Ainara Cortés-Avizanda

Dietary shifts in two vultures after the demise of supplementary feeding stations: consequences of the EU sanitary legislation

Among vertebrates, specialization in scavenging has appeared only in “true” Gyps vultures, which usually base their diet almost exclusively on carcasses of medium and large-sized mammals, whereas all other scavengers rely on broader ranges of prey. The availability of food for scavengers in Western Europe has not been limited during recent decades permitting the existence and growth of huge vulture populations. From 2000 onwards, however, EU sanitary legislation has progressively limited the abandonment of dead animals in the field resulting in a sudden reduction of food availability with unknown ecological and conservation consequences. Here, we examine the dietary response of a tandem of carrion eaters, the griffon vulture (Gyps fulvus) and the Egyptian vulture (Neophron percnopterus), showing different degrees of dietary specialization. Our results showed that after the reduction in numbers of supplementary feeding stations (vulture restaurants) the niche breadth of the griffon vulture has broadened and now includes significant amounts of wild rabbits (Oryctolagus cuniculus) and garbage. The diet of the Egyptian vulture, on the contrary, did not vary substantially. The diet overlap showed patterns probably conditioned by interspecific competition and the progressive exploitation of unpredictable carcasses. On a short-term scale, consequences for smaller scavengers could be negative due to the monopolization of resources by the dominant and much more abundant griffon vulture, however in the long-term all guild species would benefit from the exploitation of unpredictable carcasses, which could enhance the possibilities of coexistence.

Resource unpredictability promotes species diversity and coexistence in an avian scavenger guild: a field experiment

Chance per se plays a key role in ecology and evolution, e.g., genetic mutation, resource spatiotemporal unpredictability. In community ecology, chance is recognized as a key factor in community assemblage, but less is known about its role in intraguild processes leading to species coexistence. Here we study the relevance of resource unpredictability per se as a promoter of intraguild positive interspecific interactions and as a biodiversity enhancer in an Old World avian scavenger guild, which has evolved to feed upon spatially and temporally unpredictable resources, i.e., carcasses. We performed a large-scale field experiment in which 58 carcasses were disposed of and observed until complete consumption, either in continuously active supplementary feeding stations (predictable carcasses) or disposed of at random in the field (unpredictable carcasses). Richness of scavenger species was similar at unpredictable and predictable carcasses, but their relative abundances were highly uneven at predictable carcasses leading to higher scavenger diversity (Shannon index) at unpredictable carcasses. Facilitatory interspecific processes only occurred at unpredictable resources but were disrupted in predictable conditions because the dominant specialist species (in our case, the Griffon Vulture Gyps fulvus) arrived earlier and in larger numbers, monopolizing the resource. Small, endangered scavengers congregated at supplementary feeding stations but profited less compared to unpredictable carcasses, suggesting that they could constitute an ecological trap. Our findings offer new insights into the relevance of unpredictability of trophic resources in promoting both positive facilitatory interspecific interactions and species diversity and thus maintaining the function of guilds. Finally, the preservation of randomness in resource availability and the processes associated with its exploitation should be a major goal of conservation strategies aimed to preserve scavenger guilds evolved under naturally unpredictable trophic resources.

Roles of raptors in a changing world: from flagships to providers of key ecosystem services

Summary. 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.

Spatial Heterogeneity in Resource Distribution Promotes Facultative Sociality in Two Trans-Saharan Migratory Birds

Background Migrant populations must cope not only with environmental changes in different biomes, but also with the continuous constraints imposed by human-induced changes through landscape transformation and resource patchiness. Theoretical studies suggest that changes in food distribution can promote changes in the social arrangement of individuals without apparent adaptive value. Empirical research on this subject has only been performed at reduced geographical scales and/or for single species. However, the relative contribution of food patchiness and predictability, both in space and time, to abundance and sociality can vary among species, depending on their degree of flexibility. Methodology/Principal Findings By means of constrained zero-inflated Generalized Additive Models we analysed the spatial distribution of two trans-Saharan avian scavengers that breed (Europe) and winter (Africa) sympatrically, in relation to food availability. In the summering grounds, the probability of finding large numbers of both species increases close to predictable feeding sources, whereas in the wintering grounds, where food resources are widespread, we did not find such aggregation patterns, except for the black kite, which aggregated at desert locust outbreaks. The comparison of diets in both species through stable isotopes revealed that their diets overlapped during summering, but not during wintering. Conclusions/Significance Our results suggest that bird sociality at feeding grounds is closely linked to the pattern of spatial distribution and predictability of trophic resources, which are ultimately induced by human activities. Migrant species can show adaptive foraging strategies to face changing distribution of food availability in both wintering and summering quarters. Understanding these effects is a key aspect for predicting the fitness costs and population consequences of habitat transformations on the viability of endangered migratory species.

Long-term trends in population size and breeding success in the Egyptian vulture (Neophron percnopterus) in Northern Spain.

Abstract The Egyptian Vulture (Neophron percnopterus) is considered a globally endangered avian scavenger. In the 1980s, Bardenas Reales Natural Park in northern Spain held the densest populations in Europe. There, the population of the wild rabbit (Oryctolagus cuniculus), the main prey of this vulture, decreased dramatically after the arrival of the rabbit hemorrhagic disease (RHD) in 1989, and did not recover. We monitored the population of Egyptian Vultures in Bardenas Reales from 1989–2007. During the study period, the number of breeding territories decreased from 56 to 26 (−54%). In contrast, the percentage of occupying pairs that laid eggs, the number of fledglings per pair, and the number of fledglings per successful nest remained stable, suggesting that the population decline was not attributable to reduced productivity. However, we found 34 dead birds, most of them poisoned, particularly in the second half of the study period (in 1996–1997 and 2004–2007), suggesting that high mortality rates could be contributing to the decline of this species. The fact that poisoning events mainly occurred outside the park suggested that the reduction in numbers of wild rabbits in Bardenas Reales Natural Park forced Egyptian Vultures to move into areas with greater human populations and higher mortality risks. We recommend implementing management measures and environmental education programs to prevent the illegal use of poisoned baits in the area surrounding the park.

Mast Pulses Shape Trophic Interactions between Fluctuating Rodent Populations in a Primeval Forest

How different functional responses of consumers exploiting pulsed resources affect community dynamics is an ongoing question in ecology. Tree masting is a common resource pulse in terrestrial ecosystems that can drive rodent population cycles. Using stable isotope (δ13C, δ15N) analyses, we investigated the dietary response of two fluctuating rodent species, the yellow-necked mouse Apodemus flavicollis and the bank vole Myodes glareolus, to mast events in Białowieża Forest (NE Poland). Rodent hair samples were obtained non-invasively from faeces of their predators for an 11-year period that encompassed two mast events. Spectacular seed crops of deciduous trees, namely oak Quercus robur and hornbeam Carpinus betulus, occur after several intermediate years of moderate seed production, with a post-mast year characterised by a nil crop. While a Bayesian isotopic (SIAR) mixing model showed a variety of potential vegetation inputs to rodent diets, the isotopic niche of the yellow-necked mouse was strongly associated with mast of deciduous trees (>80% of diet), showing no variation among years of different seed crop. However, bank voles showed a strong functional response; in mast years the vole shifted its diet from herbs in deciduous forest (∼66% of diet) to mast (∼74%). Only in mast years did the isotopic niche of both rodent species overlap. Previous research showed that bank voles, subordinate and more generalist than mice, showed higher fluctuations in numbers in response to masting. This study provides unique data on the functional response of key pulse consumers in forest food webs, and contributes to our understanding of rodent population fluctuations and the mechanisms governing pulse–consumer interactions.

Stress associated with group living in a long-lived bird

Many long-lived avian species adopt life strategies that involve a gregarious way of life at juvenile and sub-adult stages and territoriality during adulthood. However, the potential associated costs of these life styles, such as stress, are poorly understood. We examined the effects of group living, sex and parasite load on the baseline concentration of faecal stress hormone (corticosterone) metabolites in a wild population of common ravens (Corvus corax). Corticosterone concentrations were significantly higher in non-breeding gregarious ravens than in territorial adults. Among territorial birds, males showed higher stress levels than their mates. Parasite burdens did not affect hormone levels. Our results suggest a key role of the social context in the stress profiles of the two population fractions, and that group living may be more energetically demanding than maintaining a territory. These findings have implications for understanding hormonal mechanisms under different life styles and may inspire further research on the link between hormone levels and selective pressures modulating gregarious and territorial strategies in long-lived birds.

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

Summary Protected areas are one of the most common strategies for wildlife conservation worldwide. 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). 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. 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. 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 ca. 55.7% of GHG emissions compared to pre-PAF. 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 of greenhouse gas emissions: in Spain, extensive livestock carrion availability might increase 33,474 t/year, 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. This article is protected by copyright. All rights reserved.

Density-dependent productivity in a colonial vulture at two spatial scales.

Understanding how density dependence modifies demographic parameters in long-lived vertebrates is a challenge for ecologists. Two alternative hypotheses have been used to explain the mechanisms behind density-dependent effects on breeding output: habitat heterogeneity and individual adjustment (also known as interference competition). A number of studies have highlighted the importance of habitat heterogeneity in density dependence in territorial species, but less information exists on demographic processes in colonial species. For these, we expect density-dependent mechanisms to operate at two spatial scales: colony and breeding unit. In this study, we used long-term data from a recovering population of Cinereous Vultures (Aegypius monachus) in southern Spain. We analyzed a long-term data set with information on 2162 breeding attempts at four colonies over a nine-year period (2002-2010) to evaluate environmental and population parameters influencing breeding output. Our results suggest that breeding productivity is subject to density-dependent processes at the colony and the nest site scale and is best explained by interference competition. Factors intrinsic to each colony, as well as environmental constraints linked to physiography and human presence, also play a role in regulatory processes. We detected the existence of a trade-off between the disadvantages of nesting too close to conspecifics and the benefits of coloniality. These could be mediated by the agonistic interactions between breeding pairs and the benefits derived from social sharing of information by breeding individuals. We propose that this trade-off may play a role in defining colony structure and may hold true for other colonial breeding bird species. Our findings also have important management implications for the conservation of this threatened species.

Modeling the consequences of the demise and potential recovery of a keystone-species: wild rabbits and avian scavengers in Mediterranean landscapes

Restoration of demised keystone-species populations is an overriding concern in conservation biology. However, since no population is independent of its environment, progress is needed in predicting the efficacy of restoration in unstable ecological contexts. Here, by means of Population Dynamics P-system Models (PDP), we studied long-term changes in the population size of Egyptian vultures (Neophron percnopterus) inhabiting a Natural Park, northern Spain, to changes in the numbers of wild rabbits (Oryctolagus cuniculus), a keystone-species of Mediterranean ecosystems that have suffered >90% population decline after a hemorrhagic disease outbreak. Low availability of rabbit carcasses leads Egyptian vultures to extend their foraging activities to unprotected areas with higher non-natural mortality whereas growing numbers of griffon vultures (Gyps fulvus), a dominant competitor, progressively monopolize trophic resources resulting in a focal population decrease. Modeling shows that, even if keystone-species populations recover in core protected areas, the return to the original studied population size may be unfeasible, due to both the high non-natural mortality rates in humanized areas and long-term changes in the scavenger guild structure. Policy decisions aimed to restore keystone-species should rely on holistic approaches integrating the effects of spatial heterogeneity on both producer and consumer populations as well as within-guild processes.