons inareas of high use by kites)
201
Endang Species Res 38 189ndash204 2019
Until this information becomes available below welist some tentative figures and priorities for conserva-tion First of all restoring the current population toformer levels would undoubtedly be challenging andprobably unrealistic given the profound changesincurred by the wider Dontildeana ecosystem in recentdecades Thus we propose an initial target of 60pairs as a long-term restoration goal Elasticity analy-sis suggested that optimal management should focuson improving adult survival which had the largestimpact on population growth as in other long-livedspecies (Saether amp Bakke 2000 Whitfield et al 2004Kruumlger et al 2010) This could be attempted by in -creasing food availability especially of key prey suchas rabbits and by curtailing mortality threats such asillegal poisoning which still continues despite mucheffort to eradicate it by the local administration Thetelemetry program outlined above could help toidentify local perpetrators as occurred in other pop-ulations (Smart et al 2010 Tavecchia et al 2012) Onthe other hand despite their low elasticities repro-ductive rates are currently so low that it would befundamental to increase them eg by increasingfood availability and ensuring proper inundation ofthe marshes Based on Fig 5 we propose as initialtargets for restoration (1) survival rates equal orhigher than the European mean (adult survivalge087) and (2) a number of young fledged per territo-rial pair above 10 which would produce an increas-ing population provided that adult survival is equalto or above the European mean Note that Fig 5could be applied to any European population as atool to check its potential viability Given the highlythreatened status of red kites the speciesrsquo limitedrange confined to Europe and its ongoing declinesviability assessments such as ours may sadly becomemore important for the management and recovery ofmany populations
In conclusion red kites would probably be extinctin southern Spain without the institution of a largenational park In this sense this example well illus-trates how protected areas will continue to be corner-stones of global conservation of threatened taxaHowever their safety is not ensured by park institu-tion per se and performance monitoring and focusedaction will be needed to avoid potential extinctiondebts which may be more protracted than previouslyappreciated In our exemplary case despite the pres-ence of a large national park on prime fertile landwithin a developed country with adequate institu-tional and financial support a key threatened speciessuffered latent but steady declines for decadesobscured by problems of perception lack and frag-
mentation of information and likely caused by acomplex array of within-park threats and growingexternal pressures Viability maintenance and recov-ery will probably require concerted actions withinand outside of the park but only after detailed infor-mation on crucial aspects becomes available whichis probably the most urgent current priority We sus-pect that dynamics like the ones illustrated here aremore common than currently appreciated and willbecome more widespread as anthropogenic pres-sures increase around protected areas and as theirperformance monitoring becomes more prevalent
Acknowledgements We thank all the (too many to mention)researchers field workers visitors volunteers gamekeep-ers park managers and wardens that have provided datasince the 1960s In particular we thank F G Vilches L Gar-ciacutea and the Equipo de Seguimiento de Procesos Naturales ofthe Estacioacuten Bioloacutegica de Dontildeana-CSIC for help in the fieldSpecial thanks to F G Vilches for the priceless help with thecollation and organization of historical information Wethank J P Castellano I Redondo and all the lsquoArea de Con-servacioacutenrsquo of Dontildeana National Park for constant interest andsupport We thank R Cadenas J Madrid R Arenas J RBenitez and all the pertinent personnel of the Consejeriacutea deMedio Ambiente of the Junta de Andaluciacutea for informationon current nest locations in the Sierra de Huelva and fortheir constant attentive support We are grateful to Dr NBunnefeld and 2 anonymous reviewers for constructivecomments that improved the manuscript This study wasfunded by the Foundation Jaime Gonzaacutelez-Gordon and bythe research project 16022015 of the Spanish Ministry ofAgriculture Food and the Environment (National ParksAutonomous Agency)
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Scott JM Davis FW McGhie RG Wright RG Groves CEstes J (2001) Nature reserves Do they capture the fullrange of Americarsquos biological diversity Ecol Appl 11 999minus1007
Seoane J Vintildeuela J Diacuteaz-Delgado R Bustamante J (2003)The effects of land use and climate on red kite distribu-tion in the Iberian peninsula Biol Conserv 111 401minus414
Sergio F Blas J Feroro M Fernaacutendez N Donaacutezar JAHiraldo F (2005) Preservation of wide-ranging top pred-ators by site-protection black and red kites in DontildeanaNational Park Biol Conserv 125 11minus21
Sergio F Tanferna A Blas J Blanco G Hiraldo F (2019) Reli-able methods for identifying animal deaths in GPS- andsatellite-tracking data review testing and calibrationJ Appl Ecol 56562ndash572
Smart J Amar A Sim IMW Etheridge B Cameron DChristie G Wilson JD (2010) Illegal killing slows popula-tion recovery of a re-introduced raptor of high conserva-tion concern mdash the red kite Milvus milvus Biol Conserv143 1278minus1286
Tavecchia G Adrover J Muntildeoz Navarro A Pradel R (2012)Modelling mortality causes in longitudinal data in thepresence of tag loss application to raptor poisoning andelectrocution J Appl Ecol 49 297minus305
Tenan S Adrover J Muntildeoz Navarro A Sergio F TavecchiaG (2012) Demographic consequences of poison-relatedmortality in a threatened bird of prey PLOS ONE 7 e49187
Tilman D May RM Lehman CL Nowak MA (1994) Habitatdestruction and the extinction debt Nature 371 65minus66
Torres Esquivias JA Jordano P Leoacuten A (1981) Aves de presadiurnas de la provincia de Coacuterdoba Publicaciones CA yMP Coacuterdoba
Veiga JP Hiraldo F (1990) Food habits and the survival andgrowth of nestlings in two sympatric kites (Milvus milvus
203
Endang Species Res 38 189ndash204 2019
and Milvus migrans) Holarct Ecol 13 62minus71 Villafuerte R Vintildeuela J Blanco JC (1998) Extensive preda-
tor persecution caused by population crash in a gamespecies the case of red kites and rabbits in Spain BiolConserv 84 181minus188
Vintildeuela J (2004) Milano real Milvus milvus In Madrontildeo AGonzaacutelez C Atienza JC (eds) Libro rojo de las aves deEspantildea Direccioacuten General para la BiodiversidadminusSEOBirdLife Madrid p 120minus125
Vintildeuela J Villafuerte R (2003) Predators and rabbits (Oryc-tolagus cuniculus) in Spain a key conflict for Europeanraptor conservation In Thompson DBA Redpath SMFielding AH Marquiss M Galbraith CA (eds) Birds ofprey in a changing environment The Stationery OfficeEdinburgh p 511minus526
Vintildeuela J Martiacute R Ruiz A (eds) (1999) El milano real enEspantildea SEOBirdlife Madrid
Watson JEM Dudley N Segan DB Hockings M (2014) Theperformance and potential of protected areas Nature515 67minus73
Whitfield SM Bell KE Philippi T Sasa M and others (2007)Amphibian and reptile declines over 35 years at La SelvaCosta Rica Proc Natl Acad Sci USA 104 8352minus8356
Whitfield DP Fielding AH McLeod DRA Haworth PF(2004) Modelling the effects of persecution on the popu-lation dynamics of golden eagles in Scotland Biol Con-serv 119 319minus333
Zuur A Ieno EN Walker N Saveliev AA Smith GM (2009)Mixed effects models and extensions in ecology with RSpringer New York NY
204
Editorial responsibility Nils BunnefeldStirling UK
Submitted October 8 2018 Accepted January 28 2019Proofs received from author(s) April 7 2019
Endang Species Res 38 189ndash204 2019
Based on the model with minimum survival rateswhich gave the best fit to past declines the popula-tion of 37 pairs censused in 2017 would be reduced to7 pairs within 10 yr and virtually extinct (le2 pairs) in17 yr The less supported scenario of mean Europeansurvival estimates projected a population of 25 pairsin 10 yr while the most optimistic scenario of maxi-mum survival predicted a full recovery to the 1980spopulation level of 70 pairs in 10 yr
Despite the current extremely lowbreeding success under all 3 scenar-ios of survival the population growthrate was least sensitive to changes infledglings production [E(F) = 0048minus0079 S(F) = 0137minus 0277] and mostsensitive to variations in adult survivalprobability [E(θ) = 0843minus 0904 S(θ) =0929minus 0955] In Fig 9 we plot thecombination of fledgling productionand adult survival that produce differ-ent levels of population growth Atcurrent levels of reproduction adultsurvival would have to be around090minus095 to attain a stable or slightlyincreasing population while restoringbreeding success to the levels of the1980s of 13 young per pair wouldimply a stable population even with arelatively low adult survival of ~077ie below the minimum ever recordedfor the species (Fig 9)
4 DISCUSSION
Our results showed that the currentdeteriorated condition of the Dontildeanared kite population was not a recentphenomenon but the tip of the ice-berg of decades of regional and localdegradation Although the protectedarea slowed the background levels ofregional decline and likely saved thespecies from local extinction its via-bility maintenance performance wasfar from satisfactory In a way the ob -served long-term deterioration actedas a protracted diluted form of extinc-tion debt (Tilman et al 1994) paidover a time-frame of several decadesWe suspect that similar conditionsmay be common in other protectedareas making this a classical example
of gradual underlying pressures diluted over such along time-frame that their severity becomes evidentonly through a large-scale long-term asses sment oronce population degradation has reached its extremeconsequences Note that for many parameters dete-rioration was not especially alarming from onedecade to the next making it difficult for the succes-sion of local field observers to appreciate the overallseverity of the long-term trends This difficulty in
196
Fig 4 Distribution range of red kites in Dontildeana (a) in the 1980s and (b) in2017 The pink outer polygon represents a 95 kernel constructed aroundthe territory locations while the red polygon is a 50 kernel showing the corearea of distribution The overall and core distribution range contracted by 534and 581 respectively Territory locations have been moved slightly for
conservation reasons
Sergio et al Predator extinction debt in national park 197
12
3 R
BD
4 V
era
56
7 C
oto
8 N
W9
NE
10
11
12
Tot
al
RB
DR
BD
san
dA
lgai
da
Inte
rior
Pu
nta
ld
elp
ine-
pin
e-M
aris
-S
anlu
car
Ab
alar
iod
ecli
ne
vera
inte
rior
du
nes
Man
ecor
roR
eyw
ood
sw
ood
sm
illa
sp
inew
ood
a) M
ean
no
of
pai
rs19
80minus
1989
141
52
33
40a
20a
80b
50
107
44
50
30
40b
687
1990
minus19
9915
35
11
37
74
08
03
34
40
74
5e2
5c4
0a60
8minus
115
2000
minus20
0916
05
21
47
05
06
31
01
00
14
5e2
03
1a52
5minus
236
2010
minus20
1713
03
42
56
63
98
41
90
50
13
01
72
147
1minus
315
2017
100
35
211
00
03
12
37minus
462
b)
No
of
you
ng
pro
du
ced
an
nu
ally
1980
minus19
8916
14
25
66
43
09
610
020
311
06
04
56
010
26
1990
minus19
999
82
60
68
44
06
92
46
60
95
13
86
056
9minus
445
2000
minus20
0913
21
61
27
25
83
71
21
60
24
53
04
647
7minus
535
2010
minus20
172
60
61
11
82
33
50
90
30
01
62
91
919
4minus
811
2017
10
03
07
00
00
22
150
minus85
4
c)
of
the
tota
l p
op
ula
tio
n i
n e
ach
sec
tor
1980
minus19
8920
57
64
85
82
911
67
315
56
47
34
45
819
90minus
1999
251
84
21
126
66
131
55
73
12
74
41
66
2000
minus20
0929
49
62
612
99
211
51
81
80
28
33
79
120
10minus
2017
276
72
53
141
82
178
40
11
03
64
36
45
2017
270
00
81
135
54
297
00
00
00
81
27
54
d)
c
on
trib
uti
on
of
each
sec
tor
to t
ota
l an
nu
al y
ou
ng
pro
du
ctio
n19
80minus
1989
157
41
54
94
62
29
97
198
107
58
44
58
1990
minus19
9917
24
61
112
114
77
04
211
61
68
96
610
520
00minus
2009
277
33
24
78
151
121
24
34
04
94
63
96
2010
minus20
1713
43
35
418
19
411
74
81
30
08
215
09
620
176
70
00
046
720
00
00
00
00
00
013
313
3
a Cro
ss-c
omb
ined
est
imat
e b
Sta
tic
bac
k-e
stim
ate
c In
terp
olat
ed e
stim
ate
See
Sec
tion
23
for
det
ails
Tab
le 2
(a
) M
ean
nu
mb
er o
f p
airs
an
d (
b)
cum
ula
tive
nu
mb
er o
f of
fsp
rin
g p
rod
uce
d a
nn
ual
ly b
y th
e D
ontildean
a re
d k
ite
pop
ula
tion
wit
hin
eac
h s
ecto
r an
d i
n t
he
wh
ole
par
k o
ver
the
pas
t d
ecad
es a
nd
in 2
017
Per
cen
tag
e of
(c)
pai
rs a
nd
(d
) yo
un
g c
ontr
ibu
ted
by
each
sec
tor
to t
he
over
all p
opu
lati
on S
ecto
rs c
ontr
ibu
tin
g m
ore
than
10
ar
e h
igh
lig
hte
d i
n b
old
T
otal
ref
ers
to t
he
sum
of
all
sect
ors
d
ecli
ne
is t
he
dec
lin
e co
mp
ared
to
the
1980
s P
rop
orti
onal
con
trib
uti
ons
are
also
ill
ust
rate
d i
n F
ig
5
RB
D R
eser
va B
iolo
gic
a d
e D
ontildean
a
Endang Species Res 38 189ndash204 2019
detecting the problem was likely exacerbated by thefollowing factors that could be defined as lsquoperceptionobstaclesrsquo (1) The fact that a population becomesmore and more restricted to a park is often used toillustrate the positive role of protected areas byfocusing their performance assessments on range
coverage ie the capability of protected areas tocover a large portion of a species range (eg Czech2005 Godet et al 2007) This diverts attention fromthe wider problems of range contraction and from theactual performance of the park in terms of viabilitymaintenance (Gaston et al 2008) (2) Confinement to
198
of nests in each sector
of annual young generated by each sector
1980s 2010s
1980s 2010s
a) b)
c) d)
Fig 5 Percentage of the total red kite population in each of 12 sectors of Dontildeana (a) in the 1980s and (b) in the 2010s percent-age of the annual young production generated by each sector (c) in the 1980s and (d) in the 2010s (a) In the 1980s the bulk ofthe population was concentrated in northern sectors (7 and 8) and in the southern shores of the marshes (sectors 1 6 and 10)(b) In the 2010s the population virtually disappeared from the northern sectors and became essentially confined to the na-tional park where it concentrated along the marshes (c) In the 1980s the population generated more than 100 young eachyear most of them produced by the northern sectors (7 8 9) and by the northern shores of the marshes (sectors 1 and 4) (d) Inthe 2010s the population generated less than 10 young mostly generated close to wetlands (sectors 1 4 11) with homo -geneously low numbers elsewhere Colors (yellow rarr orange rarr red) classify sectors by tertiles of the range of percentage
contribution
Sergio et al Predator extinction debt in national park
a protected area is usually accompanied by the auto-matic presumption that this will act as a source areawith limited anthropogenic impacts an assumptionthat is increasingly disproved (Hansen amp DeFries2007 Gaston et al 2008 Watson et al 2014) (3) Long-term assessments such as ours required the lengthy
collation of fragmented informationfrom a large number of sequentialfield workers and administrationseach of which had a very limited per-ception of the overall situation (4)Much monitoring was conducted inthe core areas of the park like theRBD where the species has alwaysbeen most abundant and relativelystable (eg Sergio et al 2005) con-fusing the perception of broaderdeclines (5) Finally large numbersof wintering migrants boost the pop-ulation in the winter and earlyspring often producing an optimisticimpression of apparent abundance
even in relatively expert members of the public or oflocal administrations as we frequently noted in pub-lic talks and private conversations
Overall the decline occurred at multiple levels redkites were originally widespread throughout south-ern Spain (Loacutepez 1861) but became progressively
199
2030405060708090
100110
Bree
ding
su
cces
sful
()
a breeding pairs successful pairs
202122232425262728
Clut
ch si
ze
b
25
35
45
55
65
75
85
1970-79 1980-89 1990-99 2000-09 2010-17
Hatc
hing
succ
ess
broo
d re
duct
ion
()
Decade
c Hatching successBrood reduction
03
06
09
12
15
18
21
1970-79 1980-89 1990-99 2000-09 2010-17
Youn
g fle
dged
Decade
d Young breeding pairYoung successful pair
Fig 6 Reproductive parameters of the red kite population of Dontildeana (a) percentage of pairs laying eggs (black dots n = 804)and successfully raising fledglings (white dots n = 1185) (b) mean clutch size (n = 469) (c) hatching success (percentage ofeggs that hatched black dots n = 353) and brood reduction (percentage of chicks that disappeared during the nestling periodwhite dots n = 240) (d) mean number of young fledged per territorial pair (black dots n = 1145) and per successful pair (white
dots n = 576)
0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75
Young fledgedsuccessful pairYoung fledgedbreeding pairYoung fledgedterritorial pair
Probability of successful breedingBrood reduction
Hatching successClutch size
Probability of laying
Deterioration ()
Breeding parameter
Fig 7 Percentage deterioration of breeding parameters of the red kite popu-lation of Dontildeana between the 1980s and the 2010s
Endang Species Res 38 189ndash204 2019
confined to the protected area of Dontildeana in recentdecades However the park did not confer automaticsafety and declines and range contraction also con-tinued within the protected area suggesting perva-sive pressures and range erosion at multiple spatialscales In particular almost one third of the Dontildeana
population was virtually eradicatedfrom the northern pinewoods of thebuffering Natural Park in 5 to 7 yrbetween the late 1980s and early1990s Several lines of evidence sug-gest that illegal poisoning was themain cause of this eradication (1) Sev-eral adults were found poisoned undertheir nest in those sectors and years(2) Large-scale poisoning campaignsof raptors were reported throughoutSpain in those exact same years asa consequence of huntersrsquo illegalattempts to control predator popula-tions to increase the rapidly deterio-rating numbers of small game (rabbitsand partridges Villafuerte et al 1998Vintildeuela amp Villafuerte 2003 Cano et al2008) In this sense the National Parksuffered much wider national-level
pressures (3) The northern sectors of the parkwhere the eradication took place included or wereclose to private small-game reserves and predatorcontrol was well known to occur in some of them (4)Finally the rapidity of the eradication of such a long-lived species (maximum longevity of 29 yr in Dontilde -ana) implied a causative agent that directly affectedadult mortality (Saether amp Bakke 2000) such as poi-soning The marked impact of poisoning on adult sur-vival and population growth are well recognized forthis species whose facultative scavenging habits andforaging method of meticulous low and slow quar-tering of the ground make it particularly sensitive tothis threat (Smart et al 2010 Tavecchia et al 2012Tenan et al 2012 Sanz-Aguilar et al 2015)
Spikes of rapid local eradication were superim-posed on more gradual but steady deterioration ofoffspring production Gradual and continuous ratherthan sudden degradation of performance suggestedthat poisoning was not the only threat in effect Inthis context several factors may have contributed togradually deteriorate ecological conditions for kitesin recent decades (1) Rabbit epidemics have causedprogressive declines in the availability of this keyprey (Vintildeuela amp Villafuerte 2003) (2) Lower preyavailability may have exacerbated competition withthe dense populations of other raptors with similardiets such as the ecologically similar and in creasingblack kite (3) Predation rates on adults and nestlingsmay have increased with the expansion of the popu-lations of potential predators such as eagle owls Bubobubo and goshawks Accipiter gentilis (4) Recentassessments have detected alarming levels of toxic
200
00
02
04
06
08
10
12
1980sndash1990s 1990sndash2000s 2000sndash2010s
Popu
latio
n gr
owth
rate
Period
Observed populationgrowth
Scenario 1 minimumEuropean survival
Scenario 2 meanEuropean survival
Scenario 3 maximumEuropean survival
Fig 8 Population growth of the Dontildeana red kite population during the past 4decades as predicted by matrix demographic models based on 3 scenarioswhich assumed that survival was equal to minimum mean or maximum sur-vival rates reported for other European populations (reviewed in Table 1)Predicted values are compared with observed declines from one decade to
the next
Fig 9 Population growth rate of red kites in relation to adultsurvival and breeding performance (mean number of youngfledged per territorial pair) based on a matrix populationmodel Note that the graph could be applied to any Euro-pean population The 3 points at the base of the graph repre-sent the minimum (black) mean (grey) and maximum (blue)survival published for European populations (reviewed in
Table 1)
Sergio et al Predator extinction debt in national park
chemicals in red kite eggs from Dontildeana (Goacutemara etal 2008) (5) Climate change and agricultural man-agement have lowered the water table with likelyimpacts on marsh inundation levels and aquatic prey(Garciacutea Novo amp Mariacuten Cabrera 2005 Diacuteaz-Paniaguaamp Aragoneacutes 2015 Schmidt et al 2017) (6) Conver-sion to intensive farmland in surrounding lands haseroded habitat and prey availability outside the pro-tected area which may have buffered kites fromperiods of low prey availability within the park (egduring droughts in the marshes) Some of the pat-terns of observed reproductive deterioration lendsupport to some of these impacts For exampledeclining clutch sizes and increasing rates of broodreduction suggest that food was not sufficient to sus-tain earlier reproductive levels while lowered hatch-ing success is often the result of chemical contamina-tion in raptors (review in Newton 1979) While eachof these threats will be quantitatively investigated indetail in the immediate future in the present contextthey illustrate the frequent and complex challengesfaced by (1) protected areas in maintaining biodiver-sity and viable populations of imperiled species and(2) conservation biologists in identifying causes ofdecline for subsequent management interventioneven in lsquoprivilegedrsquo sites such as reserves
Redistribution declining numbers and perform-ance had important repercussions for future viability(1) The population passed from producing gt100annual young to lt10minus20 which will make mainte-nance and recovery difficult (2) These young wereincreasingly produced in the core sectors of themarsh-ecotone within the National Park which prob-ably increased the dependence of the population onmarsh inundation in turn affected by problems oper-ating outside the park (Garciacutea Novo amp Mariacuten Cabrera2005 Diacuteaz-Paniagua amp Aragoneacutes 2015 Schmidt et al2017) (3) Steep declines in the percentage of suc-cessful pairs implied that future generations wereproduced by a progressively more restricted numberof pairs which will make the population more sub-ject to inbreeding and stochastic events For exam-ple in the last 3 yr all the annual young were pro-duced by 6 8 and 9 pairs respectively suggesting aneffective population size 4 to 9 times lower than theoverall abundance
Given all the above it is no surprise that demo-graphic models suggested a negative growth and apopulation incapable of self-sustenance In particu-lar the model that gave the best fit to past observeddeclines was the one based on minimum Europeansurvival estimates followed by the scenario based onmean European survival estimates Given the above-
mentioned threats declines and performance deteri-oration we would expect survival to be closer to min-imum than mean European levels as supported bythe observed fit to past and recent declines Theseresults have 2 main implications (1) If survival is aslow as we suspect demographic models predict vir-tual extinction within a few years demanding anurgent need for identification and management ofmortality threats as well as quantification of actualsurvival to refine predictions Note that virtual ex -tinction could be even earlier when taking intoaccount effective rather than total population sizeand a stochastic rather than deterministic populationmodel (2) Should actual survival be confirmed lowbut further declines not observed the populationwould be a sink sustained by external sources whichwould make it even more at risk from anthropogenicthreats outside the park and thus more challengingto manage (eg Hansen amp DeFries 2007 Blanco et al2017)
5 Conclusions and implications for conservation
The decades-long degradation that we depictedwas likely generated by a combination of factorsboth internal to the park (eg rabbit availabilitymarsh inundation rates predation and competitionwith other species) and external (eg illegal poi-soning contamination farmland intensification)Some of them will be amenable to managementand others less so but the first priority will be tofind rapid ways to identify the key factors thatdrive population growth so as to optimize conserva-tion action before it is too late For example focus-ing conservation lsquoblindlyrsquo on supplementary feedingcould be useless if the problem is chemical contam-ination The quickest way to obtain such informa-tion would be a satelliteGSM (Global System forMobile communication) tagging program that wouldallow to (1) obtain rapid estimates of health andsurvival for young and adults (eg Sergio et al2019) so as to recalibrate future projections andgoals (2) assess the relative contribution of mainmortality causes which is an essential first step inany recovery program (eg Gonzaacutelez et al 2007Margalida et al 2008 Smart et al 2010) and (3)identify the areas used by breeding and non-breed-ing individuals inside and outside of the park toassess their risk-exposure and intervene before orafter death (eg to prosecute perpetrators of illegalpoisoning or re trofit dangerous electricity pylons inareas of high use by kites)
201
Endang Species Res 38 189ndash204 2019
Until this information becomes available below welist some tentative figures and priorities for conserva-tion First of all restoring the current population toformer levels would undoubtedly be challenging andprobably unrealistic given the profound changesincurred by the wider Dontildeana ecosystem in recentdecades Thus we propose an initial target of 60pairs as a long-term restoration goal Elasticity analy-sis suggested that optimal management should focuson improving adult survival which had the largestimpact on population growth as in other long-livedspecies (Saether amp Bakke 2000 Whitfield et al 2004Kruumlger et al 2010) This could be attempted by in -creasing food availability especially of key prey suchas rabbits and by curtailing mortality threats such asillegal poisoning which still continues despite mucheffort to eradicate it by the local administration Thetelemetry program outlined above could help toidentify local perpetrators as occurred in other pop-ulations (Smart et al 2010 Tavecchia et al 2012) Onthe other hand despite their low elasticities repro-ductive rates are currently so low that it would befundamental to increase them eg by increasingfood availability and ensuring proper inundation ofthe marshes Based on Fig 5 we propose as initialtargets for restoration (1) survival rates equal orhigher than the European mean (adult survivalge087) and (2) a number of young fledged per territo-rial pair above 10 which would produce an increas-ing population provided that adult survival is equalto or above the European mean Note that Fig 5could be applied to any European population as atool to check its potential viability Given the highlythreatened status of red kites the speciesrsquo limitedrange confined to Europe and its ongoing declinesviability assessments such as ours may sadly becomemore important for the management and recovery ofmany populations
In conclusion red kites would probably be extinctin southern Spain without the institution of a largenational park In this sense this example well illus-trates how protected areas will continue to be corner-stones of global conservation of threatened taxaHowever their safety is not ensured by park institu-tion per se and performance monitoring and focusedaction will be needed to avoid potential extinctiondebts which may be more protracted than previouslyappreciated In our exemplary case despite the pres-ence of a large national park on prime fertile landwithin a developed country with adequate institu-tional and financial support a key threatened speciessuffered latent but steady declines for decadesobscured by problems of perception lack and frag-
mentation of information and likely caused by acomplex array of within-park threats and growingexternal pressures Viability maintenance and recov-ery will probably require concerted actions withinand outside of the park but only after detailed infor-mation on crucial aspects becomes available whichis probably the most urgent current priority We sus-pect that dynamics like the ones illustrated here aremore common than currently appreciated and willbecome more widespread as anthropogenic pres-sures increase around protected areas and as theirperformance monitoring becomes more prevalent
Acknowledgements We thank all the (too many to mention)researchers field workers visitors volunteers gamekeep-ers park managers and wardens that have provided datasince the 1960s In particular we thank F G Vilches L Gar-ciacutea and the Equipo de Seguimiento de Procesos Naturales ofthe Estacioacuten Bioloacutegica de Dontildeana-CSIC for help in the fieldSpecial thanks to F G Vilches for the priceless help with thecollation and organization of historical information Wethank J P Castellano I Redondo and all the lsquoArea de Con-servacioacutenrsquo of Dontildeana National Park for constant interest andsupport We thank R Cadenas J Madrid R Arenas J RBenitez and all the pertinent personnel of the Consejeriacutea deMedio Ambiente of the Junta de Andaluciacutea for informationon current nest locations in the Sierra de Huelva and fortheir constant attentive support We are grateful to Dr NBunnefeld and 2 anonymous reviewers for constructivecomments that improved the manuscript This study wasfunded by the Foundation Jaime Gonzaacutelez-Gordon and bythe research project 16022015 of the Spanish Ministry ofAgriculture Food and the Environment (National ParksAutonomous Agency)
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202
Sergio et al Predator extinction debt in national park
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Gaston KJ Jackson SF Cantuacute-Salazar L Cruz-Pintildeoacuten G(2008) The ecological performance of protected areasAnnu Rev Ecol Evol Syst 39 93minus113
Godet L Devictor V Jiguet F (2007) Estimating relative pop-ulation size included within protected areas BiodiversConserv 16 2587minus2598
Goacutemara B Gonzaacutelez MJ Baos R Hiraldo F Abad E RiveraJ Jimeacutenez B (2008) Unexpected high PCB and total DDTlevels in the breeding population of red kite (Milvus mil-vus) from Dontildeana National Park south-western SpainEnviron Int 34 73minus78
Gonzaacutelez LM Margalida A Mantildeosa S Saacutenchez R and oth-ers (2007) Causes and spatio-temporal variations of non-natural mortality in the vulnerable Spanish imperialeagle Aquila adalberti during a recovery period Oryx41 495minus502
Hansen AJ DeFries R (2007) Ecological mechanisms linkingprotected areas to surrounding lands Ecol Appl 17 974minus988
Hernaacutendez FJ Donaacutezar JA Hiraldo F (2001) Evaluacioacuten deluso de venenos para el control de predadores en laComunidad Autoacutenoma Andaluza y su impacto en la con-servacioacuten de especies amenazadas de vertebrados Con-sejeria de Medio Ambiente and Estacioacuten Bioloacutegica deDontildeana Sevilla
IUCN (The World Conservation Union) (1994) Guidelines forprotected area management categories IUCN Gland
Knott J Newbery P Barov B (2009) Action plan for the redkite Milvus milvus in the European Union EuropeanCommission Brussels
Kruumlger O Gruumlnkorn T Struwe-Juhl B (2010) The return ofthe white-tailed eagle (Haliaeetus albicilla) to northernGermany modelling the past to predict the future BiolConserv 143 710minus721
Loacutepez V (1861) Cataacutelogo de las aves observadas enAndaluciacutea Madrid
Loacutepez G and others (2009) Management measures to controla feline leukemia virus outbreak in the endangered Iber-ian lynx Anim Conserv 12 173minus182
Margalida A Heredia R Razin M Hernaacutendez M (2008)Sources of variation in mortality of the bearded vultureGypaetus barbatus in Europe Bird Conserv Int 18 1minus10
Naughton-Treves L Holland MB Brandon K (2005) The roleof protected areas in conserving biodiversity and sustain-
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Newton I (1979) Population ecology of raptors T amp AD PoyserBerkhamsted
Newton I Davis PE Davis JE (1989) Age of first breedingdispersal and survival of red kites Milvus milvus inWales Ibis 131 16minus21
Otero C Castieacuten E Senosiaiacuten R Portillo F (1978) Fauna deCazorla vertebrados Publicaciones del Ministerio deAgricultura Madrid
Parks SA Harcourt AH (2002) Reserve size local humandensity and mammalian extinctions in US protectedareas Conserv Biol 16 800minus808
R Development Core Team (2018) R a language and envi-ronment for statistical computing R Foundation for Sta-tistical Computing Vienna wwwr-projectorg
Saeligther BE Bakke Oslash (2000) Avian life history variation andcontribution of demographic traits to the populationgrowth rate Ecology 81 642minus653
Sanz-Aguilar A De Pablo F Donaacutezar JA (2015) Age-depen-dent survival of island vs mainland populations of twoavian scavengers delving into migration costs Oecolo-gia 179 405minus414
Schaub M (2012) Spatial distribution of wind turbines is cru-cial for the survival of red kite populations Biol Conserv155 111minus118
Schmidt G Saacutenchez Navarro R Hernaacutendez E Carmona JJFuentelsaz F Seiz R (2017) The state of water in Dontildeana an evaluation of the state of the water and of the ecosys-tems of the protected space WWFAdena Madrid
Scott JM Davis FW McGhie RG Wright RG Groves CEstes J (2001) Nature reserves Do they capture the fullrange of Americarsquos biological diversity Ecol Appl 11 999minus1007
Seoane J Vintildeuela J Diacuteaz-Delgado R Bustamante J (2003)The effects of land use and climate on red kite distribu-tion in the Iberian peninsula Biol Conserv 111 401minus414
Sergio F Blas J Feroro M Fernaacutendez N Donaacutezar JAHiraldo F (2005) Preservation of wide-ranging top pred-ators by site-protection black and red kites in DontildeanaNational Park Biol Conserv 125 11minus21
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204
Editorial responsibility Nils BunnefeldStirling UK
Submitted October 8 2018 Accepted January 28 2019Proofs received from author(s) April 7 2019
Sergio et al Predator extinction debt in national park 197
12
3 R
BD
4 V
era
56
7 C
oto
8 N
W9
NE
10
11
12
Tot
al
RB
DR
BD
san
dA
lgai
da
Inte
rior
Pu
nta
ld
elp
ine-
pin
e-M
aris
-S
anlu
car
Ab
alar
iod
ecli
ne
vera
inte
rior
du
nes
Man
ecor
roR
eyw
ood
sw
ood
sm
illa
sp
inew
ood
a) M
ean
no
of
pai
rs19
80minus
1989
141
52
33
40a
20a
80b
50
107
44
50
30
40b
687
1990
minus19
9915
35
11
37
74
08
03
34
40
74
5e2
5c4
0a60
8minus
115
2000
minus20
0916
05
21
47
05
06
31
01
00
14
5e2
03
1a52
5minus
236
2010
minus20
1713
03
42
56
63
98
41
90
50
13
01
72
147
1minus
315
2017
100
35
211
00
03
12
37minus
462
b)
No
of
you
ng
pro
du
ced
an
nu
ally
1980
minus19
8916
14
25
66
43
09
610
020
311
06
04
56
010
26
1990
minus19
999
82
60
68
44
06
92
46
60
95
13
86
056
9minus
445
2000
minus20
0913
21
61
27
25
83
71
21
60
24
53
04
647
7minus
535
2010
minus20
172
60
61
11
82
33
50
90
30
01
62
91
919
4minus
811
2017
10
03
07
00
00
22
150
minus85
4
c)
of
the
tota
l p
op
ula
tio
n i
n e
ach
sec
tor
1980
minus19
8920
57
64
85
82
911
67
315
56
47
34
45
819
90minus
1999
251
84
21
126
66
131
55
73
12
74
41
66
2000
minus20
0929
49
62
612
99
211
51
81
80
28
33
79
120
10minus
2017
276
72
53
141
82
178
40
11
03
64
36
45
2017
270
00
81
135
54
297
00
00
00
81
27
54
d)
c
on
trib
uti
on
of
each
sec
tor
to t
ota
l an
nu
al y
ou
ng
pro
du
ctio
n19
80minus
1989
157
41
54
94
62
29
97
198
107
58
44
58
1990
minus19
9917
24
61
112
114
77
04
211
61
68
96
610
520
00minus
2009
277
33
24
78
151
121
24
34
04
94
63
96
2010
minus20
1713
43
35
418
19
411
74
81
30
08
215
09
620
176
70
00
046
720
00
00
00
00
00
013
313
3
a Cro
ss-c
omb
ined
est
imat
e b
Sta
tic
bac
k-e
stim
ate
c In
terp
olat
ed e
stim
ate
See
Sec
tion
23
for
det
ails
Tab
le 2
(a
) M
ean
nu
mb
er o
f p
airs
an
d (
b)
cum
ula
tive
nu
mb
er o
f of
fsp
rin
g p
rod
uce
d a
nn
ual
ly b
y th
e D
ontildean
a re
d k
ite
pop
ula
tion
wit
hin
eac
h s
ecto
r an
d i
n t
he
wh
ole
par
k o
ver
the
pas
t d
ecad
es a
nd
in 2
017
Per
cen
tag
e of
(c)
pai
rs a
nd
(d
) yo
un
g c
ontr
ibu
ted
by
each
sec
tor
to t
he
over
all p
opu
lati
on S
ecto
rs c
ontr
ibu
tin
g m
ore
than
10
ar
e h
igh
lig
hte
d i
n b
old
T
otal
ref
ers
to t
he
sum
of
all
sect
ors
d
ecli
ne
is t
he
dec
lin
e co
mp
ared
to
the
1980
s P
rop
orti
onal
con
trib
uti
ons
are
also
ill
ust
rate
d i
n F
ig
5
RB
D R
eser
va B
iolo
gic
a d
e D
ontildean
a
Endang Species Res 38 189ndash204 2019
detecting the problem was likely exacerbated by thefollowing factors that could be defined as lsquoperceptionobstaclesrsquo (1) The fact that a population becomesmore and more restricted to a park is often used toillustrate the positive role of protected areas byfocusing their performance assessments on range
coverage ie the capability of protected areas tocover a large portion of a species range (eg Czech2005 Godet et al 2007) This diverts attention fromthe wider problems of range contraction and from theactual performance of the park in terms of viabilitymaintenance (Gaston et al 2008) (2) Confinement to
198
of nests in each sector
of annual young generated by each sector
1980s 2010s
1980s 2010s
a) b)
c) d)
Fig 5 Percentage of the total red kite population in each of 12 sectors of Dontildeana (a) in the 1980s and (b) in the 2010s percent-age of the annual young production generated by each sector (c) in the 1980s and (d) in the 2010s (a) In the 1980s the bulk ofthe population was concentrated in northern sectors (7 and 8) and in the southern shores of the marshes (sectors 1 6 and 10)(b) In the 2010s the population virtually disappeared from the northern sectors and became essentially confined to the na-tional park where it concentrated along the marshes (c) In the 1980s the population generated more than 100 young eachyear most of them produced by the northern sectors (7 8 9) and by the northern shores of the marshes (sectors 1 and 4) (d) Inthe 2010s the population generated less than 10 young mostly generated close to wetlands (sectors 1 4 11) with homo -geneously low numbers elsewhere Colors (yellow rarr orange rarr red) classify sectors by tertiles of the range of percentage
contribution
Sergio et al Predator extinction debt in national park
a protected area is usually accompanied by the auto-matic presumption that this will act as a source areawith limited anthropogenic impacts an assumptionthat is increasingly disproved (Hansen amp DeFries2007 Gaston et al 2008 Watson et al 2014) (3) Long-term assessments such as ours required the lengthy
collation of fragmented informationfrom a large number of sequentialfield workers and administrationseach of which had a very limited per-ception of the overall situation (4)Much monitoring was conducted inthe core areas of the park like theRBD where the species has alwaysbeen most abundant and relativelystable (eg Sergio et al 2005) con-fusing the perception of broaderdeclines (5) Finally large numbersof wintering migrants boost the pop-ulation in the winter and earlyspring often producing an optimisticimpression of apparent abundance
even in relatively expert members of the public or oflocal administrations as we frequently noted in pub-lic talks and private conversations
Overall the decline occurred at multiple levels redkites were originally widespread throughout south-ern Spain (Loacutepez 1861) but became progressively
199
2030405060708090
100110
Bree
ding
su
cces
sful
()
a breeding pairs successful pairs
202122232425262728
Clut
ch si
ze
b
25
35
45
55
65
75
85
1970-79 1980-89 1990-99 2000-09 2010-17
Hatc
hing
succ
ess
broo
d re
duct
ion
()
Decade
c Hatching successBrood reduction
03
06
09
12
15
18
21
1970-79 1980-89 1990-99 2000-09 2010-17
Youn
g fle
dged
Decade
d Young breeding pairYoung successful pair
Fig 6 Reproductive parameters of the red kite population of Dontildeana (a) percentage of pairs laying eggs (black dots n = 804)and successfully raising fledglings (white dots n = 1185) (b) mean clutch size (n = 469) (c) hatching success (percentage ofeggs that hatched black dots n = 353) and brood reduction (percentage of chicks that disappeared during the nestling periodwhite dots n = 240) (d) mean number of young fledged per territorial pair (black dots n = 1145) and per successful pair (white
dots n = 576)
0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75
Young fledgedsuccessful pairYoung fledgedbreeding pairYoung fledgedterritorial pair
Probability of successful breedingBrood reduction
Hatching successClutch size
Probability of laying
Deterioration ()
Breeding parameter
Fig 7 Percentage deterioration of breeding parameters of the red kite popu-lation of Dontildeana between the 1980s and the 2010s
Endang Species Res 38 189ndash204 2019
confined to the protected area of Dontildeana in recentdecades However the park did not confer automaticsafety and declines and range contraction also con-tinued within the protected area suggesting perva-sive pressures and range erosion at multiple spatialscales In particular almost one third of the Dontildeana
population was virtually eradicatedfrom the northern pinewoods of thebuffering Natural Park in 5 to 7 yrbetween the late 1980s and early1990s Several lines of evidence sug-gest that illegal poisoning was themain cause of this eradication (1) Sev-eral adults were found poisoned undertheir nest in those sectors and years(2) Large-scale poisoning campaignsof raptors were reported throughoutSpain in those exact same years asa consequence of huntersrsquo illegalattempts to control predator popula-tions to increase the rapidly deterio-rating numbers of small game (rabbitsand partridges Villafuerte et al 1998Vintildeuela amp Villafuerte 2003 Cano et al2008) In this sense the National Parksuffered much wider national-level
pressures (3) The northern sectors of the parkwhere the eradication took place included or wereclose to private small-game reserves and predatorcontrol was well known to occur in some of them (4)Finally the rapidity of the eradication of such a long-lived species (maximum longevity of 29 yr in Dontilde -ana) implied a causative agent that directly affectedadult mortality (Saether amp Bakke 2000) such as poi-soning The marked impact of poisoning on adult sur-vival and population growth are well recognized forthis species whose facultative scavenging habits andforaging method of meticulous low and slow quar-tering of the ground make it particularly sensitive tothis threat (Smart et al 2010 Tavecchia et al 2012Tenan et al 2012 Sanz-Aguilar et al 2015)
Spikes of rapid local eradication were superim-posed on more gradual but steady deterioration ofoffspring production Gradual and continuous ratherthan sudden degradation of performance suggestedthat poisoning was not the only threat in effect Inthis context several factors may have contributed togradually deteriorate ecological conditions for kitesin recent decades (1) Rabbit epidemics have causedprogressive declines in the availability of this keyprey (Vintildeuela amp Villafuerte 2003) (2) Lower preyavailability may have exacerbated competition withthe dense populations of other raptors with similardiets such as the ecologically similar and in creasingblack kite (3) Predation rates on adults and nestlingsmay have increased with the expansion of the popu-lations of potential predators such as eagle owls Bubobubo and goshawks Accipiter gentilis (4) Recentassessments have detected alarming levels of toxic
200
00
02
04
06
08
10
12
1980sndash1990s 1990sndash2000s 2000sndash2010s
Popu
latio
n gr
owth
rate
Period
Observed populationgrowth
Scenario 1 minimumEuropean survival
Scenario 2 meanEuropean survival
Scenario 3 maximumEuropean survival
Fig 8 Population growth of the Dontildeana red kite population during the past 4decades as predicted by matrix demographic models based on 3 scenarioswhich assumed that survival was equal to minimum mean or maximum sur-vival rates reported for other European populations (reviewed in Table 1)Predicted values are compared with observed declines from one decade to
the next
Fig 9 Population growth rate of red kites in relation to adultsurvival and breeding performance (mean number of youngfledged per territorial pair) based on a matrix populationmodel Note that the graph could be applied to any Euro-pean population The 3 points at the base of the graph repre-sent the minimum (black) mean (grey) and maximum (blue)survival published for European populations (reviewed in
Table 1)
Sergio et al Predator extinction debt in national park
chemicals in red kite eggs from Dontildeana (Goacutemara etal 2008) (5) Climate change and agricultural man-agement have lowered the water table with likelyimpacts on marsh inundation levels and aquatic prey(Garciacutea Novo amp Mariacuten Cabrera 2005 Diacuteaz-Paniaguaamp Aragoneacutes 2015 Schmidt et al 2017) (6) Conver-sion to intensive farmland in surrounding lands haseroded habitat and prey availability outside the pro-tected area which may have buffered kites fromperiods of low prey availability within the park (egduring droughts in the marshes) Some of the pat-terns of observed reproductive deterioration lendsupport to some of these impacts For exampledeclining clutch sizes and increasing rates of broodreduction suggest that food was not sufficient to sus-tain earlier reproductive levels while lowered hatch-ing success is often the result of chemical contamina-tion in raptors (review in Newton 1979) While eachof these threats will be quantitatively investigated indetail in the immediate future in the present contextthey illustrate the frequent and complex challengesfaced by (1) protected areas in maintaining biodiver-sity and viable populations of imperiled species and(2) conservation biologists in identifying causes ofdecline for subsequent management interventioneven in lsquoprivilegedrsquo sites such as reserves
Redistribution declining numbers and perform-ance had important repercussions for future viability(1) The population passed from producing gt100annual young to lt10minus20 which will make mainte-nance and recovery difficult (2) These young wereincreasingly produced in the core sectors of themarsh-ecotone within the National Park which prob-ably increased the dependence of the population onmarsh inundation in turn affected by problems oper-ating outside the park (Garciacutea Novo amp Mariacuten Cabrera2005 Diacuteaz-Paniagua amp Aragoneacutes 2015 Schmidt et al2017) (3) Steep declines in the percentage of suc-cessful pairs implied that future generations wereproduced by a progressively more restricted numberof pairs which will make the population more sub-ject to inbreeding and stochastic events For exam-ple in the last 3 yr all the annual young were pro-duced by 6 8 and 9 pairs respectively suggesting aneffective population size 4 to 9 times lower than theoverall abundance
Given all the above it is no surprise that demo-graphic models suggested a negative growth and apopulation incapable of self-sustenance In particu-lar the model that gave the best fit to past observeddeclines was the one based on minimum Europeansurvival estimates followed by the scenario based onmean European survival estimates Given the above-
mentioned threats declines and performance deteri-oration we would expect survival to be closer to min-imum than mean European levels as supported bythe observed fit to past and recent declines Theseresults have 2 main implications (1) If survival is aslow as we suspect demographic models predict vir-tual extinction within a few years demanding anurgent need for identification and management ofmortality threats as well as quantification of actualsurvival to refine predictions Note that virtual ex -tinction could be even earlier when taking intoaccount effective rather than total population sizeand a stochastic rather than deterministic populationmodel (2) Should actual survival be confirmed lowbut further declines not observed the populationwould be a sink sustained by external sources whichwould make it even more at risk from anthropogenicthreats outside the park and thus more challengingto manage (eg Hansen amp DeFries 2007 Blanco et al2017)
5 Conclusions and implications for conservation
The decades-long degradation that we depictedwas likely generated by a combination of factorsboth internal to the park (eg rabbit availabilitymarsh inundation rates predation and competitionwith other species) and external (eg illegal poi-soning contamination farmland intensification)Some of them will be amenable to managementand others less so but the first priority will be tofind rapid ways to identify the key factors thatdrive population growth so as to optimize conserva-tion action before it is too late For example focus-ing conservation lsquoblindlyrsquo on supplementary feedingcould be useless if the problem is chemical contam-ination The quickest way to obtain such informa-tion would be a satelliteGSM (Global System forMobile communication) tagging program that wouldallow to (1) obtain rapid estimates of health andsurvival for young and adults (eg Sergio et al2019) so as to recalibrate future projections andgoals (2) assess the relative contribution of mainmortality causes which is an essential first step inany recovery program (eg Gonzaacutelez et al 2007Margalida et al 2008 Smart et al 2010) and (3)identify the areas used by breeding and non-breed-ing individuals inside and outside of the park toassess their risk-exposure and intervene before orafter death (eg to prosecute perpetrators of illegalpoisoning or re trofit dangerous electricity pylons inareas of high use by kites)
201
Endang Species Res 38 189ndash204 2019
Until this information becomes available below welist some tentative figures and priorities for conserva-tion First of all restoring the current population toformer levels would undoubtedly be challenging andprobably unrealistic given the profound changesincurred by the wider Dontildeana ecosystem in recentdecades Thus we propose an initial target of 60pairs as a long-term restoration goal Elasticity analy-sis suggested that optimal management should focuson improving adult survival which had the largestimpact on population growth as in other long-livedspecies (Saether amp Bakke 2000 Whitfield et al 2004Kruumlger et al 2010) This could be attempted by in -creasing food availability especially of key prey suchas rabbits and by curtailing mortality threats such asillegal poisoning which still continues despite mucheffort to eradicate it by the local administration Thetelemetry program outlined above could help toidentify local perpetrators as occurred in other pop-ulations (Smart et al 2010 Tavecchia et al 2012) Onthe other hand despite their low elasticities repro-ductive rates are currently so low that it would befundamental to increase them eg by increasingfood availability and ensuring proper inundation ofthe marshes Based on Fig 5 we propose as initialtargets for restoration (1) survival rates equal orhigher than the European mean (adult survivalge087) and (2) a number of young fledged per territo-rial pair above 10 which would produce an increas-ing population provided that adult survival is equalto or above the European mean Note that Fig 5could be applied to any European population as atool to check its potential viability Given the highlythreatened status of red kites the speciesrsquo limitedrange confined to Europe and its ongoing declinesviability assessments such as ours may sadly becomemore important for the management and recovery ofmany populations
In conclusion red kites would probably be extinctin southern Spain without the institution of a largenational park In this sense this example well illus-trates how protected areas will continue to be corner-stones of global conservation of threatened taxaHowever their safety is not ensured by park institu-tion per se and performance monitoring and focusedaction will be needed to avoid potential extinctiondebts which may be more protracted than previouslyappreciated In our exemplary case despite the pres-ence of a large national park on prime fertile landwithin a developed country with adequate institu-tional and financial support a key threatened speciessuffered latent but steady declines for decadesobscured by problems of perception lack and frag-
mentation of information and likely caused by acomplex array of within-park threats and growingexternal pressures Viability maintenance and recov-ery will probably require concerted actions withinand outside of the park but only after detailed infor-mation on crucial aspects becomes available whichis probably the most urgent current priority We sus-pect that dynamics like the ones illustrated here aremore common than currently appreciated and willbecome more widespread as anthropogenic pres-sures increase around protected areas and as theirperformance monitoring becomes more prevalent
Acknowledgements We thank all the (too many to mention)researchers field workers visitors volunteers gamekeep-ers park managers and wardens that have provided datasince the 1960s In particular we thank F G Vilches L Gar-ciacutea and the Equipo de Seguimiento de Procesos Naturales ofthe Estacioacuten Bioloacutegica de Dontildeana-CSIC for help in the fieldSpecial thanks to F G Vilches for the priceless help with thecollation and organization of historical information Wethank J P Castellano I Redondo and all the lsquoArea de Con-servacioacutenrsquo of Dontildeana National Park for constant interest andsupport We thank R Cadenas J Madrid R Arenas J RBenitez and all the pertinent personnel of the Consejeriacutea deMedio Ambiente of the Junta de Andaluciacutea for informationon current nest locations in the Sierra de Huelva and fortheir constant attentive support We are grateful to Dr NBunnefeld and 2 anonymous reviewers for constructivecomments that improved the manuscript This study wasfunded by the Foundation Jaime Gonzaacutelez-Gordon and bythe research project 16022015 of the Spanish Ministry ofAgriculture Food and the Environment (National ParksAutonomous Agency)
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Blanco G Cardells J Garijo-Toledo MM (2017) Supplemen-tary feeding and endoparasites in threatened avian scav-engers coprologic evidence from red kites in their win-tering stronghold Environ Res 155 22minus30
Brashares JS Arcese P Sam MK (2001) Human demographyand reserve size predict wildlife extinction in WestAfrica Proc Biol Sci 268 2473minus2478
Bustamante J (1993) Post-fledging dependence period anddevelopment of flight and hunting behaviour in the redkite Milvus milvus Bird Study 40 181minus188
Cano C Ayerza P Fernaacutendez J (2008) Poisoning in Spain(1990minus2005) analysis of the problem incidence andcauses WWFAdena Madrid (in Spanish)
Caswell H (2001) Matrix population models Sinauer Sun-derland MA
Ceballos JJ Guimeraacute VM (1992) Guiacutea de las aves de Jerez yde la Provincia de Caacutediz atlas ornitoloacutegico de lasespecies nidificantes Ayuntamiento de Jerez Jerez
Craigie ID Baillie JEM Balmford A Carbone C Collen BGreen RE Hutton JM (2010) Large mammal population
202
Sergio et al Predator extinction debt in national park
declines in Africarsquos protected areas Biol Conserv 143 2221minus2228
Czech B (2005) The capacity of the National WildlifeRefuge System to conserve threatened and endangeredanimal species in the United States Conserv Biol 19 1246minus1253
Delibes M Garciacutea L (1984) Haacutebitos alimenticios del milanoreal en Dontildeana durante el periodo de criacutea Ardeola 31 115minus121
Diacuteaz-Paniagua C Aragoneacutes D (2015) Permanent and tempo-rary ponds in Dontildeana National Park (SW Spain) arethreatened by desiccation Limnetica 34 407minus424
Evans IM Summers RW OrsquoToole L Orr-Ewing DC Snell NSmith J (1999) Evaluating the success of translocatingred kites Milvus milvus to the UK Bird Study 46 129minus144
Ferrer M Hiraldo F (1991) Evaluation of management tech-niques for the Spanish imperial eagle Wildl Soc Bull 19 436minus442
Garciacutea Novo F Mariacuten Cabrera C (2005) Dontildeana water andbiosphere Dontildeana 2005 Project Spanish Ministry of theEnvironment Madrid
Gaston KJ Jackson SF Cantuacute-Salazar L Cruz-Pintildeoacuten G(2008) The ecological performance of protected areasAnnu Rev Ecol Evol Syst 39 93minus113
Godet L Devictor V Jiguet F (2007) Estimating relative pop-ulation size included within protected areas BiodiversConserv 16 2587minus2598
Goacutemara B Gonzaacutelez MJ Baos R Hiraldo F Abad E RiveraJ Jimeacutenez B (2008) Unexpected high PCB and total DDTlevels in the breeding population of red kite (Milvus mil-vus) from Dontildeana National Park south-western SpainEnviron Int 34 73minus78
Gonzaacutelez LM Margalida A Mantildeosa S Saacutenchez R and oth-ers (2007) Causes and spatio-temporal variations of non-natural mortality in the vulnerable Spanish imperialeagle Aquila adalberti during a recovery period Oryx41 495minus502
Hansen AJ DeFries R (2007) Ecological mechanisms linkingprotected areas to surrounding lands Ecol Appl 17 974minus988
Hernaacutendez FJ Donaacutezar JA Hiraldo F (2001) Evaluacioacuten deluso de venenos para el control de predadores en laComunidad Autoacutenoma Andaluza y su impacto en la con-servacioacuten de especies amenazadas de vertebrados Con-sejeria de Medio Ambiente and Estacioacuten Bioloacutegica deDontildeana Sevilla
IUCN (The World Conservation Union) (1994) Guidelines forprotected area management categories IUCN Gland
Knott J Newbery P Barov B (2009) Action plan for the redkite Milvus milvus in the European Union EuropeanCommission Brussels
Kruumlger O Gruumlnkorn T Struwe-Juhl B (2010) The return ofthe white-tailed eagle (Haliaeetus albicilla) to northernGermany modelling the past to predict the future BiolConserv 143 710minus721
Loacutepez V (1861) Cataacutelogo de las aves observadas enAndaluciacutea Madrid
Loacutepez G and others (2009) Management measures to controla feline leukemia virus outbreak in the endangered Iber-ian lynx Anim Conserv 12 173minus182
Margalida A Heredia R Razin M Hernaacutendez M (2008)Sources of variation in mortality of the bearded vultureGypaetus barbatus in Europe Bird Conserv Int 18 1minus10
Naughton-Treves L Holland MB Brandon K (2005) The roleof protected areas in conserving biodiversity and sustain-
ing local livelihoods Annu Rev Environ Resour 30 219minus252
Newton I (1979) Population ecology of raptors T amp AD PoyserBerkhamsted
Newton I Davis PE Davis JE (1989) Age of first breedingdispersal and survival of red kites Milvus milvus inWales Ibis 131 16minus21
Otero C Castieacuten E Senosiaiacuten R Portillo F (1978) Fauna deCazorla vertebrados Publicaciones del Ministerio deAgricultura Madrid
Parks SA Harcourt AH (2002) Reserve size local humandensity and mammalian extinctions in US protectedareas Conserv Biol 16 800minus808
R Development Core Team (2018) R a language and envi-ronment for statistical computing R Foundation for Sta-tistical Computing Vienna wwwr-projectorg
Saeligther BE Bakke Oslash (2000) Avian life history variation andcontribution of demographic traits to the populationgrowth rate Ecology 81 642minus653
Sanz-Aguilar A De Pablo F Donaacutezar JA (2015) Age-depen-dent survival of island vs mainland populations of twoavian scavengers delving into migration costs Oecolo-gia 179 405minus414
Schaub M (2012) Spatial distribution of wind turbines is cru-cial for the survival of red kite populations Biol Conserv155 111minus118
Schmidt G Saacutenchez Navarro R Hernaacutendez E Carmona JJFuentelsaz F Seiz R (2017) The state of water in Dontildeana an evaluation of the state of the water and of the ecosys-tems of the protected space WWFAdena Madrid
Scott JM Davis FW McGhie RG Wright RG Groves CEstes J (2001) Nature reserves Do they capture the fullrange of Americarsquos biological diversity Ecol Appl 11 999minus1007
Seoane J Vintildeuela J Diacuteaz-Delgado R Bustamante J (2003)The effects of land use and climate on red kite distribu-tion in the Iberian peninsula Biol Conserv 111 401minus414
Sergio F Blas J Feroro M Fernaacutendez N Donaacutezar JAHiraldo F (2005) Preservation of wide-ranging top pred-ators by site-protection black and red kites in DontildeanaNational Park Biol Conserv 125 11minus21
Sergio F Tanferna A Blas J Blanco G Hiraldo F (2019) Reli-able methods for identifying animal deaths in GPS- andsatellite-tracking data review testing and calibrationJ Appl Ecol 56562ndash572
Smart J Amar A Sim IMW Etheridge B Cameron DChristie G Wilson JD (2010) Illegal killing slows popula-tion recovery of a re-introduced raptor of high conserva-tion concern mdash the red kite Milvus milvus Biol Conserv143 1278minus1286
Tavecchia G Adrover J Muntildeoz Navarro A Pradel R (2012)Modelling mortality causes in longitudinal data in thepresence of tag loss application to raptor poisoning andelectrocution J Appl Ecol 49 297minus305
Tenan S Adrover J Muntildeoz Navarro A Sergio F TavecchiaG (2012) Demographic consequences of poison-relatedmortality in a threatened bird of prey PLOS ONE 7 e49187
Tilman D May RM Lehman CL Nowak MA (1994) Habitatdestruction and the extinction debt Nature 371 65minus66
Torres Esquivias JA Jordano P Leoacuten A (1981) Aves de presadiurnas de la provincia de Coacuterdoba Publicaciones CA yMP Coacuterdoba
Veiga JP Hiraldo F (1990) Food habits and the survival andgrowth of nestlings in two sympatric kites (Milvus milvus
203
Endang Species Res 38 189ndash204 2019
and Milvus migrans) Holarct Ecol 13 62minus71 Villafuerte R Vintildeuela J Blanco JC (1998) Extensive preda-
tor persecution caused by population crash in a gamespecies the case of red kites and rabbits in Spain BiolConserv 84 181minus188
Vintildeuela J (2004) Milano real Milvus milvus In Madrontildeo AGonzaacutelez C Atienza JC (eds) Libro rojo de las aves deEspantildea Direccioacuten General para la BiodiversidadminusSEOBirdLife Madrid p 120minus125
Vintildeuela J Villafuerte R (2003) Predators and rabbits (Oryc-tolagus cuniculus) in Spain a key conflict for Europeanraptor conservation In Thompson DBA Redpath SMFielding AH Marquiss M Galbraith CA (eds) Birds ofprey in a changing environment The Stationery OfficeEdinburgh p 511minus526
Vintildeuela J Martiacute R Ruiz A (eds) (1999) El milano real enEspantildea SEOBirdlife Madrid
Watson JEM Dudley N Segan DB Hockings M (2014) Theperformance and potential of protected areas Nature515 67minus73
Whitfield SM Bell KE Philippi T Sasa M and others (2007)Amphibian and reptile declines over 35 years at La SelvaCosta Rica Proc Natl Acad Sci USA 104 8352minus8356
Whitfield DP Fielding AH McLeod DRA Haworth PF(2004) Modelling the effects of persecution on the popu-lation dynamics of golden eagles in Scotland Biol Con-serv 119 319minus333
Zuur A Ieno EN Walker N Saveliev AA Smith GM (2009)Mixed effects models and extensions in ecology with RSpringer New York NY
204
Editorial responsibility Nils BunnefeldStirling UK
Submitted October 8 2018 Accepted January 28 2019Proofs received from author(s) April 7 2019
Endang Species Res 38 189ndash204 2019
detecting the problem was likely exacerbated by thefollowing factors that could be defined as lsquoperceptionobstaclesrsquo (1) The fact that a population becomesmore and more restricted to a park is often used toillustrate the positive role of protected areas byfocusing their performance assessments on range
coverage ie the capability of protected areas tocover a large portion of a species range (eg Czech2005 Godet et al 2007) This diverts attention fromthe wider problems of range contraction and from theactual performance of the park in terms of viabilitymaintenance (Gaston et al 2008) (2) Confinement to
198
of nests in each sector
of annual young generated by each sector
1980s 2010s
1980s 2010s
a) b)
c) d)
Fig 5 Percentage of the total red kite population in each of 12 sectors of Dontildeana (a) in the 1980s and (b) in the 2010s percent-age of the annual young production generated by each sector (c) in the 1980s and (d) in the 2010s (a) In the 1980s the bulk ofthe population was concentrated in northern sectors (7 and 8) and in the southern shores of the marshes (sectors 1 6 and 10)(b) In the 2010s the population virtually disappeared from the northern sectors and became essentially confined to the na-tional park where it concentrated along the marshes (c) In the 1980s the population generated more than 100 young eachyear most of them produced by the northern sectors (7 8 9) and by the northern shores of the marshes (sectors 1 and 4) (d) Inthe 2010s the population generated less than 10 young mostly generated close to wetlands (sectors 1 4 11) with homo -geneously low numbers elsewhere Colors (yellow rarr orange rarr red) classify sectors by tertiles of the range of percentage
contribution
Sergio et al Predator extinction debt in national park
a protected area is usually accompanied by the auto-matic presumption that this will act as a source areawith limited anthropogenic impacts an assumptionthat is increasingly disproved (Hansen amp DeFries2007 Gaston et al 2008 Watson et al 2014) (3) Long-term assessments such as ours required the lengthy
collation of fragmented informationfrom a large number of sequentialfield workers and administrationseach of which had a very limited per-ception of the overall situation (4)Much monitoring was conducted inthe core areas of the park like theRBD where the species has alwaysbeen most abundant and relativelystable (eg Sergio et al 2005) con-fusing the perception of broaderdeclines (5) Finally large numbersof wintering migrants boost the pop-ulation in the winter and earlyspring often producing an optimisticimpression of apparent abundance
even in relatively expert members of the public or oflocal administrations as we frequently noted in pub-lic talks and private conversations
Overall the decline occurred at multiple levels redkites were originally widespread throughout south-ern Spain (Loacutepez 1861) but became progressively
199
2030405060708090
100110
Bree
ding
su
cces
sful
()
a breeding pairs successful pairs
202122232425262728
Clut
ch si
ze
b
25
35
45
55
65
75
85
1970-79 1980-89 1990-99 2000-09 2010-17
Hatc
hing
succ
ess
broo
d re
duct
ion
()
Decade
c Hatching successBrood reduction
03
06
09
12
15
18
21
1970-79 1980-89 1990-99 2000-09 2010-17
Youn
g fle
dged
Decade
d Young breeding pairYoung successful pair
Fig 6 Reproductive parameters of the red kite population of Dontildeana (a) percentage of pairs laying eggs (black dots n = 804)and successfully raising fledglings (white dots n = 1185) (b) mean clutch size (n = 469) (c) hatching success (percentage ofeggs that hatched black dots n = 353) and brood reduction (percentage of chicks that disappeared during the nestling periodwhite dots n = 240) (d) mean number of young fledged per territorial pair (black dots n = 1145) and per successful pair (white
dots n = 576)
0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75
Young fledgedsuccessful pairYoung fledgedbreeding pairYoung fledgedterritorial pair
Probability of successful breedingBrood reduction
Hatching successClutch size
Probability of laying
Deterioration ()
Breeding parameter
Fig 7 Percentage deterioration of breeding parameters of the red kite popu-lation of Dontildeana between the 1980s and the 2010s
Endang Species Res 38 189ndash204 2019
confined to the protected area of Dontildeana in recentdecades However the park did not confer automaticsafety and declines and range contraction also con-tinued within the protected area suggesting perva-sive pressures and range erosion at multiple spatialscales In particular almost one third of the Dontildeana
population was virtually eradicatedfrom the northern pinewoods of thebuffering Natural Park in 5 to 7 yrbetween the late 1980s and early1990s Several lines of evidence sug-gest that illegal poisoning was themain cause of this eradication (1) Sev-eral adults were found poisoned undertheir nest in those sectors and years(2) Large-scale poisoning campaignsof raptors were reported throughoutSpain in those exact same years asa consequence of huntersrsquo illegalattempts to control predator popula-tions to increase the rapidly deterio-rating numbers of small game (rabbitsand partridges Villafuerte et al 1998Vintildeuela amp Villafuerte 2003 Cano et al2008) In this sense the National Parksuffered much wider national-level
pressures (3) The northern sectors of the parkwhere the eradication took place included or wereclose to private small-game reserves and predatorcontrol was well known to occur in some of them (4)Finally the rapidity of the eradication of such a long-lived species (maximum longevity of 29 yr in Dontilde -ana) implied a causative agent that directly affectedadult mortality (Saether amp Bakke 2000) such as poi-soning The marked impact of poisoning on adult sur-vival and population growth are well recognized forthis species whose facultative scavenging habits andforaging method of meticulous low and slow quar-tering of the ground make it particularly sensitive tothis threat (Smart et al 2010 Tavecchia et al 2012Tenan et al 2012 Sanz-Aguilar et al 2015)
Spikes of rapid local eradication were superim-posed on more gradual but steady deterioration ofoffspring production Gradual and continuous ratherthan sudden degradation of performance suggestedthat poisoning was not the only threat in effect Inthis context several factors may have contributed togradually deteriorate ecological conditions for kitesin recent decades (1) Rabbit epidemics have causedprogressive declines in the availability of this keyprey (Vintildeuela amp Villafuerte 2003) (2) Lower preyavailability may have exacerbated competition withthe dense populations of other raptors with similardiets such as the ecologically similar and in creasingblack kite (3) Predation rates on adults and nestlingsmay have increased with the expansion of the popu-lations of potential predators such as eagle owls Bubobubo and goshawks Accipiter gentilis (4) Recentassessments have detected alarming levels of toxic
200
00
02
04
06
08
10
12
1980sndash1990s 1990sndash2000s 2000sndash2010s
Popu
latio
n gr
owth
rate
Period
Observed populationgrowth
Scenario 1 minimumEuropean survival
Scenario 2 meanEuropean survival
Scenario 3 maximumEuropean survival
Fig 8 Population growth of the Dontildeana red kite population during the past 4decades as predicted by matrix demographic models based on 3 scenarioswhich assumed that survival was equal to minimum mean or maximum sur-vival rates reported for other European populations (reviewed in Table 1)Predicted values are compared with observed declines from one decade to
the next
Fig 9 Population growth rate of red kites in relation to adultsurvival and breeding performance (mean number of youngfledged per territorial pair) based on a matrix populationmodel Note that the graph could be applied to any Euro-pean population The 3 points at the base of the graph repre-sent the minimum (black) mean (grey) and maximum (blue)survival published for European populations (reviewed in
Table 1)
Sergio et al Predator extinction debt in national park
chemicals in red kite eggs from Dontildeana (Goacutemara etal 2008) (5) Climate change and agricultural man-agement have lowered the water table with likelyimpacts on marsh inundation levels and aquatic prey(Garciacutea Novo amp Mariacuten Cabrera 2005 Diacuteaz-Paniaguaamp Aragoneacutes 2015 Schmidt et al 2017) (6) Conver-sion to intensive farmland in surrounding lands haseroded habitat and prey availability outside the pro-tected area which may have buffered kites fromperiods of low prey availability within the park (egduring droughts in the marshes) Some of the pat-terns of observed reproductive deterioration lendsupport to some of these impacts For exampledeclining clutch sizes and increasing rates of broodreduction suggest that food was not sufficient to sus-tain earlier reproductive levels while lowered hatch-ing success is often the result of chemical contamina-tion in raptors (review in Newton 1979) While eachof these threats will be quantitatively investigated indetail in the immediate future in the present contextthey illustrate the frequent and complex challengesfaced by (1) protected areas in maintaining biodiver-sity and viable populations of imperiled species and(2) conservation biologists in identifying causes ofdecline for subsequent management interventioneven in lsquoprivilegedrsquo sites such as reserves
Redistribution declining numbers and perform-ance had important repercussions for future viability(1) The population passed from producing gt100annual young to lt10minus20 which will make mainte-nance and recovery difficult (2) These young wereincreasingly produced in the core sectors of themarsh-ecotone within the National Park which prob-ably increased the dependence of the population onmarsh inundation in turn affected by problems oper-ating outside the park (Garciacutea Novo amp Mariacuten Cabrera2005 Diacuteaz-Paniagua amp Aragoneacutes 2015 Schmidt et al2017) (3) Steep declines in the percentage of suc-cessful pairs implied that future generations wereproduced by a progressively more restricted numberof pairs which will make the population more sub-ject to inbreeding and stochastic events For exam-ple in the last 3 yr all the annual young were pro-duced by 6 8 and 9 pairs respectively suggesting aneffective population size 4 to 9 times lower than theoverall abundance
Given all the above it is no surprise that demo-graphic models suggested a negative growth and apopulation incapable of self-sustenance In particu-lar the model that gave the best fit to past observeddeclines was the one based on minimum Europeansurvival estimates followed by the scenario based onmean European survival estimates Given the above-
mentioned threats declines and performance deteri-oration we would expect survival to be closer to min-imum than mean European levels as supported bythe observed fit to past and recent declines Theseresults have 2 main implications (1) If survival is aslow as we suspect demographic models predict vir-tual extinction within a few years demanding anurgent need for identification and management ofmortality threats as well as quantification of actualsurvival to refine predictions Note that virtual ex -tinction could be even earlier when taking intoaccount effective rather than total population sizeand a stochastic rather than deterministic populationmodel (2) Should actual survival be confirmed lowbut further declines not observed the populationwould be a sink sustained by external sources whichwould make it even more at risk from anthropogenicthreats outside the park and thus more challengingto manage (eg Hansen amp DeFries 2007 Blanco et al2017)
5 Conclusions and implications for conservation
The decades-long degradation that we depictedwas likely generated by a combination of factorsboth internal to the park (eg rabbit availabilitymarsh inundation rates predation and competitionwith other species) and external (eg illegal poi-soning contamination farmland intensification)Some of them will be amenable to managementand others less so but the first priority will be tofind rapid ways to identify the key factors thatdrive population growth so as to optimize conserva-tion action before it is too late For example focus-ing conservation lsquoblindlyrsquo on supplementary feedingcould be useless if the problem is chemical contam-ination The quickest way to obtain such informa-tion would be a satelliteGSM (Global System forMobile communication) tagging program that wouldallow to (1) obtain rapid estimates of health andsurvival for young and adults (eg Sergio et al2019) so as to recalibrate future projections andgoals (2) assess the relative contribution of mainmortality causes which is an essential first step inany recovery program (eg Gonzaacutelez et al 2007Margalida et al 2008 Smart et al 2010) and (3)identify the areas used by breeding and non-breed-ing individuals inside and outside of the park toassess their risk-exposure and intervene before orafter death (eg to prosecute perpetrators of illegalpoisoning or re trofit dangerous electricity pylons inareas of high use by kites)
201
Endang Species Res 38 189ndash204 2019
Until this information becomes available below welist some tentative figures and priorities for conserva-tion First of all restoring the current population toformer levels would undoubtedly be challenging andprobably unrealistic given the profound changesincurred by the wider Dontildeana ecosystem in recentdecades Thus we propose an initial target of 60pairs as a long-term restoration goal Elasticity analy-sis suggested that optimal management should focuson improving adult survival which had the largestimpact on population growth as in other long-livedspecies (Saether amp Bakke 2000 Whitfield et al 2004Kruumlger et al 2010) This could be attempted by in -creasing food availability especially of key prey suchas rabbits and by curtailing mortality threats such asillegal poisoning which still continues despite mucheffort to eradicate it by the local administration Thetelemetry program outlined above could help toidentify local perpetrators as occurred in other pop-ulations (Smart et al 2010 Tavecchia et al 2012) Onthe other hand despite their low elasticities repro-ductive rates are currently so low that it would befundamental to increase them eg by increasingfood availability and ensuring proper inundation ofthe marshes Based on Fig 5 we propose as initialtargets for restoration (1) survival rates equal orhigher than the European mean (adult survivalge087) and (2) a number of young fledged per territo-rial pair above 10 which would produce an increas-ing population provided that adult survival is equalto or above the European mean Note that Fig 5could be applied to any European population as atool to check its potential viability Given the highlythreatened status of red kites the speciesrsquo limitedrange confined to Europe and its ongoing declinesviability assessments such as ours may sadly becomemore important for the management and recovery ofmany populations
In conclusion red kites would probably be extinctin southern Spain without the institution of a largenational park In this sense this example well illus-trates how protected areas will continue to be corner-stones of global conservation of threatened taxaHowever their safety is not ensured by park institu-tion per se and performance monitoring and focusedaction will be needed to avoid potential extinctiondebts which may be more protracted than previouslyappreciated In our exemplary case despite the pres-ence of a large national park on prime fertile landwithin a developed country with adequate institu-tional and financial support a key threatened speciessuffered latent but steady declines for decadesobscured by problems of perception lack and frag-
mentation of information and likely caused by acomplex array of within-park threats and growingexternal pressures Viability maintenance and recov-ery will probably require concerted actions withinand outside of the park but only after detailed infor-mation on crucial aspects becomes available whichis probably the most urgent current priority We sus-pect that dynamics like the ones illustrated here aremore common than currently appreciated and willbecome more widespread as anthropogenic pres-sures increase around protected areas and as theirperformance monitoring becomes more prevalent
Acknowledgements We thank all the (too many to mention)researchers field workers visitors volunteers gamekeep-ers park managers and wardens that have provided datasince the 1960s In particular we thank F G Vilches L Gar-ciacutea and the Equipo de Seguimiento de Procesos Naturales ofthe Estacioacuten Bioloacutegica de Dontildeana-CSIC for help in the fieldSpecial thanks to F G Vilches for the priceless help with thecollation and organization of historical information Wethank J P Castellano I Redondo and all the lsquoArea de Con-servacioacutenrsquo of Dontildeana National Park for constant interest andsupport We thank R Cadenas J Madrid R Arenas J RBenitez and all the pertinent personnel of the Consejeriacutea deMedio Ambiente of the Junta de Andaluciacutea for informationon current nest locations in the Sierra de Huelva and fortheir constant attentive support We are grateful to Dr NBunnefeld and 2 anonymous reviewers for constructivecomments that improved the manuscript This study wasfunded by the Foundation Jaime Gonzaacutelez-Gordon and bythe research project 16022015 of the Spanish Ministry ofAgriculture Food and the Environment (National ParksAutonomous Agency)
LITERATURE CITED
Beissinger SR Ackerly DD Doremus H Machlis G (2017)Science conservation and national parks University ofChicago Press Chicago IL
Blanco G Cardells J Garijo-Toledo MM (2017) Supplemen-tary feeding and endoparasites in threatened avian scav-engers coprologic evidence from red kites in their win-tering stronghold Environ Res 155 22minus30
Brashares JS Arcese P Sam MK (2001) Human demographyand reserve size predict wildlife extinction in WestAfrica Proc Biol Sci 268 2473minus2478
Bustamante J (1993) Post-fledging dependence period anddevelopment of flight and hunting behaviour in the redkite Milvus milvus Bird Study 40 181minus188
Cano C Ayerza P Fernaacutendez J (2008) Poisoning in Spain(1990minus2005) analysis of the problem incidence andcauses WWFAdena Madrid (in Spanish)
Caswell H (2001) Matrix population models Sinauer Sun-derland MA
Ceballos JJ Guimeraacute VM (1992) Guiacutea de las aves de Jerez yde la Provincia de Caacutediz atlas ornitoloacutegico de lasespecies nidificantes Ayuntamiento de Jerez Jerez
Craigie ID Baillie JEM Balmford A Carbone C Collen BGreen RE Hutton JM (2010) Large mammal population
202
Sergio et al Predator extinction debt in national park
declines in Africarsquos protected areas Biol Conserv 143 2221minus2228
Czech B (2005) The capacity of the National WildlifeRefuge System to conserve threatened and endangeredanimal species in the United States Conserv Biol 19 1246minus1253
Delibes M Garciacutea L (1984) Haacutebitos alimenticios del milanoreal en Dontildeana durante el periodo de criacutea Ardeola 31 115minus121
Diacuteaz-Paniagua C Aragoneacutes D (2015) Permanent and tempo-rary ponds in Dontildeana National Park (SW Spain) arethreatened by desiccation Limnetica 34 407minus424
Evans IM Summers RW OrsquoToole L Orr-Ewing DC Snell NSmith J (1999) Evaluating the success of translocatingred kites Milvus milvus to the UK Bird Study 46 129minus144
Ferrer M Hiraldo F (1991) Evaluation of management tech-niques for the Spanish imperial eagle Wildl Soc Bull 19 436minus442
Garciacutea Novo F Mariacuten Cabrera C (2005) Dontildeana water andbiosphere Dontildeana 2005 Project Spanish Ministry of theEnvironment Madrid
Gaston KJ Jackson SF Cantuacute-Salazar L Cruz-Pintildeoacuten G(2008) The ecological performance of protected areasAnnu Rev Ecol Evol Syst 39 93minus113
Godet L Devictor V Jiguet F (2007) Estimating relative pop-ulation size included within protected areas BiodiversConserv 16 2587minus2598
Goacutemara B Gonzaacutelez MJ Baos R Hiraldo F Abad E RiveraJ Jimeacutenez B (2008) Unexpected high PCB and total DDTlevels in the breeding population of red kite (Milvus mil-vus) from Dontildeana National Park south-western SpainEnviron Int 34 73minus78
Gonzaacutelez LM Margalida A Mantildeosa S Saacutenchez R and oth-ers (2007) Causes and spatio-temporal variations of non-natural mortality in the vulnerable Spanish imperialeagle Aquila adalberti during a recovery period Oryx41 495minus502
Hansen AJ DeFries R (2007) Ecological mechanisms linkingprotected areas to surrounding lands Ecol Appl 17 974minus988
Hernaacutendez FJ Donaacutezar JA Hiraldo F (2001) Evaluacioacuten deluso de venenos para el control de predadores en laComunidad Autoacutenoma Andaluza y su impacto en la con-servacioacuten de especies amenazadas de vertebrados Con-sejeria de Medio Ambiente and Estacioacuten Bioloacutegica deDontildeana Sevilla
IUCN (The World Conservation Union) (1994) Guidelines forprotected area management categories IUCN Gland
Knott J Newbery P Barov B (2009) Action plan for the redkite Milvus milvus in the European Union EuropeanCommission Brussels
Kruumlger O Gruumlnkorn T Struwe-Juhl B (2010) The return ofthe white-tailed eagle (Haliaeetus albicilla) to northernGermany modelling the past to predict the future BiolConserv 143 710minus721
Loacutepez V (1861) Cataacutelogo de las aves observadas enAndaluciacutea Madrid
Loacutepez G and others (2009) Management measures to controla feline leukemia virus outbreak in the endangered Iber-ian lynx Anim Conserv 12 173minus182
Margalida A Heredia R Razin M Hernaacutendez M (2008)Sources of variation in mortality of the bearded vultureGypaetus barbatus in Europe Bird Conserv Int 18 1minus10
Naughton-Treves L Holland MB Brandon K (2005) The roleof protected areas in conserving biodiversity and sustain-
ing local livelihoods Annu Rev Environ Resour 30 219minus252
Newton I (1979) Population ecology of raptors T amp AD PoyserBerkhamsted
Newton I Davis PE Davis JE (1989) Age of first breedingdispersal and survival of red kites Milvus milvus inWales Ibis 131 16minus21
Otero C Castieacuten E Senosiaiacuten R Portillo F (1978) Fauna deCazorla vertebrados Publicaciones del Ministerio deAgricultura Madrid
Parks SA Harcourt AH (2002) Reserve size local humandensity and mammalian extinctions in US protectedareas Conserv Biol 16 800minus808
R Development Core Team (2018) R a language and envi-ronment for statistical computing R Foundation for Sta-tistical Computing Vienna wwwr-projectorg
Saeligther BE Bakke Oslash (2000) Avian life history variation andcontribution of demographic traits to the populationgrowth rate Ecology 81 642minus653
Sanz-Aguilar A De Pablo F Donaacutezar JA (2015) Age-depen-dent survival of island vs mainland populations of twoavian scavengers delving into migration costs Oecolo-gia 179 405minus414
Schaub M (2012) Spatial distribution of wind turbines is cru-cial for the survival of red kite populations Biol Conserv155 111minus118
Schmidt G Saacutenchez Navarro R Hernaacutendez E Carmona JJFuentelsaz F Seiz R (2017) The state of water in Dontildeana an evaluation of the state of the water and of the ecosys-tems of the protected space WWFAdena Madrid
Scott JM Davis FW McGhie RG Wright RG Groves CEstes J (2001) Nature reserves Do they capture the fullrange of Americarsquos biological diversity Ecol Appl 11 999minus1007
Seoane J Vintildeuela J Diacuteaz-Delgado R Bustamante J (2003)The effects of land use and climate on red kite distribu-tion in the Iberian peninsula Biol Conserv 111 401minus414
Sergio F Blas J Feroro M Fernaacutendez N Donaacutezar JAHiraldo F (2005) Preservation of wide-ranging top pred-ators by site-protection black and red kites in DontildeanaNational Park Biol Conserv 125 11minus21
Sergio F Tanferna A Blas J Blanco G Hiraldo F (2019) Reli-able methods for identifying animal deaths in GPS- andsatellite-tracking data review testing and calibrationJ Appl Ecol 56562ndash572
Smart J Amar A Sim IMW Etheridge B Cameron DChristie G Wilson JD (2010) Illegal killing slows popula-tion recovery of a re-introduced raptor of high conserva-tion concern mdash the red kite Milvus milvus Biol Conserv143 1278minus1286
Tavecchia G Adrover J Muntildeoz Navarro A Pradel R (2012)Modelling mortality causes in longitudinal data in thepresence of tag loss application to raptor poisoning andelectrocution J Appl Ecol 49 297minus305
Tenan S Adrover J Muntildeoz Navarro A Sergio F TavecchiaG (2012) Demographic consequences of poison-relatedmortality in a threatened bird of prey PLOS ONE 7 e49187
Tilman D May RM Lehman CL Nowak MA (1994) Habitatdestruction and the extinction debt Nature 371 65minus66
Torres Esquivias JA Jordano P Leoacuten A (1981) Aves de presadiurnas de la provincia de Coacuterdoba Publicaciones CA yMP Coacuterdoba
Veiga JP Hiraldo F (1990) Food habits and the survival andgrowth of nestlings in two sympatric kites (Milvus milvus
203
Endang Species Res 38 189ndash204 2019
and Milvus migrans) Holarct Ecol 13 62minus71 Villafuerte R Vintildeuela J Blanco JC (1998) Extensive preda-
tor persecution caused by population crash in a gamespecies the case of red kites and rabbits in Spain BiolConserv 84 181minus188
Vintildeuela J (2004) Milano real Milvus milvus In Madrontildeo AGonzaacutelez C Atienza JC (eds) Libro rojo de las aves deEspantildea Direccioacuten General para la BiodiversidadminusSEOBirdLife Madrid p 120minus125
Vintildeuela J Villafuerte R (2003) Predators and rabbits (Oryc-tolagus cuniculus) in Spain a key conflict for Europeanraptor conservation In Thompson DBA Redpath SMFielding AH Marquiss M Galbraith CA (eds) Birds ofprey in a changing environment The Stationery OfficeEdinburgh p 511minus526
Vintildeuela J Martiacute R Ruiz A (eds) (1999) El milano real enEspantildea SEOBirdlife Madrid
Watson JEM Dudley N Segan DB Hockings M (2014) Theperformance and potential of protected areas Nature515 67minus73
Whitfield SM Bell KE Philippi T Sasa M and others (2007)Amphibian and reptile declines over 35 years at La SelvaCosta Rica Proc Natl Acad Sci USA 104 8352minus8356
Whitfield DP Fielding AH McLeod DRA Haworth PF(2004) Modelling the effects of persecution on the popu-lation dynamics of golden eagles in Scotland Biol Con-serv 119 319minus333
Zuur A Ieno EN Walker N Saveliev AA Smith GM (2009)Mixed effects models and extensions in ecology with RSpringer New York NY
204
Editorial responsibility Nils BunnefeldStirling UK
Submitted October 8 2018 Accepted January 28 2019Proofs received from author(s) April 7 2019
Sergio et al Predator extinction debt in national park
a protected area is usually accompanied by the auto-matic presumption that this will act as a source areawith limited anthropogenic impacts an assumptionthat is increasingly disproved (Hansen amp DeFries2007 Gaston et al 2008 Watson et al 2014) (3) Long-term assessments such as ours required the lengthy
collation of fragmented informationfrom a large number of sequentialfield workers and administrationseach of which had a very limited per-ception of the overall situation (4)Much monitoring was conducted inthe core areas of the park like theRBD where the species has alwaysbeen most abundant and relativelystable (eg Sergio et al 2005) con-fusing the perception of broaderdeclines (5) Finally large numbersof wintering migrants boost the pop-ulation in the winter and earlyspring often producing an optimisticimpression of apparent abundance
even in relatively expert members of the public or oflocal administrations as we frequently noted in pub-lic talks and private conversations
Overall the decline occurred at multiple levels redkites were originally widespread throughout south-ern Spain (Loacutepez 1861) but became progressively
199
2030405060708090
100110
Bree
ding
su
cces
sful
()
a breeding pairs successful pairs
202122232425262728
Clut
ch si
ze
b
25
35
45
55
65
75
85
1970-79 1980-89 1990-99 2000-09 2010-17
Hatc
hing
succ
ess
broo
d re
duct
ion
()
Decade
c Hatching successBrood reduction
03
06
09
12
15
18
21
1970-79 1980-89 1990-99 2000-09 2010-17
Youn
g fle
dged
Decade
d Young breeding pairYoung successful pair
Fig 6 Reproductive parameters of the red kite population of Dontildeana (a) percentage of pairs laying eggs (black dots n = 804)and successfully raising fledglings (white dots n = 1185) (b) mean clutch size (n = 469) (c) hatching success (percentage ofeggs that hatched black dots n = 353) and brood reduction (percentage of chicks that disappeared during the nestling periodwhite dots n = 240) (d) mean number of young fledged per territorial pair (black dots n = 1145) and per successful pair (white
dots n = 576)
0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75
Young fledgedsuccessful pairYoung fledgedbreeding pairYoung fledgedterritorial pair
Probability of successful breedingBrood reduction
Hatching successClutch size
Probability of laying
Deterioration ()
Breeding parameter
Fig 7 Percentage deterioration of breeding parameters of the red kite popu-lation of Dontildeana between the 1980s and the 2010s
Endang Species Res 38 189ndash204 2019
confined to the protected area of Dontildeana in recentdecades However the park did not confer automaticsafety and declines and range contraction also con-tinued within the protected area suggesting perva-sive pressures and range erosion at multiple spatialscales In particular almost one third of the Dontildeana
population was virtually eradicatedfrom the northern pinewoods of thebuffering Natural Park in 5 to 7 yrbetween the late 1980s and early1990s Several lines of evidence sug-gest that illegal poisoning was themain cause of this eradication (1) Sev-eral adults were found poisoned undertheir nest in those sectors and years(2) Large-scale poisoning campaignsof raptors were reported throughoutSpain in those exact same years asa consequence of huntersrsquo illegalattempts to control predator popula-tions to increase the rapidly deterio-rating numbers of small game (rabbitsand partridges Villafuerte et al 1998Vintildeuela amp Villafuerte 2003 Cano et al2008) In this sense the National Parksuffered much wider national-level
pressures (3) The northern sectors of the parkwhere the eradication took place included or wereclose to private small-game reserves and predatorcontrol was well known to occur in some of them (4)Finally the rapidity of the eradication of such a long-lived species (maximum longevity of 29 yr in Dontilde -ana) implied a causative agent that directly affectedadult mortality (Saether amp Bakke 2000) such as poi-soning The marked impact of poisoning on adult sur-vival and population growth are well recognized forthis species whose facultative scavenging habits andforaging method of meticulous low and slow quar-tering of the ground make it particularly sensitive tothis threat (Smart et al 2010 Tavecchia et al 2012Tenan et al 2012 Sanz-Aguilar et al 2015)
Spikes of rapid local eradication were superim-posed on more gradual but steady deterioration ofoffspring production Gradual and continuous ratherthan sudden degradation of performance suggestedthat poisoning was not the only threat in effect Inthis context several factors may have contributed togradually deteriorate ecological conditions for kitesin recent decades (1) Rabbit epidemics have causedprogressive declines in the availability of this keyprey (Vintildeuela amp Villafuerte 2003) (2) Lower preyavailability may have exacerbated competition withthe dense populations of other raptors with similardiets such as the ecologically similar and in creasingblack kite (3) Predation rates on adults and nestlingsmay have increased with the expansion of the popu-lations of potential predators such as eagle owls Bubobubo and goshawks Accipiter gentilis (4) Recentassessments have detected alarming levels of toxic
200
00
02
04
06
08
10
12
1980sndash1990s 1990sndash2000s 2000sndash2010s
Popu
latio
n gr
owth
rate
Period
Observed populationgrowth
Scenario 1 minimumEuropean survival
Scenario 2 meanEuropean survival
Scenario 3 maximumEuropean survival
Fig 8 Population growth of the Dontildeana red kite population during the past 4decades as predicted by matrix demographic models based on 3 scenarioswhich assumed that survival was equal to minimum mean or maximum sur-vival rates reported for other European populations (reviewed in Table 1)Predicted values are compared with observed declines from one decade to
the next
Fig 9 Population growth rate of red kites in relation to adultsurvival and breeding performance (mean number of youngfledged per territorial pair) based on a matrix populationmodel Note that the graph could be applied to any Euro-pean population The 3 points at the base of the graph repre-sent the minimum (black) mean (grey) and maximum (blue)survival published for European populations (reviewed in
Table 1)
Sergio et al Predator extinction debt in national park
chemicals in red kite eggs from Dontildeana (Goacutemara etal 2008) (5) Climate change and agricultural man-agement have lowered the water table with likelyimpacts on marsh inundation levels and aquatic prey(Garciacutea Novo amp Mariacuten Cabrera 2005 Diacuteaz-Paniaguaamp Aragoneacutes 2015 Schmidt et al 2017) (6) Conver-sion to intensive farmland in surrounding lands haseroded habitat and prey availability outside the pro-tected area which may have buffered kites fromperiods of low prey availability within the park (egduring droughts in the marshes) Some of the pat-terns of observed reproductive deterioration lendsupport to some of these impacts For exampledeclining clutch sizes and increasing rates of broodreduction suggest that food was not sufficient to sus-tain earlier reproductive levels while lowered hatch-ing success is often the result of chemical contamina-tion in raptors (review in Newton 1979) While eachof these threats will be quantitatively investigated indetail in the immediate future in the present contextthey illustrate the frequent and complex challengesfaced by (1) protected areas in maintaining biodiver-sity and viable populations of imperiled species and(2) conservation biologists in identifying causes ofdecline for subsequent management interventioneven in lsquoprivilegedrsquo sites such as reserves
Redistribution declining numbers and perform-ance had important repercussions for future viability(1) The population passed from producing gt100annual young to lt10minus20 which will make mainte-nance and recovery difficult (2) These young wereincreasingly produced in the core sectors of themarsh-ecotone within the National Park which prob-ably increased the dependence of the population onmarsh inundation in turn affected by problems oper-ating outside the park (Garciacutea Novo amp Mariacuten Cabrera2005 Diacuteaz-Paniagua amp Aragoneacutes 2015 Schmidt et al2017) (3) Steep declines in the percentage of suc-cessful pairs implied that future generations wereproduced by a progressively more restricted numberof pairs which will make the population more sub-ject to inbreeding and stochastic events For exam-ple in the last 3 yr all the annual young were pro-duced by 6 8 and 9 pairs respectively suggesting aneffective population size 4 to 9 times lower than theoverall abundance
Given all the above it is no surprise that demo-graphic models suggested a negative growth and apopulation incapable of self-sustenance In particu-lar the model that gave the best fit to past observeddeclines was the one based on minimum Europeansurvival estimates followed by the scenario based onmean European survival estimates Given the above-
mentioned threats declines and performance deteri-oration we would expect survival to be closer to min-imum than mean European levels as supported bythe observed fit to past and recent declines Theseresults have 2 main implications (1) If survival is aslow as we suspect demographic models predict vir-tual extinction within a few years demanding anurgent need for identification and management ofmortality threats as well as quantification of actualsurvival to refine predictions Note that virtual ex -tinction could be even earlier when taking intoaccount effective rather than total population sizeand a stochastic rather than deterministic populationmodel (2) Should actual survival be confirmed lowbut further declines not observed the populationwould be a sink sustained by external sources whichwould make it even more at risk from anthropogenicthreats outside the park and thus more challengingto manage (eg Hansen amp DeFries 2007 Blanco et al2017)
5 Conclusions and implications for conservation
The decades-long degradation that we depictedwas likely generated by a combination of factorsboth internal to the park (eg rabbit availabilitymarsh inundation rates predation and competitionwith other species) and external (eg illegal poi-soning contamination farmland intensification)Some of them will be amenable to managementand others less so but the first priority will be tofind rapid ways to identify the key factors thatdrive population growth so as to optimize conserva-tion action before it is too late For example focus-ing conservation lsquoblindlyrsquo on supplementary feedingcould be useless if the problem is chemical contam-ination The quickest way to obtain such informa-tion would be a satelliteGSM (Global System forMobile communication) tagging program that wouldallow to (1) obtain rapid estimates of health andsurvival for young and adults (eg Sergio et al2019) so as to recalibrate future projections andgoals (2) assess the relative contribution of mainmortality causes which is an essential first step inany recovery program (eg Gonzaacutelez et al 2007Margalida et al 2008 Smart et al 2010) and (3)identify the areas used by breeding and non-breed-ing individuals inside and outside of the park toassess their risk-exposure and intervene before orafter death (eg to prosecute perpetrators of illegalpoisoning or re trofit dangerous electricity pylons inareas of high use by kites)
201
Endang Species Res 38 189ndash204 2019
Until this information becomes available below welist some tentative figures and priorities for conserva-tion First of all restoring the current population toformer levels would undoubtedly be challenging andprobably unrealistic given the profound changesincurred by the wider Dontildeana ecosystem in recentdecades Thus we propose an initial target of 60pairs as a long-term restoration goal Elasticity analy-sis suggested that optimal management should focuson improving adult survival which had the largestimpact on population growth as in other long-livedspecies (Saether amp Bakke 2000 Whitfield et al 2004Kruumlger et al 2010) This could be attempted by in -creasing food availability especially of key prey suchas rabbits and by curtailing mortality threats such asillegal poisoning which still continues despite mucheffort to eradicate it by the local administration Thetelemetry program outlined above could help toidentify local perpetrators as occurred in other pop-ulations (Smart et al 2010 Tavecchia et al 2012) Onthe other hand despite their low elasticities repro-ductive rates are currently so low that it would befundamental to increase them eg by increasingfood availability and ensuring proper inundation ofthe marshes Based on Fig 5 we propose as initialtargets for restoration (1) survival rates equal orhigher than the European mean (adult survivalge087) and (2) a number of young fledged per territo-rial pair above 10 which would produce an increas-ing population provided that adult survival is equalto or above the European mean Note that Fig 5could be applied to any European population as atool to check its potential viability Given the highlythreatened status of red kites the speciesrsquo limitedrange confined to Europe and its ongoing declinesviability assessments such as ours may sadly becomemore important for the management and recovery ofmany populations
In conclusion red kites would probably be extinctin southern Spain without the institution of a largenational park In this sense this example well illus-trates how protected areas will continue to be corner-stones of global conservation of threatened taxaHowever their safety is not ensured by park institu-tion per se and performance monitoring and focusedaction will be needed to avoid potential extinctiondebts which may be more protracted than previouslyappreciated In our exemplary case despite the pres-ence of a large national park on prime fertile landwithin a developed country with adequate institu-tional and financial support a key threatened speciessuffered latent but steady declines for decadesobscured by problems of perception lack and frag-
mentation of information and likely caused by acomplex array of within-park threats and growingexternal pressures Viability maintenance and recov-ery will probably require concerted actions withinand outside of the park but only after detailed infor-mation on crucial aspects becomes available whichis probably the most urgent current priority We sus-pect that dynamics like the ones illustrated here aremore common than currently appreciated and willbecome more widespread as anthropogenic pres-sures increase around protected areas and as theirperformance monitoring becomes more prevalent
Acknowledgements We thank all the (too many to mention)researchers field workers visitors volunteers gamekeep-ers park managers and wardens that have provided datasince the 1960s In particular we thank F G Vilches L Gar-ciacutea and the Equipo de Seguimiento de Procesos Naturales ofthe Estacioacuten Bioloacutegica de Dontildeana-CSIC for help in the fieldSpecial thanks to F G Vilches for the priceless help with thecollation and organization of historical information Wethank J P Castellano I Redondo and all the lsquoArea de Con-servacioacutenrsquo of Dontildeana National Park for constant interest andsupport We thank R Cadenas J Madrid R Arenas J RBenitez and all the pertinent personnel of the Consejeriacutea deMedio Ambiente of the Junta de Andaluciacutea for informationon current nest locations in the Sierra de Huelva and fortheir constant attentive support We are grateful to Dr NBunnefeld and 2 anonymous reviewers for constructivecomments that improved the manuscript This study wasfunded by the Foundation Jaime Gonzaacutelez-Gordon and bythe research project 16022015 of the Spanish Ministry ofAgriculture Food and the Environment (National ParksAutonomous Agency)
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Blanco G Cardells J Garijo-Toledo MM (2017) Supplemen-tary feeding and endoparasites in threatened avian scav-engers coprologic evidence from red kites in their win-tering stronghold Environ Res 155 22minus30
Brashares JS Arcese P Sam MK (2001) Human demographyand reserve size predict wildlife extinction in WestAfrica Proc Biol Sci 268 2473minus2478
Bustamante J (1993) Post-fledging dependence period anddevelopment of flight and hunting behaviour in the redkite Milvus milvus Bird Study 40 181minus188
Cano C Ayerza P Fernaacutendez J (2008) Poisoning in Spain(1990minus2005) analysis of the problem incidence andcauses WWFAdena Madrid (in Spanish)
Caswell H (2001) Matrix population models Sinauer Sun-derland MA
Ceballos JJ Guimeraacute VM (1992) Guiacutea de las aves de Jerez yde la Provincia de Caacutediz atlas ornitoloacutegico de lasespecies nidificantes Ayuntamiento de Jerez Jerez
Craigie ID Baillie JEM Balmford A Carbone C Collen BGreen RE Hutton JM (2010) Large mammal population
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Sergio et al Predator extinction debt in national park
declines in Africarsquos protected areas Biol Conserv 143 2221minus2228
Czech B (2005) The capacity of the National WildlifeRefuge System to conserve threatened and endangeredanimal species in the United States Conserv Biol 19 1246minus1253
Delibes M Garciacutea L (1984) Haacutebitos alimenticios del milanoreal en Dontildeana durante el periodo de criacutea Ardeola 31 115minus121
Diacuteaz-Paniagua C Aragoneacutes D (2015) Permanent and tempo-rary ponds in Dontildeana National Park (SW Spain) arethreatened by desiccation Limnetica 34 407minus424
Evans IM Summers RW OrsquoToole L Orr-Ewing DC Snell NSmith J (1999) Evaluating the success of translocatingred kites Milvus milvus to the UK Bird Study 46 129minus144
Ferrer M Hiraldo F (1991) Evaluation of management tech-niques for the Spanish imperial eagle Wildl Soc Bull 19 436minus442
Garciacutea Novo F Mariacuten Cabrera C (2005) Dontildeana water andbiosphere Dontildeana 2005 Project Spanish Ministry of theEnvironment Madrid
Gaston KJ Jackson SF Cantuacute-Salazar L Cruz-Pintildeoacuten G(2008) The ecological performance of protected areasAnnu Rev Ecol Evol Syst 39 93minus113
Godet L Devictor V Jiguet F (2007) Estimating relative pop-ulation size included within protected areas BiodiversConserv 16 2587minus2598
Goacutemara B Gonzaacutelez MJ Baos R Hiraldo F Abad E RiveraJ Jimeacutenez B (2008) Unexpected high PCB and total DDTlevels in the breeding population of red kite (Milvus mil-vus) from Dontildeana National Park south-western SpainEnviron Int 34 73minus78
Gonzaacutelez LM Margalida A Mantildeosa S Saacutenchez R and oth-ers (2007) Causes and spatio-temporal variations of non-natural mortality in the vulnerable Spanish imperialeagle Aquila adalberti during a recovery period Oryx41 495minus502
Hansen AJ DeFries R (2007) Ecological mechanisms linkingprotected areas to surrounding lands Ecol Appl 17 974minus988
Hernaacutendez FJ Donaacutezar JA Hiraldo F (2001) Evaluacioacuten deluso de venenos para el control de predadores en laComunidad Autoacutenoma Andaluza y su impacto en la con-servacioacuten de especies amenazadas de vertebrados Con-sejeria de Medio Ambiente and Estacioacuten Bioloacutegica deDontildeana Sevilla
IUCN (The World Conservation Union) (1994) Guidelines forprotected area management categories IUCN Gland
Knott J Newbery P Barov B (2009) Action plan for the redkite Milvus milvus in the European Union EuropeanCommission Brussels
Kruumlger O Gruumlnkorn T Struwe-Juhl B (2010) The return ofthe white-tailed eagle (Haliaeetus albicilla) to northernGermany modelling the past to predict the future BiolConserv 143 710minus721
Loacutepez V (1861) Cataacutelogo de las aves observadas enAndaluciacutea Madrid
Loacutepez G and others (2009) Management measures to controla feline leukemia virus outbreak in the endangered Iber-ian lynx Anim Conserv 12 173minus182
Margalida A Heredia R Razin M Hernaacutendez M (2008)Sources of variation in mortality of the bearded vultureGypaetus barbatus in Europe Bird Conserv Int 18 1minus10
Naughton-Treves L Holland MB Brandon K (2005) The roleof protected areas in conserving biodiversity and sustain-
ing local livelihoods Annu Rev Environ Resour 30 219minus252
Newton I (1979) Population ecology of raptors T amp AD PoyserBerkhamsted
Newton I Davis PE Davis JE (1989) Age of first breedingdispersal and survival of red kites Milvus milvus inWales Ibis 131 16minus21
Otero C Castieacuten E Senosiaiacuten R Portillo F (1978) Fauna deCazorla vertebrados Publicaciones del Ministerio deAgricultura Madrid
Parks SA Harcourt AH (2002) Reserve size local humandensity and mammalian extinctions in US protectedareas Conserv Biol 16 800minus808
R Development Core Team (2018) R a language and envi-ronment for statistical computing R Foundation for Sta-tistical Computing Vienna wwwr-projectorg
Saeligther BE Bakke Oslash (2000) Avian life history variation andcontribution of demographic traits to the populationgrowth rate Ecology 81 642minus653
Sanz-Aguilar A De Pablo F Donaacutezar JA (2015) Age-depen-dent survival of island vs mainland populations of twoavian scavengers delving into migration costs Oecolo-gia 179 405minus414
Schaub M (2012) Spatial distribution of wind turbines is cru-cial for the survival of red kite populations Biol Conserv155 111minus118
Schmidt G Saacutenchez Navarro R Hernaacutendez E Carmona JJFuentelsaz F Seiz R (2017) The state of water in Dontildeana an evaluation of the state of the water and of the ecosys-tems of the protected space WWFAdena Madrid
Scott JM Davis FW McGhie RG Wright RG Groves CEstes J (2001) Nature reserves Do they capture the fullrange of Americarsquos biological diversity Ecol Appl 11 999minus1007
Seoane J Vintildeuela J Diacuteaz-Delgado R Bustamante J (2003)The effects of land use and climate on red kite distribu-tion in the Iberian peninsula Biol Conserv 111 401minus414
Sergio F Blas J Feroro M Fernaacutendez N Donaacutezar JAHiraldo F (2005) Preservation of wide-ranging top pred-ators by site-protection black and red kites in DontildeanaNational Park Biol Conserv 125 11minus21
Sergio F Tanferna A Blas J Blanco G Hiraldo F (2019) Reli-able methods for identifying animal deaths in GPS- andsatellite-tracking data review testing and calibrationJ Appl Ecol 56562ndash572
Smart J Amar A Sim IMW Etheridge B Cameron DChristie G Wilson JD (2010) Illegal killing slows popula-tion recovery of a re-introduced raptor of high conserva-tion concern mdash the red kite Milvus milvus Biol Conserv143 1278minus1286
Tavecchia G Adrover J Muntildeoz Navarro A Pradel R (2012)Modelling mortality causes in longitudinal data in thepresence of tag loss application to raptor poisoning andelectrocution J Appl Ecol 49 297minus305
Tenan S Adrover J Muntildeoz Navarro A Sergio F TavecchiaG (2012) Demographic consequences of poison-relatedmortality in a threatened bird of prey PLOS ONE 7 e49187
Tilman D May RM Lehman CL Nowak MA (1994) Habitatdestruction and the extinction debt Nature 371 65minus66
Torres Esquivias JA Jordano P Leoacuten A (1981) Aves de presadiurnas de la provincia de Coacuterdoba Publicaciones CA yMP Coacuterdoba
Veiga JP Hiraldo F (1990) Food habits and the survival andgrowth of nestlings in two sympatric kites (Milvus milvus
203
Endang Species Res 38 189ndash204 2019
and Milvus migrans) Holarct Ecol 13 62minus71 Villafuerte R Vintildeuela J Blanco JC (1998) Extensive preda-
tor persecution caused by population crash in a gamespecies the case of red kites and rabbits in Spain BiolConserv 84 181minus188
Vintildeuela J (2004) Milano real Milvus milvus In Madrontildeo AGonzaacutelez C Atienza JC (eds) Libro rojo de las aves deEspantildea Direccioacuten General para la BiodiversidadminusSEOBirdLife Madrid p 120minus125
Vintildeuela J Villafuerte R (2003) Predators and rabbits (Oryc-tolagus cuniculus) in Spain a key conflict for Europeanraptor conservation In Thompson DBA Redpath SMFielding AH Marquiss M Galbraith CA (eds) Birds ofprey in a changing environment The Stationery OfficeEdinburgh p 511minus526
Vintildeuela J Martiacute R Ruiz A (eds) (1999) El milano real enEspantildea SEOBirdlife Madrid
Watson JEM Dudley N Segan DB Hockings M (2014) Theperformance and potential of protected areas Nature515 67minus73
Whitfield SM Bell KE Philippi T Sasa M and others (2007)Amphibian and reptile declines over 35 years at La SelvaCosta Rica Proc Natl Acad Sci USA 104 8352minus8356
Whitfield DP Fielding AH McLeod DRA Haworth PF(2004) Modelling the effects of persecution on the popu-lation dynamics of golden eagles in Scotland Biol Con-serv 119 319minus333
Zuur A Ieno EN Walker N Saveliev AA Smith GM (2009)Mixed effects models and extensions in ecology with RSpringer New York NY
204
Editorial responsibility Nils BunnefeldStirling UK
Submitted October 8 2018 Accepted January 28 2019Proofs received from author(s) April 7 2019
Endang Species Res 38 189ndash204 2019
confined to the protected area of Dontildeana in recentdecades However the park did not confer automaticsafety and declines and range contraction also con-tinued within the protected area suggesting perva-sive pressures and range erosion at multiple spatialscales In particular almost one third of the Dontildeana
population was virtually eradicatedfrom the northern pinewoods of thebuffering Natural Park in 5 to 7 yrbetween the late 1980s and early1990s Several lines of evidence sug-gest that illegal poisoning was themain cause of this eradication (1) Sev-eral adults were found poisoned undertheir nest in those sectors and years(2) Large-scale poisoning campaignsof raptors were reported throughoutSpain in those exact same years asa consequence of huntersrsquo illegalattempts to control predator popula-tions to increase the rapidly deterio-rating numbers of small game (rabbitsand partridges Villafuerte et al 1998Vintildeuela amp Villafuerte 2003 Cano et al2008) In this sense the National Parksuffered much wider national-level
pressures (3) The northern sectors of the parkwhere the eradication took place included or wereclose to private small-game reserves and predatorcontrol was well known to occur in some of them (4)Finally the rapidity of the eradication of such a long-lived species (maximum longevity of 29 yr in Dontilde -ana) implied a causative agent that directly affectedadult mortality (Saether amp Bakke 2000) such as poi-soning The marked impact of poisoning on adult sur-vival and population growth are well recognized forthis species whose facultative scavenging habits andforaging method of meticulous low and slow quar-tering of the ground make it particularly sensitive tothis threat (Smart et al 2010 Tavecchia et al 2012Tenan et al 2012 Sanz-Aguilar et al 2015)
Spikes of rapid local eradication were superim-posed on more gradual but steady deterioration ofoffspring production Gradual and continuous ratherthan sudden degradation of performance suggestedthat poisoning was not the only threat in effect Inthis context several factors may have contributed togradually deteriorate ecological conditions for kitesin recent decades (1) Rabbit epidemics have causedprogressive declines in the availability of this keyprey (Vintildeuela amp Villafuerte 2003) (2) Lower preyavailability may have exacerbated competition withthe dense populations of other raptors with similardiets such as the ecologically similar and in creasingblack kite (3) Predation rates on adults and nestlingsmay have increased with the expansion of the popu-lations of potential predators such as eagle owls Bubobubo and goshawks Accipiter gentilis (4) Recentassessments have detected alarming levels of toxic
200
00
02
04
06
08
10
12
1980sndash1990s 1990sndash2000s 2000sndash2010s
Popu
latio
n gr
owth
rate
Period
Observed populationgrowth
Scenario 1 minimumEuropean survival
Scenario 2 meanEuropean survival
Scenario 3 maximumEuropean survival
Fig 8 Population growth of the Dontildeana red kite population during the past 4decades as predicted by matrix demographic models based on 3 scenarioswhich assumed that survival was equal to minimum mean or maximum sur-vival rates reported for other European populations (reviewed in Table 1)Predicted values are compared with observed declines from one decade to
the next
Fig 9 Population growth rate of red kites in relation to adultsurvival and breeding performance (mean number of youngfledged per territorial pair) based on a matrix populationmodel Note that the graph could be applied to any Euro-pean population The 3 points at the base of the graph repre-sent the minimum (black) mean (grey) and maximum (blue)survival published for European populations (reviewed in
Table 1)
Sergio et al Predator extinction debt in national park
chemicals in red kite eggs from Dontildeana (Goacutemara etal 2008) (5) Climate change and agricultural man-agement have lowered the water table with likelyimpacts on marsh inundation levels and aquatic prey(Garciacutea Novo amp Mariacuten Cabrera 2005 Diacuteaz-Paniaguaamp Aragoneacutes 2015 Schmidt et al 2017) (6) Conver-sion to intensive farmland in surrounding lands haseroded habitat and prey availability outside the pro-tected area which may have buffered kites fromperiods of low prey availability within the park (egduring droughts in the marshes) Some of the pat-terns of observed reproductive deterioration lendsupport to some of these impacts For exampledeclining clutch sizes and increasing rates of broodreduction suggest that food was not sufficient to sus-tain earlier reproductive levels while lowered hatch-ing success is often the result of chemical contamina-tion in raptors (review in Newton 1979) While eachof these threats will be quantitatively investigated indetail in the immediate future in the present contextthey illustrate the frequent and complex challengesfaced by (1) protected areas in maintaining biodiver-sity and viable populations of imperiled species and(2) conservation biologists in identifying causes ofdecline for subsequent management interventioneven in lsquoprivilegedrsquo sites such as reserves
Redistribution declining numbers and perform-ance had important repercussions for future viability(1) The population passed from producing gt100annual young to lt10minus20 which will make mainte-nance and recovery difficult (2) These young wereincreasingly produced in the core sectors of themarsh-ecotone within the National Park which prob-ably increased the dependence of the population onmarsh inundation in turn affected by problems oper-ating outside the park (Garciacutea Novo amp Mariacuten Cabrera2005 Diacuteaz-Paniagua amp Aragoneacutes 2015 Schmidt et al2017) (3) Steep declines in the percentage of suc-cessful pairs implied that future generations wereproduced by a progressively more restricted numberof pairs which will make the population more sub-ject to inbreeding and stochastic events For exam-ple in the last 3 yr all the annual young were pro-duced by 6 8 and 9 pairs respectively suggesting aneffective population size 4 to 9 times lower than theoverall abundance
Given all the above it is no surprise that demo-graphic models suggested a negative growth and apopulation incapable of self-sustenance In particu-lar the model that gave the best fit to past observeddeclines was the one based on minimum Europeansurvival estimates followed by the scenario based onmean European survival estimates Given the above-
mentioned threats declines and performance deteri-oration we would expect survival to be closer to min-imum than mean European levels as supported bythe observed fit to past and recent declines Theseresults have 2 main implications (1) If survival is aslow as we suspect demographic models predict vir-tual extinction within a few years demanding anurgent need for identification and management ofmortality threats as well as quantification of actualsurvival to refine predictions Note that virtual ex -tinction could be even earlier when taking intoaccount effective rather than total population sizeand a stochastic rather than deterministic populationmodel (2) Should actual survival be confirmed lowbut further declines not observed the populationwould be a sink sustained by external sources whichwould make it even more at risk from anthropogenicthreats outside the park and thus more challengingto manage (eg Hansen amp DeFries 2007 Blanco et al2017)
5 Conclusions and implications for conservation
The decades-long degradation that we depictedwas likely generated by a combination of factorsboth internal to the park (eg rabbit availabilitymarsh inundation rates predation and competitionwith other species) and external (eg illegal poi-soning contamination farmland intensification)Some of them will be amenable to managementand others less so but the first priority will be tofind rapid ways to identify the key factors thatdrive population growth so as to optimize conserva-tion action before it is too late For example focus-ing conservation lsquoblindlyrsquo on supplementary feedingcould be useless if the problem is chemical contam-ination The quickest way to obtain such informa-tion would be a satelliteGSM (Global System forMobile communication) tagging program that wouldallow to (1) obtain rapid estimates of health andsurvival for young and adults (eg Sergio et al2019) so as to recalibrate future projections andgoals (2) assess the relative contribution of mainmortality causes which is an essential first step inany recovery program (eg Gonzaacutelez et al 2007Margalida et al 2008 Smart et al 2010) and (3)identify the areas used by breeding and non-breed-ing individuals inside and outside of the park toassess their risk-exposure and intervene before orafter death (eg to prosecute perpetrators of illegalpoisoning or re trofit dangerous electricity pylons inareas of high use by kites)
201
Endang Species Res 38 189ndash204 2019
Until this information becomes available below welist some tentative figures and priorities for conserva-tion First of all restoring the current population toformer levels would undoubtedly be challenging andprobably unrealistic given the profound changesincurred by the wider Dontildeana ecosystem in recentdecades Thus we propose an initial target of 60pairs as a long-term restoration goal Elasticity analy-sis suggested that optimal management should focuson improving adult survival which had the largestimpact on population growth as in other long-livedspecies (Saether amp Bakke 2000 Whitfield et al 2004Kruumlger et al 2010) This could be attempted by in -creasing food availability especially of key prey suchas rabbits and by curtailing mortality threats such asillegal poisoning which still continues despite mucheffort to eradicate it by the local administration Thetelemetry program outlined above could help toidentify local perpetrators as occurred in other pop-ulations (Smart et al 2010 Tavecchia et al 2012) Onthe other hand despite their low elasticities repro-ductive rates are currently so low that it would befundamental to increase them eg by increasingfood availability and ensuring proper inundation ofthe marshes Based on Fig 5 we propose as initialtargets for restoration (1) survival rates equal orhigher than the European mean (adult survivalge087) and (2) a number of young fledged per territo-rial pair above 10 which would produce an increas-ing population provided that adult survival is equalto or above the European mean Note that Fig 5could be applied to any European population as atool to check its potential viability Given the highlythreatened status of red kites the speciesrsquo limitedrange confined to Europe and its ongoing declinesviability assessments such as ours may sadly becomemore important for the management and recovery ofmany populations
In conclusion red kites would probably be extinctin southern Spain without the institution of a largenational park In this sense this example well illus-trates how protected areas will continue to be corner-stones of global conservation of threatened taxaHowever their safety is not ensured by park institu-tion per se and performance monitoring and focusedaction will be needed to avoid potential extinctiondebts which may be more protracted than previouslyappreciated In our exemplary case despite the pres-ence of a large national park on prime fertile landwithin a developed country with adequate institu-tional and financial support a key threatened speciessuffered latent but steady declines for decadesobscured by problems of perception lack and frag-
mentation of information and likely caused by acomplex array of within-park threats and growingexternal pressures Viability maintenance and recov-ery will probably require concerted actions withinand outside of the park but only after detailed infor-mation on crucial aspects becomes available whichis probably the most urgent current priority We sus-pect that dynamics like the ones illustrated here aremore common than currently appreciated and willbecome more widespread as anthropogenic pres-sures increase around protected areas and as theirperformance monitoring becomes more prevalent
Acknowledgements We thank all the (too many to mention)researchers field workers visitors volunteers gamekeep-ers park managers and wardens that have provided datasince the 1960s In particular we thank F G Vilches L Gar-ciacutea and the Equipo de Seguimiento de Procesos Naturales ofthe Estacioacuten Bioloacutegica de Dontildeana-CSIC for help in the fieldSpecial thanks to F G Vilches for the priceless help with thecollation and organization of historical information Wethank J P Castellano I Redondo and all the lsquoArea de Con-servacioacutenrsquo of Dontildeana National Park for constant interest andsupport We thank R Cadenas J Madrid R Arenas J RBenitez and all the pertinent personnel of the Consejeriacutea deMedio Ambiente of the Junta de Andaluciacutea for informationon current nest locations in the Sierra de Huelva and fortheir constant attentive support We are grateful to Dr NBunnefeld and 2 anonymous reviewers for constructivecomments that improved the manuscript This study wasfunded by the Foundation Jaime Gonzaacutelez-Gordon and bythe research project 16022015 of the Spanish Ministry ofAgriculture Food and the Environment (National ParksAutonomous Agency)
LITERATURE CITED
Beissinger SR Ackerly DD Doremus H Machlis G (2017)Science conservation and national parks University ofChicago Press Chicago IL
Blanco G Cardells J Garijo-Toledo MM (2017) Supplemen-tary feeding and endoparasites in threatened avian scav-engers coprologic evidence from red kites in their win-tering stronghold Environ Res 155 22minus30
Brashares JS Arcese P Sam MK (2001) Human demographyand reserve size predict wildlife extinction in WestAfrica Proc Biol Sci 268 2473minus2478
Bustamante J (1993) Post-fledging dependence period anddevelopment of flight and hunting behaviour in the redkite Milvus milvus Bird Study 40 181minus188
Cano C Ayerza P Fernaacutendez J (2008) Poisoning in Spain(1990minus2005) analysis of the problem incidence andcauses WWFAdena Madrid (in Spanish)
Caswell H (2001) Matrix population models Sinauer Sun-derland MA
Ceballos JJ Guimeraacute VM (1992) Guiacutea de las aves de Jerez yde la Provincia de Caacutediz atlas ornitoloacutegico de lasespecies nidificantes Ayuntamiento de Jerez Jerez
Craigie ID Baillie JEM Balmford A Carbone C Collen BGreen RE Hutton JM (2010) Large mammal population
202
Sergio et al Predator extinction debt in national park
declines in Africarsquos protected areas Biol Conserv 143 2221minus2228
Czech B (2005) The capacity of the National WildlifeRefuge System to conserve threatened and endangeredanimal species in the United States Conserv Biol 19 1246minus1253
Delibes M Garciacutea L (1984) Haacutebitos alimenticios del milanoreal en Dontildeana durante el periodo de criacutea Ardeola 31 115minus121
Diacuteaz-Paniagua C Aragoneacutes D (2015) Permanent and tempo-rary ponds in Dontildeana National Park (SW Spain) arethreatened by desiccation Limnetica 34 407minus424
Evans IM Summers RW OrsquoToole L Orr-Ewing DC Snell NSmith J (1999) Evaluating the success of translocatingred kites Milvus milvus to the UK Bird Study 46 129minus144
Ferrer M Hiraldo F (1991) Evaluation of management tech-niques for the Spanish imperial eagle Wildl Soc Bull 19 436minus442
Garciacutea Novo F Mariacuten Cabrera C (2005) Dontildeana water andbiosphere Dontildeana 2005 Project Spanish Ministry of theEnvironment Madrid
Gaston KJ Jackson SF Cantuacute-Salazar L Cruz-Pintildeoacuten G(2008) The ecological performance of protected areasAnnu Rev Ecol Evol Syst 39 93minus113
Godet L Devictor V Jiguet F (2007) Estimating relative pop-ulation size included within protected areas BiodiversConserv 16 2587minus2598
Goacutemara B Gonzaacutelez MJ Baos R Hiraldo F Abad E RiveraJ Jimeacutenez B (2008) Unexpected high PCB and total DDTlevels in the breeding population of red kite (Milvus mil-vus) from Dontildeana National Park south-western SpainEnviron Int 34 73minus78
Gonzaacutelez LM Margalida A Mantildeosa S Saacutenchez R and oth-ers (2007) Causes and spatio-temporal variations of non-natural mortality in the vulnerable Spanish imperialeagle Aquila adalberti during a recovery period Oryx41 495minus502
Hansen AJ DeFries R (2007) Ecological mechanisms linkingprotected areas to surrounding lands Ecol Appl 17 974minus988
Hernaacutendez FJ Donaacutezar JA Hiraldo F (2001) Evaluacioacuten deluso de venenos para el control de predadores en laComunidad Autoacutenoma Andaluza y su impacto en la con-servacioacuten de especies amenazadas de vertebrados Con-sejeria de Medio Ambiente and Estacioacuten Bioloacutegica deDontildeana Sevilla
IUCN (The World Conservation Union) (1994) Guidelines forprotected area management categories IUCN Gland
Knott J Newbery P Barov B (2009) Action plan for the redkite Milvus milvus in the European Union EuropeanCommission Brussels
Kruumlger O Gruumlnkorn T Struwe-Juhl B (2010) The return ofthe white-tailed eagle (Haliaeetus albicilla) to northernGermany modelling the past to predict the future BiolConserv 143 710minus721
Loacutepez V (1861) Cataacutelogo de las aves observadas enAndaluciacutea Madrid
Loacutepez G and others (2009) Management measures to controla feline leukemia virus outbreak in the endangered Iber-ian lynx Anim Conserv 12 173minus182
Margalida A Heredia R Razin M Hernaacutendez M (2008)Sources of variation in mortality of the bearded vultureGypaetus barbatus in Europe Bird Conserv Int 18 1minus10
Naughton-Treves L Holland MB Brandon K (2005) The roleof protected areas in conserving biodiversity and sustain-
ing local livelihoods Annu Rev Environ Resour 30 219minus252
Newton I (1979) Population ecology of raptors T amp AD PoyserBerkhamsted
Newton I Davis PE Davis JE (1989) Age of first breedingdispersal and survival of red kites Milvus milvus inWales Ibis 131 16minus21
Otero C Castieacuten E Senosiaiacuten R Portillo F (1978) Fauna deCazorla vertebrados Publicaciones del Ministerio deAgricultura Madrid
Parks SA Harcourt AH (2002) Reserve size local humandensity and mammalian extinctions in US protectedareas Conserv Biol 16 800minus808
R Development Core Team (2018) R a language and envi-ronment for statistical computing R Foundation for Sta-tistical Computing Vienna wwwr-projectorg
Saeligther BE Bakke Oslash (2000) Avian life history variation andcontribution of demographic traits to the populationgrowth rate Ecology 81 642minus653
Sanz-Aguilar A De Pablo F Donaacutezar JA (2015) Age-depen-dent survival of island vs mainland populations of twoavian scavengers delving into migration costs Oecolo-gia 179 405minus414
Schaub M (2012) Spatial distribution of wind turbines is cru-cial for the survival of red kite populations Biol Conserv155 111minus118
Schmidt G Saacutenchez Navarro R Hernaacutendez E Carmona JJFuentelsaz F Seiz R (2017) The state of water in Dontildeana an evaluation of the state of the water and of the ecosys-tems of the protected space WWFAdena Madrid
Scott JM Davis FW McGhie RG Wright RG Groves CEstes J (2001) Nature reserves Do they capture the fullrange of Americarsquos biological diversity Ecol Appl 11 999minus1007
Seoane J Vintildeuela J Diacuteaz-Delgado R Bustamante J (2003)The effects of land use and climate on red kite distribu-tion in the Iberian peninsula Biol Conserv 111 401minus414
Sergio F Blas J Feroro M Fernaacutendez N Donaacutezar JAHiraldo F (2005) Preservation of wide-ranging top pred-ators by site-protection black and red kites in DontildeanaNational Park Biol Conserv 125 11minus21
Sergio F Tanferna A Blas J Blanco G Hiraldo F (2019) Reli-able methods for identifying animal deaths in GPS- andsatellite-tracking data review testing and calibrationJ Appl Ecol 56562ndash572
Smart J Amar A Sim IMW Etheridge B Cameron DChristie G Wilson JD (2010) Illegal killing slows popula-tion recovery of a re-introduced raptor of high conserva-tion concern mdash the red kite Milvus milvus Biol Conserv143 1278minus1286
Tavecchia G Adrover J Muntildeoz Navarro A Pradel R (2012)Modelling mortality causes in longitudinal data in thepresence of tag loss application to raptor poisoning andelectrocution J Appl Ecol 49 297minus305
Tenan S Adrover J Muntildeoz Navarro A Sergio F TavecchiaG (2012) Demographic consequences of poison-relatedmortality in a threatened bird of prey PLOS ONE 7 e49187
Tilman D May RM Lehman CL Nowak MA (1994) Habitatdestruction and the extinction debt Nature 371 65minus66
Torres Esquivias JA Jordano P Leoacuten A (1981) Aves de presadiurnas de la provincia de Coacuterdoba Publicaciones CA yMP Coacuterdoba
Veiga JP Hiraldo F (1990) Food habits and the survival andgrowth of nestlings in two sympatric kites (Milvus milvus
203
Endang Species Res 38 189ndash204 2019
and Milvus migrans) Holarct Ecol 13 62minus71 Villafuerte R Vintildeuela J Blanco JC (1998) Extensive preda-
tor persecution caused by population crash in a gamespecies the case of red kites and rabbits in Spain BiolConserv 84 181minus188
Vintildeuela J (2004) Milano real Milvus milvus In Madrontildeo AGonzaacutelez C Atienza JC (eds) Libro rojo de las aves deEspantildea Direccioacuten General para la BiodiversidadminusSEOBirdLife Madrid p 120minus125
Vintildeuela J Villafuerte R (2003) Predators and rabbits (Oryc-tolagus cuniculus) in Spain a key conflict for Europeanraptor conservation In Thompson DBA Redpath SMFielding AH Marquiss M Galbraith CA (eds) Birds ofprey in a changing environment The Stationery OfficeEdinburgh p 511minus526
Vintildeuela J Martiacute R Ruiz A (eds) (1999) El milano real enEspantildea SEOBirdlife Madrid
Watson JEM Dudley N Segan DB Hockings M (2014) Theperformance and potential of protected areas Nature515 67minus73
Whitfield SM Bell KE Philippi T Sasa M and others (2007)Amphibian and reptile declines over 35 years at La SelvaCosta Rica Proc Natl Acad Sci USA 104 8352minus8356
Whitfield DP Fielding AH McLeod DRA Haworth PF(2004) Modelling the effects of persecution on the popu-lation dynamics of golden eagles in Scotland Biol Con-serv 119 319minus333
Zuur A Ieno EN Walker N Saveliev AA Smith GM (2009)Mixed effects models and extensions in ecology with RSpringer New York NY
204
Editorial responsibility Nils BunnefeldStirling UK
Submitted October 8 2018 Accepted January 28 2019Proofs received from author(s) April 7 2019
Sergio et al Predator extinction debt in national park
chemicals in red kite eggs from Dontildeana (Goacutemara etal 2008) (5) Climate change and agricultural man-agement have lowered the water table with likelyimpacts on marsh inundation levels and aquatic prey(Garciacutea Novo amp Mariacuten Cabrera 2005 Diacuteaz-Paniaguaamp Aragoneacutes 2015 Schmidt et al 2017) (6) Conver-sion to intensive farmland in surrounding lands haseroded habitat and prey availability outside the pro-tected area which may have buffered kites fromperiods of low prey availability within the park (egduring droughts in the marshes) Some of the pat-terns of observed reproductive deterioration lendsupport to some of these impacts For exampledeclining clutch sizes and increasing rates of broodreduction suggest that food was not sufficient to sus-tain earlier reproductive levels while lowered hatch-ing success is often the result of chemical contamina-tion in raptors (review in Newton 1979) While eachof these threats will be quantitatively investigated indetail in the immediate future in the present contextthey illustrate the frequent and complex challengesfaced by (1) protected areas in maintaining biodiver-sity and viable populations of imperiled species and(2) conservation biologists in identifying causes ofdecline for subsequent management interventioneven in lsquoprivilegedrsquo sites such as reserves
Redistribution declining numbers and perform-ance had important repercussions for future viability(1) The population passed from producing gt100annual young to lt10minus20 which will make mainte-nance and recovery difficult (2) These young wereincreasingly produced in the core sectors of themarsh-ecotone within the National Park which prob-ably increased the dependence of the population onmarsh inundation in turn affected by problems oper-ating outside the park (Garciacutea Novo amp Mariacuten Cabrera2005 Diacuteaz-Paniagua amp Aragoneacutes 2015 Schmidt et al2017) (3) Steep declines in the percentage of suc-cessful pairs implied that future generations wereproduced by a progressively more restricted numberof pairs which will make the population more sub-ject to inbreeding and stochastic events For exam-ple in the last 3 yr all the annual young were pro-duced by 6 8 and 9 pairs respectively suggesting aneffective population size 4 to 9 times lower than theoverall abundance
Given all the above it is no surprise that demo-graphic models suggested a negative growth and apopulation incapable of self-sustenance In particu-lar the model that gave the best fit to past observeddeclines was the one based on minimum Europeansurvival estimates followed by the scenario based onmean European survival estimates Given the above-
mentioned threats declines and performance deteri-oration we would expect survival to be closer to min-imum than mean European levels as supported bythe observed fit to past and recent declines Theseresults have 2 main implications (1) If survival is aslow as we suspect demographic models predict vir-tual extinction within a few years demanding anurgent need for identification and management ofmortality threats as well as quantification of actualsurvival to refine predictions Note that virtual ex -tinction could be even earlier when taking intoaccount effective rather than total population sizeand a stochastic rather than deterministic populationmodel (2) Should actual survival be confirmed lowbut further declines not observed the populationwould be a sink sustained by external sources whichwould make it even more at risk from anthropogenicthreats outside the park and thus more challengingto manage (eg Hansen amp DeFries 2007 Blanco et al2017)
5 Conclusions and implications for conservation
The decades-long degradation that we depictedwas likely generated by a combination of factorsboth internal to the park (eg rabbit availabilitymarsh inundation rates predation and competitionwith other species) and external (eg illegal poi-soning contamination farmland intensification)Some of them will be amenable to managementand others less so but the first priority will be tofind rapid ways to identify the key factors thatdrive population growth so as to optimize conserva-tion action before it is too late For example focus-ing conservation lsquoblindlyrsquo on supplementary feedingcould be useless if the problem is chemical contam-ination The quickest way to obtain such informa-tion would be a satelliteGSM (Global System forMobile communication) tagging program that wouldallow to (1) obtain rapid estimates of health andsurvival for young and adults (eg Sergio et al2019) so as to recalibrate future projections andgoals (2) assess the relative contribution of mainmortality causes which is an essential first step inany recovery program (eg Gonzaacutelez et al 2007Margalida et al 2008 Smart et al 2010) and (3)identify the areas used by breeding and non-breed-ing individuals inside and outside of the park toassess their risk-exposure and intervene before orafter death (eg to prosecute perpetrators of illegalpoisoning or re trofit dangerous electricity pylons inareas of high use by kites)
201
Endang Species Res 38 189ndash204 2019
Until this information becomes available below welist some tentative figures and priorities for conserva-tion First of all restoring the current population toformer levels would undoubtedly be challenging andprobably unrealistic given the profound changesincurred by the wider Dontildeana ecosystem in recentdecades Thus we propose an initial target of 60pairs as a long-term restoration goal Elasticity analy-sis suggested that optimal management should focuson improving adult survival which had the largestimpact on population growth as in other long-livedspecies (Saether amp Bakke 2000 Whitfield et al 2004Kruumlger et al 2010) This could be attempted by in -creasing food availability especially of key prey suchas rabbits and by curtailing mortality threats such asillegal poisoning which still continues despite mucheffort to eradicate it by the local administration Thetelemetry program outlined above could help toidentify local perpetrators as occurred in other pop-ulations (Smart et al 2010 Tavecchia et al 2012) Onthe other hand despite their low elasticities repro-ductive rates are currently so low that it would befundamental to increase them eg by increasingfood availability and ensuring proper inundation ofthe marshes Based on Fig 5 we propose as initialtargets for restoration (1) survival rates equal orhigher than the European mean (adult survivalge087) and (2) a number of young fledged per territo-rial pair above 10 which would produce an increas-ing population provided that adult survival is equalto or above the European mean Note that Fig 5could be applied to any European population as atool to check its potential viability Given the highlythreatened status of red kites the speciesrsquo limitedrange confined to Europe and its ongoing declinesviability assessments such as ours may sadly becomemore important for the management and recovery ofmany populations
In conclusion red kites would probably be extinctin southern Spain without the institution of a largenational park In this sense this example well illus-trates how protected areas will continue to be corner-stones of global conservation of threatened taxaHowever their safety is not ensured by park institu-tion per se and performance monitoring and focusedaction will be needed to avoid potential extinctiondebts which may be more protracted than previouslyappreciated In our exemplary case despite the pres-ence of a large national park on prime fertile landwithin a developed country with adequate institu-tional and financial support a key threatened speciessuffered latent but steady declines for decadesobscured by problems of perception lack and frag-
mentation of information and likely caused by acomplex array of within-park threats and growingexternal pressures Viability maintenance and recov-ery will probably require concerted actions withinand outside of the park but only after detailed infor-mation on crucial aspects becomes available whichis probably the most urgent current priority We sus-pect that dynamics like the ones illustrated here aremore common than currently appreciated and willbecome more widespread as anthropogenic pres-sures increase around protected areas and as theirperformance monitoring becomes more prevalent
Acknowledgements We thank all the (too many to mention)researchers field workers visitors volunteers gamekeep-ers park managers and wardens that have provided datasince the 1960s In particular we thank F G Vilches L Gar-ciacutea and the Equipo de Seguimiento de Procesos Naturales ofthe Estacioacuten Bioloacutegica de Dontildeana-CSIC for help in the fieldSpecial thanks to F G Vilches for the priceless help with thecollation and organization of historical information Wethank J P Castellano I Redondo and all the lsquoArea de Con-servacioacutenrsquo of Dontildeana National Park for constant interest andsupport We thank R Cadenas J Madrid R Arenas J RBenitez and all the pertinent personnel of the Consejeriacutea deMedio Ambiente of the Junta de Andaluciacutea for informationon current nest locations in the Sierra de Huelva and fortheir constant attentive support We are grateful to Dr NBunnefeld and 2 anonymous reviewers for constructivecomments that improved the manuscript This study wasfunded by the Foundation Jaime Gonzaacutelez-Gordon and bythe research project 16022015 of the Spanish Ministry ofAgriculture Food and the Environment (National ParksAutonomous Agency)
LITERATURE CITED
Beissinger SR Ackerly DD Doremus H Machlis G (2017)Science conservation and national parks University ofChicago Press Chicago IL
Blanco G Cardells J Garijo-Toledo MM (2017) Supplemen-tary feeding and endoparasites in threatened avian scav-engers coprologic evidence from red kites in their win-tering stronghold Environ Res 155 22minus30
Brashares JS Arcese P Sam MK (2001) Human demographyand reserve size predict wildlife extinction in WestAfrica Proc Biol Sci 268 2473minus2478
Bustamante J (1993) Post-fledging dependence period anddevelopment of flight and hunting behaviour in the redkite Milvus milvus Bird Study 40 181minus188
Cano C Ayerza P Fernaacutendez J (2008) Poisoning in Spain(1990minus2005) analysis of the problem incidence andcauses WWFAdena Madrid (in Spanish)
Caswell H (2001) Matrix population models Sinauer Sun-derland MA
Ceballos JJ Guimeraacute VM (1992) Guiacutea de las aves de Jerez yde la Provincia de Caacutediz atlas ornitoloacutegico de lasespecies nidificantes Ayuntamiento de Jerez Jerez
Craigie ID Baillie JEM Balmford A Carbone C Collen BGreen RE Hutton JM (2010) Large mammal population
202
Sergio et al Predator extinction debt in national park
declines in Africarsquos protected areas Biol Conserv 143 2221minus2228
Czech B (2005) The capacity of the National WildlifeRefuge System to conserve threatened and endangeredanimal species in the United States Conserv Biol 19 1246minus1253
Delibes M Garciacutea L (1984) Haacutebitos alimenticios del milanoreal en Dontildeana durante el periodo de criacutea Ardeola 31 115minus121
Diacuteaz-Paniagua C Aragoneacutes D (2015) Permanent and tempo-rary ponds in Dontildeana National Park (SW Spain) arethreatened by desiccation Limnetica 34 407minus424
Evans IM Summers RW OrsquoToole L Orr-Ewing DC Snell NSmith J (1999) Evaluating the success of translocatingred kites Milvus milvus to the UK Bird Study 46 129minus144
Ferrer M Hiraldo F (1991) Evaluation of management tech-niques for the Spanish imperial eagle Wildl Soc Bull 19 436minus442
Garciacutea Novo F Mariacuten Cabrera C (2005) Dontildeana water andbiosphere Dontildeana 2005 Project Spanish Ministry of theEnvironment Madrid
Gaston KJ Jackson SF Cantuacute-Salazar L Cruz-Pintildeoacuten G(2008) The ecological performance of protected areasAnnu Rev Ecol Evol Syst 39 93minus113
Godet L Devictor V Jiguet F (2007) Estimating relative pop-ulation size included within protected areas BiodiversConserv 16 2587minus2598
Goacutemara B Gonzaacutelez MJ Baos R Hiraldo F Abad E RiveraJ Jimeacutenez B (2008) Unexpected high PCB and total DDTlevels in the breeding population of red kite (Milvus mil-vus) from Dontildeana National Park south-western SpainEnviron Int 34 73minus78
Gonzaacutelez LM Margalida A Mantildeosa S Saacutenchez R and oth-ers (2007) Causes and spatio-temporal variations of non-natural mortality in the vulnerable Spanish imperialeagle Aquila adalberti during a recovery period Oryx41 495minus502
Hansen AJ DeFries R (2007) Ecological mechanisms linkingprotected areas to surrounding lands Ecol Appl 17 974minus988
Hernaacutendez FJ Donaacutezar JA Hiraldo F (2001) Evaluacioacuten deluso de venenos para el control de predadores en laComunidad Autoacutenoma Andaluza y su impacto en la con-servacioacuten de especies amenazadas de vertebrados Con-sejeria de Medio Ambiente and Estacioacuten Bioloacutegica deDontildeana Sevilla
IUCN (The World Conservation Union) (1994) Guidelines forprotected area management categories IUCN Gland
Knott J Newbery P Barov B (2009) Action plan for the redkite Milvus milvus in the European Union EuropeanCommission Brussels
Kruumlger O Gruumlnkorn T Struwe-Juhl B (2010) The return ofthe white-tailed eagle (Haliaeetus albicilla) to northernGermany modelling the past to predict the future BiolConserv 143 710minus721
Loacutepez V (1861) Cataacutelogo de las aves observadas enAndaluciacutea Madrid
Loacutepez G and others (2009) Management measures to controla feline leukemia virus outbreak in the endangered Iber-ian lynx Anim Conserv 12 173minus182
Margalida A Heredia R Razin M Hernaacutendez M (2008)Sources of variation in mortality of the bearded vultureGypaetus barbatus in Europe Bird Conserv Int 18 1minus10
Naughton-Treves L Holland MB Brandon K (2005) The roleof protected areas in conserving biodiversity and sustain-
ing local livelihoods Annu Rev Environ Resour 30 219minus252
Newton I (1979) Population ecology of raptors T amp AD PoyserBerkhamsted
Newton I Davis PE Davis JE (1989) Age of first breedingdispersal and survival of red kites Milvus milvus inWales Ibis 131 16minus21
Otero C Castieacuten E Senosiaiacuten R Portillo F (1978) Fauna deCazorla vertebrados Publicaciones del Ministerio deAgricultura Madrid
Parks SA Harcourt AH (2002) Reserve size local humandensity and mammalian extinctions in US protectedareas Conserv Biol 16 800minus808
R Development Core Team (2018) R a language and envi-ronment for statistical computing R Foundation for Sta-tistical Computing Vienna wwwr-projectorg
Saeligther BE Bakke Oslash (2000) Avian life history variation andcontribution of demographic traits to the populationgrowth rate Ecology 81 642minus653
Sanz-Aguilar A De Pablo F Donaacutezar JA (2015) Age-depen-dent survival of island vs mainland populations of twoavian scavengers delving into migration costs Oecolo-gia 179 405minus414
Schaub M (2012) Spatial distribution of wind turbines is cru-cial for the survival of red kite populations Biol Conserv155 111minus118
Schmidt G Saacutenchez Navarro R Hernaacutendez E Carmona JJFuentelsaz F Seiz R (2017) The state of water in Dontildeana an evaluation of the state of the water and of the ecosys-tems of the protected space WWFAdena Madrid
Scott JM Davis FW McGhie RG Wright RG Groves CEstes J (2001) Nature reserves Do they capture the fullrange of Americarsquos biological diversity Ecol Appl 11 999minus1007
Seoane J Vintildeuela J Diacuteaz-Delgado R Bustamante J (2003)The effects of land use and climate on red kite distribu-tion in the Iberian peninsula Biol Conserv 111 401minus414
Sergio F Blas J Feroro M Fernaacutendez N Donaacutezar JAHiraldo F (2005) Preservation of wide-ranging top pred-ators by site-protection black and red kites in DontildeanaNational Park Biol Conserv 125 11minus21
Sergio F Tanferna A Blas J Blanco G Hiraldo F (2019) Reli-able methods for identifying animal deaths in GPS- andsatellite-tracking data review testing and calibrationJ Appl Ecol 56562ndash572
Smart J Amar A Sim IMW Etheridge B Cameron DChristie G Wilson JD (2010) Illegal killing slows popula-tion recovery of a re-introduced raptor of high conserva-tion concern mdash the red kite Milvus milvus Biol Conserv143 1278minus1286
Tavecchia G Adrover J Muntildeoz Navarro A Pradel R (2012)Modelling mortality causes in longitudinal data in thepresence of tag loss application to raptor poisoning andelectrocution J Appl Ecol 49 297minus305
Tenan S Adrover J Muntildeoz Navarro A Sergio F TavecchiaG (2012) Demographic consequences of poison-relatedmortality in a threatened bird of prey PLOS ONE 7 e49187
Tilman D May RM Lehman CL Nowak MA (1994) Habitatdestruction and the extinction debt Nature 371 65minus66
Torres Esquivias JA Jordano P Leoacuten A (1981) Aves de presadiurnas de la provincia de Coacuterdoba Publicaciones CA yMP Coacuterdoba
Veiga JP Hiraldo F (1990) Food habits and the survival andgrowth of nestlings in two sympatric kites (Milvus milvus
203
Endang Species Res 38 189ndash204 2019
and Milvus migrans) Holarct Ecol 13 62minus71 Villafuerte R Vintildeuela J Blanco JC (1998) Extensive preda-
tor persecution caused by population crash in a gamespecies the case of red kites and rabbits in Spain BiolConserv 84 181minus188
Vintildeuela J (2004) Milano real Milvus milvus In Madrontildeo AGonzaacutelez C Atienza JC (eds) Libro rojo de las aves deEspantildea Direccioacuten General para la BiodiversidadminusSEOBirdLife Madrid p 120minus125
Vintildeuela J Villafuerte R (2003) Predators and rabbits (Oryc-tolagus cuniculus) in Spain a key conflict for Europeanraptor conservation In Thompson DBA Redpath SMFielding AH Marquiss M Galbraith CA (eds) Birds ofprey in a changing environment The Stationery OfficeEdinburgh p 511minus526
Vintildeuela J Martiacute R Ruiz A (eds) (1999) El milano real enEspantildea SEOBirdlife Madrid
Watson JEM Dudley N Segan DB Hockings M (2014) Theperformance and potential of protected areas Nature515 67minus73
Whitfield SM Bell KE Philippi T Sasa M and others (2007)Amphibian and reptile declines over 35 years at La SelvaCosta Rica Proc Natl Acad Sci USA 104 8352minus8356
Whitfield DP Fielding AH McLeod DRA Haworth PF(2004) Modelling the effects of persecution on the popu-lation dynamics of golden eagles in Scotland Biol Con-serv 119 319minus333
Zuur A Ieno EN Walker N Saveliev AA Smith GM (2009)Mixed effects models and extensions in ecology with RSpringer New York NY
204
Editorial responsibility Nils BunnefeldStirling UK
Submitted October 8 2018 Accepted January 28 2019Proofs received from author(s) April 7 2019
Endang Species Res 38 189ndash204 2019
Until this information becomes available below welist some tentative figures and priorities for conserva-tion First of all restoring the current population toformer levels would undoubtedly be challenging andprobably unrealistic given the profound changesincurred by the wider Dontildeana ecosystem in recentdecades Thus we propose an initial target of 60pairs as a long-term restoration goal Elasticity analy-sis suggested that optimal management should focuson improving adult survival which had the largestimpact on population growth as in other long-livedspecies (Saether amp Bakke 2000 Whitfield et al 2004Kruumlger et al 2010) This could be attempted by in -creasing food availability especially of key prey suchas rabbits and by curtailing mortality threats such asillegal poisoning which still continues despite mucheffort to eradicate it by the local administration Thetelemetry program outlined above could help toidentify local perpetrators as occurred in other pop-ulations (Smart et al 2010 Tavecchia et al 2012) Onthe other hand despite their low elasticities repro-ductive rates are currently so low that it would befundamental to increase them eg by increasingfood availability and ensuring proper inundation ofthe marshes Based on Fig 5 we propose as initialtargets for restoration (1) survival rates equal orhigher than the European mean (adult survivalge087) and (2) a number of young fledged per territo-rial pair above 10 which would produce an increas-ing population provided that adult survival is equalto or above the European mean Note that Fig 5could be applied to any European population as atool to check its potential viability Given the highlythreatened status of red kites the speciesrsquo limitedrange confined to Europe and its ongoing declinesviability assessments such as ours may sadly becomemore important for the management and recovery ofmany populations
In conclusion red kites would probably be extinctin southern Spain without the institution of a largenational park In this sense this example well illus-trates how protected areas will continue to be corner-stones of global conservation of threatened taxaHowever their safety is not ensured by park institu-tion per se and performance monitoring and focusedaction will be needed to avoid potential extinctiondebts which may be more protracted than previouslyappreciated In our exemplary case despite the pres-ence of a large national park on prime fertile landwithin a developed country with adequate institu-tional and financial support a key threatened speciessuffered latent but steady declines for decadesobscured by problems of perception lack and frag-
mentation of information and likely caused by acomplex array of within-park threats and growingexternal pressures Viability maintenance and recov-ery will probably require concerted actions withinand outside of the park but only after detailed infor-mation on crucial aspects becomes available whichis probably the most urgent current priority We sus-pect that dynamics like the ones illustrated here aremore common than currently appreciated and willbecome more widespread as anthropogenic pres-sures increase around protected areas and as theirperformance monitoring becomes more prevalent
Acknowledgements We thank all the (too many to mention)researchers field workers visitors volunteers gamekeep-ers park managers and wardens that have provided datasince the 1960s In particular we thank F G Vilches L Gar-ciacutea and the Equipo de Seguimiento de Procesos Naturales ofthe Estacioacuten Bioloacutegica de Dontildeana-CSIC for help in the fieldSpecial thanks to F G Vilches for the priceless help with thecollation and organization of historical information Wethank J P Castellano I Redondo and all the lsquoArea de Con-servacioacutenrsquo of Dontildeana National Park for constant interest andsupport We thank R Cadenas J Madrid R Arenas J RBenitez and all the pertinent personnel of the Consejeriacutea deMedio Ambiente of the Junta de Andaluciacutea for informationon current nest locations in the Sierra de Huelva and fortheir constant attentive support We are grateful to Dr NBunnefeld and 2 anonymous reviewers for constructivecomments that improved the manuscript This study wasfunded by the Foundation Jaime Gonzaacutelez-Gordon and bythe research project 16022015 of the Spanish Ministry ofAgriculture Food and the Environment (National ParksAutonomous Agency)
LITERATURE CITED
Beissinger SR Ackerly DD Doremus H Machlis G (2017)Science conservation and national parks University ofChicago Press Chicago IL
Blanco G Cardells J Garijo-Toledo MM (2017) Supplemen-tary feeding and endoparasites in threatened avian scav-engers coprologic evidence from red kites in their win-tering stronghold Environ Res 155 22minus30
Brashares JS Arcese P Sam MK (2001) Human demographyand reserve size predict wildlife extinction in WestAfrica Proc Biol Sci 268 2473minus2478
Bustamante J (1993) Post-fledging dependence period anddevelopment of flight and hunting behaviour in the redkite Milvus milvus Bird Study 40 181minus188
Cano C Ayerza P Fernaacutendez J (2008) Poisoning in Spain(1990minus2005) analysis of the problem incidence andcauses WWFAdena Madrid (in Spanish)
Caswell H (2001) Matrix population models Sinauer Sun-derland MA
Ceballos JJ Guimeraacute VM (1992) Guiacutea de las aves de Jerez yde la Provincia de Caacutediz atlas ornitoloacutegico de lasespecies nidificantes Ayuntamiento de Jerez Jerez
Craigie ID Baillie JEM Balmford A Carbone C Collen BGreen RE Hutton JM (2010) Large mammal population
202
Sergio et al Predator extinction debt in national park
declines in Africarsquos protected areas Biol Conserv 143 2221minus2228
Czech B (2005) The capacity of the National WildlifeRefuge System to conserve threatened and endangeredanimal species in the United States Conserv Biol 19 1246minus1253
Delibes M Garciacutea L (1984) Haacutebitos alimenticios del milanoreal en Dontildeana durante el periodo de criacutea Ardeola 31 115minus121
Diacuteaz-Paniagua C Aragoneacutes D (2015) Permanent and tempo-rary ponds in Dontildeana National Park (SW Spain) arethreatened by desiccation Limnetica 34 407minus424
Evans IM Summers RW OrsquoToole L Orr-Ewing DC Snell NSmith J (1999) Evaluating the success of translocatingred kites Milvus milvus to the UK Bird Study 46 129minus144
Ferrer M Hiraldo F (1991) Evaluation of management tech-niques for the Spanish imperial eagle Wildl Soc Bull 19 436minus442
Garciacutea Novo F Mariacuten Cabrera C (2005) Dontildeana water andbiosphere Dontildeana 2005 Project Spanish Ministry of theEnvironment Madrid
Gaston KJ Jackson SF Cantuacute-Salazar L Cruz-Pintildeoacuten G(2008) The ecological performance of protected areasAnnu Rev Ecol Evol Syst 39 93minus113
Godet L Devictor V Jiguet F (2007) Estimating relative pop-ulation size included within protected areas BiodiversConserv 16 2587minus2598
Goacutemara B Gonzaacutelez MJ Baos R Hiraldo F Abad E RiveraJ Jimeacutenez B (2008) Unexpected high PCB and total DDTlevels in the breeding population of red kite (Milvus mil-vus) from Dontildeana National Park south-western SpainEnviron Int 34 73minus78
Gonzaacutelez LM Margalida A Mantildeosa S Saacutenchez R and oth-ers (2007) Causes and spatio-temporal variations of non-natural mortality in the vulnerable Spanish imperialeagle Aquila adalberti during a recovery period Oryx41 495minus502
Hansen AJ DeFries R (2007) Ecological mechanisms linkingprotected areas to surrounding lands Ecol Appl 17 974minus988
Hernaacutendez FJ Donaacutezar JA Hiraldo F (2001) Evaluacioacuten deluso de venenos para el control de predadores en laComunidad Autoacutenoma Andaluza y su impacto en la con-servacioacuten de especies amenazadas de vertebrados Con-sejeria de Medio Ambiente and Estacioacuten Bioloacutegica deDontildeana Sevilla
IUCN (The World Conservation Union) (1994) Guidelines forprotected area management categories IUCN Gland
Knott J Newbery P Barov B (2009) Action plan for the redkite Milvus milvus in the European Union EuropeanCommission Brussels
Kruumlger O Gruumlnkorn T Struwe-Juhl B (2010) The return ofthe white-tailed eagle (Haliaeetus albicilla) to northernGermany modelling the past to predict the future BiolConserv 143 710minus721
Loacutepez V (1861) Cataacutelogo de las aves observadas enAndaluciacutea Madrid
Loacutepez G and others (2009) Management measures to controla feline leukemia virus outbreak in the endangered Iber-ian lynx Anim Conserv 12 173minus182
Margalida A Heredia R Razin M Hernaacutendez M (2008)Sources of variation in mortality of the bearded vultureGypaetus barbatus in Europe Bird Conserv Int 18 1minus10
Naughton-Treves L Holland MB Brandon K (2005) The roleof protected areas in conserving biodiversity and sustain-
ing local livelihoods Annu Rev Environ Resour 30 219minus252
Newton I (1979) Population ecology of raptors T amp AD PoyserBerkhamsted
Newton I Davis PE Davis JE (1989) Age of first breedingdispersal and survival of red kites Milvus milvus inWales Ibis 131 16minus21
Otero C Castieacuten E Senosiaiacuten R Portillo F (1978) Fauna deCazorla vertebrados Publicaciones del Ministerio deAgricultura Madrid
Parks SA Harcourt AH (2002) Reserve size local humandensity and mammalian extinctions in US protectedareas Conserv Biol 16 800minus808
R Development Core Team (2018) R a language and envi-ronment for statistical computing R Foundation for Sta-tistical Computing Vienna wwwr-projectorg
Saeligther BE Bakke Oslash (2000) Avian life history variation andcontribution of demographic traits to the populationgrowth rate Ecology 81 642minus653
Sanz-Aguilar A De Pablo F Donaacutezar JA (2015) Age-depen-dent survival of island vs mainland populations of twoavian scavengers delving into migration costs Oecolo-gia 179 405minus414
Schaub M (2012) Spatial distribution of wind turbines is cru-cial for the survival of red kite populations Biol Conserv155 111minus118
Schmidt G Saacutenchez Navarro R Hernaacutendez E Carmona JJFuentelsaz F Seiz R (2017) The state of water in Dontildeana an evaluation of the state of the water and of the ecosys-tems of the protected space WWFAdena Madrid
Scott JM Davis FW McGhie RG Wright RG Groves CEstes J (2001) Nature reserves Do they capture the fullrange of Americarsquos biological diversity Ecol Appl 11 999minus1007
Seoane J Vintildeuela J Diacuteaz-Delgado R Bustamante J (2003)The effects of land use and climate on red kite distribu-tion in the Iberian peninsula Biol Conserv 111 401minus414
Sergio F Blas J Feroro M Fernaacutendez N Donaacutezar JAHiraldo F (2005) Preservation of wide-ranging top pred-ators by site-protection black and red kites in DontildeanaNational Park Biol Conserv 125 11minus21
Sergio F Tanferna A Blas J Blanco G Hiraldo F (2019) Reli-able methods for identifying animal deaths in GPS- andsatellite-tracking data review testing and calibrationJ Appl Ecol 56562ndash572
Smart J Amar A Sim IMW Etheridge B Cameron DChristie G Wilson JD (2010) Illegal killing slows popula-tion recovery of a re-introduced raptor of high conserva-tion concern mdash the red kite Milvus milvus Biol Conserv143 1278minus1286
Tavecchia G Adrover J Muntildeoz Navarro A Pradel R (2012)Modelling mortality causes in longitudinal data in thepresence of tag loss application to raptor poisoning andelectrocution J Appl Ecol 49 297minus305
Tenan S Adrover J Muntildeoz Navarro A Sergio F TavecchiaG (2012) Demographic consequences of poison-relatedmortality in a threatened bird of prey PLOS ONE 7 e49187
Tilman D May RM Lehman CL Nowak MA (1994) Habitatdestruction and the extinction debt Nature 371 65minus66
Torres Esquivias JA Jordano P Leoacuten A (1981) Aves de presadiurnas de la provincia de Coacuterdoba Publicaciones CA yMP Coacuterdoba
Veiga JP Hiraldo F (1990) Food habits and the survival andgrowth of nestlings in two sympatric kites (Milvus milvus
203
Endang Species Res 38 189ndash204 2019
and Milvus migrans) Holarct Ecol 13 62minus71 Villafuerte R Vintildeuela J Blanco JC (1998) Extensive preda-
tor persecution caused by population crash in a gamespecies the case of red kites and rabbits in Spain BiolConserv 84 181minus188
Vintildeuela J (2004) Milano real Milvus milvus In Madrontildeo AGonzaacutelez C Atienza JC (eds) Libro rojo de las aves deEspantildea Direccioacuten General para la BiodiversidadminusSEOBirdLife Madrid p 120minus125
Vintildeuela J Villafuerte R (2003) Predators and rabbits (Oryc-tolagus cuniculus) in Spain a key conflict for Europeanraptor conservation In Thompson DBA Redpath SMFielding AH Marquiss M Galbraith CA (eds) Birds ofprey in a changing environment The Stationery OfficeEdinburgh p 511minus526
Vintildeuela J Martiacute R Ruiz A (eds) (1999) El milano real enEspantildea SEOBirdlife Madrid
Watson JEM Dudley N Segan DB Hockings M (2014) Theperformance and potential of protected areas Nature515 67minus73
Whitfield SM Bell KE Philippi T Sasa M and others (2007)Amphibian and reptile declines over 35 years at La SelvaCosta Rica Proc Natl Acad Sci USA 104 8352minus8356
Whitfield DP Fielding AH McLeod DRA Haworth PF(2004) Modelling the effects of persecution on the popu-lation dynamics of golden eagles in Scotland Biol Con-serv 119 319minus333
Zuur A Ieno EN Walker N Saveliev AA Smith GM (2009)Mixed effects models and extensions in ecology with RSpringer New York NY
204
Editorial responsibility Nils BunnefeldStirling UK
Submitted October 8 2018 Accepted January 28 2019Proofs received from author(s) April 7 2019
Sergio et al Predator extinction debt in national park
declines in Africarsquos protected areas Biol Conserv 143 2221minus2228
Czech B (2005) The capacity of the National WildlifeRefuge System to conserve threatened and endangeredanimal species in the United States Conserv Biol 19 1246minus1253
Delibes M Garciacutea L (1984) Haacutebitos alimenticios del milanoreal en Dontildeana durante el periodo de criacutea Ardeola 31 115minus121
Diacuteaz-Paniagua C Aragoneacutes D (2015) Permanent and tempo-rary ponds in Dontildeana National Park (SW Spain) arethreatened by desiccation Limnetica 34 407minus424
Evans IM Summers RW OrsquoToole L Orr-Ewing DC Snell NSmith J (1999) Evaluating the success of translocatingred kites Milvus milvus to the UK Bird Study 46 129minus144
Ferrer M Hiraldo F (1991) Evaluation of management tech-niques for the Spanish imperial eagle Wildl Soc Bull 19 436minus442
Garciacutea Novo F Mariacuten Cabrera C (2005) Dontildeana water andbiosphere Dontildeana 2005 Project Spanish Ministry of theEnvironment Madrid
Gaston KJ Jackson SF Cantuacute-Salazar L Cruz-Pintildeoacuten G(2008) The ecological performance of protected areasAnnu Rev Ecol Evol Syst 39 93minus113
Godet L Devictor V Jiguet F (2007) Estimating relative pop-ulation size included within protected areas BiodiversConserv 16 2587minus2598
Goacutemara B Gonzaacutelez MJ Baos R Hiraldo F Abad E RiveraJ Jimeacutenez B (2008) Unexpected high PCB and total DDTlevels in the breeding population of red kite (Milvus mil-vus) from Dontildeana National Park south-western SpainEnviron Int 34 73minus78
Gonzaacutelez LM Margalida A Mantildeosa S Saacutenchez R and oth-ers (2007) Causes and spatio-temporal variations of non-natural mortality in the vulnerable Spanish imperialeagle Aquila adalberti during a recovery period Oryx41 495minus502
Hansen AJ DeFries R (2007) Ecological mechanisms linkingprotected areas to surrounding lands Ecol Appl 17 974minus988
Hernaacutendez FJ Donaacutezar JA Hiraldo F (2001) Evaluacioacuten deluso de venenos para el control de predadores en laComunidad Autoacutenoma Andaluza y su impacto en la con-servacioacuten de especies amenazadas de vertebrados Con-sejeria de Medio Ambiente and Estacioacuten Bioloacutegica deDontildeana Sevilla
IUCN (The World Conservation Union) (1994) Guidelines forprotected area management categories IUCN Gland
Knott J Newbery P Barov B (2009) Action plan for the redkite Milvus milvus in the European Union EuropeanCommission Brussels
Kruumlger O Gruumlnkorn T Struwe-Juhl B (2010) The return ofthe white-tailed eagle (Haliaeetus albicilla) to northernGermany modelling the past to predict the future BiolConserv 143 710minus721
Loacutepez V (1861) Cataacutelogo de las aves observadas enAndaluciacutea Madrid
Loacutepez G and others (2009) Management measures to controla feline leukemia virus outbreak in the endangered Iber-ian lynx Anim Conserv 12 173minus182
Margalida A Heredia R Razin M Hernaacutendez M (2008)Sources of variation in mortality of the bearded vultureGypaetus barbatus in Europe Bird Conserv Int 18 1minus10
Naughton-Treves L Holland MB Brandon K (2005) The roleof protected areas in conserving biodiversity and sustain-
ing local livelihoods Annu Rev Environ Resour 30 219minus252
Newton I (1979) Population ecology of raptors T amp AD PoyserBerkhamsted
Newton I Davis PE Davis JE (1989) Age of first breedingdispersal and survival of red kites Milvus milvus inWales Ibis 131 16minus21
Otero C Castieacuten E Senosiaiacuten R Portillo F (1978) Fauna deCazorla vertebrados Publicaciones del Ministerio deAgricultura Madrid
Parks SA Harcourt AH (2002) Reserve size local humandensity and mammalian extinctions in US protectedareas Conserv Biol 16 800minus808
R Development Core Team (2018) R a language and envi-ronment for statistical computing R Foundation for Sta-tistical Computing Vienna wwwr-projectorg
Saeligther BE Bakke Oslash (2000) Avian life history variation andcontribution of demographic traits to the populationgrowth rate Ecology 81 642minus653
Sanz-Aguilar A De Pablo F Donaacutezar JA (2015) Age-depen-dent survival of island vs mainland populations of twoavian scavengers delving into migration costs Oecolo-gia 179 405minus414
Schaub M (2012) Spatial distribution of wind turbines is cru-cial for the survival of red kite populations Biol Conserv155 111minus118
Schmidt G Saacutenchez Navarro R Hernaacutendez E Carmona JJFuentelsaz F Seiz R (2017) The state of water in Dontildeana an evaluation of the state of the water and of the ecosys-tems of the protected space WWFAdena Madrid
Scott JM Davis FW McGhie RG Wright RG Groves CEstes J (2001) Nature reserves Do they capture the fullrange of Americarsquos biological diversity Ecol Appl 11 999minus1007
Seoane J Vintildeuela J Diacuteaz-Delgado R Bustamante J (2003)The effects of land use and climate on red kite distribu-tion in the Iberian peninsula Biol Conserv 111 401minus414
Sergio F Blas J Feroro M Fernaacutendez N Donaacutezar JAHiraldo F (2005) Preservation of wide-ranging top pred-ators by site-protection black and red kites in DontildeanaNational Park Biol Conserv 125 11minus21
Sergio F Tanferna A Blas J Blanco G Hiraldo F (2019) Reli-able methods for identifying animal deaths in GPS- andsatellite-tracking data review testing and calibrationJ Appl Ecol 56562ndash572
Smart J Amar A Sim IMW Etheridge B Cameron DChristie G Wilson JD (2010) Illegal killing slows popula-tion recovery of a re-introduced raptor of high conserva-tion concern mdash the red kite Milvus milvus Biol Conserv143 1278minus1286
Tavecchia G Adrover J Muntildeoz Navarro A Pradel R (2012)Modelling mortality causes in longitudinal data in thepresence of tag loss application to raptor poisoning andelectrocution J Appl Ecol 49 297minus305
Tenan S Adrover J Muntildeoz Navarro A Sergio F TavecchiaG (2012) Demographic consequences of poison-relatedmortality in a threatened bird of prey PLOS ONE 7 e49187
Tilman D May RM Lehman CL Nowak MA (1994) Habitatdestruction and the extinction debt Nature 371 65minus66
Torres Esquivias JA Jordano P Leoacuten A (1981) Aves de presadiurnas de la provincia de Coacuterdoba Publicaciones CA yMP Coacuterdoba
Veiga JP Hiraldo F (1990) Food habits and the survival andgrowth of nestlings in two sympatric kites (Milvus milvus
203
Endang Species Res 38 189ndash204 2019
and Milvus migrans) Holarct Ecol 13 62minus71 Villafuerte R Vintildeuela J Blanco JC (1998) Extensive preda-
tor persecution caused by population crash in a gamespecies the case of red kites and rabbits in Spain BiolConserv 84 181minus188
Vintildeuela J (2004) Milano real Milvus milvus In Madrontildeo AGonzaacutelez C Atienza JC (eds) Libro rojo de las aves deEspantildea Direccioacuten General para la BiodiversidadminusSEOBirdLife Madrid p 120minus125
Vintildeuela J Villafuerte R (2003) Predators and rabbits (Oryc-tolagus cuniculus) in Spain a key conflict for Europeanraptor conservation In Thompson DBA Redpath SMFielding AH Marquiss M Galbraith CA (eds) Birds ofprey in a changing environment The Stationery OfficeEdinburgh p 511minus526
Vintildeuela J Martiacute R Ruiz A (eds) (1999) El milano real enEspantildea SEOBirdlife Madrid
Watson JEM Dudley N Segan DB Hockings M (2014) Theperformance and potential of protected areas Nature515 67minus73
Whitfield SM Bell KE Philippi T Sasa M and others (2007)Amphibian and reptile declines over 35 years at La SelvaCosta Rica Proc Natl Acad Sci USA 104 8352minus8356
Whitfield DP Fielding AH McLeod DRA Haworth PF(2004) Modelling the effects of persecution on the popu-lation dynamics of golden eagles in Scotland Biol Con-serv 119 319minus333
Zuur A Ieno EN Walker N Saveliev AA Smith GM (2009)Mixed effects models and extensions in ecology with RSpringer New York NY
204
Editorial responsibility Nils BunnefeldStirling UK
Submitted October 8 2018 Accepted January 28 2019Proofs received from author(s) April 7 2019
Endang Species Res 38 189ndash204 2019
and Milvus migrans) Holarct Ecol 13 62minus71 Villafuerte R Vintildeuela J Blanco JC (1998) Extensive preda-
tor persecution caused by population crash in a gamespecies the case of red kites and rabbits in Spain BiolConserv 84 181minus188
Vintildeuela J (2004) Milano real Milvus milvus In Madrontildeo AGonzaacutelez C Atienza JC (eds) Libro rojo de las aves deEspantildea Direccioacuten General para la BiodiversidadminusSEOBirdLife Madrid p 120minus125
Vintildeuela J Villafuerte R (2003) Predators and rabbits (Oryc-tolagus cuniculus) in Spain a key conflict for Europeanraptor conservation In Thompson DBA Redpath SMFielding AH Marquiss M Galbraith CA (eds) Birds ofprey in a changing environment The Stationery OfficeEdinburgh p 511minus526
Vintildeuela J Martiacute R Ruiz A (eds) (1999) El milano real enEspantildea SEOBirdlife Madrid
Watson JEM Dudley N Segan DB Hockings M (2014) Theperformance and potential of protected areas Nature515 67minus73
Whitfield SM Bell KE Philippi T Sasa M and others (2007)Amphibian and reptile declines over 35 years at La SelvaCosta Rica Proc Natl Acad Sci USA 104 8352minus8356
Whitfield DP Fielding AH McLeod DRA Haworth PF(2004) Modelling the effects of persecution on the popu-lation dynamics of golden eagles in Scotland Biol Con-serv 119 319minus333
Zuur A Ieno EN Walker N Saveliev AA Smith GM (2009)Mixed effects models and extensions in ecology with RSpringer New York NY
204
Editorial responsibility Nils BunnefeldStirling UK
Submitted October 8 2018 Accepted January 28 2019Proofs received from author(s) April 7 2019