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.].

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.

Ten simple rules for a mom-friendly Academia.

Women (and all gender-discriminated people) are underrepresented in science, especially in leadership positions and higher stages of the scientific career. One of the main causes of career abandonment by women is maternity, with many women leaving Academia after having their first child because of the career penalties associated with motherhood. Thus, more actions to help scientific moms to balance family and academic work are urgently needed to increase representation of women and other gender discriminated people in Academia. Besides mothers, these rules may also benefit other groups such as mothers-to-be, fathers, caregivers, and women in general. Increasing women representation in science, including mothers, is critical because equality is a fundamental right, and because more diverse working environments are more productive and get to more optimal solutions. Here, we describe 10 simple rules that can be adopted in Academia to halt the abandonment of scientific careers by women after motherhood. We strongly encourage their implementation to increase gender diversity and equality in science.

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.

Interspecific synchrony on breeding performance and the role of anthropogenic food subsidies.

Synchrony can have important consequences for long-term metapopulations persistence, community dynamics and ecosystems functioning. While the causes and consequences of intra-specific synchrony on population size and demographic rates have received considerable attention only a few factors that may affect inter-specific synchrony have been described. We formulate the hypothesis that food subsidies can buffer the influence of environmental stochasticity on community dynamics, disrupting and masking originally synchronized systems. To illustrate this hypothesis, we assessed the consequences of European policies implementation affecting subsidy availability on the temporal synchrony of egg volume as a proxy of breeding investment in two sympatric marine top predators with differential subsidy use. We show how 7-year synchrony appears on egg volume fluctuations after subsidy cessation suggesting that food subsidies could disrupt interspecific synchrony. Moreover, cross correlation increased after subsidy cessation and environmental buffering seems to act during synchronization period. We emphasize that subsidies dynamics and waste management provide novel insights on the emergence of synchrony in natural populations.

It's not all abundance: Detectability and accessibility of food also explain breeding investment in long-lived marine animals.

Large-scale climatic indices are extensively used as predictors of ecological processes, but the mechanisms and the spatio-temporal scales at which climatic indices influence these processes are often speculative. Here, we use long-term data to evaluate how a measure of individual breeding investment (the egg volume) of three long-lived and long-distance-migrating seabirds is influenced by i) a large-scale climatic index (the North Atlantic Oscillation) and ii) local-scale variables (food abundance, foraging conditions, and competition). Winter values of the North Atlantic Oscillation did not correlate with local-scale variables measured in spring, but surprisingly, both had a high predictive power of the temporal variability of the egg volume in the three study species, even though they have different life-history strategies. The importance of the winter North Atlantic Oscillation suggests carry-over effects of winter conditions on subsequent breeding investment. Interestingly, the most important local-scale variables measured in spring were associated with food detectability (foraging conditions) and the factors influencing its accessibility (foraging conditions and competition by density-dependence). Large-scale climatic indices may work better as predictors of foraging conditions when organisms perform long distance migrations, while local-scale variables are more appropriate when foraging areas are more restricted (e.g. during the breeding season). Contrary to what is commonly assumed, food abundance does not directly translate into food intake and its detectability and accessibility should be considered in the study of food-related ecological processes.

Multi-species prey dynamics influence local survival in resident and wintering generalist predators.

Stochasticity in food availability influences vital rates such as survival and fertility. Life-history theory predicts that in long-lived organisms, survival should be buffered against environmental stochasticity showing little temporal variability. Furthermore, to optimize survival prospects, many animal species perform migrations to wintering areas where food availability is larger. Species with large latitudinal distribution ranges may show populations that migrate and others that are resident, and they may co-occur in winter. One example of these species is the predatory raptor buzzard Buteo buteo. Here, we test whether temporal variability in the density of five small mammal species of prey inhabiting different habitats (shrubland and forests) influences local annual survival of buzzards in a wintering area depending on their age and residency status (residents versus wintering individuals). We found that prey density explained a considerable amount of annual changes in local survival, which was higher for older and resident birds. This difference in local survival likely corresponded to philopatry to the wintering area, which was larger for residents and increased when prey density was larger. The total density of prey inhabiting open shrublands was the variable explaining more variance in temporal variability of local survival, even though the study area is mostly occupied by woodlands. Temporal population dynamics of the different small mammals inhabiting shrublands were not synchronous, which suggests that buzzards preyed opportunistically on the most abundant prey each winter. Generalist predation may buffer the impact of resource unpredictability for pulsed and asynchronous prey dynamics, typical of small mammals in winter.

The trade-offs of foraging at landfills: Landfill use enhances hatching success but decrease the juvenile survival of their offspring on white storks (Ciconia ciconia).

During the last decades, landfills have become a valuable food source for wildlife, being in some cases determinants of large avian population increases. Superabundant food resources at landfills can increase reproductive and/or survival parameters; however, negative effects such as intoxication, plastic ingestion, skeletal deformities, unbalanced oxidative stress, and other health problems have also been reported. White stork (Ciconia ciconia) commonly benefits from landfill resources. Here, we evaluate potential landfill effects on demographic parameters (reproduction and offspring survival) at the individual level in a single population. Our results show that a more intense use of landfills by breeders has a positive effect on hatching success but a negative effect on juvenile survival probability after emancipation, at least during the first year of life. High amount of food and proximity to landfill may explain their beneficial effect on reproductive parameters. On the other hand, poor quality food, pollutants, and pathogens acquired during early development from a diet based on refuse may be responsible for reduced future survival probability. Consequently, both positive and negative effects were detected, being foraging at landfills at low to medium levels the better strategy. Although our study shows that intense foraging on rubbish can imply both costs and benefits at an individual level, the benefits of superabundant food provisioning observed at population level by other studies cannot be ignored. Management actions should be designed to improve natural food resources, reduce non-natural mortality and/or human disturbances to guarantee the species viability under current European Union regulations designed to ban open-air landfills in a near future.

Urban life promotes delayed dispersal and family living in a non-social bird species.

In some vertebrate species, family units are typically formed when sexually mature individuals delay dispersal and independent breeding to remain as subordinates in a breeding group. This behaviour has been intensively studied in gregarious species but has also been described in non-social species where ecological and evolutionary drivers are less known. Here, we explore factors that favour delayed dispersal and family living and potential benefits associated with this strategy in a non-social, monogamous species (the burrowing owl, Athene cunicularia) occupying urban and rural habitats. Our results show that family units arise when first-year individuals, mainly males, delay their dispersal to stay in their natal nests with their parents. This delayed dispersal, while still uncommon, was more prevalent in urban (7%) than in rural (3%) habitats, and in areas with high conspecific density and productivity. Birds delaying dispersal contributed to the genetic pool of the offspring in 25% of the families analysed, but did not increase the productivity of the nests where they remained. However, their presence was related to an improvement in the body condition of chicks, which was ultimately linked to a slightly positive effect in offspring future survival probabilities. Finally, delayed dispersers were recruited as breeders in high-quality urban territories and closer to their natal nests than individuals dispersing during their first year of life. Thus, our results suggest that delaying dispersal may be mainly related to opportunities to inheriting a good quality territory, especially for males. Our study contributes to understanding the role played by habitat quality in promoting delayed dispersal and family living, not only in social but also non-social species, highlighting its impact in the ecology and evolution of animal populations.

Sperm storage reduces the strength of the mate-finding Allee effect.

Mate searching is a key component of sexual reproduction that can have important implications for population viability, especially for the mate-finding Allee effect. Interannual sperm storage by females may be an adaptation that potentially attenuates mate limitation, but the demographic consequences of this functional trait have not been studied. Our goal is to assess the effect of female sperm storage durability on the strength of the mate-finding Allee effect and the viability of populations subject to low population density and habitat alteration. We used an individual-based simulation model that incorporates realistic representations of the demographic and spatial processes of our model species, the spur-thighed tortoise (Testudo graeca). This allowed for a detailed assessment of reproductive rates, population growth rates, and extinction probabilities. We also studied the relationship between the number of reproductive males and the reproductive rates for scenarios combining different levels of sperm storage durability, initial population density, and landscape alteration. Our results showed that simulated populations parameterized with the field-observed demographic rates collapsed for short sperm storage durability, but were viable for a durability of one year or longer. In contrast, the simulated populations with a low initial density were only viable in human-altered landscapes for sperm storage durability of 4 years. We find that sperm storage is an effective mechanism that can reduce the strength of the mate-finding Allee effect and contribute to the persistence of low-density populations. Our study highlights the key role of sperm storage in the dynamics of species with limited movement ability to facilitate reproduction in patchy landscapes or during population expansion. This study represents the first quantification of the effect of sperm storage durability on population dynamics in different landscapes and population scenarios.

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

There is a growing need to understand how species respond to habitat changes and the potential key role played by natal dispersal in population dynamics, structure and gene flow. However, few studies have explored differences in this process between conspecifics living in natural habitats and those inhabiting landscapes highly transformed by humans, such as cities. Here, we investigate how individual traits and social characteristics can influence the natal dispersal decisions of burrowing owls (Athene cunicularia) living in urban and rural areas, as well as the consequences in terms of reproductive success and apparent survival. We found short dispersal movements among individuals, with differences between urban and rural birds (i.e., the former covering shorter distances than the latter), maybe because of the higher conspecific density of urban compared to rural areas. Moreover, we found that urban and rural females as well as bold individuals (i.e., individuals with shorter flight initiation distance) exhibited longer dispersal distances than their counterparts. These dispersal decisions have effects on individual fitness. Individuals traveling longer distances increased their reproductive prospects (productivity during the first breeding attempt, and long term productivity). However, the apparent survival of females decreased when they dispersed farther from their natal territory. Although further research is needed to properly understand the ecological and evolutionary consequences of dispersal patterns in transformed habitats, our results provide information about the drivers and the consequences of the restricted natal movements of this species, which may explain its population structuring through restricted gene flow between and within urban and rural areas.

Author Correction: Personality-dependent breeding dispersal in rural but not urban burrowing owls.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Infestation of small seabirds by Ornithodoros maritimus ticks: Effects on chick body condition, reproduction and associated infectious agents.

Ticks can negatively affect their host by direct effects as blood feeding causing anaemia or discomfort, or by pathogen transmission. Consequently, ticks can have an important role in the population dynamics of their hosts. However, specific studies on the demographic effects of tick infestation on seabirds are still scarce. Seabird ticks have also the potential to be responsible for the circulation of little known tick-borne agents, which could have implications for non-seabird species. Here, we report the results of investigations on potential associations between soft tick Ornithodoros maritimus load and reproductive parameters of storm petrels Hydrobates pelagicus breeding in a large colony in a cave of Espartar Island, in the Balearic archipelago. We also investigated by molecular analyses the potential viral and bacterial pathogens associated with O. maritimus ticks present at the colony. Lower nestling survival was recorded in the most infested area, deep in the cave, compared to the area near the entrance. The parasite load was negatively associated with the body condition of the nestlings. One pool of ticks tested positive for West Nile virus and 4 pools tested positive for a Borrelia species which was determined by targeted nested PCR to have a 99% sequence identity with B. turicatae, a relapsing fever Borrelia. Overall, these results show that further investigations are needed to better understand the ecology and epidemiology of the interactions between ticks, pathogens and Procellariiform species.

Unravelling the sex- and age-specific impact of poaching mortality with multievent modeling.

BACKGROUND: Poaching is a prominent source of 'hidden hurdles', cryptic impacts of human activities that may hinder the conservation of animal populations. Estimating poaching mortality is challenging, as the evidence for illegal killing is not outwardly obvious. Using resighting and recovery data collected on 141 marked red deer Cervus elaphus within the Stelvio National Park (central Italian Alps), we show how multievent models allow to assess the direct impacts of illegal harvesting on age- and sex-specific survival, accounting for uncertainty over mortality causes. RESULTS: Mortality caused by poaching was consistently higher for males than for females in all age classes. In males, the probability of dying from poaching was higher for extreme age classes, while in females all age classes showed fairly similar values of poaching mortality. The strong bias in sex-specific poaching mortality was possibly due to trophy killing in adult males and 'bushmeat-like' killing for private or commercial gain in young males and in females. CONCLUSIONS: A robust assessment of age- and sex-specific prevalence of poaching in wildlife populations is pivotal when illegal killing is of conservation concern. This provides timely information on what segment of the population is most likely to be affected. Besides obvious demographic consequences on small populations, age- and sex-biased poaching prevalence may contrast with the need to maintain ecosystem complexity and may alter behavioral responses to human presence. The information provided by multievent models, whose flexibility makes them adaptable to many systems where individual-based data is part of population monitoring, offers a support to design appropriate strategies for the conservation of wildlife populations.

Personality-dependent breeding dispersal in rural but not urban burrowing owls.

Dispersal propensity has been correlated with personality traits, conspecific density and predation risk in a variety of species. Thus, changes in the relative frequency of behavioural phenotypes or in the ecological pressures faced by individuals in contrasting habitats can have unexpected effects on their dispersal strategies. Here, using the burrowing owl Athene cunicularia as a study model, we test whether changes in the behavioural profile of individuals and changes in conspecific density and predation pressure associated with urban life influence their breeding dispersal decisions compared to rural conspecifics. Our results show that breeding dispersal behaviour differs between rural and urban individuals. Site fidelity was lower among rural than among urban birds, and primarily related to an individual's behaviours (fear of humans), which has been reported to reflect individual personality. In contrast, the main determinant of site fidelity among urban owls was conspecific density. After taking the decision of dispersing, urban owls moved shorter distances than rural ones, with females dispersing farther than males. Our results support a personality-dependent dispersal pattern that might vary with predation risk. However, as multiple individuals of two populations (one urban, one rural) were used for this research, differences can thus also be caused by other factors differing between the two populations. Further research is needed to properly understand the ecological and evolutionary consequences of changes in dispersal behaviours, especially in terms of population structuring and gene flow between urban and rural populations.

Estimating age-dependent survival when juveniles resemble females: Invasive ring-necked parakeets as an example.

Many species only show sexual dimorphism at the age of maturity, such that juveniles typically resemble females. Under these circumstances, estimating accurate age-specific demographic parameters is challenging. Here, we propose a multievent model parameterization able to estimate age-dependent survival using capture-recapture data with uncertainty in age and sex assignment of individuals. We illustrate this modeling approach with capture-recapture data from the ring-necked parakeet Psittacula krameri. We analyzed capture, recapture, and resighting data (439 recaptures/resightings) of 156 ring-necked parakeets tagged with neck collars in Barcelona city from 2003 to 2016 to estimate the juvenile and adult survival rate. Our models successfully estimated the survival probabilities of the different age classes considered. Survival probability was similar between adults (0.83, 95% CI = 0.77-0.87) and juveniles during their second (0.79, 95% CI = 0.58-0.87) and third winter (0.83, 95% CI = 0.65-0.88). The youngest juveniles (1st winter) showed a slightly lower survival (0.57, 95% CI = 0.37-0.79). Among adults, females showed a slightly higher survival than males (0.87, 95% CI = 0.78-0.93; and 0.80, 95% CI = 0.73-0.86, respectively). These high survival figures predict high population persistence in this species and urge management policies. The analysis also stresses the usefulness of multievent models to estimate juvenile survival when age cannot be fully ascertained.

Sex- and age-dependent patterns of survival and breeding success in a long-lived endangered avian scavenger.

In long-lived species, the age-, stage- and/or sex-dependent patterns of survival and reproduction determine the evolution of life history strategies, the shape of the reproductive value, and ultimately population dynamics. We evaluate the combined effects of age and sex in recruitment, breeder survival and breeding success of the globally endangered Egyptian vulture (Neophron percnopterus), using 31-years of exhaustive data on marked individuals in Spain. Mean age of first reproduction was 7-yrs for both sexes, but females showed an earlier median and a larger variance than males. We found an age-related improvement in breeding success at the population level responding to the selective appearance and disappearance of phenotypes of different quality but unrelated to within-individual aging effects. Old males (≥8 yrs) showed a higher survival than both young males (≤7 yrs) and females, these later in turn not showing aging effects. Evolutionary trade-offs between age of recruitment and fitness (probably related to costs of territory acquisition and defense) as well as human-related mortality may explain these findings. Sex- and age-related differences in foraging strategies and susceptibility to toxics could be behind the relatively low survival of females and young males, adding a new concern for the conservation of this endangered species.

Oceanographic drivers and mistiming processes shape breeding success in a seabird.

Understanding the processes driving seabirds' reproductive performance through trophic interactions requires the identification of seasonal pulses in marine productivity. We investigated the sequence of environmental and biological processes driving the reproductive phenology and performance of the storm petrel (Hydrobates pelagicus) in the Western Mediterranean. The enhanced light and nutrient availability at the onset of water stratification (late winter/early spring) resulted in annual consecutive peaks in relative abundance of phytoplankton, zooplankton and ichthyoplankton. The high energy-demanding period of egg production and chick rearing coincided with these successive pulses in food availability, pointing to a phenological adjustment to such seasonal patterns with important fitness consequences. Indeed, delayed reproduction with respect to the onset of water stratification resulted in both hatching and breeding failure. This pattern was observed at the population level, but also when confounding factors such as individuals' age or experience were also accounted for. We provide the first evidence of oceanographic drivers leading to the optimal time-window for reproduction in an inshore seabird at southern European latitudes, along with a suitable framework for assessing the impact of environmentally driven changes in marine productivity patterns in seabird performance.

Links between fear of humans, stress and survival support a non-random distribution of birds among urban and rural habitats.

Urban endocrine ecology aims to understand how organisms cope with new sources of stress and maintain allostatic load to thrive in an increasingly urbanized world. Recent research efforts have yielded controversial results based on short-term measures of stress, without exploring its fitness effects. We measured feather corticosterone (CORTf, reflecting the duration and amplitude of glucocorticoid secretion over several weeks) and subsequent annual survival in urban and rural burrowing owls. This species shows high individual consistency in fear of humans (i.e., flight initiation distance, FID), allowing us to hypothesize that individuals distribute among habitats according to their tolerance to human disturbance. FIDs were shorter in urban than in rural birds, but CORTf levels did not differ, nor were correlated to FIDs. Survival was twice as high in urban as in rural birds and links with CORTf varied between habitats: while a quadratic relationship supports stabilizing selection in urban birds, high predation rates may have masked CORTf-survival relationship in rural ones. These results evidence that urban life does not constitute an additional source of stress for urban individuals, as shown by their near identical CORTf values compared with rural conspecifics supporting the non-random distribution of individuals among habitats according to their behavioural phenotypes.