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Open Access

Peer-reviewed

Research Article

Who Are We Feeding? Asymmetric Individual Use of Surplus Food Resources in an Insular Population of the Endangered Egyptian Vulture Neophron percnopterus

  • Marie-Sophie García-Heras ,

    ms.garciaheras@gmail.com

    Affiliations Department of Conservation Biology, Estación Biológica de Doñana C.S.I.C., Sevilla, Spain, Percy FitzPatrick Institute of African Ornithology, DST/NRF Centre of Excellence, University of Cape Town, Rondebosch, South Africa

    ⨯
  • Ainara Cortés-Avizanda,

    Affiliations Department of Conservation Biology, Estación Biológica de Doñana C.S.I.C., Sevilla, Spain, Theoretical Ecology and Biodiversity Change Group, Centro de Biologia Ambiental, Faculdade de Ciências da Universidade de Lisboa, Lisbon, Portugal

    ⨯
  • José-Antonio Donázar

    Affiliation Department of Conservation Biology, Estación Biológica de Doñana C.S.I.C., Sevilla, Spain

    ⨯

Abstract

Supplementary feeding stations, or “vulture restaurants”, are common conservation management tools. While a number of studies have investigated the consequences of surplus food on the population dynamics of scavengers, relatively little is known about the effects of such practices at the individual level. Within the long-term monitored breeding population of Canarian Egyptian vultures (Neophron percnopterus majorensis) we investigated individual bird’s patterns of use of a supplementary feeding station at Fuerteventura (Canary Islands), over the course of breeding (2001, 2002; 2004-2011) and non-breeding seasons (2000-2010). Our results show that during the breeding season the individual use of the supplementary feeding station was inversely related to the distance to the breeding territory, which suggests the existence of central-place foraging constraints. In addition, larger birds of poor body-condition and individuals that ultimately failed to fledge young were detected more frequently at the feeding station. During the non-breeding season, and because most breeding birds abandoned the breeding territories, the overall abundance of Egyptian vultures at the feeding station grew. Moreover, the only variable increasing the probability of presence of individuals was poor body condition so that birds with lower wing residual visited the feeding station more frequently. Supplementary feeding may benefit individuals who would otherwise have been subject to selective pressures. From our results it follows that this conservation strategy must be used with caution because it can have consequences on an individual level and thus potentially affect the viability of endangered populations.

Citation: García-Heras M-S, Cortés-Avizanda A, Donázar J-A (2013) Who Are We Feeding? Asymmetric Individual Use of Surplus Food Resources in an Insular Population of the Endangered Egyptian Vulture Neophron percnopterus . PLoS ONE 8(11): e80523. https://doi.org/10.1371/journal.pone.0080523

Editor: Tapio Mappes, University of Jyväskylä, Finland

Received: March 8, 2013; Accepted: October 15, 2013; Published: November 11, 2013

Copyright: © 2013 GARCÍA-HERAS et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: This work was funded by the, Ministerio de Ciencia e Innovación Project CGL2009-12753-C02-02 and CGL2012-40013-C02-01. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

Competing interests: The authors have declared that no competing interests exist.

Introduction

Almost every area of an animal’s ecology, from individual behaviour, survival, or demography to population distribution, may be affected by changes in food availability [1-8]. The foraging activities of wild animals are shaped by the spatial distribution of trophic resources, which may be profoundly modified in space and time by human activities, inducing ecological consequences for populations [1,9-11]. To counteract these negative effects, supplementary feeding has become a widely used conservation tool to achieve rapid recovery of endangered taxa [5,7,12-16]. This is particularly true for threatened scavengers. The provision of surplus food at supplementary feeding stations (SFS), or so-called “vulture restaurants”, is a worldwide practice to facilitate the recovery of populations of these birds [9,17]. At those sites, food is provided to counter both the scarcity of natural food sources and illegal poisoning with the hope of improving demographic parameters and ultimately population viability [18].

The effects of supplementary feeding programs on populations have received considerable attention [9,16]. An increasing number of studies have reported that the SFS may increase breeding output, individual survival and territory persistence [16,19-21]. Conversely, supplementary feeding favors the aggregation of non-breeders (floaters), which have been demonstrated to induce negative density-dependent processes affecting reproductive success [22]. Moreover, the predictability inherent in the SFS favors dominant and abundant species that monopolize food to the detriment of other less competitive scavengers of higher conservation interest [9]. Finally, the effects of food predictability may permeate through other trophic levels even affecting primary consumers through predation risk derived from facultative predator-scavengers that concentrate near SFS [23,24]. However, there is almost a total lack of knowledge on the effects that these practices may have at the individual level. Since populations are formed by individuals with different responses to similar environmental pressures, we could expect that the use of SFS would promote changes in selective pressures related to the use of trophic resources [4]. Thus, a deeper understanding of those responses is necessary in order to optimize the management of supplementary feeding to enhance the viability of threatened populations.

By becoming predictable in space, supplementary feeding may impose significant constraints from the point of view of foraging ecology and individual decisions. Many breeding birds exhibiting a central-place foraging behaviour, which leads them to exploit space differentially, depending on the time and energy expenditure involved in hauling prey to the nest [25]. Thus, only those individuals breeding in close vicinity to the feeding place would benefit from additional trophic contributions. Apart from this, it is well known that the individuals differ not only in relation to physical characteristics such as size and body condition, which in turn may determine the possibility of exploiting these surplus food resources where the degree of competition may be high (see e.g. 26), but also in personality traits (correlated behavioural tendencies forming syndromes) thus determining, the exploration-avoidance of the novel food resources [27,28].

Here we study the individual use of a supplementary feeding station by an insular Egyptian Vulture (Neophron percnopterus) population endemic to the Canary archipelago [29-31]. We took advantage of a long-term intensive monitoring program that has allowed the individual identification of 85% of the birds. Particularly, we test to what extent the presence at SFS of adult territorial vultures was determined by extrinsic (environmental) and/or intrinsic (individual) factors. Among the first group of variables, we paid special attention to the distance from the SFS to the breeding territory. Specifically and because of central-place foraging constraints we predict an inverse relationship between them. Within the second group of variables we looked particularly at the relationship between the use of the SFS and variables evaluating individual quality. We predict that parents in inferior condition may depend more heavily upon the supplementary food [4,5,32].

Materials and Methods

Ethics statement

The entire study was observational and did not require approval of the animal ethics committee. Visits to the feeding station were done within a research-monitoring program in collaboration with the Cabildo Insular of Fuerteventura which has the competences to regulate observation and research on wildlife and endangered species.

Focal species and study area

The Canarian Egyptian vulture (N. p. majorensis) is a sedentary and endemic threatened long-lived bird of prey having undergone a severe decline during the 20th century, leading to its classification as “critically endangered” [29-31,33-35]. Fuerteventura is the stronghold of the population, although some individuals are also present on Lanzarote Island and adjacent islets (Figure 1). Long-term intensive monitoring of this population began in 1998 when only 23 territories were occupied. The population has subsequently increased to 50 territories in 2011 (total population size N=200). Individuals were captured at the nest (fledglings) or by means of cannon-nets in the areas surrounding the SFS (i.e., immatures and adults). All were ringed with metal and plastic colour rings with alphanumeric codes permitting identification from a distance. During our study period (2000-2011) a total of 170 individuals were ringed. The number of occupied territories per year was variable: a total number of 56 different territories of Egyptian vultures were located during the study period; of these 50 had at least one ringed breeder. The annual number varied between 3 (2000) to 39 (2011) (see Figure 1 for the distribution of the breeding territories during the last year). A total of 102 breeding birds (45 males and 57 females) were monitored during the study period.

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Figure 1. Study area and active Egyptian vulture territories between 2000-2011.

Territories with both unringed and at least one ringed breeding adult are shown by white and black circles, respectively. The star denotes the position of the supplementary feeding station.

https://doi.org/10.1371/journal.pone.0080523.g001

A SFS was implemented in 1998 by local authorities as a management tool for the conservation of this endangered population. This site is supplied regularly with goat (Capra hircus) and pig (Sus scrofa var. dom.) carcasses (1-4 per week) and slaughterhouse remains (c. 200 kg per week). There, Egyptian vultures congregate in large numbers (up to 130 different individuals in a single day), especially during the non-breeding season, together with large numbers of other facultative scavenger species such as common buzzards (Buteo buteo) and common ravens (Corvux corax) [36]. Outside of the SFS, the Egyptian vultures consume randomly encountered carcasses, especially those of goats and small-sized vertebrates, mainly wild rabbits (Oryctolagus cuniculus) and birds [33,37].

Field procedures

The presence of territorial Egyptian vultures at the SFS was monitored during the breeding period (January-June) in 2001, 2002, and 2004-2011 (n=119 days, 5-23 days/year) and the non-breeding period (July-December) in 2000-2010 (n=210 days, 5-41 days/year).

Observations were concentrated on those days when food was supplied. All the observations were conducted under good weather conditions. The observer was in a hidden area 15m from the food, and the birds showed no reaction to this structure. Observations began when the food was deposited (usually around 9.00-10.00 a.m.) and finished at dusk. Plastic rings were read by means of telescopes (20-60X). 

Analytical procedures

Generalized linear mixed models (GLMM) [38] were fitted independently for data collected in both breeding and non-breeding seasons. We used a binomial distribution of errors and a logistic link function, testing for significance of each variable by using F tests. Instead of using a single figure representing the proportion of days that each individual was present, we modelled the response variable as the number of days present with the total number of observation days as a binomial denominator (see e.g. 39). By doing so, more relevance was given to proportions coming from larger sample sizes [40].

In the two trials of analyses we fitted ten explanatory variables. Three of them (1), individual (2), year and (3) territory, were fitted as random terms to avoid non-independence of data because of inter-annual variability. The following variables (4), distance (km) between the territory and the feeding station and (5) island (a two-level factor: Fuerteventura and Lanzarote), evaluated environmental features inherent to the breeding areas and their spatial position in relation to the SFS. Another three variables described intrinsic individual factors: (6) sex, (7) wing chord (cm between the carpal joint of the bent wing and the tip of the longest straightened primary [41,42]) and (8) body condition, estimated from wing residuals (linear regression between body mass and wing chord, taking into account the sex of each individual [31,43,44]). We also examined the relationship to (9) breeding success (presence or absence of fledglings in the nest). Finally (10) we considered the reproductive stage distinguishing between those observations carried out during courtship and incubation (“early” stage: January-April) and chick rearing (“late” stage: May-July). Modeling was performed using a forward stepwise procedure [9,45], with the SAS 9.2. program [38,46]. Macro GLIMMIX were automatically adjusts for over dispersion [38]. All tests were two tailed.

Results

Between 2000-2011, 45.3% and 77.5% of the territorial ringed Egyptian vultures (N=102) visited the SFS during the breeding and non-breeding seasons, respectively, with the rates being clearly higher during the non-reproductive period (Table 1). In addition, there were large variations between individuals (0-100%) in the rate of visits, females using the station slightly more than males.

BreedingNon-breeding
Early (Jan-Apr)Late (May-Jul)
Means.d.rangeNaMeans.d.rangeNaMeans.d.rangeNa
Males20.821.00-924111.820.40-893931.823.60-7534
Females25.721.10-815614.621.30-835438.125.20-10050
Means.d.rangeNaMeans.d.rangeNa
Total18.621.60-919736.024.60-10084

Table 1. Summary of the individual rates of visits (%) of territorial ringed Egyptian vultures, to the supplementary feeding station between 2000-2011.

anumber of territorial Egyptian vultures monitored
CSV
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Modelling procedures showed that during the breeding season the probability of presence of territorial vultures at the SFS was higher for those birds breeding at closer distances, of greater size (wing chord) and showing more negative values for body condition (wing-weight residuals) (Table 2). In addition, visits were more probable during the early stage of the reproductive cycle and for those birds that ultimately failed to fledge young. Finally, it was very remarkable that although the SFS was placed in Fuerteventura, vultures breeding on this island were globally less frequently detected than those holding territories in Lanzarote. During the non-breeding season the presence of birds at the feeding site was only related (inversely) to the wing-weight residual.

Season/EffectEstimateSEF-value(df)P
Breeding
Intercept-5.2041.412-3.69a (9)0.0050
Wing 0.0060.0035.22 (1,438)0.0228
Body condition-6.5882.5466.69 (1,438)0.0100
Distance-0.0230.0087.34 (1,438)0.0070
Islandb-0.9320.3019.58 (1,438)0.0021
Breeding successc 0.4050.1329.34 (1,438)0.0024
Staged 1.6050.26626.43 (1,438)<0.0001
Individuale 0.3010.105
Yeare 0.3520.102
Territorye 0.7780.258
Non-breeding
Intercept0.7590.2652.87a (10)0.0168
Body condition-3.9751.8964.39 (1,240)0.0373
Individuale0.8400.261
Yeare0.2630.122
Territorye1.0670.420

Table 2. Summary of the results from the GLMMs explaining the frequency of days on which the feeding station was visited by individual Egyptian vultures.

Number of visits to the feeding station/Number of controls (in days) was the response variable. Estimated effects, SE (standard error), F-values, df (degrees of freedom) and associated probabilities are shown for those variables significantly improving the fitting of the models.
at-test
Estimates correspond to: bFuerteventura Island; cBreeding failure; dEarly breeding stage; levels for Lanzarote Island, positive breeding success and late breeding stage were 0.
eRandom effect
CSV
Download CSV

Discussion

Our results suggest that variables related to the breeding site (distance to the feeding station, island) as well as those inherent to the individual (size, body condition) and its breeding success are related to the use of a supplementary feeding station during the breeding season. The location of the breeding territory may be determinant because in central-place foragers, the distance to the trophic resource and the breeding site implies costs associated with the time and energy devoted to displacements and food-carrying [25]. In fact, the Canarian Egyptian vulture is, as are many birds of prey, a single-prey loader (i.e., one prey item per food-trip, [47]) having to bring food back frequently to their nests to feed young [48,49]. Satellite radiotelemetry studies carried out in continental regions of Spain also show that trophic resources are obtained mostly within short ranges (up to 8 km) from the nest but occasionally breeding birds can visit places up to 30 km away (unpublished data). In our case, adult birds breeding up to 103 km away have been observed in the SFS, corresponding to a nest placed in the north of Lanzarote Island. These long-distance visits are likely linked to very poor food conditions in the habitually exploited home ranges [50]. The fact that birds holding territories in Lanzarote show, as a whole, higher probabilities of visiting the feeding station despite the long distance to travel instead again indicates that inter-island variability in food conditions are determinant and provides insights about how availability of trophic resources, among other factors, can shape movements between islands and ultimately meta-population dynamics [51].

Three other variables significantly related to the probability of presence were size, body condition, and breeding success. The two first variables indicate that individual quality may be decisive in relation to the exploitation of surplus food resources. Thus, large birds with higher competitive abilities [26] but of lower body-condition would be more prone to exploit these predictable resources where food should be shared with conspecifics and other social and aggressive species like common ravens and common buzzards [33]. In regards to the relationship to breeding success, this could be interpreted preliminarily as a consequence of breeding failure: those birds exempt from breeding tasks would visit the station more frequently but the fact that “breeding stage” fit significantly into the model and in an opposite way (higher estimates in early breeding periods) suggests that again this variable reflects that poor-quality birds are more likely to visit the feeding station. This result is also reinforced by the fact that during the late breeding periods, only 47.4% of the territorial birds visited the SFS vs. 77.3% during the early breeding periods.

What proximal factors are behind the relationship between the frequency of visits and breeding success? First, this could be related to individual and/or territory (home range) quality. Quality of breeders may be reflected in better body reserves, foraging skills or nest defense ability [52,53] whereas territory quality may be apparent in the quality, abundance and diversity of trophic resources, safe nest-sites and refuges, and distance to the nearest neighbor [32,42,54-58]. In our case, breeders of higher physiological quality and/or exploiting foraging habitats of better quality would be better able to find unpredictable food in the wild. As was stated above, Egyptian vultures exploit small and medium-sized vertebrate carcasses, which may provide indispensable elements to the diet, such as calcium [22,59-61]. These very arguments may explain why individuals of good body condition are less attached to the feeding station in the winter: they are probably more able to exploit high-quality resources without having to share them with conspecific and interspecific competitors.

The absence of breeding tasks is clearly behind the increase in the presence of adult vultures at the feeding station during the non-breeding season. The fact that the main wild prey of Egyptian vultures (carcasses of small vertebrates like young mammals, birds and reptiles [62]) is scarcer during the cold season may also be at play, driving the birds to exploit predictable resources. Apart from this, it cannot be ruled out that social factors also favor concentrations of birds during the non-breeding seasons. Thus, as has been demonstrated in other bird species, socialization may be an important pressure leading birds to join communal roosts during non-breeding seasons [30,63,64]. Virtually all the Egyptian vultures in our study area gather in a large (>100 individuals) roost [33].

Individual sex had no significant influence but it seems likely that during the breeding season females visited the supplementary feeding station slightly more frequently than males. Egyptian vultures show reversed sexual dimorphism see 29, which could lead to asymmetric foraging strategies and differential use of food resources [65]. Females dominate in contests for food (authors, unpublished data) and may obtain greater benefits from places supplied with large carcasses where many birds congregate. This is corroborated by the lower susceptibility of female Canarian Egyptian vultures to poisoning by lead ammunition; this suggests that they preferentially exploit large ungulate carcasses (found in predictable places) over the remains of small vertebrates [66].

To our knowledge, our paper represents the first attempt to examine how individuals of a long-lived scavenger species use surplus food provided for conservation purposes. Supplementary feeding makes the availability of carrion resources predictable (both in space and time), which is otherwise unpredictable in the wild, having consequences at both population and community levels, from passerines to seabirds and scavengers [19-24]. Here, we show how these predictable resources can be used asymmetrically by individual breeding vultures. The long-term population consequences of these facts are unknown. First, because of time and energy constraints, supplementary feeding stations may favor the settlement of breeding individuals within relatively short and medium distances, thus promoting spatial heterogeneity within the population leading to effects like territory shrinkage and productivity depression within the SFS radius of influence [22,67]. In fact, the Egyptian vulture breeding density is maximum in the central area of Fuerteventura Island (80% of the territories are less than 30 km away from the SFS), which may suggest that the SFS has determined local nest bunching. Second, feeding sites seem to be used preferentially by individuals with relatively low breeding performance and body condition. This kind of scenario is purposely promoted by game managers who seek to reduce natural herbivore mortality in order to improve hunting activities [68,69] but has been almost neglected within conservation strategies of threatened vertebrates subject to spatial subsides. The issue is not trivial because this kind of habitat manipulation may be benefiting a fraction of the population that otherwise would be subject to strong selective pressures [4]. Long-term effects of supplementary feeding, therefore, are not limited to the alteration of basic demographic parameters [5,6] but individual-scale qualitative changes can also occur with unknown population viability consequences.

Acknowledgments

We are particularly grateful to C. Díez Rivera, M. Mallo Leira and R. Agudo for the data collection and their help during fieldwork. M. de la Riva helped with GIS and B.Arroyo, M. Carrete, N. Selva and D. Serrano with the data analyses. R. Jovani and two anonymous reviewers much improved earlier versions of the manuscripts. The Cabildo Insular de Fuerteventura gave logistic support.

Author Contributions

Conceived and designed the experiments: MSGH ACA JAD. Performed the experiments: MSGH JAD. Analyzed the data: MSGH ACA JAD. Contributed reagents/materials/analysis tools: MSGH ACA JAD. Wrote the manuscript: MSGH ACA JAD.

References

  1. 1. Monsarrat S, Benhamou S, Sarrazin F, Bessa-Gomes C, Bouten W et al. (2013) How predictability of feeding patches affects home range and foraging habitat selection in avian social scavengers? PLOS ONE 8 (1): e53077. doi:https://doi.org/10.1371/journal.pone.0053077. PubMed: 23301024.
  2. 2. Boutin S (1990) Food supplementation experiments with terrestrial vertebrates: patterns, problems, and the future. Can J Zool 68: 203–220. doi:https://doi.org/10.1139/z90-031.
  3. 3. Marzluff J, Millspaugh JJ, Hurvitz P, Handcock MS (2004) Relating resources to a probabilistic measure of space use: forest fragments and Steller's Jays. Ecology 85: 1411-1427. doi:https://doi.org/10.1890/03-0114.
  4. 4. Blanco G (2006) Natural selection and the risk of artificial selection in the wild: nestling quality or quantity from supplementary feeding in the Spanish imperial eagle. Ardeola 53: 341-351.
  5. 5. Robb GN, Mcdonald RA, Chamberlain DE, Bearhop S (2008) Food for thought: supplementary feeding as a driver of ecological change in avian populations. Front Ecol Environ 6: 476–484. doi:https://doi.org/10.1890/060152.
  6. 6. Robb GN, Mcdonald RA, Chamberlain DE, Reynolds SJ, Harrison TJE et al. (2008) Winter feeding of birds increases productivity in the subsequent breeding season. Biol Lett 4: 220-223. doi:https://doi.org/10.1098/rsbl.2007.0622. PubMed: 18252663.
  7. 7. López-Bao JV, Palomares F, Rodríguez A, Delibes M (2010) Effects of food supplementation on home-range size, reproductive success, productivity and recruitment in a small population of Iberian lynx. Anim Conserv 13: 35-42. doi:https://doi.org/10.1111/j.1469-1795.2009.00300.x.
  8. 8. Harrison TJE, Smith JA, Martin GR, Chamberlain DE, Bearhop S et al. (2010) Does food supplementation really enhance productivity of breeding birds? Oecologia 164: 311-320. doi:https://doi.org/10.1007/s00442-010-1645-x. PubMed: 20473622.
  9. 9. Cortés-Avizanda A, Carrete M, Donázar JA (2010) Managing supplementary feeding for avian scavengers: Guidelines for optimal design using ecological criteria. Biol Conserv 143: 1707-1715. doi:https://doi.org/10.1016/j.biocon.2010.04.016.
  10. 10. Margalida A, Colomer MA, Sanuy D (2011) Can wild ungulate carcasses provide enough biomass to maintain avian scavenger populations? An empirical assessment using a bio-inspired computational model. PLOS ONE 6 (5): e20248. doi:https://doi.org/10.1371/journal.pone.0020248. PubMed: 21629647.
  11. 11. Margalida A, Colomer MA (2012) Modelling the effects of sanitary policies on European vulture conservation. Sci Rep 2: 753. PubMed: 23082243.
  12. 12. Newton I (1979) Population ecology of raptors. Berkhamsted: T. & A.D. Poyser. 399 p.
    • 13. Newton I (1991) Population limitation in birds of prey: a comparative approach. In: CM PerrinsJD LebretonTJM Hirons. Bird population studies. Oxf: Ornithol S: 3-21.
      • 14. Newton I (1992) Experiments on the limitation of bird numbers by territorial behaviour. Biol Rev 67: 129–173. doi:https://doi.org/10.1111/j.1469-185X.1992.tb01017.x.
      • 15. Newton I (1998) Population limitation in birds. London: Academic Press Limited. 597 p.
        • 16. González LM, Margalida A, Sánchez R, Oria J (2006) Supplementary feeding as an effective tool for improving breeding success in the Spanish imperial eagle (Aquila adalberti). Biol Conser 129: 477–486. doi:https://doi.org/10.1016/j.biocon.2005.11.014.
        • 17. Koenig R (2006) Vulture research soars as the scavenger’s numbers decline. Science 312: 1591-1592. doi:https://doi.org/10.1126/science.312.5780.1591. PubMed: 16778034.
        • 18. Piper SE (2006) Supplementary feeding programs: how necessary are they for the maintenance of numerous and healthy vulture populations? In: DC HoustonSE Piper. Proceedings of the international conference on conservation and management of vulture populations. Thessaloniki: Natural History Museum of Crete and WWF Greece. pp. 41-50.
          • 19. Oro D, Margalida A, Carrete M, Heredia R, Donázar JA (2008) Testing the Goodness of Supplementary Feeding to Enhance Population Viability in an Endangered Vulture. PLOS ONE 3(12): e4084. doi:https://doi.org/10.1371/journal.pone.0004084. PubMed: 19115009.
          • 20. Benítez JR, Cortés-Avizanda A, Ávila E, García R (2009) Effects of the creation of a vulture restaurant for the conservation of an Egyptian vulture Neophron percnopterus population en Andalucía (Southern Spain). In: JA DonázarA. MargalidaD. Campión. Munibe supplement 29, Vultures, feeding stations and sanitary legislation: a conflict and its consequences from the perspective of conservation biology. San Sebastián: Sociedad de Ciencias Aranzadi. pp. 276-283.
            • 21. Grande JM, Carrete M, Ceballos O, Tella JL, Donázar JA (2009) Relevance of vulture restaurants for the conservation of Egyptian vulture Neophron percnopterus in Spain. In: JA DonázarA. MaragalidaD. Campión. Munibe supplement 29, Vultures, feeding stations and sanitary legislation: a conflict and its consequences from the perspective of conservation biology. San Sebastián: Sociedad de Ciencias Aranzadi. pp. 254-267.
              • 22. Carrete M, Donázar JA, Margalida A (2006) Density-dependent productivity depression in Pyrenean Bearbed vulture: implication for conservation. Ecol Appl 16: 1674-1682. doi:https://doi.org/10.1890/1051-0761(2006)016[1674:DPDIPB]2.0.CO;2. PubMed: 17069362.
              • 23. Cortés-Avizanda A, Carrete M, Serrano D, Donázar JA (2009) Carcasses increase the probability of predation of ground-nesting birds: a caveat regarding the conservation value of vulture restaurants. Anim Conserv 12: 85-88. doi:https://doi.org/10.1111/j.1469-1795.2008.00231.x.
              • 24. Cortés-Avizanda A, Selva N, Carrete M, Donázar JA (2009) Effects of carrion resources on herbivore spatial distribution are mediated by facultative scavengers. Basic Appl Ecol 10: 265-272.
              • 25. Orians GH, Pearson NE (1979) On the theory of central place foraging. In: BJ HornGR StairsRD Mitchell. Analysis of Ecological Systems. Columbus: Ohio State University Press. pp. 155-177.
                • 26. Renison D, Boersma D, Martella MB (2002) Winning and losing: causes for variability in outcome of fights in male Magellanic penguins (Spheniscus magellanicus). Behav Ecol 13: 462-466. doi:https://doi.org/10.1093/beheco/13.4.462.
                • 27. Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Q Rev Biol 79: 241-277. doi:https://doi.org/10.1086/422893. PubMed: 15529965.
                • 28. Dingemanse NJ, Wright J, Kazem JN, Thomas DK, Hickling R et al. (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76: 1128-1138. doi:https://doi.org/10.1111/j.1365-2656.2007.01284.x. PubMed: 17922709.
                • 29. Donázar JA, Negro JJ, Palacios CJ, Gangoso L, Godoy JA et al. (2002) Description of a new subspecies of the Egyptian vulture (Accipitridae: Neophron percnopterus) from the Canary Islands. J Raptor Res 36: 17-23.
                • 30. Gangoso L (2006) Insularidad y conservación: el caso del alimoche (Neophron percnopterus) en Canarias. PhD-thesis. Universidad de Sevilla. 244 p.
                  • 31. Agudo R (2010) Conservation Genetics on Islands, a case of the Canarian Egyptian Vulture. PhD thesis Universidad Complutense: Madrid. 230 p.
                    • 32. Sergio F, Newton I (2003) Occupancy as a measure of territory quality. J Anim Ecol 72: 857–865. doi:https://doi.org/10.1046/j.1365-2656.2003.00758.x.
                    • 33. Donázar JA, Palacios CJ, Gangoso L, Ceballos O, González MJ et al. (2002) Conservation status and limiting factors in the endangered population of Egyptian vulture (Neophron percnopterus) in the Canary Islands. Biol Conserv 107: 89-97. doi:https://doi.org/10.1016/S0006-3207(02)00049-6.
                    • 34. Donázar JA (2004) Alimoche común Neophron percnopterus. In: A. MadroñoC. GonzálezJC Atienza. Libro Rojo de las Aves de España. Madrid: Dirección General para la Biodiversidad-SEO/BirdLife. pp. 129-131.
                      • 35. BirdLife International (2008) Neophron percnopterus. In: IUCN Red List of Threatened Species.
                      • 36. Donázar JA, Gangoso L, Forero MG, Juste J (2002) Presence, richness and exctinction of birds of prey in the Mediterranean and Macaronesian island. J Biogeogr 32: 1701-1713.
                      • 37. Gangoso L, Palacios CJ (2005) Ground nesting by Egyptian vultures (Neophron percnopterus) in the Canary Islands. J Raptor Res 39: 186-187.
                      • 38. Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS for Mixed Models, Second Edition. Cary, NC: SAS Institute Inc. 814 p.
                        • 39. Jovani R, Serrano D (2001) Feather mites (Astigmata) avoid moulting wing feathers of passerine birds. Anim Behav 62: 723-727. doi:https://doi.org/10.1006/anbe.2001.1814.
                        • 40. Crawley MJ (1993) GLIM for Ecologists. Oxford: Blackwell Scientific Publishing House. 379 p.
                          • 41. Mendelssohn JM, Kemp AC, Biggs HC, Biggs R, Brown CJ (1989) Wing areas, wing loadings and wing spans of 66 species of African raptors. Ostrich 60: 35-42. doi:https://doi.org/10.1080/00306525.1989.9634503.
                          • 42. Zając T, Solarz W, Bielański W (2008) Site-dependent population dynamics: the influence of spatial habitat heterogeneity on individual fitness in the sedge warbler Acrocephalus schoenobaenus. J Avian Biol 39: 206-214.
                          • 43. Green AJ (2001) Mass/length residuals: measures of body condition or generators of spurious results? Ecology 82: 1473–1483. doi:https://doi.org/10.1890/0012-9658(2001)082[1473:MLRMOB]2.0.CO;2.
                          • 44. Peig J, Green A (2010) The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Funct Ecol 24: 1323-1332. doi:https://doi.org/10.1111/j.1365-2435.2010.01751.x.
                          • 45. Donázar JA, Hiraldo F, Bustamante J (1993) Factors influencing nest site selection, breeding density and breeding success in the bearded vulture Gypaetus barbatus. J Appl Ecol 30: 500–514.
                          • 46. McCullagh P, Nelder JA (1989) Generalized Linear Models. London: Chapman and Hall. 532 pp.
                            • 47. Houston A, Mcnamara JM (1985) A general theory of central place foraging for single- prey loaders. Theor Popul Biol 28: 233-262. doi:https://doi.org/10.1016/0040-5809(85)90029-2.
                            • 48. Donázar JA, Ceballos O (1990) Post-Fledging dependence period and development of flight and foraging behaviour in the Egyptian Vulture Neophron percnopterus. Ardea 78: 387-394.
                            • 49. Donázar JA (1993) Los Buitres Ibéricos. Biología y Conservación. Madr J.M. Reyero: 256.
                            • 50. Marzluff JM, Kimsey BA, Schueck LS, McFadzen ME, Vekasy MS et al. (1997) The influence of habitat, prey abundance, sex, and breeding success on the ranging behavior of prairie falcons. Condor 99: 567-584. doi:https://doi.org/10.2307/1370470.
                            • 51. Margalida A, Carrete M, Hegglin D, Serrano D, Arenas R et al. (2013) Uneven large-scale movement patterns in wild and reintroduced pre-adult bearded vultures: conservation implications. PLOS ONE (. (2013)) PubMed: 23776559.
                            • 52. Coulson JC (1968) Differences in the quality of birds nesting in the centre and on the edge of a colony. Nature 217: 478-479. doi:https://doi.org/10.1038/217478a0.
                            • 53. Winkler DW, Allen PE (1996) The seasonal decline in Tree Swallow clutch size: physiological constraint or strategic adjustment? Ecology 77: 922-932. doi:https://doi.org/10.2307/2265512.
                            • 54. Rodenhouse NL, Sheery TW, Holmes RT (1997) Site dependent regulation of population size: a new synthesis. Ecology 78: 2025-2042. doi:https://doi.org/10.1890/0012-9658(1997)078[2025:SDROPS]2.0.CO;2.
                            • 55. Chamberlain DE, Fuller RJ (1999) Density-dependent habitat distribution in birds: issues of scale, habitat definition and habitat availability. J Avian Biol 30: 427-436.
                            • 56. Zając T, Bielański W, Solarz W (2011) Territory choice during the breeding tenure of male sedge. Behav Ecol Sociobiol 65: 2305-2317. doi:https://doi.org/10.1007/s00265-011-1241-z. PubMed: 22162903.
                            • 57. Margalida M, Benítez JR, Sánchez-Zapata JA, Ávila E, Arenas R et al. (2012) Long-term relationships between diet and breeding success in a declining population of Egyptian Vultures Neophron percnopterus. Ibis 154: 184-188. doi:https://doi.org/10.1111/j.1474-919X.2011.01189.x.
                            • 58. Whitfield DP, Reid R, Waworth PF, Madders M, Marquiss M et al. (2009) Diet specificity is not associated with increased productive performance of Golden Eagles Aquila chrysaetos in Western Scotland. Ibis 151: 255–264. doi:https://doi.org/10.1111/j.1474-919X.2009.00924.x.
                            • 59. Reynolds SJ, Mänd R, Tilgar V (2004) Calcium supplementation of breeding birds: directions for future research. Ibis 146: 601-614. doi:https://doi.org/10.1111/j.1474-919x.2004.00298.x.
                            • 60. Richardson PRK, Mundy PJ, Plug I (1986) Bone crushing carnivores and their significance to osteodystrophy in griffon vulture chicks. J Zool 210: 23–43.
                            • 61. Carrete M, Donázar JA (2005) Application of central-place foraging theory shows the importance of Mediterranean dehesas for the conservation of the Cinereous Vulture. Biol Conserv 126: 582-590. doi:https://doi.org/10.1016/j.biocon.2005.06.031.
                            • 62. Donázar JA, Cortés-Avizanda A, Carrete M (2010) Dietary shifts in two vultures after the demise of supplementary feeding stations: consequences of the EU sanitary legislation. Eur J Wildl Res 56: 613-621. doi:https://doi.org/10.1007/s10344-009-0358-0.
                            • 63. Carrete M, Grande JM, Tella JL, Sánchez-Zapata JA, Donázar JA et al. (2007) Habitat, human pressure, and social behavior: Partialling out factors affecting large-scale territory extinction in an endangered vulture. Biol Conserv 136: 143-154. doi:https://doi.org/10.1016/j.biocon.2006.11.025.
                            • 64. Deygout C, Gault A, Duriez O, Sarrazin F, Bessa-Gomes C (2010) Impact of food predictability on social facilitation by foraging scavengers. Behav Ecol 21: 1131-1139. doi:https://doi.org/10.1093/beheco/arq120.
                            • 65. Schaffer SA, Weimerskircht H, Costa DP (2001) Functional significance of sexual dimorphism in wandering albatrosses Diomedea exulans. Funct Ecol 15: 203-210. doi:https://doi.org/10.1046/j.1365-2435.2001.00514.x.
                            • 66. Gangoso L, Alvarez-LLoret P, Rodríguez-Navarro AA, Mateo R, Hiraldo F et al. (2009) Long-term effects of lead poisoning on bone mineralization in vultures exposed to ammunition sources. Environ Pollut 157: 569-574. doi:https://doi.org/10.1016/j.envpol.2008.09.015. PubMed: 18995938.
                            • 67. Margalida A, Donázar JA, Bustamante J, Hernández FJ, Romero-Pujante M (2008) Application of a predictive model to detect long-term changes in nest-site selection in the Bearded Vulture Gypaetus barbatus: conservation in relation to territory shrinkage. Ibis 150: 242-249.
                            • 68. Peterson C, Messmer TA (2007) Effects of winter-feeding on mule deer in Northern Utah. J Wildl Manage 71: 1440-1445. doi:https://doi.org/10.2193/2006-202.
                            • 69. Putman RJ, Staines BW (2004) Supplementary winter feeding of wild red deer Cervus elaphus in Europe and North America: justifications, feeding and effectiveness. Mamm Rev 34: 285–306. doi:https://doi.org/10.1111/j.1365-2907.2004.00044.x.