Bridging Evolutionary History and Conservation of New World Vultures.

The New World Vultures (Cathartidae) include seven species of obligate scavengers that, despite their ecological relevance, present critical information gaps around their evolutionary history and conservation. Insights into their phylogenetic relationships in recent years has enabled the addressing of such information gaps through approaches based on phylogeny. We reconstructed the ancestral area in America of the current species using two regionalization schemes and methods: Biogeography with Bayesian Evolutionary Analysis (BioGeoBears) and Bayesian Binary Model-Monte Carlo Markov Chains (BBM-MCMC). Then, we identified the priority species and areas for conservation by means of the Evolutionary Distinctiveness index (ED), as a proxy of the uniqueness of species according to phylogeny, and the Global Endangerment index (GE), mapping phylogenetic diversity. We found that the ancestral area of New World Vultures in America corresponds to South America, with dispersal processes that led to a recolonization of North America by Coragyps atratus, Gymnogyps californianus and Cathartes aura. We identified the Black Vulture, G. californianus and Vultur gryphus as priority species based on ED and "Evolutionary Distinct Globally Endangered" (EDGE) indexes, and the lowlands of Amazon River basin and the Orinoco basin and some tributaries areas of the Guiana Shield were identified as the priority areas when mapping the phylogenetic diversity. This study highlights the importance of filling knowledge gaps of species of conservation concern through the integration of evolutionary and ecological information and tools and, thus, developing adequate strategies to enhance the preservation of these species in the face of the current loss of biodiversity.

Non-Invasive Sex Determination of Nestlings and Adult Bonelli's Eagles Using Morphometrics.

Biometric analysis allows the sexing of most vertebrates, particularly birds. Birds of prey, and, especially, the Bonelli's eagle (Aquila fasciata), show reverse sexual dimorphism (i.e., females are usually larger than males). In contrast to blood sampling, the use of morphometrics allows sex determination using a non-invasive method, and, therefore, it facilitates fieldwork. By means of a linear discriminant analysis of biometric variables, we obtained different equations that allow the sexing of nestlings and adult Bonelli's eagles. We sampled 137 Bonelli's eagles, 82 nestlings and 55 adults in eastern Spain during the period 2015-2022. The sexes obtained after linear discriminant analysis were compared with their molecular sexing. The validation procedure of the linear discriminant equations facilitated the reduction of the number of variables used and, consequently, optimised working time and sexing accuracy. After validation, some equations showed a 100% sexing efficiency for Bonelli's eagles, particularly for adults. Our results showed that the variables with smaller overlap between the sexes were the lateral tarsus length and dorso-ventral tarsus length, particularly in nestlings. The rest of the variables showed some overlap between the sexes in both age classes. The results we obtained enable the sexing of juvenile and adult Bonelli's eagles in the field using just these two measurements. Hence, this is an easy, accurate, quick and non-invasive method with multiple applications, including in studies on population dynamics, survival analysis or extinction risk assessments, which, ultimately, could contribute to the improvement of the conservation status of this endangered species.

Potential negative effects of the installation of video surveillance cameras in raptors' nests.

Video surveillance cameras installed on birds' nests are a cost-effective tool to study many aspects of ecology and behaviour that would otherwise be practically impossible to obtain. However, although most studies report neutral effects of cameras on birds, very few studies analyse in detail the potential negative effects of their use, particularly on raptors. Here, using a long-term database of a population of Bonelli's eagle (Aquila fasciata) collected from 2000 to 2022, I show how the inappropriate use of video surveillance cameras could result in negative effects on the reproduction of a threatened species through a before-and-after control-impact study design. Pairs under video surveillance showed lower productivity, lower breeding success and unusual delayed laying dates. The installation of cameras close to the laying date, coinciding with the mating phase of individuals, most of them subadult inexperienced birds; in combination to the reiteration of visits to the nests once the cameras were installed to check the system, particularly during the incubation period and early stages of breeding; and the installation of cameras in a particular area subject to constant human disturbance, might explain these results. Potential management actions to mitigate the effect of the installation of video cameras on birds' behaviour should include the need to plan the intervention dates, testing the systems beforehand under controlled conditions and adequate post-installation monitoring to avoid unnecessary disturbance to animals. Finally, I urge the scientific community to report the potential negative effects observed in their studies, especially if the target species are threatened with extinction.

Tri-axial accelerometry shows differences in energy expenditure and parental effort throughout the breeding season in long-lived raptors.

Cutting-edge technologies are extremely useful to develop new workflows in studying ecological data, particularly to understand animal behavior and movement trajectories at the individual level. Although parental care is a well-studied phenomenon, most studies have been focused on direct observational or video recording data, as well as experimental manipulation. Therefore, what happens out of our sight still remains unknown. Using high-frequency GPS/GSM dataloggers and tri-axial accelerometers we monitored 25 Bonelli's eagles Aquila fasciata during the breeding season to understand parental activities from a broader perspective. We used recursive data, measured as number of visits and residence time, to reveal nest attendance patterns of biparental care with role specialization between sexes. Accelerometry data interpreted as the overall dynamic body acceleration, a proxy of energy expenditure, showed strong differences in parental effort throughout the breeding season and between sexes. Thereby, males increased substantially their energetic requirements, due to the increased workload, while females spent most of the time on the nest. Furthermore, during critical phases of the breeding season, a low percentage of suitable hunting spots in eagles' territories led them to increase their ranging behavior in order to find food, with important consequences in energy consumption and mortality risk. Our results highlight the crucial role of males in raptor species exhibiting biparental care. Finally, we exemplify how biologging technologies are an adequate and objective method to study parental care in raptors as well as to get deeper insight into breeding ecology of birds in general.

Differential survival throughout the full annual cycle of a migratory bird presents a life-history trade-off.

Long-distance migrations are among the most physically demanding feats animals perform. Understanding the potential costs and benefits of such behaviour is a fundamental question in ecology and evolution. A hypothetical cost of migration should be outweighed by higher productivity and/or higher annual survival, but few studies on migratory species have been able to directly quantify patterns of survival throughout the full annual cycle and across the majority of a species' range. Here, we use telemetry data from 220 migratory Egyptian vultures Neophron percnopterus, tracked for 3,186 bird months and across approximately 70% of the species' global distribution, to test for differences in survival throughout the annual cycle. We estimated monthly survival probability relative to migration and latitude using a multi-event capture-recapture model in a Bayesian framework that accounted for age, origin, subpopulation and the uncertainty of classifying fates from tracking data. We found lower survival during migration compared to stationary periods (ß = -0.816; 95% credible interval: -1.290 to -0.318) and higher survival on non-breeding grounds at southern latitudes (<25°N; ß = 0.664; 0.076-1.319) compared to on breeding grounds. Survival was also higher for individuals originating from Western Europe (ß = 0.664; 0.110-1.330) as compared to further east in Europe and Asia, and improved with age (ß = 0.030; 0.020-0.042). Anthropogenic mortalities accounted for half of the mortalities with a known cause and occurred mainly in northern latitudes. Many juveniles drowned in the Mediterranean Sea on their first autumn migration while there were few confirmed mortalities in the Sahara Desert, indicating that migration barriers are likely species-specific. Our study advances the understanding of important fitness trade-offs associated with long-distance migration. We conclude that there is lower survival associated with migration, but that this may be offset by higher non-breeding survival at lower latitudes. We found more human-caused mortality farther north, and suggest that increasing anthropogenic mortality could disrupt the delicate migration trade-off balance. Research to investigate further potential benefits of migration (e.g. differential productivity across latitudes) could clarify how migration evolved and how migrants may persist in a rapidly changing world.

Winter movement patterns of a globally endangered avian scavenger in south-western Europe.

Partial migration, whereby some individuals migrate and some do not, is relatively common and widespread among animals. Switching between migration tactics (from migratory to resident or vice versa) occurs at individual and population levels. Here, we describe for the first time the movement ecology of the largest wintering population of Egyptian Vultures (Neophron percnopterus) in south-west Europe. We combined field surveys and GPS tracking data from December to February during four wintering seasons (2014-2018). The wintering population consisted on average of 85 individuals (range 58-121; 76% adults and 24% subadults). Individuals were counted at five different roosting sites located near farms, unauthorized carcass deposition sites and authorized carcass deposition sites. Our results show that vultures tend to remain close to the roosting site. Moreover, we observed that females exhibited smaller home range sizes than males, which suggests a possible differential use of food sources. Overall, birds relied more on farms than other available food resources, particularly subadult individuals which exploited more intensively these sites. Our results showed that Egyptian Vultures congregate in significant numbers at specific sites throughout the winter period in south-west Spain and that these roosting and feeding sites should be given some level of legal protection and regular monitoring. Furthermore, predictable food sources might be driving the apparent increase in the non-migratory population of Egyptian Vultures, as observed in other avian species which are also changing their migratory behavior.

Current and future suitability of wintering grounds for a long-distance migratory raptor.

Conservation of migratory species faces the challenge of understanding the ecological requirements of individuals living in two geographically separated regions. In some cases, the entire population of widely distributed species congregates at relatively small wintering areas and hence, these areas become a priority for the species' conservation. Satellite telemetry allows fine tracking of animal movements and distribution in those less known, often remote areas. Through integrating satellite and GPS data from five separated populations comprising most of the breeding range, we created a wide habitat suitability model for the Eleonora's falcon on its wintering grounds in Madagascar. On this basis, we further investigated, for the first time, the impact of climate change on the future suitability of the species' wintering areas. Eleonora's falcons are mainly distributed in the north and along the east of Madagascar, exhibiting strong site fidelity over years. The current species' distribution pattern is associated with climatic factors, which are likely related to food availability. The extent of suitable areas for Eleonora's falcon is expected to increase in the future. The integration of habitat use information and climatic projections may provide insights on the consequences of global environmental changes for the long-term persistence of migratory species populations.

Wind effects on the migration routes of trans-Saharan soaring raptors: geographical, seasonal, and interspecific variation.

Wind is among the most important environmental factors shaping birds' migration patterns. Birds must deal with the displacement caused by crosswinds and their behavior can vary according to different factors such as flight mode, migratory season, experience, and distance to goal areas. Here we analyze the relationship between wind and migratory movements of three raptor species which migrate by soaring-gliding flight: Egyptian vulture Neophron percnopterus, booted eagle Aquila pennata, and short-toed snake eagle Circaetus gallicus. We analyzed daily migratory segments (i.e., the path joining consecutive roosting locations) using data recorded by GPS satellite telemetry. Daily movements of Egyptian vultures and booted eagles were significantly affected by tailwinds during both autumn and spring migrations. In contrast, daily movements of short-toed eagles were only significantly affected by tailwinds during autumn migration. The effect of crosswinds was significant in all cases. Interestingly, Egyptian vultures and booted eagles showed latitudinal differences in their behavior: both species compensated more frequently at the onset of autumn migration and, at the end of the season when reaching their wintering areas, the proportion of drift segments was higher. In contrast, there was a higher drift at the onset of spring migration and a higher compensation at the end. Our results highlight the effect of wind patterns on the migratory routes of soaring raptors, with different outcomes in relation to species, season, and latitude, ultimately shaping the loop migration patterns that current tracking techniques are showing to be widespread in many long distance migrants.

Low prevalence of blood parasites in a long-distance migratory raptor: the importance of host habitat.

BACKGROUND: The low prevalence of blood parasites in some bird species may be related to the habitats they frequent, the inexistence of the right host-parasite assemblage or the immunological capacity of the host. Here, we assess the parasite load of breeding populations of Eleonora's falcon (Falco eleonorae), a medium-sized long-distance migratory raptor that breeds on small isolated islets throughout the Mediterranean basin and overwinters in inland Madagascar. METHODS: We examined the prevalence and genetic diversity of the blood parasites belonging to the genera Plasmodium, Haemoproteus and Leucocytozoon in Eleonora's falcon nestlings from five colonies and in adults from two colonies from nesting sites distributed throughout most of the species' breeding range. RESULTS: None of the 282 nestlings analysed were infected by blood parasites; on the other hand, the lineages of Plasmodium, Haemoproteus and Leucocytozoon were all found to infect adults. Our results support the idea of no local transmission of vector-borne parasites in marine habitats. Adult Eleonora's falcons thus may be infected by parasites when on migration or in their wintering areas. CONCLUSION: The characteristics of marine environments with a lack of appropriate vectors may thus be the key factor determining the absence of local transmission of blood parasites. By comparing the parasite lineages isolated in this species with those previously found in other birds we were able to infer the most likely areas for the transmission of the various parasite lineages.

Nest site selection by Kentish plover suggests a trade-off between nest-crypsis and predator detection strategies.

Predation is one of the main causes of adult mortality and breeding failure for ground-nesting birds. Micro-habitat structure around nests plays a critical role in minimizing predation risk. Plovers nest in sites with little vegetation cover to maximize the incubating adult visibility, but many studies suggest a trade-off between nest-crypsis and predator detection strategies. However, this trade-off has not been explored in detail because methods used so far do not allow estimating the visibility with regards to critical factors such as slope or plant permeability to vision. Here, we tested the hypothesis that Kentish plovers select exposed sites according to a predator detection strategy, and the hypothesis that more concealed nests survive longer according to a crypsis strategy. To this end, we obtained an accurate estimation of the incubating adult's field of vision through a custom built inverted periscope. Our results showed that plovers selected nest sites with higher visibility than control points randomly selected with regards to humans and dogs, although nests located in sites with higher vegetation cover survived longer. In addition, the flushing distance (i.e., the distance at which incubating adults leave the nest when they detect a potential predator) decreased with vegetation cover. Consequently, the advantages of concealing the nest were limited by the ability to detect predators, thus indirectly supporting the existence of the trade-off between crypsis and predator detection. Finally, human disturbance also constrained nest choice, forcing plovers to move to inland sites that were less suitable because of higher vegetation cover, and modulated flushing behavior, since plovers that were habituated to humans left their nests closer to potential predators. This constraint on the width of suitable breeding habitat is particularly relevant for the conservation of Kentish Plover in sand beaches, especially under the current context of coastal regression and increase of recreational activities.

Food predictability determines space use of endangered vultures: implications for management of supplementary feeding.

Understanding space use of free-living endangered animals is key to informing management decisions for conservation planning. Like most scavengers, vultures have evolved under a context of unpredictability of food resources (i.e., exploiting scattered carcasses that are intermittently available). However, the role of predictable sources of food in shaping spatial ecology of vultures has seldom been studied in detail. Here, we quantify the home range of the Egyptian Vulture (Neophron percnopterus), a long-lived raptor that has experienced severe population decline throughout its range and is qualified as endangered worldwide. To this end, six adults were tracked by satellite telemetry in Spain during the breeding season, from 2007 to 2012, recording 10360 GPS locations. Using Resource Utilization Functions, we assessed the topology of the Utilization Distribution, a three-dimensional measure that shows the probability of finding an animal within the home range. Our results showed how food availability, and principally, how food predictability, determines ranging behavior of this species. Egyptian Vultures showed consistent site fidelity across years, measured as the two- and three-dimensional overlap in their home ranges. Space use varied considerably within the home range and remarkably, places located far from nesting sites were used more frequently than some areas located closer. Therefore, traditional conservation measures based on establishing restrictive rules within a fixed radius around nesting sites could be biologically meaningless if other areas within the home range are not protected too. Finally, our results emphasize the importance of anthropogenic predictable sources of food (mainly vulture restaurants) in shaping the space use of scavengers, which is in agreement with recent findings. Hence, measures aimed at ensuring food availability are essential to preserve this endangered vulture, especially in the present context of limiting carrion dumping in the field due to sanitary regulations according to European legislation.

Ecological specialization to fluctuating resources prevents long-distance migratory raptors from becoming sedentary on islands.

BACKGROUND: The adaptive transition between behavioral strategies, such as the shift from migratoriness to sedentariness, remains an outstanding question in evolutionary ecology. Density-dependent variation in the age of first breeding has been proposed as a feasible mechanism through which long-lived migratory birds with deferred sexual maturity should become sedentary to persist on islands. Although this pattern seems to hold for most raptors and herons, a few exceptions have been identified. One of these exceptions is the Eleonora's falcon, a long-distance migratory bird, which shows one of the most peculiar adaptations in the timing of reproduction and food requirements among raptors. METHODOLOGY/PRINCIPAL FINDINGS: Here, we compiled data concerning demography, banding recoveries and satellite tracking of Eleonora's falcons to discuss likely explanations for the exceptional behavior of this insular long-distance migratory species. CONCLUSIONS/SIGNIFICANCE: New data reveal that Eleonora's falcons do return to the natal colonies in their first year and young birds are able to breed. However, in contrast to previous hypothesis, the highly specialized strategy of this and other ecologically similar species, as well as the virtual lack of food during winter at breeding areas prevent them from becoming sedentary on islands. Although the ultimate mechanisms underlying the process of sedentarization remain poorly understood, the evidence provided reveal the existence of important trade-offs associated with ecological specialization that may become particularly relevant in the present context of global change.

Scavengers on the move: behavioural changes in foraging search patterns during the annual cycle.

BACKGROUND: Optimal foraging theory predicts that animals will tend to maximize foraging success by optimizing search strategies. However, how organisms detect sparsely distributed food resources remains an open question. When targets are sparse and unpredictably distributed, a Lévy strategy should maximize foraging success. By contrast, when resources are abundant and regularly distributed, simple brownian random movement should be sufficient. Although very different groups of organisms exhibit Lévy motion, the shift from a Lévy to a brownian search strategy has been suggested to depend on internal and external factors such as sex, prey density, or environmental context. However, animal response at the individual level has received little attention. METHODOLOGY/PRINCIPAL FINDINGS: We used GPS satellite-telemetry data of Egyptian vultures Neophron percnopterus to examine movement patterns at the individual level during consecutive years, with particular interest in the variations in foraging search patterns during the different periods of the annual cycle (i.e. breeding vs. non-breeding). Our results show that vultures followed a brownian search strategy in their wintering sojourn in Africa, whereas they exhibited a more complex foraging search pattern at breeding grounds in Europe, including Lévy motion. Interestingly, our results showed that individuals shifted between search strategies within the same period of the annual cycle in successive years. CONCLUSIONS/SIGNIFICANCE: Results could be primarily explained by the different environmental conditions in which foraging activities occur. However, the high degree of behavioural flexibility exhibited during the breeding period in contrast to the non-breeding period is challenging, suggesting that not only environmental conditions explain individuals' behaviour but also individuals' cognitive abilities (e.g., memory effects) could play an important role. Our results support the growing awareness about the role of behavioural flexibility at the individual level, adding new empirical evidence about how animals in general, and particularly scavengers, solve the problem of efficiently finding food resources.

Interspecific comparison of the performance of soaring migrants in relation to morphology, meteorological conditions and migration strategies.

BACKGROUND: Performance of migrating birds can be affected by a number of intrinsic and extrinsic factors like morphology, meteorological conditions and migration strategies. We compared travel speeds of four raptor species during their crossing of the Sahara desert. Focusing the analyses on this region allows us to compare different species under equivalent conditions in order to disentangle which factors affect migratory performance. METHODOLOGY/PRINCIPAL FINDING: We tracked raptors using GPS satellite transmitters from Sweden, Spain and Italy, and evaluated their migratory performance at both an hourly and a daily scale. Hourly data (flight speed and altitude for intervals of two hours) were analyzed in relation to time of day, species and season, and daily data (distance between roosting sites) in relation to species, season, day length and tailwind support. CONCLUSIONS/SIGNIFICANCE: Despite a clear variation in morphology, interspecific differences were generally very small, and did only arise in spring, with long-distance migrants (>5000 km: osprey and Western marsh-harrier) being faster than species that migrate shorter distances (Egyptian vulture and short-toed eagle). Our results suggest that the most important factor explaining hourly variation in flight speed is time of day, while at a daily scale, tailwind support is the most important factor explaining variation in daily distance, raising new questions about the consequences of possible future changes in worldwide wind patterns.

Living on the edge: assessing the extinction risk of critically endangered Bonelli's eagle in Italy.

BACKGROUND: The population of Bonelli's eagle (Aquila fasciata) has declined drastically throughout its European range due to habitat degradation and unnatural elevated mortality. There are less than 1500 breeding pairs accounted for in Europe, and the species is currently catalogued as Critically Endangered in Italy, where the 22 territories of Sicily, represent nearly 95% of the entire Italian population. However, despite national and European conservation concerns, the species currently lacks a specific conservation plan, and no previous attempts to estimate the risk of extinction have been made. METHODOLOGY/PRINCIPAL FINDINGS: We incorporated the most updated demographic information available to assess the extinction risk of endangered Bonelli's eagle in Italy through a Population Viability Analysis. Using perturbation analyses (sensitivity and elasticity), and a combination of demographic data obtained from an assortment of independent methods, we evaluated which demographic parameters have more influence on the population's fate. We also simulated different scenarios to explore the effects of possible management actions. Our results showed that under the current conditions, Bonelli's eagle is expected to become extinct in Italy in less than 50 years. Stand-alone juvenile mortality was the most critical demographic parameter with the strongest influence on population persistence with respect to other demographic parameters. Measures aimed at either decreasing juvenile mortality, adult mortality or decreasing both juvenile and adult mortality resulted in equivalent net positive effects on population persistence (population growth rate λ>1). In contrast, changes aimed at increasing breeding success had limited positive effects on demographic trends. CONCLUSIONS/SIGNIFICANCE: Our PVA provides essential information to direct the decision-making process and exposes gaps in our previous knowledge. To ensure the long-term persistence of the species in Italy, measures are urgently needed to decrease both adult mortality due to poaching and juvenile mortality due to nest plundering, the top ranking mortality causes.

Solving man-induced large-scale conservation problems: the Spanish imperial eagle and power lines.

BACKGROUND: Man-induced mortality of birds caused by electrocution with poorly-designed pylons and power lines has been reported to be an important mortality factor that could become a major cause of population decline of one of the world rarest raptors, the Spanish imperial eagle (Aquila adalberti). Consequently it has resulted in an increasing awareness of this problem amongst land managers and the public at large, as well as increased research into the distribution of electrocution events and likely mitigation measures. METHODOLOGY/PRINCIPAL FINDINGS: We provide information of how mitigation measures implemented on a regional level under the conservation program of the Spanish imperial eagle have resulted in a positive shift of demographic trends in Spain. A 35 years temporal data set (1974-2009) on mortality of Spanish imperial eagle was recorded, including population censuses, and data on electrocution and non-electrocution of birds. Additional information was obtained from 32 radio-tracked young eagles and specific field surveys. Data were divided into two periods, before and after the approval of a regional regulation of power line design in 1990 which established mandatory rules aimed at minimizing or eliminating the negative impacts of power lines facilities on avian populations. Our results show how population size and the average annual percentage of population change have increased between the two periods, whereas the number of electricuted birds has been reduced in spite of the continuous growing of the wiring network. CONCLUSIONS: Our results demonstrate that solving bird electrocution is an affordable problem if political interest is shown and financial investment is made. The combination of an adequate spatial planning with a sustainable development of human infrastructures will contribute positively to the conservation of the Spanish imperial eagle and may underpin population growth and range expansion, with positive side effects on other endangered species.

Weather conditions promote route flexibility during open ocean crossing in a long-distance migratory raptor.

Weather conditions are paramount in shaping birds' migratory routes, promoting the evolution of behavioural plasticity and allowing for adaptive decisions on when to depart or stop during migration. Here, we describe and analyze the influence of weather conditions in shaping the sea-crossing stage of the pre-breeding journey made by a long-distance migratory bird, the Eleonora's falcon (Falco eleonorae), tracked by satellite telemetry from the wintering grounds in the Southern Hemisphere to the breeding sites in the Northern Hemisphere. As far as we know, the data presented here are the first report of repeated oceanic journeys of the same individuals in consecutive years. Our results show inter-annual variability in the routes followed by Eleonora's falcons when crossing the Strait of Mozambique, between Madagascar and eastern continental Africa. Interestingly, our observations illustrate that individuals show high behavioural plasticity and are able to change their migration route from one year to another in response to weather conditions, thus minimising the risk of long ocean crossing by selecting winds blowing towards Africa for departure and changing the routes to avoid low pressure areas en route. Our results suggest that weather conditions can really act as obstacles during migration, and thus, besides ecological barriers, the migratory behaviour of birds could also be shaped by "meteorological barriers". We briefly discuss orientation mechanisms used for navigation. Since environmental conditions during migration could cause carry-over effects, we consider that forecasting how global changes of weather patterns will shape the behaviour of migratory birds is of the utmost importance.