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Low heritability in tool use skills in a wild vulture population

Digital.CSIC. Repositorio Institucional del CSIC
  • Carrete, Martina
  • Centeno-Cuadros, A.
  • Méndez, María
  • Agudo, Rosa
  • Donázar, José A.
Tool use is widespread among animals and has been under intense study due to its prominence in human society and evolution. A lack of detailed genetic information for wild populations has perpetuated assumptions regarding associations between individual differences in tool use and cognition and learning processes. However, captive birds and mammals can use tools in the absence of opportunities for social learning, indicating a genetic basis. Here, we used animal models and relatedness analysis to disentangle the role played by genetics and learning in tool use in an insular population of a long-lived vulture, Neophron percnopterus. Our results show a low heritability in this behaviour, perhaps because of the low variability observed among birds. However, not all individuals used stones to break eggs, and those that did so behaved consistently. Importantly, there was no evidence of learning at the timescale considered. Our results suggest that repeatability in tool use within individuals may indicate a link with some personality traits, with strong evolutionary and ecological consequences., Projects CGL2004-00270/BOS, CGL2012-40013-C02-01, CGL2015-66966-C2-1-2-R from MINECO/FEDER EU and the Cabildo Insular de Fuerteventura funded this research.




Cosmetic coloration in Egyptian vultures: Mud bathing as a tool for social communication?

Digital.CSIC. Repositorio Institucional del CSIC
  • Overveld, Thijs van
  • Riva, Manuel de la
  • Donázar, José A.
It is well‐established that plumage colors are important for avian visual communication and are used to signal social information (Andersson 1994). Most plumage colors are static traits with a relatively fixed information content. Little is known about the ability of birds to modify the expression of plumage colors with exogenous materials after feather development, a phenomenon also known as avian cosmetics (Delhey et al. 2007). Whereas the use of secretions and feather powder are widespread, the use of external sources (mainly red soil) for cosmetics seem restricted to a few groups like cranes and ptarmigans and for camouflage purposes only (reviewed in Delhey et al. 2007). The deliberate staining of feathers in a social signaling context has so far only been described in the Bearded vulture (Gypaetus barbatus) (Negro et al. 1999), but the exact function of this behavior is still hypothetical because of the extreme rarity of field data. Hence, we were extremely excited to observe this feather painting behavior in another Old‐World scavenger, the Egyptian vulture (Neophron percnopterus)., Financial support was received by a Marie Curie Fellowship by TVO and to JD by project CGL2015‐66966‐C2‐1‐2‐R (Spanish Ministry of Economy and Competitiveness and EU/FEDER) and by the Canarian Government and Cabildo Insular de Fuerteventura.




Carnivore carcasses are avoided by carnivores

Digital.CSIC. Repositorio Institucional del CSIC
  • Moleón, Marcos
  • Martínez-Carrasco, Carlos
  • Muellerklein, Oliver C.
  • Getz, Wayne M.
  • Muñoz-Lozano, Carlos
  • Sánchez-Zapata, José A.
Ecologists have traditionally focused on herbivore carcasses as study models in scavenging research. However, some observations of scavengers avoiding feeding on carnivore carrion suggest that different types of carrion may lead to differential pressures. Untested assumptions about carrion produced at different trophic levels could therefore lead ecologists to overlook important evolutionary processes and their ecological consequences. Our general goal was to investigate the use of mammalian carnivore carrion by vertebrate scavengers. In particular, we aimed to test the hypothesis that carnivore carcasses are avoided by other carnivores, especially at the intraspecific level, most likely to reduce exposure to parasitism. We take a three-pronged approach to study this principle by: (i) providing data from field experiments, (ii) carrying out evolutionary simulations of carnivore scavenging strategies under risks of parasitic infection, and (iii) conducting a literature-review to test two predictions regarding parasite life-history strategies. First, our field experiments showed that the mean number of species observed feeding at carcasses and the percentage of consumed carrion biomass were substantially higher at herbivore carcasses than at carnivore carcasses. This occurred even though the number of scavenger species visiting carcasses and the time needed by scavengers to detect carcasses were similar between both types of carcasses. In addition, we did not observe cannibalism. Second, our evolutionary simulations demonstrated that a risk of parasite transmission leads to the evolution of scavengers with generally low cannibalistic tendencies, and that the emergence of cannibalism-avoidance behaviour depends strongly on assumptions about parasite-based mortality rates. Third, our literature review indicated that parasite species potentially able to follow a carnivore–carnivore indirect cycle, as well as those transmitted via meat consumption, are rare in our study system. Our findings support the existence of a novel coevolutionary relation between carnivores and their parasites, and suggest that carnivore and herbivore carcasses play very different roles in food webs and ecosystems., Dirección General del Medio Natural (Murcia Region), Sierra Espuña Regional Park and Sierras de Cazorla, Segura y Las Villas Natural Park provided with logistics, permissions and financial support. M.M. acknowledges financial support through the Severo Ochoa Program for Centres of Excellence in R+D+I (SEV‐2012‐0262) and by a research contract Ramón y Cajal from the MINECO (RYC‐2015‐19231). This study was partly funded by the Spanish Ministry of Economy and Competitiveness and EU ERDF funds through projects CGL2006‐10689/BOS, CGL2009‐12753‐C02‐02, CGL2012‐40013‐C02‐01/02 and CGL2015‐66966‐C2‐1‐2‐R. A. Kane and one anonymous reviewer improved the first version of the manuscript.




How to fit the distribution of apex scavengers into land-abandonment scenarios? The Cinereous vulture in the Mediterranean biome

Digital.CSIC. Repositorio Institucional del CSIC
  • García-Barón, Isabel
  • Cortés-Avizanda, Ainara
  • Verburg, Peter H.
  • Marques, Tiago A.
  • Moreno-Opo, Rubén
  • Pereira, Henrique M.
  • Donázar, José A.
[Aim] Farmland abandonment or “ecological rewilding” shapes species distribution and ecological process ultimately affecting the biodiversity and functionality of ecosystems. Land abandonment predictions based on alternative future socioeconomic scenarios allow foretell the future of biota in Europe. From here, we predict how these forecasts may affect large-scale distribution of the Cinereous vulture (Aegypius monachus), an apex scavenger closely linked to Mediterranean agro-grazing systems., [Location] Iberian Peninsula., [Methods] Firstly, we modelled nest-site and foraging habitat selection in relation to variables quantifying physiography, trophic resources and human disturbance. Secondly, we evaluate to what extent land abandonment may affect the life traits of the species and finally we determined how potential future distribution of the species would vary according to asymmetric socioeconomic land-abandonment predictions for year 2040., [Results] Cinereous vultures selected breeding areas with steep slopes and low human presence whereas foraging areas are characterized by high abundance of European rabbits (Oryctolagus cuniculus) and wild ungulates. Liberalization of the Common Agricultural Policy (CAP) could potentially transform positively 66% of the current nesting habitat, favouring the recovery of mature forest. Contrarily, land abandonment would negatively affect the 63% of the current foraging habitat reducing the availability of preferred food resources (wild European rabbit). On the other hand, the maintenance of the CAP would determine lower frequencies (24%–22%) of nesting and foraging habitat change., [Main conclusions] Land abandonment may result into opposite effects on the focal species because of the increase in nesting habitats and wild ungulates populations and, on the other hand, lower availability of open areas with poorer densities of European rabbits. Land-abandonment models’ scenarios are still coarse-grained; the apparition of new human uses in natural areas may take place at small-sized and medium-sized scales, ultimately adding complexity to the prediction on the future of biota and ecosystems., I.G.‐B. was supported by a Pre‐Doctoral contract from the Spanish Ministry of Economy and Competitiveness (BES‐2014‐070597). A.CA. was supported by a contract Juan de la Cierva Incorporación (IJCI‐2014‐20744; Spanish Ministry of Economy and Competitiveness, Spain) and a PostDoc contract Programa Viçent Mut of Govern Balear, Spain (PD/039/2017). This work was partially funded by projects RNM‐1925 (Consejería de Innovación, Ciencia y Empleo, Junta de Andalucía) and CGL2015‐66966‐C2‐1‐2‐R MINECO/FEDER EU and the Severo Ochoa Excellence Award from the Spanish Ministry of Economy and Competitiveness (SEV‐2012‐0262). T.A.M. thanks partial support by CEAUL (funded by FCT—Fundação para a Ciência e a Tecnologia, Portugal, through the project UID/MAT/00006/2013).




Rewilding traditional grazing areas affects scavenger assemblages and carcass consumption patterns

Digital.CSIC. Repositorio Institucional del CSIC
  • Arrondo, Eneko
  • Morales-Reyes, Zebensui
  • Moleón, Marcos
  • Cortés-Avizanda, Ainara
  • Donázar, José A.
  • Sánchez-Zapata, José A.
The abandonment of traditional livestock farming systems in Mediterranean countries is triggering a large-scale habitat transformation, which, in general, consists of the replacement of open grazing areas by woodlands through non-managed regeneration. As a consequence, wild ungulates are occupying rapidly the empty niche left by domestic ungulates. Both types of ungulates represent the main trophic resource for large vertebrate scavengers. However, a comparison of how vertebrate scavengers consume ungulate carcasses in different habitats with different ungulate species composition is lacking. This knowledge is essential to forecast the possible consequences of the current farmland abandonment on scavenger species. Here, we compared the scavenging patterns of 24 wild and 24 domestic ungulate carcasses in a mountainous region of southern Spain monitored through camera trapping. Our results show that carcasses of domestic ungulates, which concentrate in large numbers in open pasturelands, were detected and consumed earlier than those of wild ungulate carcasses, which frequently occur in much lower densities at more heterogenous habitats such as shrublands and forest. Richness and abundance of scavengers were also higher at domestic ungulate carcasses in open habitats. Vultures, mainly griffons (Gyps fulvus), consumed most of the carcasses, although mammalian facultative scavengers, mainly wild boar (Sus scrofa) and red fox (Vulpes vulpes), also contributed importantly to the consumption of wild ungulate carcasses in areas with higher vegetation cover. Our findings evidence that the abandonment of traditional grazing may entail consequences for the scavenger community, which should be considered by ecologists and wildlife managers., The research was funded by the Project RNM-1925 (Junta de Andalucía), Project CGL2015-66966-C2-1-2-R and project RTI2018-099609-B-C21 (Spanish Ministry of Economy and Competitiveness and EU/ERDF). EA was supported by La Caixa-Severo Ochoa International PhD Program 2015, ZMR by a pre-doctoral grant from the MECD (FPU12/00823), MM by the Severo Ochoa Program for Centres of Excellence in R + D + I (SEV-2012-0262) and by a research contract Ramón y Cajal from the MINECO (RYC-2015-19231), and ACA by a Post-Doctoral Juan de la Cierva Incorporación IJCI-2014-20744 Ministerio de Economía y Competitividad and a Post-Doctoral contract (PD/039/2017) Vicepresidencia y Consejería de Innovación, Investigación y Turismo del Govern de les Illes Balears. “Roads Less Travelled” project (DiversEarth, Trashumancia y Naturaleza and Yolda Initiative) also contributed to this research.




Species and individual replacements contribute more than nestedness to shape vertebrate scavenger metacommunities

Digital.CSIC. Repositorio Institucional del CSIC
  • Mateo-Tomás, Patricia
  • Olea, Pedro P.
  • Selva, Nuria
  • Sánchez-Zapata, José A.
Understanding the mechanisms that organize biodiversity is central in ecology and conservation. Beta diversity links local (alfa) and regional (gamma) diversity, giving insight into how communities organize spatially. Metacommunity ecology provides the framework to interpret regional and local processes interacting to shape communities. However, the lack of metacommunity studies for large vertebrates may limit the understanding and compromise the preservation of ecosystem functions and services. We aim to understand the mechanisms underlying differences in species composition among vertebrate scavenger communities ‒ which provide key ecosystem functions, e.g. carrion consumption ‒ within a metacommunity context. We obtained species richness and abundances at scavenger communities consuming ungulate carcasses monitored through motion‐triggered remote cameras in seven terrestrial ecosystems in Spain. We partitioned beta diversity to decompose incidence‐based (species presence/absence) and abundance‐based dissimilarities into their components (turnover/balanced variation and nestedness/abundance gradient, respectively). We identified the environmental factors explaining the observed patterns. The vertebrate scavenger metacommunity consisted of 3101 individuals from 30 species. Changes in composition among ecosystems were mostly (> 84%) due to species or individual replacement (i.e. turnover or balanced variation). Species or individual loss/gain (i.e. nestedness or abundance gradient) accounted for 13–16% of these changes. Mean carcass weight, elevation and habitat diversity were the main factors explaining species/individual replacement. Our findings suggest that local processes such as species‐sorting through habitat heterogeneity would dominate scavenger metacommunity dynamics together with stochastic forces (i.e. related to carrion unpredictability and scavenging being a widespread strategy among vertebrates). The presence of structured patterns (i.e. nestedness) in beta diversity could reflect a role of deterministic processes: mass‐effects through dispersal and defaunation. Vultures are long‐distance foragers and functionally dominant species, which would connect local assemblages within the metacommunity, supporting scavenger diversity and functions across space. These results highlight the importance of managing vertebrate scavenger assemblages within a metacommunity context., PMT was funded by Portuguese FCT (SFRH/BPD/112437/2015). The study was funded by the Spanish Ministry of Economy and Competitiveness (projects CGL2012–40013‐bib2‐01/02, CGL2015–66966‐C2‐1‐2‐R) and EU FEDER funds. Data collection in Doñana was supported by the project 23/2007 ICTS‐RBD ‘Access to Unique Technological and Scientific Infrastructure Programme’. NS was partially supported by the National Science Center in Poland (DEC‐2013/08/M/NZ9/00469)., Peer reviewed




Dust and bullets: Stable isotopes and GPS tracking disentangle lead sources for a large avian scavenger

Digital.CSIC. Repositorio Institucional del CSIC
  • Arrondo, Eneko
  • Navarro, Joan
  • Pérez-García, Juan M.
  • Mateo, Rafael
  • Camarero, Pablo R.
  • Rodríguez Martín-Doimeadios, Rosa C.
  • Jiménez-Moreno, María
  • Cortés-Avizanda, Ainara
  • Navas, Isabel
  • García-Fernández, Antonio J.
  • Sánchez-Zapata, José A.
  • Donázar, José A.
9 pages, 3 figures, 2 tables, supplementary data https://doi.org/10.1016/j.envpol.2020.115022, Lead intoxication is an important threat to human health and a large number of wildlife species. Animals are exposed to several sources of lead highlighting hunting ammunition and lead that is bioavailable in topsoil. Disentangling the role of each in lead exposure is an important conservation issue, particularly for species potentially affected by lead poisoning, such as vultures. The identification of lead sources in vultures and other species has been classically addressed by means of stable-isotope comparisons, but the extremely varied isotope signatures found in ammunition hinders this identification when it overlaps with topsoil signatures. In addition, assumptions related to the exposure of individual vultures to lead sources have been made without knowledge of the actual feeding grounds exploited by the birds. Here, we combine lead concentration analysis in blood, novel stable isotope approaches to assign the origin of the lead and GPS tracking data to investigate the main foraging grounds of two Iberian griffon vulture populations (N = 58) whose foraging ranges differ in terms of topsoil lead concentration and intensity of big game hunting activity. We found that the lead signature in vultures was closer to topsoil than to ammunition, but this similarity decreased significantly in the area with higher big game hunting activity. In addition, attending to the individual home ranges of the tracked birds, models accounting for the intensity of hunting activity better explained the higher blood lead concentration in vultures than topsoil exposure. In spite of that, our finding also show that lead exposure from topsoil is more important than previously thought, The research was funded by Comunidad de Bardenas Reales de Navarra the Project RNM-1925 (Junta de Andalucía), Project CGL 2015-66966-C2-1-2-R (Spanish Ministry of Economy and Competitiveness and EU/ERDF) and Project PPII-2014-028-P (Junta de Comunidades de Castilla-La Mancha). EA was supported by La Caixa-Severo Ochoa International PhD Program 2015. JN was funded by the Spanish National Program Ramón y Cajal (RYC-2015-17809). ACA was supported by a PostDoc contract Programa Viçent Mut of Govern Balear (PD/039/2017) and and by a contract Juan de la Cierva Incorporación (IJCI-2014-20744) from the Spanish Ministry of Economy and Competitiveness, With the funding support of the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S), of the Spanish Research Agency (AEI)




Landscape anthropization shapes the survival of a top avian scavenger

Digital.CSIC. Repositorio Institucional del CSIC
  • Arrondo, Eneko
  • Sanz-Aguilar, Ana
  • Pérez-García, Juan M.
  • Cortés-Avizanda, Ainara
  • Sánchez-Zapata, José A.
  • Donázar, José A.
Events of non-natural mortality in human-dominated landscapes are especially challenging for populations of large vertebrates with K strategies. Among birds, vultures are one of the most threatened groups experiencing sharp population declines due to non-natural mortality. Factors causing non-natural mortality are usually studied separately. However, the potential use of an integrated index able to predict large-scale mortality risks of avian scavengers could be especially useful for planning conservation strategies. Here, we used the Human Footprint index to examine the impact of landscape anthropization on the survival rates of 66 GPS-tagged adult Eurasian griffon vultures (Gyps fulvus) in two Spanish regions. Foraging in more anthropized areas resulted in a significantly higher individual mortality risk mainly due to collisions with vehicles, poisonings, electrocutions and fatalities with wind turbines. Mean yearly survival rates were estimated at 0.817 ± 0.043 SE and 0.968 ± 0.018 SE for individuals from the more and less anthropized regions, respectively. Additional research should investigate whether some vulture populations could be acting as sinks unnoticed due to metapopulation dynamics. From a broader point of view, our study shows that a straightforward Human Footprint was a useful index to predict the survival of top scavengers and can be highly applicable to planning large-scale conservation measures., This research was funded by the Project RNM-1925 (Junta de Andalucía), the Project CGL2015-66966-C2-1-2-R (Spanish Ministry of Economy and Competitiveness and EU/ERDF) and the Project RTI2018-099609-B-C21 (Spanish Ministry of Economy and Competitiveness and EU/ERDF). “Roads Less Travelled” project (DiversEarth, Trashumancia y Naturaleza and Yolda Initiative) also contributed to this research. EA was supported by La Caixa-Severo Ochoa International PhD Program 2015. ASA and ACA by a post-doctoral contract Viçent Mut (PD/003/2016 and PD/039/2017, respectiely) co-funded by the Govern Balear and European Social Funds. ASA was also supported by a Spanish Ramón y Cajal contract (RYC-2017-22796) funded by the Ministerio de Ciencia, Innovación y Universidades, the Agencia Estatal de Investigación and the European Social Found. JMPG was supported by a Juan de la Cierva research contract (FJCI-2015-25632)., Peer reviewed




Epizootics and sanitary regulations drive long-term changes in fledgling body condition of a threatened vulture

Digital.CSIC. Repositorio Institucional del CSIC
  • Donázar, José A.
  • Cortés-Avizanda, Ainara
  • Ceballos, Olga
  • Arrondo, Eneko
  • Grande, Juan Manuel
  • Serrano, David
Under a Creative Commons license., Epizootics and deliberate changes in policies affecting the environment may affect large groups of species and the functioning of entire ecosystems. Although these effects often overlap in time, their simultaneous effect is rarely examined despite their importance as causes of current biodiversity loss. Here, based on the monitoring of an Egyptian vulture (Neophron percnopterus) population over thirty-three years (1986–2018), we increase our knowledge about the effects of anthropogenic-induced changes in food availability, both direct (sanitary policies limiting livestock carcass disposal) and indirect (a wild rabbit epizootic), on brood size and body condition of fledglings at nests. We compared the body mass of fledglings of broods with one chick (Single) and two chicks (within which we distinguished First and Second-hatched). The mass of Second-hatched chicks decreased after the plummet in rabbit populations (in the year 1990) and the regulations limiting carcass disposal (2005), reaching minimum values during the period with lowest food availability (i.e. 2005–2013). Recent sanitary legislation allowing carcass disposal by farmers coincides with a slight recovery in the observed body masses. Overall, this study shows that environmental changes of disparate origin can have synergistic effects on individual condition. Conservation of endangered vultures will require multi-targeted conservation plans aimed at ensuring nutritional requirements, in addition to detailed long-term monitoring, in order to detect obscure/masked drivers that affect body condition of fledglings., This research was funded by the Comunidad de Bardenas Reales de Navarra and the Projects CGL2015-66966-C2-1-2-R and RTI2018-099609-B-C21 (Spanish Ministry of Economy and Competitiveness and EU/FEDER), AAEE123/2017 (accions especials d’R+D Conselleria d’Innovació, Recerca I Turisme, Govern Balear). ACA was supported by a Post-Doctoral contract Juan de la Cierva Incorporación (IJCI-2014-20744) from Ministerio de Economía y Competitividad, Spain and a post-doctoral contract Programa Viçent Mut of Govern Balear, Spain (PD/039/2017). EA was supported by La Caixa-Severo Ochoa International PhD Program 2015., Peer reviewed




Roles of raptors in a changing world: from flagships to providers of key ecosystem services, El papel de las rapaces en un mundo en cambio: de especies bandera a proveedores de servicios ecosistémicos

Digital.CSIC. Repositorio Institucional del CSIC
  • Donázar, José A.
  • Cortés-Avizanda, Ainara
  • Fargallo, Juan A.
  • Margalida, Antoni
  • Moleón, Marcos
  • Morales-Reyes, Zebensui
  • Moreno-Opo, Rubén
  • Pérez-García, Juan M.
  • Sánchez-Zapata, José A.
  • Zuberogoitia, Íñigo
  • Serrano, David
Open Access., [EN]: Birds of prey have been, in comparison to other avian groups, an uncommon study model, mainly due to the limitations imposed by their conservative life strategy (low population density and turnover). Nonetheless, they have attracted a strong interest from the point of view of conservation biology because many populations have been close to extinction and because of their recognised role in ecosystems as top predators and scavengers and as flagship species. Today, after more than a century of persecution, and with the exception of some vultures still very much affected by illegal poisoning, many populations of birds of prey have experienced significant recoveries in many regions of Spain and the European Mediterranean. These changes pose new challenges when addressing the conservation of raptors in the coming decades. On this basis, and from a preferentially Mediterranean perspective, we have focused our attention on the need of describing and quantifying the role of these birds as providers of both regulating (rodent pest control and removal of livestock carcasses) and cultural ecosystem services. Moreover, we revisited persisting conflicts with human interests (predation of game species) and call attention to the emergence of new conflicts with a strong social and media component such as the predation on live cattle by vultures. Also, the rampant humanization of the environment determines the need for new solutions to the growing, yet scarcely explored, problem of accidents in new infrastructures such as mortality in wind farms. Finally, we explored in depth the ecological response of birds of prey to large-scale habitat changes such as urbanisation and abandonment of marginal lands that are also expected to increase in the near future. We urgently need more scientific knowledge to provide adequate responses to the challenge of keeping healthy populations of avian predators and scavengers in a rapidly changing world., [ES]: Las aves de presa han sido, en comparación con otros grupos de aves, más raramente utilizadas como sujeto de estudios en ecología en razón de las limitaciones que impone su estrategia de vida (baja densidad de población, alta longevidad y baja natalidad). Por el contrario, han suscitado un gran interés desde el punto de vista de la biología de la conservación, debido a que sus poblaciones en muchos casos se han aproximado a la extinción, así como al reconocimiento de su papel en los ecosistemas como superpredadores y carroñeros como especies bandera. Hoy en día, tras más de un siglo de persecución, y con la excepción de algunos buitres todavía muy afectados por envenenamientos ilegales, muchas especies de aves de presa han experimentado importantes crecimientos poblacionales en muchas regiones de España y del Mediterráneo europeo. Este escenario plantea nuevos desafíos para abordar la conservación de las rapaces en las próximas décadas. Sobre esta base hemos focalizado nuestra atención en la necesidad de describir y cuantificar el papel de estas aves como proveedores de servicios ecosistémicos, tanto reguladores (control de plagas de roedores y eliminación de restos de ganado) como culturales y de apoyo. Por otra parte, llamamos la atención hacia el reavivamiento de conflictos con intereses humanos (predación sobre especies cinegéticas) y a la aparición de nuevos conflictos con un fuerte componente social y mediático como la predación de aves carroñeras sobre ganado vivo. De igual modo, la creciente humanización del medio y de las poblaciones de aves de presa de mayor tamaño determinan que haya que buscar nuevas soluciones a problemas ya conocidos como los accidentes en infraestructuras, pero que tienen nuevas facetas complejas y aun poco exploradas como la mortalidad en parques eólicos. Finalmente, nos adentramos en la respuesta de las aves de presa a cambios a gran escala en el hábitat, como la urbanización y el abandono de tierras marginales que ya están ocurriendo y se prevé que se incrementen en las próximas décadas. Debe generarse más conocimiento científico para poder dar adecuada respuesta al reto que supone mantener poblaciones sanas de aves predadoras y carroñeras en un mundo que cambia vertiginosamente., M. M. acknowledges financial support through the Severo Ochoa Program for Centres of Excellence in R+D+I (SEV-2012-0262), z. M. R. was supported by a pre-doctoral grant FPU12/00823. A. M. was
supported by a Ramón y Cajal research contract (Ministry of Economy and Competitiveness,
RYC-2012-11867). ACA was supported by a Post-Doctoral grant from the Fundação para
a Ciência e a Tecnologia (FCT) (SFRH / BPD / 91609 / 2012) and a contract Juan de la Cierva
Incorporación IJCI-2014-20744 of the Ministry of Economy and Competitiveness. JAD, JMPG,
AM, zM and JASz were funded by project CGL2015-66966-C2-1-2-R, MINECO/FEDER,
UE., Peer Reviewed




Egyptian Vulture CR data

Digital.CSIC. Repositorio Institucional del CSIC
  • Badia-Boher, Jaume Adrià
  • Sanz-Aguilar, Ana
  • Riva, Manuel de la
  • Gangoso, Laura
  • van Overveld, Thijs
  • García-Alfonso, Marina
  • Donázar, José A.
This dataset was used to analyze survival probabilities of Egyptian Vultures at Canary Islands from 1998 to 2017., We acknowledge financial support through the projects REN 2000–1556 GLO, CGL2004-00270/BOS, CGL2009-12753-C02-02, CGL2012-40013-C02-01, and CGL2015-66966-C2-1-2-R (Spanish Ministry of Economy and Competitiveness and EU/FEDER)., The data file contains capture, resight and recovery histories of Egyptian vultures at Canary Islands (Fuerteventura and Lanzarote) during breeding seasons 1998 to 2017. This file contains one line per individual; one column per encounter occasion (from column 1 to 20 were code “0” indicate that the individual was not observed in a particular year; code “1” is used for individuals detected (marked at capture or resighted) with both coloured and steel metal butt-end rings; code “2” is used for individuals detected (marked at capture or resighted) with coloured and steel metal lock-on rings; code “3” is used for individuals resighted only retaining their coloured rings, code “4” is used for individuals resighted only retaining steel metal butt-end rings; and code “5” is used for individuals recovered freshly dead. There are six further columns (21 to 26) indicating the group (starting age at marking form 1-year-old to ≥6 year-old) for each individual., No




Both rare and common species support ecosystem services in scavenger communities

Digital.CSIC. Repositorio Institucional del CSIC
  • Mateo-Tomás, Patricia
  • Olea, Pedro P.
  • Moleón, Marcos
  • Selva, Nuria
  • Sánchez-Zapata, José A.
[Aim]: Recent works on biodiversity–ecosystem functioning (BEF) relationships highlight abundance fluctuations of common species as more important for delivering ecosystem services than changes in species richness and composition in real-world ecosystems. However, evidence on BEF relationships in natural ecosystems is still limited, especially for large vertebrates. Here, we aimed to disentangle the relative roles of species richness, composition and abundance of vertebrate scavenger communities in the ecological process of carcass elimination, a pivotal ecosystem service, in natural ecosystems. We evaluated the variability in the scavenging function across ecosystems, and examined the factors explaining it. [Location]: Nine natural ecosystems, seven in Europe and two in Africa. [Major taxa studied]: Vertebrates. [Time period]: 2006–2013. [Methods]: We obtained BEF relationships from vertebrate scavengers consuming ungulate carcasses monitored through motion-triggered remote cameras. We used the Price equation to tease out the relative roles of species richness, composition and abundance in the scavenging efficiency of vertebrates. [Results]: We recorded 46 vertebrate scavenging species, 30 in Spain and 16 in South Africa. Two main patterns drove BEF relationships. Species richness and composition drove carcass consumption in ecosystems where functionally dominant scavengers were rare, whilst context dependent effects (including species abundance) did so where functionally dominant species were common. Contrastingly to previous studies, abundance fluctuations in vertebrate scavengers were not exclusively related to common species but to the specialization of obligate scavengers (i.e., Gyps vultures) to rapidly gather at carcasses and to the top-down control exerted by large predators. [Main conclusions]: Rare and threatened species such as vultures and top predators become functionally key species in scavenging processes, highlighting that the delivery of ecosystem services still stands as a general argument for biodiversity conservation in vertebrate communities. Human persecution of vultures and top predators worldwide is expected to alter ecosystem functioning and services such as nutrient recycling or disease control., Portuguese FCT, Grant/Award Number: SFRH/BPD/112437/2015; Severo Ochoa Program for Centers of Excellence in R1D1I, Grant/Award Number: SEV-2012-0262; National Science Center in Poland,Grant/Award Number: DEC-2013/08/M/NZ9/00469; Spanish Ministry of Economy and Competitiveness, Grant/Award Number: CGL2012-40013-C02-01/02 (Accessto Unique Technological and Scientific Infrastructure Programme ‘Doñana Scientific Reserve’ project 23/2007 ICTS-RBD) and CGL2015-66966-C2-1-2-R; EU FEDER funds., Peer Reviewed




Evaluation of the network of protection areas for the feeding of scavengers in Spain: from biodiversity conservation to greenhouse gas emission savings

Digital.CSIC. Repositorio Institucional del CSIC
  • Morales-Reyes, Zebensui
  • Pérez-García, Juan M.
  • Moleón, Marcos
  • Botella, Francisco
  • Carrete, Martina
  • Donázar, José A.
  • Cortés-Avizanda, Ainara
  • Arrondo, Eneko
  • Moreno-Opo, Rubén
  • Jiménez, José
  • Margalida, Antoni
  • Sánchez-Zapata, José A.
1. Protected areas are one of the most common strategies for wildlife conservation world-wide. However, their effectiveness is rarely evaluated. In Europe, after the outbreak of bovine spongiform encephalopathy, a restrictive sanitary regulation (EC 1774/2002) prohibited the abandonment of dead livestock in extensive farming (extensive livestock) in the field, which led to negative consequences for scavengers. As an attempt to mitigate this negative impact, a new regulation was approved (EC 142/2011) to allow farmers to leave extensive livestock carcasses in the so-called `Protection areas for the feeding of necrophagous species of European interest' (PAFs). 2. Our general aims were to quantify (i) the proportion of breeding distribution of targeted scavenger species overlapping PAFs; (ii) the extensive livestock carrion biomass available inside PAFs; (iii) the proportion of breeding distribution of non-targeted scavenger species falling within PAFs; (iv) the overlap between the home range of vultures and PAFs, as well as the extent to which vultures move through different administrative units; and (v) the savings in greenhouse gas (GHG) emissions in relation to the pre-PAF scenario. 3. After assessing the status of PAF implementation in every region of peninsular Spain, we analysed the large-scale spatial information of extensive livestock carrion availability and scavenger breeding distribution, movement data of GPS-tracked vultures, and the annual GHG emissions associated with the transport of livestock carcasses. 4. Most regions established PAFs in their territories, although design criteria were variable. The breeding distribution of targeted species was better represented within PAFs than that of non-targeted species. The extensive livestock carrion biomass potentially available for scavengers within PAFs represented 34·9% of the annual extensive livestock biomass generated in peninsular Spain. The overlap between the home range of GPS-marked vulture populations and PAFs ranged between 63·4% and 100%. The minimum convex polygon of these and other GPS-tracked vulture populations in peninsular Spain encompassed 3-14 Spanish regions and 1-4 countries. Post-PAF there was a potential reduction of c. 55·7% of GHG emissions compared to pre-PAF. 5. Synthesis and applications. The implementation of the new sanitary regulation by means of areas for the feeding of scavengers could mean an important improvement in scavenger conservation and a noteworthy reduction in greenhouse gas emissions: in Spain, extensive livestock carrion availability might increase to 33 474 t yr-1, and 43 344 t of CO2 eq. might be saved annually. However, we identified some gaps related to the distribution of endangered facultative scavengers. Moreover, given that vultures are highly mobile organisms, the design and management of these feeding areas should be coordinated at both the supra-regional and supra-national scales., The study was funded by the regional governments of Andalusia (project RNM‐1925) and Catalonia, the Spanish Ministry of Agriculture, Food and Environment (MAGRAMA), and the Spanish Ministry of Economy and Competitiveness and EU FEDER funds (projects CGL2012‐40013‐C02‐01/02 and CGL2015‐66966‐C2‐1‐2‐R). Additional information was supplied by the Organismo Autónomo Parques Nacionales (OAPN) and the MAGRAMA. Z.M.R. was supported by a pre‐doctoral grant FPU12/00823, M.M. by a Severo Ochoa Program for Centres of Excellence in R+D+I (SEV‐2012‐0262), A.C.A. by a post‐doctoral grant FCT‐SFRH/BPD/91609/2012 and a contract IJCI‐2014‐20744, E.A. by La Caixa‐Severo Ochoa International PhD Programme and A.M. by a Ramón y Cajal research contract (RYC‐2012‐11867)., Peer Reviewed




Invisible barriers: Differential sanitary regulations constrain vulture movements across country borders

Digital.CSIC. Repositorio Institucional del CSIC
  • Arrondo, Eneko
  • Moleón, Marcos
  • Cortés-Avizanda, Ainara
  • Jiménez, José
  • Beja, Pedro
  • Sánchez-Zapata, José A.
  • Donázar, José A.
Political boundaries may represent ecological barriers due to differences in wildlife management policies. In the European Union, it might be expected that these differences should be highly diluted, because all countries have to comply with common directives issued by the European Commission. However, the subsidiarity principle may lead to the uneven uptake of European Union regulations, which can impact on biodiversity conservation due to unequal legislation in neighboring countries, particularly in the case of highly mobile organisms. Here we ad- dress this issue, by analyzing how EU regulations issued in response to the Bovine Spongiform Encephalopathy (BSE) crisis differentially affected vulture conservation in Portugal and Spain. Taking advantage of the intensive GPS-tracking of 60 griffon (Gyps fulvus) and 11 cinereous vultures (Aegypius monachus) from Spain, we found that the Spanish-Portuguese border acts as a quasi-impermeable barrier. In fact, there was an abrupt decline in the number of vulture locations across the Spanish-Portuguese border, with modelling showing that this was un- likely to be related to differences in land cover or topography. Instead, the pattern found was likely due to differences in trophic resource availability, namely carcasses from extensive livestock husbandry, resulting from the differential application of European sanitary legislation regarding the mandatory removal of dead livestock from the field. Overall, our results should be seen as a warning signal to policy makers and conservation managers, highlighting the need for a stronger integration of sanitary and environmental policies at the European level., This research was funded by the Consejeria de economia innovacion ciencia y empleo Junta de Andalucia (Proyecto de Excelencia 2012 RNM-1925) (Junta de Andalucía), Comunidad de Bardenas Reales de Navarra (Convenios EBD-CSIC 2014-2017), and MInisterio de Economia, Industria y competitividad (Projecto CGL2015-66966-C2-1-2-R) (Spanish Ministry of Economy and Competitiveness and EU/FEDER). EA was supported by La Caixa-Severo Ochoa International PhD Program 2015, MM by the Severo Ochoa Program for Centres of Excellence in R + D + I (SEV-2012-0262) and by a research contract Ramón y Cajal from the MINECO (RYC-2015-19231), ACA by a post-doctoral contract Juan de la Cierva Incorporación (IJCI-2014-20744) of the Spanish Ministry of Economy and Competitiveness, and PB by EDP Biodiversity Chair., Peer Reviewed




Potential threat to Eurasian griffon vultures in Spain from veterinary use of the drug diclofenac

Digital.CSIC. Repositorio Institucional del CSIC
  • Green, Rhys E.
  • Donázar, José A.
  • Sánchez-Zapata, José A.
  • Margalida, Antoni
Spain holds > 95% of the European breeding population of the Eurasian griffon vulture Gyps fulvus. Vultures provide important ecosystem services in carcass removal and influence emissions of greenhouse gases. Despite the known toxicity of the non-steroidal anti-inflammatory drug diclofenac to this species and other Gyps vultures, in March 2013 the Agencia Española de Medicamentos y Productos Sanitarios (AEMPS) approved the use of two medicines containing diclofenac for veterinary use in horses, pigs and cattle in Spain. To assess the potential impact of medicated ungulate carcasses on Eurasian griffon vulture populations in Spain, we first used information on the metabolism and elimination of diclofenac from medicated cattle and pigs to calculate residue levels in relation to time elapsed between dosing and death. Secondly, probabilities of the death of a vulture per meal were calculated based upon experimental studies of diclofenac toxicity. Finally, annual numbers of vulture deaths expected to be caused by diclofenac were obtained by multiplying the death rates per meal by the estimated numbers of vulture meals taken from expected numbers of medicated carcasses suggested by AEMPS. Assuming that vultures feed on carcasses that were treated with diclofenac 8 h before the animal's death, the annual number of vulture deaths caused by diclofenac was estimated at 715–6389, depending upon the estimate of numbers of medicated carcasses assumed and the version of the dose–response model used. Using a density-independent simulation model of a vulture population, the expected rate of decline of the Spanish population of Eurasian griffon vultures caused by these deaths is 0·9–7·7% per year. A density-dependent simulation model also indicated substantial population-level effects. Formal estimates of precision and sensitivity analyses of effects of unmeasured variables highlight the uncertainty of estimates using currently available data. Synthesis and applications. Due to the possibility of causing an important impact on vulture populations, our findings justify a precautionary ban on the veterinary use of diclofenac in Spain and encourage the use of meloxicam, a vulture-safe alternative drug. A programme of monitoring of non-steroidal anti-inflammatory drug contamination of ungulate carcasses available to vultures and of moribund and dead obligate and facultative avian scavengers would be needed to be confident that a damaging level of contamination is not present., A. Margalida was upported by a Ramón y Cajal research contract from the Ministry of Economy and Competitiveness (RYC-2012-11867). J.A. Sanchez-Zapata, J. A. Donázar and A. Margalida were funded by project CGL2012-40013-CO2-01-02 and CGL2015-66966-C2-1-2-R., Peer Reviewed