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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

When and where mortality occurs throughout the annual cycle changes with age in a migratory bird: individual vs population implications.

The annual cycle of most animals is structured into discrete stages, such as breeding, migration and dispersal. While there is growing appreciation of the importance of different stages of an organism's annual cycle for its fitness and population dynamics, almost nothing is known about if and how such seasonal effects can change through a species lifespan. Here, we take advantage of the opportunity offered by a long-term satellite/GPS-tracking study and a reliable method of remote death-detection to show that certain stages of both the annual and life cycle of a migratory long-lived raptor, the Black kite Milvus migrans, may represent sensitive bottlenecks for survival. In particular, migratory journeys caused bursts of concentrated-mortality throughout life, but the relative importance of stage-specific survival changed with age. On the other hand, the balance between short-stages of high mortality and long-stages of low mortality made population-growth similarly dependent on all portions of the annual cycle. Our results illustrate how the population dynamics of migratory organisms can be inextricably linked to ecological pressures balanced over multiple stages of the annual cycle and thus multiple areas of the globe, suggesting the frequent need for challenging conservation strategies targeting all portions of a species year-round range.

The extent, frequency and ecological functions of food wasting by parrots.

Anecdotic citations of food wasting have been described for parrots, but we lack a comprehensive knowledge about the extent of this behaviour, and its ecological and evolutionary implications. Here, we combine experimental and observational approaches to evaluate the spatial, temporal, typological and taxonomic extent of food wasting by parrots, to identify the ecological and evolutionary factors driving food wasting, and to assess the incidence of two ecological functions derived from food wasting, such as food facilitation to other animal species and secondary seed dispersal. We found that food wasting is a widespread behaviour found in all the studied parrot species. However, the proportion of food wasted differed among species and throughout the year. Parrots wasted more food during the non-breeding season, when they relied on exotic plants and on unripe fruits or seeds. We also recorded 86 animal species feeding on the food wasted by parrots, 27 of which potentially acted as secondary seed dispersers. Overall, our study emphasizes the universality of food wasting among parrots, and the important implications that this behaviour may have for the species involved (i.e., the parrot, the plant, the other species feeding on wasted food), and for the functioning of the whole ecosystem.

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.

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.

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.

Cities may save some threatened species but not their ecological functions.

BACKGROUND: Urbanization is one of the main causes of biodiversity loss worldwide. Wildlife responses to urbanization, however, are greatly variable and, paradoxically, some threatened species may achieve much larger populations in urban than in natural habitats. Urban conservation hotspots may therefore help some species avoid regional or even global extinctions, but not conserve their often overlooked ecological functions in the wild. We aim to draw attention to this issue using two species of globally threatened parrots occurring in the Dominican Republic: the Hispaniolan amazon (Amazona ventralis) and the Hispaniolan parakeet (Psittacara chloropterus). METHODS: We conducted a large-scale roadside survey in June 2017 across the country to estimate the relative abundance of parrots in natural habitats, rural habitats, and cities. We combined this with informal interviews with local people to collect information on past and current human impacts on parrot populations. We also looked for foraging parrots to assess their potential role as seed dispersers, an ecological function that has been overlooked until very recently. RESULTS: Relative abundances of both parrot species were negligible in rural areas and very low in natural habitats. They were generally between one and two orders of magnitude lower than that of congeneric species inhabiting other Neotropical ecosystems. Relative abundances were six times higher in cities than in natural habitats in the case of the Hispaniolan parakeet and three times higher in the case of the Hispaniolan amazon. People indicated hunting for a source food and to mitigate crop damage as causes of parrot population declines, and a vigorous illegal trade for parrots (131 individuals recorded, 75% of them poached very recently), mostly obtained from protected areas where the last small wild populations remain. We observed parrots foraging on 19 plant species from 11 families, dispersing the fruits of 14 species by carrying them in their beaks and consuming them in distant perching trees. They discarded undamaged mature seeds, with the potential to germinate, in 99.5% of cases (n = 306), and minimum dispersal distances ranged from 8 to 155 m (median = 37 m). DISCUSSION: The loss of ecological functions provided by some species when they disappear from natural habitats and only persist in cities may have long-term, unexpected effects on ecosystems. Our example demonstrates how two cities may soon be the last refuges for two endemic parrots if overharvesting continues, in which case their overlooked role as seed dispersers would be completely lost in nature. The functional extinction of these species could strongly affect vegetation communities in an island environment where seed-dispersal species are naturally scarce. While conservation plans must include urban populations of threatened species, greater efforts are needed to restore their populations in natural habitats to conserve ecological functions.

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.