Assessing the role of habitat, climate, and anthropization gradients on terrestrial mammal diversity in the western Mediterranean basin.

Mammal species globally exhibit distribution patterns conditioned by environmental conditions and human impact. The Mediterranean basin provides an ideal system to study these effects due to its diverse climate, and habitat conditions. In this work, we aim to assess the impact of landscape heterogeneity and anthropization degree on terrestrial mammal diversity in this region. Accordingly, we deployed over 300 camera traps across 28 sites for 3 months. Detected mammal species (weighing more than 1kg) were classified as domestic carnivores, domestic ungulates, wild carnivores, wild ungulates, lagomorphs, and large rodents. Alpha and beta diversity were calculated for each group and all wild mammals. Simple linear regressions and multimodal analysis were conducted between mammal diversities and climate, environmental conditions, landscape heterogeneity, and anthropization degree variables. Redundancy analyses were performed to identify variables and species determining the mammalian community composition. Indexes measuring landscape heterogeneity, anthropization degree, and its 30-year change did not correlate with mammal diversity. However, the difference in elevation within sites and domestic carnivore abundance showed a significant positive correlation with some of the diversity indexes. Nonetheless, rainfall and mean elevation factors generally showed the highest correlation with mammal diversity. Instead, a few influential species, including generalists and open-habitat specialists, highlighted the importance of conserving open areas, as well as the importance of the Pyrenees region as a key habitat for certain species. Therefore, climatic variables emerged as the key determinants of mammal diversity, highlighting climate change as a potential threat to mammal diversity in this area.

Age-Specific Demographic Response of a Long-Lived Scavenger Species to Reduction of Organic Matter in a Landfill.

Food availability shapes demographic parameters and population dynamics. Certain species have adapted to predictable anthropogenic food resources like landfills. However, abrupt shifts in food availability can negatively impact such populations. While changes in survival are expected, the age-related effects remain poorly understood, particularly in long-lived scavenger species. We investigated the age-specific demographic response of a Griffon vulture (Gyps fulvus) population to a reduction in organic matter in a landfill and analyzed apparent survival and the probability of transience after initial capture using a Bayesian Cormack-Jolly-Seber model on data from 2012-2022. The proportion of transients among newly captured immatures and adults increased after the reduction in food. Juvenile apparent survival declined, increased in immature residents, and decreased in adult residents. These results suggest that there was a greater likelihood of permanent emigration due to intensified intraspecific competition following the reduction in food. Interestingly, resident immatures showed the opposite trend, suggesting the persistence of high-quality individuals despite the food scarcity. Although the reasons behind the reduced apparent survival of resident adults in the final four years of the study remain unclear, non-natural mortality potentially plays a part. In Europe landfill closure regulations are being implemented and pose a threat to avian scavenger populations, which underlines the need for research on food scarcity scenarios and proper conservation measures.

Key Factors behind the Dynamic Stability of Pairs of Egyptian Vultures in Continental Spain.

Conservation science aims to identify the factors influencing the distribution of threatened species, thereby permitting the implementation of effective management strategies. This is key for long-lived species that require long-term monitoring such as the worldwide endangered Egyptian vulture (Neophron percnopterus). We studied temporal and spatial variations in the distribution of breeding pairs and examined the intrinsic and anthropic factors that may be influencing the abundance of breeding territories in continental Spain. Based on the census data of breeding pairs from 2000, 2008, and 2018, we used Rank Occupancy-Abundance Profiles to assess the temporal stability of the population and identified the spatial heterogeneity through a Local Index of Spatial Autocorrelation analysis. The GLMs showed that the abundance distribution was mainly influenced by the abundance of griffon vultures (Gyps fulvus) and cattle at a regional scale. Nonparametric comparisons showed that the presence of wind farms had a significant negative effect on local breeding pairs abundance, but that supplementary feeding stations and food resource-related variables had a positive impact. In light of these findings, we recommend a hierarchical approach in future conservation programs involving actions promoting regional-scale food resource availability and highlight the need to address the negative impact of wind farms at local levels.

Resource predictability modulates spatial-use networks in an endangered scavenger species.

BACKGROUND: Changes in human-induced resource availability can alter the behaviour of free-living species and affect their foraging strategies. The future European Landfill Waste Directive and Circular Economy Action Plan will reduce the number of predictable anthropogenic food subsidies (PAFS), above all, by closing landfills to preclude negative effects on human health. Obligate avian scavengers, the most threatened group of birds worldwide, are the most likely group of species that will be forced to change their behaviour and use of space in response to landfill site closures. Here, we examine the possible consequences of these management decisions on the foraging patterns of Egyptian vultures (Neophron percnopterus) in an expanding population in the Iberian Peninsula. METHODS: We tracked 16 individuals in 2018-2021, including breeders and non-breeders, and, using a combination of spatial-use and spatial-network modelling, assessed landscape connectivity between key resources based on movement patterns. We then carried out simulations of future scenarios based on the loss of PAFS to predict likely changes in the movement patterns of both non-breeders and breeders. RESULTS: Our results show that foraging strategies in non-breeders and breeders differ significantly: non-breeders performed more dispersal movements than breeding birds across a spatial-use network. Non-breeding and breeding networks were found to be vulnerable to the removal of central foraging areas containing landfill sites, a highly predictable resource, while perturbation analysis showed dissimilar foraging responses to the gradual reduction of other predictable resources. Under a context of the non-availability of landfills for breeders and non-breeders, vultures will increase their use of extensive livestock as a trophic resource. CONCLUSIONS: Future environmental policies should thus extend the areas used by scavengers in which livestock carcasses are allowed to remain in the wild, a strategy that will also mitigate the lack of food caused by any reduction in available waste if landfills close. In general, our results emphasize the capabilities of a spatial network approaches to address questions on movement ecology. They can be used to infer the behavioural response of animal species and, also demonstrate the importance of applying such approaches to endangered species conservation within a context of changing humanized scenarios.

Joint estimation of survival and dispersal effectively corrects the permanent emigration bias in mark-recapture analyses.

Robust and reliable estimates of demographic parameters are essential to understand population dynamics. Natal dispersal is a common process in monitored populations and can cause underestimations of survival and dispersal due to permanent emigration. Here, we present a multistate Bayesian capture-mark-recapture approach based on a joint estimation of natal dispersal kernel and detection probabilities to address biases in survival, dispersal, and related demographic parameters when dispersal information is limited. We implement this approach to long-term data of a threatened population: the Bonelli's eagle in Catalonia (SW Europe). To assess the method's performance, we compare demographic estimates structured by sex, age, and breeding status in cases of limited versus large data scales, with those of classical models where dispersal and detection probabilities are estimated separately. Results show substantial corrections of demographic estimates. Natal dispersal and permanent emigration probabilities were larger in females, and consequently, female non-breeder survival showed larger differences between separate and joint estimation models. Moreover, our results suggest that estimates are sensitive to the choice of the dispersal kernel, fat-tailed kernels providing larger values in cases of data limitation. This study provides a general multistate framework to model demographic parameters while correcting permanent emigration biases caused by natal dispersal.

A comprehensive but practical methodology for selecting biological indicators for long-term monitoring.

The selection of the many biological indicators described in scientific literature is rarely based on systematic or clear-cut processes, and often takes into account only a single or very few taxa, or even disregards the complex interactions that exist between the components of biodiversity. In certain cases, the particular context of a site-for example in the Mediterranean Basin-makes it difficult to apply the choice of indicators to other regions proposed in the literature. Therefore, the selection of appropriate methodologies for generating relevant indicators for a particular site is of crucial importance. Here, we present a simple quantitative methodology capable of incorporating multidisciplinary information for assessing and selecting appropriate methods and indicators for monitoring local biodiversity. The methodology combines several ecological levels (species, habitats, processes, and ecosystem disturbances), and embraces biological interactions and common functional guilds (detritivores, producers, herbivores, and carnivores). We followed an iterative selection procedure consisting of five phases: 1) collection focal area useful information; 2) classification of this information into interrelated datasets; 3) assessment and selection of the relevant components using a quantitative relevance index; 4) the adding of taxonomic, physiognomic and functional similarities to the relevant components; and 5) the quantitative selection of the priority indicators in the study area. To demonstrate the potential of this methodology, we took as a case study the biodiversity components and their ecological interactions present in a protected area. We show that our methodology can help select appropriate local and long-term indicators, reduce the number of components required for thorough biodiversity monitoring, and underline the importance of ecological processes.

Accumulation of pollutants in nestlings of an endangered avian scavenger related to territory urbanization and physiological biomarkers.

We monitor pollutant accumulation and investigate associated changes at the physiological level within the population of an obligate avian scavenger, the Egyptian Vulture (Neophron percnopterus), from Catalonia (NE Spain). This population is expanding its range, presumably because of the use of human waste disposal sites as food resource. We hypothesized that habitat urbanization, presumably associated with feeding from human wastes, could influence the accumulation of persistent organic pollutants and metals. The aim of this study was to explore the relationship between accumulated pollutants and biochemical parameters in nestling blood. We used the proportion of urban surface within an 8 km radius of each nest as a proxy to study the relationship between anthropic influence and pollutant accumulation. Observed blood levels of metals, organochlorine pesticides, polychlorinated biphenyls (PCBs), per- and polyfluoroalkylated substances (PFAS) and polybrominated diphenyl ethers (PBDEs) were relatively low, as expected for nestling individuals due to short-term exposures. CB-180 and PBDEs were associated with variations in blood biochemistry parameters; hexa-BDEs appeared positively associated with activities of the enzymes aspartate aminotransferase and lactate dehydrogenase, whereas CB-180 accumulation was associated with an increased activity of creatine phosphokinase and elevated glutathione levels. Increased CB-180 levels were also related to decreased blood concentrations of calcium, cholesterol, α-tocopherol and lutein. A proportion of urban surfaces as low as 6.56% within a radius of 8 km around the nest appears related to the accumulation of CB-180, the majority of analysed PFAS and of PBDE congeners 99 and 209, and increased urbanization was also associated with decreased plasma levels of α-tocopherol and carotenoids. These associations suggest that changes in blood profiles of vitamins, carotenoids or other analytes, despite related to increased plasma levels of CB-180, would be consequence of exploitation of artificial food sources rather than of a direct effect of the pollutants.

Domestic waste disposal sites secure food availability but diminish plasma antioxidants in Egyptian vulture.

Some domestic waste disposal sites (DWDS) accumulate enormous amounts of food that humans discard. This food resource is exploited by different species whose population dynamics have as a result been altered. The effects of feeding on human waste on individual health parameters such as body condition are still unknown. Traditionally, body condition in wildlife has been assessed using morphological indices based on size and weight. Expanding the range of indices to include the analysis of indicators at the physiological level can provide a more comprehensive picture of the animals' health status. In this work, we studied how different amounts of waste consumption (assessed using stable isotope analysis) affect nestling health and body condition in an expanding population of the endangered Egyptian Vulture (Neophron percnopterus). We used morphometric and physiological approaches, including plasma biochemistry, antioxidant defences and oxidative stress biomarkers. The results of the multivariate redundancy analysis and variance partitioning showed that the proportion of diet originating from DWDS is the main factor explaining physiological indicators in the studied vulture population. Nestlings that were fed on food from DWDS had lower levels of vitamins (e.g. α-tocopherol) and carotenoids (zeaxanthin and lutein), which have important functions as antioxidant defences, immunostimulant properties and ornamental purposes. Nevertheless, nestlings that were fed on food from DWDS were better nourished and experienced fewer food shortages than individuals not fed using this resource, which had lower levels of cholesterol. Possibly due to the easy access to food, breeding pairs using DWDS could have fewer difficulties in feeding their nestlings and thus could engender more regular brood sizes than those not exploiting this type of resource. Our integrative approach using diverse components was crucial for a reliable assessment of health and body condition in Egyptian Vulture nestlings and its relationship to the consumption of food derived from human-altered environments.

Effects of rearing conditions on natal dispersal processes in a long-lived predator bird.

Natal or prebreeding dispersal is a key driver of the functioning, dynamics, and evolution of populations. Conditions experienced by individuals during development, that is, rearing conditions, may have serious consequences for the multiple components that shape natal dispersal processes. Rearing conditions vary as a result of differences in parental and environmental quality, and it has been shown that favorable rearing conditions are beneficial for individuals throughout their lives. However, the long-term consequences of rearing conditions on natal dispersal are still not fully understood in long-lived birds. In this study, we aim to test the following hypotheses to address the relationship between rearing conditions and certain components of the natal dispersal process in Bonelli's eagle (Aquila fasciata): (1) The body condition of nestlings depends on the quality of the territory and/or breeders; and (2) the survival until recruitment, (3) the age of recruitment, and (4) the natal dispersal distance (NDD) all depend on rearing conditions. As expected, nestlings reared in territories with high past productivity of chicks had better body condition, which indicates that both body condition and past productivity reflect the rearing conditions under which chicks are raised. In addition, chicks raised in territories with high past productivity and with good body condition had greater chances of surviving until recruitment. Furthermore, birds that have better condition recruit earlier, and males recruit at a younger age than females. At last, although females in good body condition exhibited higher NDD when they recruited at younger ages, this pattern was not observed in either older females or males. Overall, this study provides evidence that rearing conditions have important long-term consequences in long-lived birds. On the basis of our results, we advocate that conservation managers work actively in the promotion of actions aimed at improving the rearing conditions under which individuals develop in threatened populations.

Assessing the applicability of stable isotope analysis to determine the contribution of landfills to vultures' diet.

Human activities cause changes to occur in the environment that affect resource availability for wildlife. The increase in the human population of cities has led to a rise in the amount of waste deposited in landfills, installations that have become a new food resource for both pest and threatened species such as vultures. In this study we used stable isotope analysis (SIA) and conventional identification of food remains from Egyptian Vultures (Neophron percnopterus) to assess the applicability of SIA as a new tool for determining the composition of the diets of vultures, a group of avian scavengers that is threatened worldwide. We focused on an expanding Egyptian Vulture population in NE Iberian Peninsula to determine the part played by landfills and livestock in the diet of these species, and aimed to reduce the biases associated with conventional ways of identifying food remains. We compared proportions of diet composition obtained with isotope mixing models and conventional analysis for five main prey. The greatest agreement between the two methods was in the categories 'landfills' and 'birds' and the greatest differences between the results from the two methods were in the categories 'livestock', 'carnivores' and 'wild herbivores'. Despite uncertainty associated to SIA, our results showed that stable isotope analysis can help to distinguish between animals that rely on waste and so present enriched levels of δ 13C than those that feed on the countryside. Indeed, a high proportion of food derived from landfills (nearly 50%) was detected in some breeding pairs. Furthermore we performed GLMM analyses that showed that high values of δ 13C in Egyptian Vulture feathers (a proxy of feeding in landfills) are related with high levels of humanization of territories. This method has the potential to be applied to other threatened vulture species for which there is a lack of information regarding resources they are consuming, being especially important as the main causes of vultures decline worldwide are related to the consumption and availability of food resources.

The role of conservative versus innovative nesting behavior on the 25-year population expansion of an avian predator.

Species ranges often change in relation to multiple environmental and demographic factors. Innovative behaviors may affect these changes by facilitating the use of novel habitats, although this idea has been little explored. Here, we investigate the importance of behavior during range change, using a 25-year population expansion of Bonelli's eagle in southern Portugal. This unique population is almost exclusively tree nesting, while all other populations in western Europe are predominantly cliff nesting. During 1991-2014, we surveyed nest sites and estimated the year when each breeding territory was established. We approximated the boundaries of 84 territories using Dirichlet tessellation and mapped topography, land cover, and the density of human infrastructures in buffers (250, 500, and 1,000 m) around nest and random sites. We then compared environmental conditions at matching nest and random sites within territories using conditional logistic regression, and used quantile regression to estimate trends in nesting habitats in relation to the year of territory establishment. Most nests (>85%, n = 197) were in eucalypts, maritime pines, and cork oaks. Nest sites were farther from the nests of neighboring territories than random points, and they were in areas with higher terrain roughness, lower cover by agricultural and built-up areas, and lower road and powerline densities. Nesting habitat selection varied little with year of territory establishment, although nesting in eucalypts increased, while cliff nesting and cork oak nesting, and terrain roughness declined. Our results suggest that the observed expansion of Bonelli's eagles was facilitated by the tree nesting behavior, which allowed the colonization of areas without cliffs. However, all but a very few breeding pairs settled in habitats comparable to those of the initial population nucleus, suggesting that after an initial trigger possibly facilitated by tree nesting, the habitat selection remained largely conservative. Overall, our study supports recent calls to incorporate information on behavior for understanding and predicting species range shifts.

The influence of diet on nestling body condition of an apex predator: a multi-biomarker approach.

Animal body condition refers to the health and physiological state of individuals, and multiple parameters have been proposed to quantify this key concept. Food intake is one of the main determinants of individual body condition and much debate has been generated on how diet relates to body condition. We investigated this relationship in free-living Bonelli's eagle (Aquila fasciata) nestlings sampled at two geographically distant populations in Spain. Nestlings' main prey consumption was estimated by isotopic analyses. A multi-biomarker approach, including morphometric and blood biochemical measures (i.e. hematocrit, plasma biochemistry and oxidative stress biomarkers), enabled us to integrate all the body condition measures taken. A greater consumption of a preferred prey [i.e. the European rabbit (Oryctolagus cuniculus)] improved nestling body condition, as indicated by lower levels of cholesterol in plasma, greater activity of enzymes mediating in protein catabolism, higher levels of tocopherol and glutathione, and less glutathione peroxidase activity, which also suggested lower degree of oxidative stress. On the other hand, increased diet diversity was positively correlated with higher levels of oxidized glutathione, which suggests that these nestlings had poorer body condition than those with a higher frequency of preferred prey consumption. Several factors other than diet [i.e. altitude of nesting areas, nestling sex and age, sampling time (before or after midday) and recent food ingestion] had an effect on certain body condition measures. Our study reveals a measurable effect of diet on a predator's body condition and demonstrates the importance of considering the potential influence of multiple intrinsic and extrinsic factors when assessing animal body condition.

Pollutant accumulation patterns in nestlings of an avian top predator: biochemical and metabolic effects.

The exposure to persistent pollutants such as organochlorine compounds (OCs) or metals has been associated with declines in top predator populations, which can accumulate high amounts of these pollutants from their prey. However, understanding how variation in OC and metal accumulation in wild species affects their biochemical and physiological responses is a big challenge, especially for endangered predators like the Bonelli's eagle (Aquila fasciata). This bird of prey is an interesting study model because the differences in diet composition among populations and territories can account for important pollutant uptake variations. We compared OC and metal accumulation in blood of Bonelli's eagle nestlings from three populations across Spain as a function of origin, age class (nestlings vs. adults), sex and number of siblings per nest, and related accumulation patterns to responses indicative of body condition, biochemistry and antioxidant status. Nestlings from Catalonia, the most industrialized area, showed the highest concentrations of PCBs and arsenic, and the lowest concentrations of zinc. The two former substances, together with DDTs, exerted an overall influence on nestling's physiology. PCBs and arsenic were associated with reduced retinol levels, pointing to oxidative damage in exposed individuals, which was also consistent with the low zinc levels in individuals from the polluted region. Increased plasma DDT levels were related to reduced body condition and lower levels of triglycerides. Mercury accumulation in Castile and Leon was higher in nestlings that were alone in the nest than in nestlings that shared it with a sibling; this suggests an increased mercury uptake from secondary prey in territories where preferred prey (i.e. rabbits) are scarce, which are also the territories where productivity is reduced. Overall, the results reveal a spatial variation in pollutant accumulation patterns and associated physiological effects, and suggest the major role that territory quality may have in such patterns.

Multi-scale effects of nestling diet on breeding performance in a terrestrial top predator inferred from stable isotope analysis.

Inter-individual diet variation within populations is likely to have important ecological and evolutionary implications. The diet-fitness relationships at the individual level and the emerging population processes are, however, poorly understood for most avian predators inhabiting complex terrestrial ecosystems. In this study, we use an isotopic approach to assess the trophic ecology of nestlings in a long-lived raptor, the Bonelli's eagle Aquila fasciata, and investigate whether nestling dietary breath and main prey consumption can affect the species' reproductive performance at two spatial scales: territories within populations and populations over a large geographic area. At the territory level, those breeding pairs whose nestlings consumed similar diets to the overall population (i.e. moderate consumption of preferred prey, but complemented by alternative prey categories) or those disproportionally consuming preferred prey were more likely to fledge two chicks. An increase in the diet diversity, however, related negatively with productivity. The age and replacements of breeding pair members had also an influence on productivity, with more fledglings associated to adult pairs with few replacements, as expected in long-lived species. At the population level, mean productivity was higher in those population-years with lower dietary breadth and higher diet similarity among territories, which was related to an overall higher consumption of preferred prey. Thus, we revealed a correspondence in diet-fitness relationships at two spatial scales: territories and populations. We suggest that stable isotope analyses may be a powerful tool to monitor the diet of terrestrial avian predators on large spatio-temporal scales, which could serve to detect potential changes in the availability of those prey on which predators depend for breeding. We encourage ecologists and evolutionary and conservation biologists concerned with the multi-scale fitness consequences of inter-individual variation in resource use to employ similar stable isotope-based approaches, which can be successfully applied to complex ecosystems such as the Mediterranean.

Changes in intrapopulation resource use patterns of an endangered raptor in response to a disease-mediated crash in prey abundance.

1. A long-standing question in ecology is how natural populations respond to a changing environment. Emergent optimal foraging theory-based models for individual variation go beyond the population level and predict how its individuals would respond to disturbances that produce changes in resource availability. 2. Evaluating variations in resource use patterns at the intrapopulation level in wild populations under changing environmental conditions would allow to further advance in the research on foraging ecology and evolution by gaining a better idea of the underlying mechanisms explaining trophic diversity. 3. In this study, we use a large spatio-temporal scale data set (western continental Europe, 1968-2006) on the diet of Bonelli's Eagle Aquila fasciata breeding pairs to analyse the predator trophic responses at the intrapopulation level to a prey population crash. In particular, we borrow metrics from studies on network structure and intrapopulation variation to understand how an emerging infectious disease [the rabbit haemorrhagic disease (RHD)] that caused the density of the eagle's primary prey (rabbit Oryctolagus cuniculus) to dramatically drop across Europe impacted on resource use patterns of this endangered raptor. 4. Following the major RHD outbreak, substantial changes in Bonelli's Eagle's diet diversity and organisation patterns at the intrapopulation level took place. Dietary variation among breeding pairs was larger after than before the outbreak. Before RHD, there were no clusters of pairs with similar diets, but significant clustering emerged after RHD. Moreover, diets at the pair level presented a nested pattern before RHD, but not after. 5. Here, we reveal how intrapopulation patterns of resource use can quantitatively and qualitatively vary, given drastic changes in resource availability. 6. For the first time, we show that a pathogen of a prey species can indirectly impact the intrapopulation patterns of resource use of an endangered predator.