Limited sexual segregation in a dimorphic avian scavenger, the Andean condor.

Sexual segregation is widely reported among sexually dimorphic species and generally attributed to intraspecific competition. Prey diversity and human activities can reinforce niche segregation by increasing resource heterogeneity. Here, we explored trophic and spatial sexual segregation in the only avian scavenger that exhibits pronounced sexual size dimorphism (up to 50% difference in body mass) and a highly despotic social system, the Andean condor (Vultur gryphus). We predicted that larger and dominant males would exclude smaller and subordinate females from high-quality resources, leading to sexual segregation particularly in human-dominated landscapes showing increased prey diversity. We compared resource use between females and males across six sites in Argentina featuring a range of prey diversity via stable isotopes analysis of molted feathers (n = 141 individuals). We then focused on two sites featuring contrasting levels of prey diversity and quantified assimilated diet via stable isotopes and space use via GPS monitoring (n = 23 and 12 tagged individuals). We found no clear differences in isotopic niche space, individual variation in isotopic signature, or assimilated diet between females and males. However, there were differences in foraging locations between sexes, with females apparently using areas of fewer food resources more frequently than males. Local conditions defined the dynamics of fine-scale sexual differences in foraging sites; yet, unpredictable and ephemeral carrion resources likely prevent segregation by sexes at the landscape scale. Our study highlights complex dynamics of sexual segregation in vultures and the relevancy of analyses under multiple spatial-temporal scales to explore segregation in social species.

Rethinking megafauna.

Concern for megafauna is increasing among scientists and non-scientists. Many studies have emphasized that megafauna play prominent ecological roles and provide important ecosystem services to humanity. But, what precisely are 'megafauna'? Here, we critically assess the concept of megafauna and propose a goal-oriented framework for megafaunal research. First, we review definitions of megafauna and analyse associated terminology in the scientific literature. Second, we conduct a survey among ecologists and palaeontologists to assess the species traits used to identify and define megafauna. Our review indicates that definitions are highly dependent on the study ecosystem and research question, and primarily rely on ad hoc size-related criteria. Our survey suggests that body size is crucial, but not necessarily sufficient, for addressing the different applications of the term megafauna. Thus, after discussing the pros and cons of existing definitions, we propose an additional approach by defining two function-oriented megafaunal concepts: 'keystone megafauna' and 'functional megafauna', with its variant 'apex megafauna'. Assessing megafauna from a functional perspective could challenge the perception that there may not be a unifying definition of megafauna that can be applied to all eco-evolutionary narratives. In addition, using functional definitions of megafauna could be especially conducive to cross-disciplinary understanding and cooperation, improvement of conservation policy and practice, and strengthening of public perception. As megafaunal research advances, we encourage scientists to unambiguously define how they use the term 'megafauna' and to present the logic underpinning their definition.

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

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.

Scavenging in the Anthropocene: Human impact drives vertebrate scavenger species richness at a global scale.

Understanding the distribution of biodiversity across the Earth is one of the most challenging questions in biology. Much research has been directed at explaining the species latitudinal pattern showing that communities are richer in tropical areas; however, despite decades of research, a general consensus has not yet emerged. In addition, global biodiversity patterns are being rapidly altered by human activities. Here, we aim to describe large-scale patterns of species richness and diversity in terrestrial vertebrate scavenger (carrion-consuming) assemblages, which provide key ecosystem functions and services. We used a worldwide dataset comprising 43 sites, where vertebrate scavenger assemblages were identified using 2,485 carcasses monitored between 1991 and 2018. First, we evaluated how scavenger richness (number of species) and diversity (Shannon diversity index) varied among seasons (cold vs. warm, wet vs. dry). Then, we studied the potential effects of human impact and a set of macroecological variables related to climatic conditions on the scavenger assemblages. Vertebrate scavenger richness ranged from species-poor to species rich assemblages (4-30 species). Both scavenger richness and diversity also showed some seasonal variation. However, in general, climatic variables did not drive latitudinal patterns, as scavenger richness and diversity were not affected by temperature or rainfall. Rainfall seasonality slightly increased the number of species in the community, but its effect was weak. Instead, the human impact index included in our study was the main predictor of scavenger richness. Scavenger assemblages in highly human-impacted areas sustained the smallest number of scavenger species, suggesting human activity may be overriding other macroecological processes in shaping scavenger communities. Our results highlight the effect of human impact at a global scale. As species-rich assemblages tend to be more functional, we warn about possible reductions in ecosystem functions and the services provided by scavengers in human-dominated landscapes in the Anthropocene.

Tracking data and retrospective analyses of diet reveal the consequences of loss of marine subsidies for an obligate scavenger, the Andean condor.

Over the last century, marine mammals have been dramatically reduced in the world's oceans. We examined evidence that this change caused dietary and foraging pattern shifts of the Andean condor (Vultur gryphus) in Patagonia. We hypothesized that, after the decrease in marine mammals and the increase in human use of coastlines, condor diet changed to a more terrestrial diet, which in turn influenced their foraging patterns. We evaluated the diet by means of stable isotope analysis (δ13C, δ15N and δ34S) of current (last decade) and historical (1841-1933) feathers. We further evaluated the movement patterns of 23 condors using satellite tracking of individuals. Condors reduced their use of marine-derived prey in recent compared with historical times from 33 ± 13% to less than 8 ± 3% respectively; however, they still breed close to the coast. The average distance between the coast and nests was 62.5 km, but some nests were located close to the sea (less than 5 km). Therefore, some birds must travel up to 86 km from nesting sites, crossing over the mountain range to find food. The worldwide reduction in marine mammal carcasses, especially whales, may have major consequences on the foraging ecology of scavengers, as well as on the flux of marine inputs within terrestrial ecosystems.

The value of transhumance for biodiversity conservation: Vulture foraging in relation to livestock movements.

In recent decades, intensive techniques of livestock raising have flourished, which has largely replaced traditional farming practices such as transhumance. These changes may have affected scavengers' behaviour and ecology, as extensive livestock is a key source of carrion. This study evaluates the spatial responses of avian scavengers to the seasonal movements of transhumant herds in south-eastern Spain. We surveyed the abundance of avian scavengers and ungulates, and analysed the factors affecting the space use by 30 GPS-tracked griffon vultures (Gyps fulvus). Griffons' foraging activity increased in the pasturelands occupied by transhumant herds, which implied greater vulture abundance at the landscape level during the livestock season. In contrast, facultative scavengers were more abundant without transhumant livestock herds, and the abundance of wild ungulates did not change in relation to livestock presence. We conclude that fostering transhumance and other traditional farming systems, to the detriment of farming intensification, could favour vulture conservation.

Major histocompatibility complex variation in insular populations of the Egyptian vulture: inferences about the roles of genetic drift and selection.

Insular populations have attracted the attention of evolutionary biologists because of their morphological and ecological peculiarities with respect to their mainland counterparts. Founder effects and genetic drift are known to distribute neutral genetic variability in these demes. However, elucidating whether these evolutionary forces have also shaped adaptive variation is crucial to evaluate the real impact of reduced genetic variation in small populations. Genes of the major histocompatibility complex (MHC) are classical examples of evolutionarily relevant loci because of their well-known role in pathogen confrontation and clearance. In this study, we aim to disentangle the partial roles of genetic drift and natural selection in the spatial distribution of MHC variation in insular populations. To this end, we integrate the study of neutral (22 microsatellites and one mtDNA locus) and MHC class II variation in one mainland (Iberia) and two insular populations (Fuerteventura and Menorca) of the endangered Egyptian vulture (Neophron percnopterus). Overall, the distribution of the frequencies of individual MHC alleles (n=17 alleles from two class II B loci) does not significantly depart from neutral expectations, which indicates a prominent role for genetic drift over selection. However, our results point towards an interesting co-evolution of gene duplicates that maintains different pairs of divergent alleles in strong linkage disequilibrium on islands. We hypothesize that the co-evolution of genes may counteract the loss of genetic diversity in insular demes, maximize antigen recognition capabilities when gene diversity is reduced, and promote the co-segregation of the most efficient allele combinations to cope with local pathogen communities.

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.

Disentangling drivers of power line use by vultures: Potential to reduce electrocutions.

Accidents on power lines are the leading cause of mortality for many raptor species. In order to prioritise corrective measures, much effort has been focused on identifying the factors associated with collision and electrocution risk. However, most studies lack of precise data about the use of pylons and its underlying driving factors, often relying on biased information based on recorded fatalities. Here, we used multiple years of high-resolution data from 49-GPS tagged Canarian Egyptian Vultures (Neophron percnopterus majorensis) to overcome these typical biases. Birds of our target population use electric pylons extensively for perching (diurnal) and roosting (nocturnal), so accidents with these infrastructures are nowadays the main cause of mortality. Predictive models of pylon intensity of use were fitted for diurnal and nocturnal behaviour, accounting for power line, environmental, and individual vulture's features. Using these measures as a proxy for mortality risk, our model predictions were validated with out-of-sample data of actual mortality recorded during 17 years. Vultures used more pylons during daytime, but those chosen at night were used more intensively. In both time periods, the intensity of use of pylons was determined by similar drivers: vultures avoided pylons close to roads and territories of conspecifics, preferentially used pylons located in areas with higher abundance of food resources, and spread their use during the breeding season. Individuals used pylons unevenly according to their sex, age, and territorial status, indicating that site-specific mitigation measures may affect different fractions of the population. Our modelling procedures predicted actual mortality reasonably well, showing that prioritising mitigation measures on relatively few pylons (6%) could drastically reduce accidents (50%). Our findings demonstrate that combining knowledge on fine-scale individual behaviour and pylon type and distribution is key to target cost-effective conservation actions aimed at effectively reducing avian mortality on power lines.

Functional traits driving species role in the structure of terrestrial vertebrate scavenger networks.

Species assemblages often have a non-random nested organization, which in vertebrate scavenger (carrion-consuming) assemblages is thought to be driven by facilitation in competitive environments. However, not all scavenger species play the same role in maintaining assemblage structure, as some species are obligate scavengers (i.e., vultures) and others are facultative, scavenging opportunistically. We used a database with 177 vertebrate scavenger species from 53 assemblages in 22 countries across five continents to identify which functional traits of scavenger species are key to maintaining the scavenging network structure. We used network analyses to relate ten traits hypothesized to affect assemblage structure with the "role" of each species in the scavenging assemblage in which it appeared. We characterized the role of a species in terms of both the proportion of monitored carcasses on which that species scavenged, or scavenging breadth (i.e., the species "normalized degree"), and the role of that species in the nested structure of the assemblage (i.e., the species "paired nested degree"), therefore identifying possible facilitative interactions among species. We found that species with high olfactory acuity, social foragers, and obligate scavengers had the widest scavenging breadth. We also found that social foragers had a large paired nested degree in scavenger assemblages, probably because their presence is easier to detect by other species to signal carcass occurrence. Our study highlights differences in the functional roles of scavenger species and can be used to identify key species for targeted conservation to maintain the ecological function of scavenger assemblages.

Vultures and Livestock: The Where, When, and Why of Visits to Farms.

Recent changes in European legislation have legalized the abandonment of carcasses around livestock farms, but our understanding of how vultures exploit these semi-predictable food sources is still very limited. For filling this gap, we determine the individual and ecological drivers influencing vulture visits to farms. We assessed the effects of individual characteristics of both birds and farms on the frequency of vultures' visits to livestock facilities using data collected from 45 GPS-tagged Egyptian Vultures (Neophron percnopterus) and 318 farms (>94% of livestock) on Fuerteventura Island, Spain. Farms were more visited during the vultures' breeding season. Farms located closer to highly predictable feeding places (i.e., vulture restaurants and garbage dumps) or with more available feeding resources were visited by more vultures, whereas those located close to roads and vultures' breeding territories received fewer visits. Younger territorial birds visited a farm more frequently than older territorial ones, whereas older non-territorial individuals concentrated those visits on farms closer to their activity core areas compared with younger ones. Our findings indicate that visits to farms were determined by their spatial distribution in relation to the age-specific birds' activity centers, the availability of carcasses, seasonality, and individual characteristics of vultures. These interacting factors should be considered in vulture conservation, avoiding very general solutions that ignore population structure.

Plasma carotenoids and immunity in a despotic avian scavenger.

Carotenoids are pigmented compounds acquired through diet that have important functions as antioxidants and immune modulators. We studied the association between immunity and circulating carotenoids in Andean condors (Vultur gryphus). We evaluated the relationship between α-, ß-, and γ-globulin blood concentrations and different circulating carotenoids in two groups of Andean condors that differ in their mean health status, rehabilitating (suffering different pathologies), and wild individuals (trapped when displaying their physiological behavior). In rehabilitating individuals, α-, ß-, and γ-globulin concentrations were higher than in wild individuals. This shows that rehabilitating individuals were developing an immune response associated with the pathologies that they were suffering at the time of sampling. In addition, circulating carotenoids were lower in rehabilitating than in wild individuals. We found negative correlations between α-, ß-, and γ-globulins and different circulating carotenoids in rehabilitating individuals, but not in wild condors. Xanthophylls were strongly related to α-, ß-, and γ-globulin blood concentrations in rehabilitating, but not in wild condors. Our results suggest that there is a potential relationship between circulating carotenoids and immunity in the Andean condor. Given that this species may display a carotenoid-based pigmentation, our results could suggest that a trade-off between the immune system and external coloration could operate in this species, which may have implications in their access to food resources and mate selection and, thus, in their conservation.

Probing into farmers' perceptions of a globally endangered ecosystem service provider.

Society's perception of ecosystem services is a key issue in conservation, particularly for endangered species providing services linked to human activities. Misperceptions may lead to wildlife-human conflicts with the risk of disappearance of the species involved. We contrasted farmers' perceptions with highly accurate quantitative data of an endangered vulture species, which provide ecosystem services. We combined surveys of 59 farmers with data from 48 GPS-tagged Canarian Egyptian vultures (Neophron percnopterus majorensis endemic to the Spanish Canary Islands) to disentangle factors influencing consistency between farmers' awareness of vulture occurrence on their properties and vulture behavior. Egyptian vultures were perceived as the main providers of scavenging services and the most beneficial avian scavenger. Consistency between farmers' perceptions (surveys) and vulture use of their farms (GPS data) was higher in the morning, in older males, and at farms with lower livestock numbers, located near vulture communal roosts, and visited more frequently by vultures. Our results underline the potential influence of modern livestock husbandry in disconnecting people from ecosystems, and how appreciation could be even lower for scarce or threatened ecosystem service providers.

Shepherds' local knowledge and scientific data on the scavenging ecosystem service: Insights for conservation.

Integrating indigenous and local knowledge (ILK) and scientific knowledge (SK) in the evaluation of ecosystem services has been recommended by the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. We examined the similarities and contradictions between shepherds' ILK and SK on the scavenging service provided by vertebrates in Spain. We conducted 73 face-to-face surveys with shepherds to evaluate their ILK. We collected scientific information on 20 scavenger species by monitoring the consumption of 45 livestock carcasses with camera traps. We found a high consistency between ILK and SK regarding the provision of the scavenging service by vertebrates, which was also consistent over the range of shepherd ages and experience. Our findings support the importance of ILK held by shepherds to better understand and to collect information on the scavenging service, particularly at the species level. The integration of ILK and SK into the management strategies of scavengers can benefit the conservation of globally endangered scavengers and the ecosystem services they provide.

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

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.