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1.  Assessing the impact of removal scenarios on population viability of a threatened, long-lived avian scavenger 
Scientific Reports  2015;5:16962.
The removal of eggs or chicks from wild populations to create captive populations, reinforce free-ranging populations or reintroduce species into the wild is a restoration tool that requires an assessment of potential detrimental effects upon the donor population. This is an absolute prerequisite when wild donor populations are scarce and small. Here, we forecast the population trend of the largest European population of the bearded vulture (Gypaetus barbatus) over the next 30 years under different demographic and management scenarios (removal of eggs, chicks or fledglings). Projections derived from the combination of a PDP model (Population Dynamic P-system) and a Box-Behnken design would lead to a decline in 77% of all 57 scenarios analysed. Among the 13 scenarios predicting a population increase, only 4 seem realistic in terms of growth rate (0.04%–1.01%), at least if current age at first breeding and productivity would remain constant over time. Our simulations thus suggest that most extraction scenarios would have detrimental effects on the demography of the donor population. Release of captive-born young or removal of only the second hatched chick for subsequent captive rearing and translocation into the wild appear to represent much better supplementation and reintroduction options in this threatened species.
PMCID: PMC4655339  PMID: 26593059
2.  Modeling the consequences of the demise and potential recovery of a keystone-species: wild rabbits and avian scavengers in Mediterranean landscapes 
Scientific Reports  2015;5:17033.
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.
PMCID: PMC4655486  PMID: 26593338
4.  Who Are We Feeding? Asymmetric Individual Use of Surplus Food Resources in an Insular Population of the Endangered Egyptian Vulture Neophron percnopterus  
PLoS ONE  2013;8(11):e80523.
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.
PMCID: PMC3823625  PMID: 24244695
5.  Population Sex Ratios: Another Consideration in the Reintroduction – Reinforcement Debate? 
PLoS ONE  2013;8(9):e75821.
Reintroduction or reinforcement (RorR) of wild populations is a common conservation strategy. Many conservation projects involve the release of individuals of poorly studied species. This may lead to inefficient results or negative impacts on the conservation efforts. Here, we provide new insights into the conservation implications and potential consequences of a skew in the sex ratio of released birds and of the number of birds supplemented for the demography of a long-lived dimorphic bird species, the Andean condor (Vulturgryphus). We demonstrate that a RorR conservation program may be less effective in conserving a species if the sex ratios of the releases and the recipient populations are not considered. We also show that releases can reduce population declines but only if carried out over long periods (i.e., several decades). This can mean high costs for release programs and the added challenge of maintaining programs over time. If RorR programs are to be implemented, bearing in mind the importance of properly assessing their effectiveness, we urge conservation researchers and managers to consider the implications of sex ratio biases for wild populations, and particularly for dimorphic species with sexually despotic behaviour.
PMCID: PMC3784389  PMID: 24086641
6.  Genetic diversity at neutral and adaptive loci determines individual fitness in a long-lived territorial bird 
There is compelling evidence about the manifest effects of inbreeding depression on individual fitness and populations' risk of extinction. The majority of studies addressing inbreeding depression on wild populations are generally based on indirect measures of inbreeding using neutral markers. However, the study of functional loci, such as genes of the major histocompatibility complex (MHC), is highly recommended. MHC genes constitute an essential component of the immune system of individuals, which is directly related to individual fitness and survival. In this study, we analyse heterozygosity fitness correlations of neutral and adaptive genetic variation (22 microsatellite loci and two loci of the MHC class II, respectively) with the age of recruitment and breeding success of a decimated and geographically isolated population of a long-lived territorial vulture. Our results indicate a negative correlation between neutral genetic diversity and age of recruitment, suggesting that inbreeding may be delaying reproduction. We also found a positive correlation between functional (MHC) genetic diversity and breeding success, together with a specific positive effect of the most frequent pair of cosegregating MHC alleles in the population. Globally, our findings demonstrate that genetic depauperation in small populations has a negative impact on the individual fitness, thus increasing the populations' extinction risk.
PMCID: PMC3385713  PMID: 22553093
MHC; heterozygosity–fitness correlation; inbreeding; breeding success; long-lived species; Egyptian vulture
7.  Need and Seek for Dietary Micronutrients: Endogenous Regulation, External Signalling and Food Sources of Carotenoids in New World Vultures 
PLoS ONE  2013;8(6):e65562.
Among birds, vultures show low concentrations of plasma carotenoids due to the combination of their large size, general dull colouration and a diet based on carrion. We recorded the concentration of each carotenoid type present in plasma of the Andean condor (Vultur gryphus) according to age and sex, that determine colour signalling and dominance hierarchies in the carcasses. We compared the carotenoid profile in wild condors with that of captive condors fed with a controlled diet of flesh to test the hypothesis that wild individuals could acquire extra carotenoids from vegetal matter contained in carcass viscera and fresh vegetation. Wild American black vultures (Coragyps atratus) were also sampled to evaluate the potential influence of colouration in the integument on absorption and accumulation patterns of plasma carotenoids. A remarkably higher concentration of lutein than β-carotene was found in wild condors, while the contrary pattern was recorded in American black vultures and captive condors. We found a consistent decrease in all plasma carotenoids with age, and a lower concentration of most xanthophylls in male compared to female wild condors. Positive correlations of all carotenoids indicated general common absorption and accumulation strategies or a single dietary source containing all pigments found in plasma. The comparatively low total concentration of carotenoids, and especially of lutein rather than β-carotene, found in captive condors fed with a diet restricted to flesh supports the hypothesis that Andean condors can efficiently acquire carotenoids from vegetal matter in the wild. Andean condors seem to be physiologically more competent in the uptake or accumulation of xanthophylls than American black vultures, which agrees with the use of colour-signalling strategies in sexual and competitive contexts in the Andean condor. This study suggests that vultures may use dietary vegetal supplements that provide pigments and micronutrients that are scarce or missing in carrion.
PMCID: PMC3681859  PMID: 23785435
8.  Uneven Large-Scale Movement Patterns in Wild and Reintroduced Pre-Adult Bearded Vultures: Conservation Implications 
PLoS ONE  2013;8(6):e65857.
After the quasi-extinction of much of the European vertebrate megafauna during the last few centuries, many reintroduction projects seek to restore decimated populations. However, the future of numerous species depends on the management scenarios of metapopulations where the flow of individuals can be critical to ensure their viability. This is the case of the bearded vulture Gypaetus barbatus, an Old World, large body-sized and long-lived scavenger living in mountain ranges. Although persecution in Western Europe restrained it to the Pyrenees, the species is nowadays present in other mountains thanks to reintroduction projects. We examined the movement patterns of pre-adult non-breeding individuals born in the wild population of the Pyrenees (n = 9) and in the reintroduced populations of the Alps (n = 24) and Andalusia (n = 13). Most birds were equipped with GPS-GSM radio transmitters, which allowed accurate determination of individual dispersal patterns. Two estimators were considered: i) step length (i.e., the distance travelled per day by each individual, calculated considering only successive days); and ii) total dispersal distance (i.e., the distance travelled between each mean daily location and the point of release). Both dispersal estimators showed a positive relationship with age but were also highly dependent on the source population, birds in Andalusia and Alps moving farther than in Pyrenees. Future research should confirm if differences in dispersal distances are the rule, in which case the dynamics of future populations would be strongly influenced. In summary, our findings highlight that inter-population differences can affect the flow of individuals among patches (a key aspect to ensure the viability of the European metapopulation of the endangered bearded vulture), and thus should be taken into account when planning reintroduction programs. This result also raises questions about whether similar scenarios may occur in other restoration projects of European megafauna.
PMCID: PMC3679195  PMID: 23776559
9.  Mast Pulses Shape Trophic Interactions between Fluctuating Rodent Populations in a Primeval Forest 
PLoS ONE  2012;7(12):e51267.
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.
PMCID: PMC3519590  PMID: 23251475
10.  Large-Scale Age-Dependent Skewed Sex Ratio in a Sexually Dimorphic Avian Scavenger 
PLoS ONE  2012;7(9):e46347.
Age-dependent skewed sex ratios have been observed in bird populations, with adult males generally outnumbering females. This trend is mainly driven by higher female mortality, sometimes associated with anthropogenic factors. Despite the large amount of work on bird sex ratios, research examining the spatial stability of adult sex ratios is extremely scarce. The Andean condor (Vultur gryphus) is the only bird of prey with strong sexual dimorphism favouring males (males are 30% heavier than females). By examining data from most of its South-American range, we show that while the juvenile sex ratio is balanced, or even female-skewed, the sex ratio becomes increasing male-skewed with age, with adult males outnumbering females by >20%, and, in some cases by four times more. This result is consistent across regions and independent of the nature of field data. Reasons for this are unknown but it can be hypothesized that the progressive disappearance of females may be associated with mortality caused by anthropogenic factors. This idea is supported by the asymmetric habitat use by the two sexes, with females scavenging in more humanized areas. Whatever the cause, male-skewed adult sex ratios imply that populations of this endangered scavenger face higher risks of extinction than previously believed.
PMCID: PMC3459903  PMID: 23029488
11.  Stress associated with group living in a long-lived bird 
Biology Letters  2011;7(4):608-610.
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.
PMCID: PMC3130225  PMID: 21307048
Białowieża forest; common raven; Corvus corax; glucocorticoids; parasites; sociality
12.  Misleading Population Estimates: Biases and Consistency of Visual Surveys and Matrix Modelling in the Endangered Bearded Vulture 
PLoS ONE  2011;6(10):e26784.
Conservation strategies for long-lived vertebrates require accurate estimates of parameters relative to the populations' size, numbers of non-breeding individuals (the “cryptic” fraction of the population) and the age structure. Frequently, visual survey techniques are used to make these estimates but the accuracy of these approaches is questionable, mainly because of the existence of numerous potential biases. Here we compare data on population trends and age structure in a bearded vulture (Gypaetus barbatus) population from visual surveys performed at supplementary feeding stations with data derived from population matrix-modelling approximations. Our results suggest that visual surveys overestimate the number of immature (<2 years old) birds, whereas subadults (3–5 y.o.) and adults (>6 y.o.) were underestimated in comparison with the predictions of a population model using a stable-age distribution. In addition, we found that visual surveys did not provide conclusive information on true variations in the size of the focal population. Our results suggest that although long-term studies (i.e. population matrix modelling based on capture-recapture procedures) are a more time-consuming method, they provide more reliable and robust estimates of population parameters needed in designing and applying conservation strategies. The findings shown here are likely transferable to the management and conservation of other long-lived vertebrate populations that share similar life-history traits and ecological requirements.
PMCID: PMC3198840  PMID: 22039550
13.  Spatial Heterogeneity in Resource Distribution Promotes Facultative Sociality in Two Trans-Saharan Migratory Birds 
PLoS ONE  2011;6(6):e21016.
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.
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.
PMCID: PMC3120827  PMID: 21731640
14.  The role of humans in the diversification of a threatened island raptor 
Anthropogenic habitat modifications have led to the extinction of many species and have favoured the expansion of others. Nonetheless, the possible role of humans as a diversifying force in vertebrate evolution has rarely been considered, especially for species with long generation times. We examine the influence that humans have had on the colonization and phenotypic and genetic differentiation of an insular population of a long-lived raptor species, the Egyptian vulture (Neophron percnopterus).
The morphological comparison between the Canarian Egyptian vultures and the main and closest population in Western Europe (Iberia) indicated that insular vultures are significantly heavier (16%) and larger (about 3%) than those from Iberia. Bayesian and standard genetic analyses also showed differentiation (FST = 0.11, p < 0.01). The inference of changes in the effective size of the Canarian deme, using two likelihood-based Bayesian approaches, suggested that the establishment of this insular population took place some 2500 years ago, matching the date of human colonization. This is consistent with the lack of earlier fossils.
Archaeological remains show that first colonizers were Berber people from northern Africa who imported goats. This new and abundant food source could have allowed vultures to colonize, expand and adapt to the island environment. Our results suggest that anthropogenic environmental change can induce diversification and that this process may take place on an ecological time scale (less than 200 generations), even in the case of a long-lived species.
PMCID: PMC3009672  PMID: 21144015
15.  Susceptibility to Infection and Immune Response in Insular and Continental Populations of Egyptian Vulture: Implications for Conservation 
PLoS ONE  2009;4(7):e6333.
A generalized decline in populations of Old World avian scavengers is occurring on a global scale. The main cause of the observed crisis in continental populations of these birds should be looked for in the interaction between two factors - changes in livestock management, including the increased use of pharmaceutical products, and disease. Insular vertebrates seem to be especially susceptible to diseases induced by the arrival of exotic pathogens, a process often favored by human activities, and sedentary and highly dense insular scavengers populations may be thus especially exposed to infection by such pathogens. Here, we compare pathogen prevalence and immune response in insular and continental populations of the globally endangered Egyptian vulture under similar livestock management scenarios, but with different ecological and evolutionary perspectives.
Methods/Principal Findings
Adult, immature, and fledgling vultures from the Canary Islands and the Iberian Peninsula were sampled to determine a) the prevalence of seven pathogen taxa and b) their immunocompetence, as measured by monitoring techniques (white blood cells counts and immunoglobulins). In the Canarian population, pathogen prevalence was higher and, in addition, an association among pathogens was apparent, contrary to the situation detected in continental populations. Despite that, insular fledglings showed lower leukocyte profiles than continental birds and Canarian fledglings infected by Chlamydophila psittaci showed poorer cellular immune response.
A combination of environmental and ecological factors may contribute to explain the high susceptibility to infection found in insular vultures. The scenario described here may be similar in other insular systems where populations of carrion-eaters are in strong decline and are seriously threatened. Higher susceptibility to infection may be a further factor contributing decisively to the extinction of island scavengers in the present context of global change and increasing numbers of emerging infectious diseases.
PMCID: PMC2709727  PMID: 19623256
16.  Testing the Goodness of Supplementary Feeding to Enhance Population Viability in an Endangered Vulture 
PLoS ONE  2008;3(12):e4084.
Human-predator conflicts are directly or indirectly threatening many species with extinction. Thus, biologists are urged to find simple solutions to complex situations while avoiding unforeseen conservation outcomes. The provision of supplementary food at artificial feeding sites (AFS) is frequently used in the conservation of scavenger bird populations currently suffering from indirect poisoning, although no scientific studies on its effectiveness have been conducted.
Methodology/Principal Findings
We used a long-term data set of 95 individually marked birds from the largest European core of the endangered bearded vulture (Gypaetus barbatus) to test the long-term effects of specific AFS for bearded vultures on their survival rates (by CMR models) and population dynamics (by Monte Carlo simulations) in an area where fatalities derived from illegal poisoning and the use of other toxics like veterinary drugs have increased over the last several years. Our data support the positive relationship between the use of AFS and survival. However, contrary to theoretical predictions (e.g. high and more stable adult survival among long-lived species), the use of AFS increased only survival of pre-adults. Moreover, AFS buffered the effects of illegal poisoning on this age-class, while adult survival decreased over years. Our simulations predicted a maximum value of extinction probability over a time horizon of 50 years. Population projections run with survival rates expected in scenarios without poisoning predicted the situation of least conservation concern, while including only AFS can maintain a large floater surplus that may delay population decline but fails to reduce poisoning risk among adults.
Although AFS are not effective to save bearded vultures from an expected population decline, they delay population extinction and can be a useful tool for prolonging population viability while combating illegal and indirect poisoning. The eradication of different sources of poisoning is of top priority to ensure the long-term viability of this and many other species.
PMCID: PMC2605265  PMID: 19115009
17.  Linking ecology, behaviour and conservation: does habitat saturation change the mating system of bearded vultures? 
Biology Letters  2006;2(4):624-627.
The social organization of a population is the consequence of the decisions made by individuals to maximize their fitness, so differences in social systems may arise from differences in ecological conditions. Here, we show how a long-lived species that used to breed monogamously, and at low densities, can change its mating system in response to habitat saturation. We found that a significant proportion of unpaired birds become potential breeders by entering high-quality territories, or by forming polyandrous trios as a strategy to increase their individual performance. However, productivity of territories was reduced when those occupied by breeding pairs changed to trios, suggesting that the third individual was costly. The decision of some individuals to enter into breeding trios as subordinates also had clear negative consequences to population demography. This unusual mating behaviour is thus compromising the conservation effort directed to this endangered species; management to encourage floaters to settle in other suitable but unoccupied areas may be beneficial.
PMCID: PMC1834000  PMID: 17148305
polyandry; raptors; population dynamics

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