Age and sex differences in pharmaceutical contamination in a keystone scavenger.

Pharmaceutical contaminants have a recognized negative impact on wildlife health. However, there are still many knowledge gaps on the factors influencing exposure and metabolic processing of compound mixtures as a function of season and individual characteristics such as age and sex. We evaluated age and sex differences in a set of seventeen compounds, including eleven antibiotics, five NSAIDs and caffeine, evaluated by HPLC-MS-TOF analysis in griffon vultures (Gyps fulvus) from central Spain. Pharmaceutical cocktails (up to 10 compounds simultaneously) were found in all individuals. Lincomycin was detected in all individuals, and fluoroquinolones were found at high frequencies, while NSAIDs were at low frequencies and concentrations, including flumixin meglumine, which can be lethal to vultures. A higher total number of compounds and sum of concentrations, as well as prevalence and concentration of several of the pharmaceuticals tested was found in females than in males for both nestlings and adults. This is the first study to present evidence of sex differences in the pharmacokinetics of dietary drug contaminants in a vulture species. Chronic exposure to "medications" in entire populations can potentially have sub-lethal health effects that affect fitness differently according to age and sex, with demographic implications for population viability. Specifically, if females have higher mortality after fledging due to high pharmaceutical contamination, this should be considered when modelling the population dynamic of this species for conservation purposes.

Identification of potential invasive alien species in Spain through horizon scanning.

Invasive alien species have widespread impacts on native biodiversity and ecosystem services. Since the number of introductions worldwide is continuously rising, it is essential to prevent the entry, establishment and spread of new alien species through a systematic examination of future potential threats. Applying a three-step horizon scanning consensus method, we evaluated non-established alien species that could potentially arrive, establish and cause major ecological impact in Spain within the next 10 years. Overall, we identified 47 species with a very high risk (e.g. Oreochromis niloticus, Popillia japonica, Hemidactylus frenatus, Crassula helmsii or Halophila stipulacea), 61 with high risk, 93 with moderate risk, and 732 species with low risk. Many of the species categorized as very high or high risk to Spanish biodiversity are either already present in Europe and neighbouring countries or have a long invasive history elsewhere. This study provides an updated list of potential invasive alien species useful for prioritizing efforts and resources against their introduction. Compared to previous horizon scanning exercises in Spain, the current study screens potential invaders from a wider range of terrestrial, freshwater, and marine organisms, and can serve as a basis for more comprehensive risk analyses to improve management and increase the efficiency of the early warning and rapid response framework for invasive alien species. We also stress the usefulness of measuring agreement and consistency as two different properties of the reliability of expert scores, in order to more easily elaborate consensus ranked lists of potential invasive alien species.

Genes acting in synapses and neuron projections are early targets of selection during urban colonization.

When a species colonizes an urban habitat, differences in the environment can create novel selection pressures. Successful colonization will further lead to demographic perturbations and genetic drift, which can interfere with selection. Here, we test for consistent urban selection signals in multiple populations of the burrowing owl (Athene cunicularia), a species that colonized South American cities just a few decades ago. We sequenced 213 owls from three urban-rural population pairs and performed a genome-wide comparison of urban against rural birds. We further studied genome-wide associations with flight initiation distance, a measure of harm avoidance in which urban and rural birds are known to differ. Based on four samples taken over nine years from one of the urban populations, we investigated temporal allele frequency changes. The genomic data were also used to identify urban-specific signatures of selective sweeps. Single genomic sites did not reach genome-wide significance for any association. However, a gene-set analysis on the strongest signals from these four selection scans suggests a significant enrichment of genes with known functions related to synapses and neuron projections. We identified 98 genes predominantly expressed in the brain, of which many may play a role in the modulation of brain connectivity and consequently in cognitive function and motivational behaviour during urbanization. Furthermore, polymorphisms in the promoter region of the synaptic SERT gene - one of the two candidates known to correlate with urban colonization in birds - associated with the habitat in which individuals lived (urban vs. rural).

A protective nesting association with native species counteracts biotic resistance for the spread of an invasive parakeet from urban into rural habitats.

BACKGROUND: Non-native species are often introduced in cities, where they take advantage of microclimatic conditions, resources provided by humans, and competitor/predator release to establish and proliferate. However, native communities in the surrounding rural or natural areas usually halt their spread through biotic resistance, mainly via top-down regulative processes (predation pressure). Here, we show an unusual commensal interaction between exotic and native bird species that favours the spread of the former from urban to rural habitats. RESULTS: We show how Monk parakeets Myiopsitta monachus, an invasive species often introduced in cities worldwide, associated for breeding with a much larger, native species (the white stork Ciconia ciconia) to reduce predation risk in central Spain, thus allowing their colonization of rural areas. Parakeets selected stork nests close to conspecifics and where breeding raptors were less abundant. Parakeets always flushed when raptors approached their nests when breeding alone, but stayed at their nests when breeding in association with storks. Moreover, when storks abandoned a nest, parakeets abandoned it in the following year, suggesting that storks actually confer protection against predators. CONCLUSIONS: Our results show how a protective-nesting association between invasive and native species can counteract biotic resistance to allow the spread of an invasive species across non-urban habitats, where they may become crop pests. Monk parakeet populations are now growing exponentially in several cities in several Mediterranean countries, where they coexist with white storks. Therefore, management plans should consider this risk of spread into rural areas and favour native predators as potential biological controllers.

Climate matching drives spread rate but not establishment success in recent unintentional bird introductions.

Understanding factors driving successful invasions is one of the cornerstones of invasion biology. Bird invasions have been frequently used as study models, and the foundation of current knowledge largely relies on species purposefully introduced during the 19th and early 20th centuries in countries colonized by Europeans. However, the profile of exotic bird species has changed radically in the last decades, as birds are now mostly introduced into the invasion process through unplanned releases from the worldwide pet and avicultural trade. Here we assessed the role of the three main drivers of invasion success (i.e., event-, species-, and location-level factors) on the establishment and spatial spread of exotic birds using an unprecedented dataset recorded throughout the last 100 y in the Iberian Peninsula. Our multimodel inference phylogenetic approach showed that the barriers that need to be overcome by a species to successfully establish or spread are not the same. Whereas establishment is largely related to event-level factors, apparently stochastic features of the introduction (time since first introduction and propagule pressure) and to the origin of introduced species (wild-caught species show higher invasiveness than captive-bred ones), the spread across the invaded region seems to be determined by the extent to which climatic conditions in the new region resemble those of the species' native range. Overall, these results contrast with what we learned from successful deliberate introductions and highlight that different management interventions should apply at different invasion stages, the most efficient strategies being related to event-level factors.

Evolution of genomic variation in the burrowing owl in response to recent colonization of urban areas.

When a species successfully colonizes an urban habitat it can be expected that its population rapidly adapts to the new environment but also experiences demographic perturbations. It is, therefore, essential to gain an understanding of the population structure and the demographic history of the urban and neighbouring rural populations before studying adaptation at the genome level. Here, we investigate populations of the burrowing owl (Athene cunicularia), a species that colonized South American cities just a few decades ago. We assembled a high-quality genome of the burrowing owl and re-sequenced 137 owls from three urban-rural population pairs at 17-fold median sequencing coverage per individual. Our data indicate that each city was independently colonized by a limited number of founders and that restricted gene flow occurred between neighbouring urban and rural populations, but not between urban populations of different cities. Using long-range linkage disequilibrium statistics in an approximate Bayesian computation approach, we estimated consistently lower population sizes in the recent past for the urban populations in comparison to the rural ones. The current urban populations all show reduced standing variation in rare single nucleotide polymorphisms (SNPs), but with different subsets of rare SNPs in different cities. This lowers the potential for local adaptation based on rare variants and makes it harder to detect consistent signals of selection in the genome.

Corticosterone implants produce stress-hyporesponsive birds.

In birds, the use of corticosterone (Cort) implants is a frequent tool aimed at simulating systemic elevations of this hormone and studying effects on biological traits (e.g. physiology, morphology, behavior). This manipulation may alter adrenocortical function, potentially changing both baseline (CortBAS) and stress-induced (CortSTRESS) plasma Cort levels. However, implant effects on the latter trait are rarely measured, disregarding downstream consequences of potentially altered stress responses. Here, we analyzed the effects of Cort implants on both CortBAS and CortSTRESS in nestling and adult European white storks, Ciconia ciconia In addition, we performed a review of 50 studies using Cort implants in birds during the last two decades to contextualize stork results, assess researchers' patterns of use and infer current study biases. High and low doses of Cort implants resulted in a decrease of both CortBAS (31-71% below controls) and CortSTRESS (63-79% below controls) in storks. Our literature review revealed that CortBAS generally increases (72% of experiments) whereas CortSTRESS decreases (78% of experiments) following implant treatment in birds. Our results challenge and expand the prevailing assumption that Cort implants increase circulating CortBAS levels because: (i) CortBAS levels show a quadratic association with implant dose across bird species, and decreased levels may occur at both high and low implant doses, and (ii) Cort implants also decrease CortSTRESS levels, thus producing stress-hyporesponsive phenotypes. It is time to work towards a better understanding of the effects of Cort implants on adrenocortical function, before addressing downstream links to variation in other biological traits.

Selection on a behaviour-related gene during the first stages of the biological invasion pathway.

Human-induced biological invasions are common worldwide and often have negative impacts on wildlife and human societies. Several studies have shown evidence for selection on invaders after introduction to the new range. However, selective processes already acting prior to introduction have been largely neglected. Here, we tested whether such early selection acts on known behaviour-related gene variants in the yellow-crowned bishop (Euplectes afer), a pet-traded African songbird. We tested for nonrandom allele frequency changes after trapping, acclimation and survival in captivity. We also compared the native source population with two independent invasive populations. Allele frequencies of two SNPs in the dopamine receptor D4 (DRD4) gene-known to be linked to behavioural activity in response to novelty in this species-significantly changed over all early invasion stages. They also differed between the African native population and the two invading European populations. The two-locus genotype associated with reduced activity declined consistently, but strongest at the trapping stage. Overall genetic diversity did not substantially decrease, and there is little evidence for new alleles in the introduced populations, indicating that selection at the DRD4 gene predominantly worked on the standing genetic variation already present in the native population. Our study demonstrates selection on a behaviour-related gene during the first stages of a biological invasion. Thus, pre-establishment stages of a biological invasion do not only determine the number of propagules that are introduced (their quantity), but also their phenotypic and genetic characteristics (their quality).

Shared genetic diversity across the global invasive range of the monk parakeet suggests a common restricted geographic origin and the possibility of convergent selection.

While genetic diversity is hypothesized to be an important factor explaining invasion success, there is no consensus yet on how variation in source populations or demographic processes affects invasiveness. We used mitochondrial DNA haplotypic and microsatellite genotypic data to investigate levels of genetic variation and reconstruct the history of replicate invasions on three continents in a globally invasive bird, the monk parakeet (Myiopsitta monachus). We evaluated whether genetic diversity at invasive sites could be explained by (i) the native source populations from which they were derived and (ii) demographic bottlenecks during introduction. Genetic data indicated a localized source area for most sampled invasive populations, with limited evidence for admixing of native source populations. This pattern largely coincides with historical data on pet trade exports. However, the invasive populations are genetically more similar than predicted from the export data alone. The extent of bottleneck effects varied among invasive populations. The observed low genetic diversity, evidence of demographic contraction and restricted source area do not support the hypothesis that invasion is favoured by the mixing and recombining of genetic variation from multiple source populations. Instead, they suggest that reduced genetic variation through random processes may not inhibit successful establishment and invasion in this species. However, convergent selection across invasive sites could also explain the observed patterns of reduction and similarity in genetic variation and/or the restricted source area. In general, the alternative explanation of intraspecific variation in invasive potential among genotypes or geographic areas is neglected, but warrants more attention as it could inform comparative studies and management of biological invaders.

Oral disease is linked to low nestling condition and brood size in a raptor species living in a highly modified environment.

Anthropogenic stressors can favor the occurrence of noninfectious disease that can be worsened by the impact of opportunistic pathogens, making the epizootiology of environmental diseases difficult to unravel. The incidence and impact of oral lesions in nestlings of a facultative scavenger species, the black kite Milvus migrans, were examined over seven breeding seasons in the highly degraded environment close to Madrid, Spain. We found an overall prevalence of 31% of nestlings with oral lesions, with no clear spatial pattern in nests with affected and unaffected individuals. The occurrence and number of oral lesions were negatively associated with nestling body condition and brood size. Broods, where all siblings had oral lesions, were smaller than those where some or all siblings were apparently healthy, suggesting that oral disease could be causing nestling mortality and, consequently, brood size reduction. In turn, nestling body condition was negatively affected by lesion occurrence, brood size, and laying date. Although these relationships were bidirectional, piecewise structural equation modeling analyses showed a greater negative effect of body condition on lesion occurrence than vice versa, indicating that nestlings in poorer body condition were more likely to develop oral lesions (which could contribute to aggravate their state of deterioration) than those in better condition. Nestlings from small broods were also more likely to have oral disease (directly or indirectly through their lower body condition) than nestlings from large broods. Nestlings that hatched last in the broods showed greater development stress than those that hatched first. Anthropogenic stressors could trigger poor body condition, and contribute to microbiota dysbiosis-related diseases. Although further research is needed to determine the consequences for the long-term fitness of individuals, actions should be taken to mitigate adverse conditions that may favor the appearance of environmental diseases associated with peri-urban areas, given their rapid expansion over natural areas.

Nestling sex ratio is unaffected by individual and population traits in the griffon vulture.

Variation in offspring sex ratios is a central topic in animal demography and population dynamics. Most studies have focused on bird species with marked sexual dimorphism and multiple-nestling broods, where the offspring sex ratio is often biased due to different individual or environmental variables. However, biases in offspring sex ratios have been far less investigated in monomorphic and single-egg laying species, and few studies have evaluated long-term and large-scale variations in the sex ratio of nestling vultures. Here, we explore individual and environmental factors potentially affecting the secondary sex ratio of the monomorphic griffon vulture Gyps fulvus. We used information collected at three breeding nuclei from central Spain over a 30-year period (1990-2020) to analyse the effects of nestling age, parental age, breeding phenology, conspecific density, population reproductive parameters, and spatial and temporal variability on nestling sex. Sex ratio did not differ from parity either at the population or the nuclei level. No significant between-year differences were detected, even under highly changing conditions of food availability associated with the mad-cow crisis. We found that tree nesting breeders tend to have more sons than daughters, but as this nesting behavior is rare and we consequently have a small sample size, this issue would require additional examination. Whereas further research is needed to assess the potential effect of breeder identity on nestling sex ratio, this study contributes to understanding the basic ecology and population dynamics of Griffon Vultures, a long-lived species with deferred maturity and low fecundity, whose minor deviations in the offspring sex ratio might imply major changes at the population level.

Correction: Sex, personality and conspecific density influence natal dispersal with lifetime fitness consequences in urban and rural burrowing owls.

[This corrects the article DOI: 10.1371/journal.pone.0226089.].

Intraspecific competition and individual behaviour but not urbanization affect the dietary patterns of a generalist avian predator.

Urbanization has reshaped ecosystems and changed natural processes, driving an intense transformation of biomes, biotic community composition and diversity. Despite the growing interest in studying urban ecology over the last decades, the consequences of these changes on species occupying these ecosystems are not yet fully understood. Trophic generalism and tolerance to human disturbance have been proposed as two key traits in the colonization of urban environments. However, most studies focused on species' average traits, paying less attention to the potential role of inter-individual variability. Here, we examined diet specialization in urban and rural breeding pairs, as well as its relationship with individual behaviour and intraspecific competition, using the burrowing owl as a study model. Our results show that both urban and rural breeding pairs behaved as trophic specialists. The diet of burrowing owl breeding pairs followed a gradient from coleopteran- to micromammal-dominated, which is related to individual behaviour (bolder individuals consuming more coleopterans than shyer ones). Besides, pairs distant from others showed a more diverse diet than those experiencing higher levels of intraspecific competition. Models fitted separately for each habitat showed that the proportion of micromammals in the diet of urban breeding pairs was related to their behavior, while the diet of rural pairs was not affected by individual behavior but by intraspecific competition. However, despite the strong selection of tame and more explorative individuals in urban environments and the higher density they reach in this habitat type, they did not differ in their degree of diet specialization from rural conspecifics. Although it would be necessary to evaluate prey availability on a small scale, our results suggest that burrowing owl breeding pairs behave as specialists, despite the generalist character of the species, and that this specialization is not affected by the occupation of urban environments but to individual behaviour and intraspecific competition.

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.

Large-scale movement patterns in a social vulture are influenced by seasonality, sex, and breeding region.

Quantifying space use and segregation, as well as the extrinsic and intrinsic factors affecting them, is crucial to increase our knowledge of species-specific movement ecology and to design effective management and conservation measures. This is particularly relevant in the case of species that are highly mobile and dependent on sparse and unpredictable trophic resources, such as vultures. Here, we used the GPS-tagged data of 127 adult Griffon Vultures Gyps fulvus captured at five different breeding regions in Spain to describe the movement patterns (home-range size and fidelity, and monthly cumulative distance). We also examined how individual sex, season, and breeding region determined the cumulative distance traveled and the size and overlap between consecutive monthly home-ranges. Overall, Griffon Vultures exhibited very large annual home-range sizes of 5027 ± 2123 km2, mean monthly cumulative distances of 1776 ± 1497 km, and showed a monthly home-range fidelity of 67.8 ± 25.5%. However, individuals from northern breeding regions showed smaller home-ranges and traveled shorter monthly distances than those from southern ones. In all cases, home-ranges were larger in spring and summer than in winter and autumn, which could be related to difference in flying conditions and food requirements associated with reproduction. Moreover, females showed larger home-ranges and less monthly fidelity than males, indicating that the latter tended to use the similar areas throughout the year. Overall, our results indicate that both extrinsic and intrinsic factors modulate the home-range of the Griffon Vulture and that spatial segregation depends on sex and season at the individual level, without relevant differences between breeding regions in individual site fidelity. These results have important implications for conservation, such as identifying key threat factors necessary to improve management actions and policy decisions.

Cuantificar el uso y la segregación del espacio, así como los factores extrínsecos e intrínsecos que los afectan, es crucial para aumentar nuestro conocimiento de la ecología de movimientos de cada especie y diseñar medidas eficaces de gestión y conservación. Esto es especialmente relevante en el caso de especies con gran movilidad y dependientes de recursos tróficos escasos e impredecibles, como son los buitres. En este trabajo se utilizaron datos GPS de 127 buitres leonados Gyps fulvus adultos capturados en cinco regiones de cría diferentes en España para describir los patrones de movimiento (tamaño y fidelidad del área de campeo y distancia acumulada mensual). También examinamos cómo el sexo, la estación del año y la región de cría determinaban la distancia acumulada recorrida y el tamaño y solapamiento entre áreas de campeo mensuales consecutivas. En conjunto, los buitres leonados mostraron un área de campeo anual muy extensa de 5027 ± 2123 km2, una distancia acumulada mensual media de 1776 ± 1497 km y una fidelidad mensual al área de campeo del 67.8 ± 25.5%. Sin embargo, los individuos de las regiones de cría más septentrionales mostraron áreas de campeo más pequeñas y recorrieron distancias mensuales más cortas que los de las más meridionales. En todos los casos, las áreas de campeo fueron mayores en primavera y verano que en otoño e invierno, lo que podría estar relacionado con las diferencias en las condiciones de vuelo y las necesidades tróficas asociadas a la reproducción. Además, las hembras mostraron mayores áreas de campeo y menor fidelidad mensual que los machos, lo que indica que estos últimos tienden a utilizar zonas similares durante todo el año. En conjunto, nuestros resultados indican que tanto los factores extrínsecos como los intrínsecos modulan el área de campeo del buitre leonado y que la segregación espacial depende del sexo y de la estación a nivel individual, sin que existan diferencias relevantes entre las regiones de cría en cuanto a la fidelidad individual al lugar. Estos resultados podrían tener importantes implicaciones para la conservación, como la identificación de los principales factores necesarios para mejorar las medidas de gestión y las decisiones políticas.

Insularity determines nestling sex ratio variation in Egyptian vulture populations.

Variation in offspring sex ratio, particularly in birds, has been frequently studied over the last century, although seldom using long-term monitoring data. In raptors, the cost of raising males and females is not equal, and several variables have been found to have significant effects on sex ratio, including food availability, parental age, and hatching order. Sex ratio differences between island populations and their mainland counterparts have been poorly documented, despite broad scientific literature on the island syndrome reporting substantial differences in population demography and ecology. Here, we assessed individual and environmental factors potentially affecting the secondary sex ratio of the long-lived Egyptian vulture Neophron percnopterus. We used data collected from Spanish mainland and island populations over a ca. 30-year period (1995-2021) to assess the effects of insularity, parental age, breeding phenology, brood size, hatching order, type of breeding unit (pairs vs. trios), and spatial and temporal variability on offspring sex ratio. No sex bias was found at the population level, but two opposite trends were observed between mainland and island populations consistent with the island syndrome. Offspring sex ratio was nonsignificantly female-biased in mainland Spain (0.47, n = 1112) but significantly male-biased in the Canary Islands (0.55, n = 499), where a male-biased mortality among immatures could be compensating for offspring biases and maintaining a paired adult sex ratio. Temporal and spatial variation in food availability might also have some influence on sex ratio, although the difficulties in quantifying them preclude us from determining the magnitude of such influence. This study shows that insularity influences the offspring sex ratio of the Egyptian vulture through several processes that can affect island and mainland populations differentially. Our research contributes to improving our understanding of sex allocation theory by investigating whether sex ratio deviations from parity are possible as a response to changing environments comprised by multiple and complexly interrelated factors.

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.

Apparent Lack of Circovirus Transmission from Invasive Parakeets to Native Birds.

The transmission of pathogens to native species has been highlighted as one of the most important impacts of biological invasions. In this study, we evaluated the presence of psittacine beak and feather disease virus (BFDV) and other circoviruses in native bird species cohabiting with invasive populations of wild rose-ringed (Psittacula krameri) and monk parakeets (Myiopsitta monachus) that were found positive for a particular BFDV genotype in Sevilla, southern Spain. None of the 290 individuals from the 18 native bird species captured showed typical signs of disease caused by BFDV. A sample of 79 individuals from 15 native species showed negative results for the presence of the BFDV genotype previously detected in the sympatric invasive parakeets, as well as any other of the circoviruses tested. Although preliminary, this study suggests a lack of circovirus transmission from invasive parakeets to native birds at the study site. Further research is needed to determine if this apparent absence in transmission depends on the BFDV genotype present in the parakeets, which requires additional screening in other invasive and native populations living in sympatry.