Demographic modeling to fine-tune conservation targets: importance of pre-adults for the decline of an endangered raptor.

Large, long-lived species with slow life histories and protracted pre-breeding stages are particularly susceptible to declines and extinction, often for unknown causes. Here, we show how demographic modeling of a medium-sized raptor, the Red Kite Milvus milvus, can aid to refocus conservation research and attention on the most likely mechanisms driving its decline. Red Kites' survival and reproduction increased through three sequential stages for 1-2, 3-6, and 7-30 yr of age, mainly corresponding to individuals that are dispersing, attempting to gain a territory, and breeding. As typical of long-lived species, elasticities were highest for adult (≥7 yr old) survival, but this was high, with little scope for improvement. Instead, the declines were driven by an extremely low survival of pre-adults in their first years of life, which weakened the whole demographic system by nullifying the offspring contribution of adults and curtailing their replacement by recruits. For example, 27 pairs were necessary to generate a single prime age adult. Simulation of management scenarios suggested that the decline could be halted most parsimoniously by increasing pre-adult survival to the mean levels recorded for other areas, while only the synergistic, simultaneous improvement of breeding success, adult and pre-adult survival could generate a recovery. We propose three actions to attain such goals through selective supplementary feeding of both breeding and non-breeding individuals, and through mortality improvement by GPS remote-sensing devices employed as surveillance monitoring tools. Our results show how improving demographic models by using real, local vital rates rather than "best guess" vital rates can dramatically improve model realism by refocusing attention on the actual stages and mortality causes in need of manipulation, thus building precious time and resources for conservation management. These results also highlight the frequent key role of pre-adult survival for the management of long-lived species, coherent with the idea of demographic systems as integrated chains only as strong as their weakest link.

Individual improvements and selective mortality shape lifelong migratory performance.

Billions of organisms, from bacteria to humans, migrate each year and research on their migration biology is expanding rapidly through ever more sophisticated remote sensing technologies. However, little is known about how migratory performance develops through life for any organism. To date, age variation has been almost systematically simplified into a dichotomous comparison between recently born juveniles at their first migration versus adults of unknown age. These comparisons have regularly highlighted better migratory performance by adults compared with juveniles, but it is unknown whether such variation is gradual or abrupt and whether it is driven by improvements within the individual, by selective mortality of poor performers, or both. Here we exploit the opportunity offered by long-term monitoring of individuals through Global Positioning System (GPS) satellite tracking to combine within-individual and cross-sectional data on 364 migration episodes from 92 individuals of a raptorial bird, aged 1-27 years old. We show that the development of migratory behaviour follows a consistent trajectory, more gradual and prolonged than previously appreciated, and that this is promoted by both individual improvements and selective mortality, mainly operating in early life and during the pre-breeding migration. Individuals of different age used different travelling tactics and varied in their ability to exploit tailwinds or to cope with wind drift. All individuals seemed aligned along a race with their contemporary peers, whose outcome was largely determined by the ability to depart early, affecting their subsequent recruitment, reproduction and survival. Understanding how climate change and human action can affect the migration of younger animals may be the key to managing and forecasting the declines of many threatened migrants.

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.

Protein electrophoresis in Andean condors (Vultur gryphus): Reference values and differences between wild and rehabilitating individuals.

The study of wildlife health greatly contributes to understanding population dynamics and detecting conservation threats. The determination of the different fractions of plasma proteins (proteinogram) is an important laboratory tool to study wildlife health. The aim of this study was to characterize protein electrophoresis in wild Andean condors (Vultur gryphus) from north-western Patagonia and to evaluate differences according to age and sex classes. Once reference values of wild, apparently healthy individuals, were established, we compared these values to those of individuals received at the Buenos Aires Zoo in Argentina for rehabilitation due to various health problems. Reference proteinograms from wild Andean condors differed only in the α 1 and ß 2-fractions between sex categories. Males showed higher concentrations of these protein fractions than females. We found clear differences between wild birds and rehabilitating individuals. Total proteins, globulins, α 1-globulins, total α-globulins, ß 2-globulins, total ß-globulins, and γ-globulins were significantly higher in rehabilitating than in wild individuals, whereas albumin, α 2, and ß1-globulins were similar between these groups. The albumin/globulin ratio, as a general indicator of health, was significantly lower in rehabilitating than in wild individuals. The results indicate the effects on different protein fractions of pathologic processes occurring in individuals undergoing rehabilitation. Our results provide useful insights, contributing to improving diagnoses and prognoses in this species. This information may also be useful to assess the health status of Andean condors in studies of wild populations and for comparisons with other bird species.

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.

Integrating population connectivity into pollution assessment: Overwintering mixing reveals flame retardant contamination in breeding areas in a migratory raptor.

Determining the exposure and magnitude at which various pollutants are differentially assimilated at the breeding and non-breeding grounds of migratory wildlife is challenging. Here, the possibility of applying the migratory connectivity framework to understanding contamination in birds is illustrated by considering flame retardants in inviable eggs of a migratory raptor, the black kite (Milvus migrans). The occurrence and concentration of legacy and emerging compounds in eggs from the southeastern peri-urban area of Madrid city, central Spain, were compared with those from Doñana National Park in southern Spain. A much higher occurrence and concentration of multiple polybrominated diphenyl ethers and Dechlorane 602 were found in Madrid than Doñana, but the opposite patterns were found for Dechlorane Plus. Individuals from these and other breeding areas in western Europe showed a strong intermixing pattern over widespread wintering areas in Africa, as assessed by ringing recoveries and movements tracked by satellite devices. This diffuse migratory connectivity reveals breeding areas as the main contamination grounds. High contamination burdens sequestered in eggs point to rapid assimilation of these compounds before laying, associated with important emission sources in Madrid, especially landfills of partially incinerated urban refuse, and other anthropogenic operations. Diet composition regarding aquatic vs. terrestrial prey, and bioaccumulation and biomagnification processes are suggested to explain differential assimilation of some compounds, especially Dechlorane Plus in Doñana, although a local emission source polluting this area cannot be ruled out. Insight from the migratory connectivity framework can help to disentangle large-scale patterns of contaminant uptake and refocus attention on key regions and potential causes of chemical hazards in declining migratory species and human populations.

A Potential New Threat to Wild Life: Presence of UV Filters in Bird Eggs from a Preserved Area.

The present study uses bird eggs of seven wild species as a biomonitoring tool for sunscreens occurrence. Seven UV filters (UV-Fs), including 3 hydroxy-metabolites of oxybenzone (benzophenone 3, BP3) were characterized in unhatched eggs from Doñana Natural Space (Spain). High frequency of detection was observed for all UV-Fs, ranging from 95% to 100%. The oxybenzone metabolite 4-hydroxybenzophenone (4HB) was ubiquitous at concentrations in the range 12.0-3348 ng g-1 dry weight (dw). The parent compound, oxybenzone, was also present in all samples at lower concentrations (16.9-49.3 ng g-1 dw). Due to the three BP3's metabolites, benzophenone 1 (BP1), 4HB, and 4,4'-dihydroxybenzophenone (4DHB) presence in unhatched eggs, it can be inferred that parent compounds are absorbed into the bird through the upper gut and the OH-derivatives formed are transferred by the mother to the egg before the lying. White stork (Ciconia ciconia) and western marsh harrier (Circus aeruginosus) were the most contaminated species, with mean total UV-Fs concentrations of 834 and 985 ng g-1 dw, respectively. Results evidenced that biomagnification process across the bird species studied cannot be ruled out.

Lifetime variation in feather corticosterone levels in a long-lived raptor.

In long-lived animals, the challenges that threaten individual homeostasis, and the way they are dealt with, are expected to vary in an age-related manner, encompassing the progressive selection of superior phenotypes and the acquisition and improvement of key skills (e.g. foraging, breeding and fighting abilities). Since exposure to homeostatic challenges typically elevates circulating glucocorticoid (GC) levels in vertebrates (modulating the behavioural and physiological responses that mediate allostasis), we may expect concomitant age-related changes in these hormones. Here, we investigated whether the level of corticosterone (the main avian GC) deposited in feathers during regular moult reflected the expected lifelong progression of energetic challenges in a long-lived raptor, the black kite (Milvus migrans). Feather corticosterone values were highest in the youngest birds, gradually declined to reach minimum levels in prime age, 7- to 11-year-old birds, and then increased again slightly among the oldest, senescent birds (≥12 years old). This pattern mirrored the age-related changes in reproductive success and survival rates previously reported for this population, suggesting that feather corticosterone levels captured the most vulnerable and challenging periods experienced by these birds as they proceeded through life. Moreover, feather corticosterone levels were negatively related to body size, suggesting that larger birds either experienced fewer homeostatic challenges, or were better able to cope with them. Feather corticosterone measures thus provided a valuable snapshot of how allostatic loads vary along the life of individuals, supporting the idea of a tight, long-term link between cumulative physiological responses to ecological challenges and demographic performance.

Nesting innovations in neotropical parrots associated to anthropogenic environmental changes.

Parrots are among the most diverse and widely distributed groups of birds and one of the most threatened bird orders mainly due to habitat loss and illegal poaching. Most parrots are obligate cavity nesters, so the logging of mature trees and the transformation of natural cliffs represent important threats to their conservation. Here, we report novel observations of Neotropical parrots nesting in previously unrecorded substrates. We show the first documented case of the cliff-nesting burrowing parrots trying to breed at ground level in an abandoned burrowing owl cavity. Additionally, we provide the first documented observations of this species attempting to nest in building cavities in three urbanized areas of Argentina. Moreover, we report data from four countries of 148 pairs of eight species typically breeding in tree cavity using palm tree bracts as nest sites. Behavioral plasticity in nest sites may allow parrots to maximize their nesting success by exploiting alternative breeding substrates. Moreover, these novelties could contribute to cope with habitat loss and further transformation. However, further research is needed to assess the consequences of these nesting innovations in terms of individual fitness and population dynamics as well as potential factors promoting their appearance.

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.

Novel food resources and conservation of ecological interactions between the Andean Araucaria and the Austral parakeet.

In fragile ecosystems, the introduction of exotic species could alter some ecological processes. The Austral parakeet (Enicognathus ferrugineous) shows close ecological and evolutionary relationships with the Andean Araucaria (Araucaria araucana), so any alteration in these interactions may have negative consequences for both partners and for ecosystem functioning and structure. We conducted extensive roadside surveys to estimate the abundance of parakeets in the northern Patagonian Andes over 4 years and recorded the food plants consumed by foraging flocks. The use of native habitats and humanized areas like villages and farms was influenced by the Araucaria seed crop. In masting years, the large seed crop allowed a massive use of this resource during the non-breeding season, and even during the breeding season. The exploitation of exotic plants was minor in the masting year, but became predominant in non-masting years, especially during the non-breeding season. This feeding switch towards exotic plants primarily arose because the low Araucaria seed crop in non-masting years is entirely consumed just after production by domestic and wild exotic mammals living in Araucaria forests year-round, thus forcing the displacement of parakeets towards anthropic habitats to exploit exotic plants. Given the degradation of the remaining Andean Araucaria forests due to the impact of exotic mammals on the ecological interaction between Araucaria and Austral parakeets, ambitious programs to exclude or reduce the density of these alien mammals, including livestock, are warranted.

Confounding Rules Can Hinder Conservation: Disparities in Law Regulation on Domestic and International Parrot Trade within and among Neotropical Countries.

Wildlife trade is a major driver of biodiversity loss worldwide. To regulate its impact, laws and regulations have been implemented at the international and national scales. The Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) has regulated the international legal trade since 1975. However, an important volume of illegal trade-mainly within countries-continues to threaten several vertebrate groups, which could be due to a lack of specific legislation or enforcement of existing regulations. Our aim was to gain a more accurate picture of poaching and legal possession of native parrots as pets in the Neotropics, where illegal domestic trade is currently widespread. We conducted a systematic search of the laws of each of the 50 countries and overseas territories, taking into account their year of implementation and whether the capture, possession and/or sale of parrots is permitted. We compared this information with legal exports reported by CITES to assess differences between the enforcement of international and national trade regulations. We found that only two countries (Guyana and Suriname) currently allow the capture, trade and possession of native parrots, while Peru allowed international legal trade until recently. The other countries have banned parrot trade from years to decades ago. However, the timing of implementation of international and national trade regulations varied greatly between countries, with half of them continuing to export parrots legally years or decades after banning domestic trade. The confusion created by this complex legal system may have hindered the adoption of conservation measures, allowing poaching, keeping and trade of protected species within and between neighboring countries. Most countries legally exported Neotropical parrot species which were not native to those countries, indicating that trans-border smuggling often occurred between neighboring countries prior to their legal exportations, and that this illicit activity continues for the domestic trade. Governments are urged to effectively implement current legislation that prohibits the trapping and domestic trade of native parrots, but also to develop coordinated alliances and efforts to halt illegal trade among them. Otherwise, illegal trade will continue to erode the already threatened populations of a large number of parrot species across the Neotropics.

Compensation for wind drift during raptor migration improves with age through mortality selection.

Each year, billions of flying and swimming migrants negotiate the challenging displacement imposed by travelling through a flowing medium. However, little is known about how the ability to cope with drift improves through life and what mechanisms drive its development. We examined 3,140 days of migration by 90 GPS-tagged raptorial black kites (Milvus migrans) aged 1-27 years to show that the ability to compensate for lateral drift develops gradually through many more years than previously appreciated. Drift negotiation was under strong selective pressure, with inferior navigators subject to increased mortality. This progressively selected for adults able to compensate for current cross flows and for previously accumulated drift in a flexible, context-dependent and risk-dependent manner. Displacements accumulated en route carried over to shape the wintering distribution of the population. For many migrants, migratory journeys by younger individuals represent concentrated episodes of trait selection that shape adult populations and mediate their adaptation to climate change.

Hardship at birth alters the impact of climate change on a long-lived predator.

Climate change is increasing the frequency of extreme events, such as droughts or hurricanes, with substantial impacts on human and wildlife communities. Extreme events can affect individuals through two pathways: by altering the fitness of adults encountering a current extreme, and by affecting the development of individuals born during a natal extreme, a largely overlooked process. Here, we show that the impact of natal drought on an avian predator overrode the effect of current drought for decades, so that individuals born during drought were disadvantaged throughout life. Incorporation of natal effects caused a 40% decline in forecasted population size and a 21% shortening of time to extinction. These results imply that climate change may erode populations more quickly and severely than currently appreciated, suggesting the urgency to incorporate "penalties" for natal legacies in the analytical toolkit of impact forecasts. Similar double impacts may apply to other drivers of global change.

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.

Fine-scale genetic structure in the critically endangered red-fronted macaw in the absence of geographic and ecological barriers.

Behavioural and socio-cultural traits are recognized in the restriction of gene flow in species with high cognitive capacity and complex societies. This isolation by social barriers has been generally overlooked in threatened species by assuming disrupted gene flow due to population fragmentation and decline. We examine the genetic structure and ecology of the global population of the Critically Endangered red-fronted macaw (Ara rubrogenys), an endemic species to the inter-Andean valleys of Bolivia. We found a fine-scale genetic structuring in four genetic clusters. Genetic diversity was higher in wild compared to captive-bred macaws, but similar to that of captive wild-caught macaws. We found no clear evidence of severe genetic erosion in the population in recent decades, but it was patent in historic times, overlapping with drastic human habitat transformation and macaw persecution over millennia. We found no evidence of geographical and ecological barriers, owing to the high dispersal ability, nesting and foraging habits between genetic clusters. The lack of genetic intermixing despite long-distance foraging and seasonal movements suggests recruitment in natal colonies and other social factors reinforcing philopatry-related genetic structure. Conservation efforts should be specifically focussed on major threats in each genetic cluster as independent conservation units, and also considered in ex-situ management.

Epizoochory in Parrots as an Overlooked Yet Widespread Plant-Animal Mutualism.

Plant-animal interactions are key to sustaining whole communities and ecosystem function. However, their complexity may limit our understanding of the underlying mechanisms and the species involved. The ecological effects of epizoochory remain little known compared to other seed dispersal mechanisms given the few vectors identified. In addition, epizoochory is mostly considered non-mutualistic since dispersers do not obtain nutritional rewards. Here, we show a widespread but unknown mutualistic interaction between parrots and plants through epizoochory. Combining our observations with photos from web-sources, we recorded nearly 2000 epizoochory events in 48 countries across five continents, involving 116 parrot species and nearly 100 plant species from 35 families, including both native and non-native species. The viscid pulp of fleshy fruits and anemochorous structures facilitate the adherence of tiny seeds (mean 3.7 × 2.56 mm) on the surface of parrots while feeding, allowing the dispersion of these seeds over long distances (mean = 118.5 m). This parrot-plant mutualism could be important in ecosystem functioning across a wide diversity of environments, also facilitating the spread of exotic plants. Future studies should include parrots for a better understanding of plant dispersal processes and for developing effective conservation actions against habitat loss and biological invasions.

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.

The role of humans in the diversification of a threatened island raptor.

BACKGROUND: 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). RESULTS: 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. CONCLUSIONS: 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.