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Too much is bad: increasing numbers of livestock and conspecifics reduce body mass in an avian scavenger

Docta Complutense
  • Donázar, José A.
  • Barbosa, Jomar M.
  • García Alfonso, Marina
  • Van Overveld, Thijs
  • Gangoso De La Colina, Laura Esther
  • Riva, Manuel de la
Individual traits such as body mass can serve as early warning signals of changes in the fitness prospects of animal populations facing environmental impacts. Here, taking advantage of a 19-yr monitoring, we assessed how individual, population, and environmental factors modulate long-term changes in the body mass of Canarian Egyptian vultures. Individual vulture body mass increased when primary productivity was highly variable, but decreased in years with a high abundance of livestock. We hypothesized that carcasses of wild animals, a natural food resource that can be essential for avian scavengers, could be more abundant in periods of weather instability but depleted when high livestock numbers lead to overgrazing. In addition, increasing vulture population numbers also negatively affect body mass suggesting density-dependent competition for food. Interestingly, the relative strength of individual, population and resource availability factors on body mass changed with age and territorial status, a pattern presumably shaped by differences in competitive abilities and/or age-dependent environmental knowledge and foraging skills. Our study supports that individual plastic traits may be extremely reliable tools to better understand the response of secondary consumers to current and future natural and human-induced environmental changes.




Blood lead levels in an endangered vulture decline following changes in hunting activity

Docta Complutense
  • Gangoso De La Colina, Laura Esther
  • Mateo, R.
  • Santamaría-Cervantes, C.
  • García-Alfonso, M.
  • Gimeno-Castellano, C.
  • Arrondo, E.
  • Serrano, D.
  • Van Overveld, T.
  • Riva, M. de la
  • Cabrera, M.A.
  • Donázar, J.A.
Lead ammunition stands out as one of the most pervasive pollutants affecting wildlife. Its impact on bird populations have spurred efforts for the phase-out of leaded gunshot in several countries, although with varying scopes and applications. Ongoing and future policy changes require data to assess the effectiveness of adopted measures, particularly in the current context of biodiversity loss. Here, we assessed the long-term changes in blood lead (Pb) levels of Egyptian vultures from the Canary Islands, Spain, which have been severely affected by Pb poisoning over the past two decades. During this period, the reduction in hunting pressure and changes in legislation regarding firearms usage for small game hunting likely contributed to a decrease in environmental Pb availability. As anticipated, our results show a reduction in Pb levels, especially after the ban on wild rabbit hunting with shotgun since 2010. This effect was stronger in the preadult fraction of the vulture population. However, we still observed elevated blood Pb levels above the background and clinical thresholds in 5.6% and 1.5% of individuals, respectively. Our results highlight the positive impact of reducing the availability of Pb from ammunition sources on individual health. Nonetheless, the continued use of Pb gunshot remains an important source of poisoning, even lethal, mainly affecting adult individuals. This poses a particular concern for long-lived birds, compounding by potential chronic effects associated with Pb bioaccumulation. Our findings align with recent studies indicating insufficient reductions in Pb levels among European birds of prey, attributed to limited policy changes and their uneven implementation. We anticipated further reductions in Pb levels among Egyptian vultures with expanded restrictions on hunting practices, including a blanket ban on Pb shot usage across all small game species.




Food predictability and social status drive individual resource specializations in a territorial vulture

Docta Complutense
  • Van Overveld, Thijs
  • García Alfonso, Marina
  • Dingemanse, Niels J.
  • Bouten, Willem
  • Gangoso De La Colina, Laura Esther
  • Riva, Manuel de la
  • Serrano, David
  • Donázar, José A.
Despite increasing work detailing the presence of foraging specializations across a range of taxa, limited attention so far has been given to the role of spatiotemporal variation in food predictability in shaping individual resource selection. Here, we studied the exploitation of human-provided carrion resources differing in predictability by Canarian Egyptian vultures (Neophron percnopterus majorensis). We focussed specifically on the role of individual characteristics and spatial constraints in shaping patterns of resource use. Using high-resolution GPS data obtained from 45 vultures tracked for 1 year, we show that individual vultures were repeatable in both their monthly use of predictable and semi-predicable resources (feeding station vs. farms) and monthly levels of mobility (home range size and flight activity). However, individual foraging activities were simultaneously characterized by a high degree of (temporal) plasticity in the use of the feeding station in specific months. Individual rank within dominance hierarchy revealed sex-dependent effects of social status on resource preference in breeding adults, illustrating the potential complex social mechanisms underpinning status-dependent resource use patterns. Our results show that predictable food at feeding stations may lead to broad-scale patterns of resource partitioning and affect both the foraging and social dynamics within local vulture populations.




Evaluating European LIFE conservation projects: Improvements in survival of an endangered vulture

Docta Complutense
  • Adrià Badia‐Boher, Jaume
  • Sanz Aguilar, Ana
  • De la Riva, Manuel
  • Gangoso De La Colina, Laura Esther
  • Van Overveld, Thijs
  • García Alfonso, Marina
  • Luzardo, Octavio P.
  • Suarez Pérez, Alejandro
  • Donázar, José Antonio
Long-lived avian scavengers are threatened worldwide and thus, are common targets of conservation plans. However, scientific evidence of both the factors limiting populations and effectiveness of management actions are greatly needed in order to develop more efficient and successful conservation strategies.

We assessed the effectiveness of conservation actions applied within a LIFE-Nature project aimed at improving the long-term survival of the critically endangered Canarian Egyptian vulture: including education campaigns for public awareness and control of illegal poisoning and the modification of power lines to reduce the risk of accidents. We formulated a multievent capture–mark–recapture model to obtain estimates of survival for juvenile, subadult and adult birds accounting for probabilities of resight, recovery and losses of metal and colour rings.

Models supported a substantial enhancement in survival for subadult and adult birds and a moderate improvement for juveniles after the implementation of LIFE actions. Ring loss probabilities became notably high in the middle to long term.

Poisoning events became very rare after LIFE was implemented, suggesting a positive effect of environmental education and awareness campaigns. Entanglements and collisions in power lines were also efficiently mitigated. Instead, electrocutions became the most identified cause of death in the post-LIFE stage.

Synthesis and applications. Our results highlight the improvement of survival in a threatened island vulture population after the implementation of a European LIFE conservation project. On small islands, with small human populations and few stakeholders, education and awareness campaigns can be especially effective for biodiversity conservation. We also demonstrate the need to complement conservation programmes with long-term monitoring, which is essential to evaluate the effectiveness of actions, especially for long-lived species.




Seasonal grouping dynamics in a territorial vulture: ecological drivers and social consequences

Docta Complutense
  • Van Overveld, Thijs
  • Gangoso De La Colina, Laura Esther
  • García Alfonso, Marina
  • Bouten, Willem
  • Riva, Manuel de la
  • Donázar, José Antonio
Despite widespread occurrence of seasonal sociality among animals, little is still known about the social drivers and population-level social implications of seasonal grouping behaviours, especially in birds. Here, we studied the combined effects of ecological and social factors on seasonal grouping patterns in a sedentary population of Egyptian vultures living on the Eastern Canary Islands. We focussed on the social significance of large-scale gatherings taking place outside the breeding season at a highly preferred feeding station and a nearby temporary roost. Group sizes at this feeding patch followed a strong seasonal pattern characterized by distinct monthly changes in group composition, according to sex, age and territorial status. In between reproductive periods, vulture numbers at the feeding station may reach up 50% of the total population on a single day. GPS-tracking showed that this increase in vulture numbers was in part due to a shift in foraging range towards the centre of Fuerteventura by low-ranked territorial birds breeding in remote areas. During this period, vultures may spend on average 30% of their monthly time in a social gatherings context, depending on social status. We show that seasonal grouping patterns are shaped by the complex interplay between ecological factors (reproductive constraints, resource seasonality, food predictability), age-specific traits and social competitive processes, while social attraction may be an important additional component. We propose that for facultative social foragers living in highly despotic territorial systems, collective foraging may be of particular relevance regarding the development of hierarchical social relations and maintenance of population-level social cohesion.




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




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.




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.