Vultures as an overlooked model in cognitive ecology.

Despite important recent advances in cognitive ecology, our current understanding of avian cognition still largely rests on research conducted on a few model taxa. Vultures are an ecologically distinctive group of species by being the only obligate carrion consumers across terrestrial vertebrates. Their unique scavenging lifestyle suggests they have been subject to particular selective pressures to locate scarce, unpredictable, ephemeral, and nutritionally challenging food. However, substantial variation exists among species in diet, foraging techniques and social structure of populations. Here, we provide an overview of the current knowledge on vulture cognition through a comprehensive literature review and a compilation of our own observations. We find evidence for a variety of innovative foraging behaviors, scrounging tactics, collective problem-solving abilities and tool-use, skills that are considered indicative of enhanced cognition and that bear clear connections with the eco-social lifestyles of species. However, we also find that the cognitive basis of these skills remain insufficiently studied, and identify new research areas that require further attention in the future. Despite these knowledge gaps and the challenges of working with such large animals, we conclude that vultures may provide fresh insight into our knowledge of the ecology and evolution of cognition.

Heterogeneous selection on exploration behavior within and among West European populations of a passerine bird.

Heterogeneous selection is often proposed as a key mechanism maintaining repeatable behavioral variation ("animal personality") in wild populations. Previous studies largely focused on temporal variation in selection within single populations. The relative importance of spatial versus temporal variation remains unexplored, despite these processes having distinct effects on local adaptation. Using data from >3,500 great tits (Parus major) and 35 nest box plots situated within five West-European populations monitored over 4 to 18 y, we show that selection on exploration behavior varies primarily spatially, across populations, and study plots within populations. Exploration was, simultaneously, selectively neutral in the average population and year. These findings imply that spatial variation in selection may represent a primary mechanism maintaining animal personalities, likely promoting the evolution of local adaptation, phenotype-dependent dispersal, and nonrandom settlement. Selection also varied within populations among years, which may counteract local adaptation. Our study underlines the importance of combining multiple spatiotemporal scales in the study of behavioral adaptation.

Disentangling drivers of power line use by vultures: Potential to reduce electrocutions.

Accidents on power lines are the leading cause of mortality for many raptor species. In order to prioritise corrective measures, much effort has been focused on identifying the factors associated with collision and electrocution risk. However, most studies lack of precise data about the use of pylons and its underlying driving factors, often relying on biased information based on recorded fatalities. Here, we used multiple years of high-resolution data from 49-GPS tagged Canarian Egyptian Vultures (Neophron percnopterus majorensis) to overcome these typical biases. Birds of our target population use electric pylons extensively for perching (diurnal) and roosting (nocturnal), so accidents with these infrastructures are nowadays the main cause of mortality. Predictive models of pylon intensity of use were fitted for diurnal and nocturnal behaviour, accounting for power line, environmental, and individual vulture's features. Using these measures as a proxy for mortality risk, our model predictions were validated with out-of-sample data of actual mortality recorded during 17 years. Vultures used more pylons during daytime, but those chosen at night were used more intensively. In both time periods, the intensity of use of pylons was determined by similar drivers: vultures avoided pylons close to roads and territories of conspecifics, preferentially used pylons located in areas with higher abundance of food resources, and spread their use during the breeding season. Individuals used pylons unevenly according to their sex, age, and territorial status, indicating that site-specific mitigation measures may affect different fractions of the population. Our modelling procedures predicted actual mortality reasonably well, showing that prioritising mitigation measures on relatively few pylons (6%) could drastically reduce accidents (50%). Our findings demonstrate that combining knowledge on fine-scale individual behaviour and pylon type and distribution is key to target cost-effective conservation actions aimed at effectively reducing avian mortality on power lines.

Vultures and Livestock: The Where, When, and Why of Visits to Farms.

Recent changes in European legislation have legalized the abandonment of carcasses around livestock farms, but our understanding of how vultures exploit these semi-predictable food sources is still very limited. For filling this gap, we determine the individual and ecological drivers influencing vulture visits to farms. We assessed the effects of individual characteristics of both birds and farms on the frequency of vultures' visits to livestock facilities using data collected from 45 GPS-tagged Egyptian Vultures (Neophron percnopterus) and 318 farms (>94% of livestock) on Fuerteventura Island, Spain. Farms were more visited during the vultures' breeding season. Farms located closer to highly predictable feeding places (i.e., vulture restaurants and garbage dumps) or with more available feeding resources were visited by more vultures, whereas those located close to roads and vultures' breeding territories received fewer visits. Younger territorial birds visited a farm more frequently than older territorial ones, whereas older non-territorial individuals concentrated those visits on farms closer to their activity core areas compared with younger ones. Our findings indicate that visits to farms were determined by their spatial distribution in relation to the age-specific birds' activity centers, the availability of carcasses, seasonality, and individual characteristics of vultures. These interacting factors should be considered in vulture conservation, avoiding very general solutions that ignore population structure.

Too much is bad: increasing numbers of livestock and conspecifics reduce body mass in an avian scavenger.

Individual traits such as body mass can serve as early warning signals of changes in the fitness prospects of animal populations facing environmental impacts. Here, taking advantage of a 19-yr monitoring, we assessed how individual, population, and environmental factors modulate long-term changes in the body mass of Canarian Egyptian vultures. Individual vulture body mass increased when primary productivity was highly variable, but decreased in years with a high abundance of livestock. We hypothesized that carcasses of wild animals, a natural food resource that can be essential for avian scavengers, could be more abundant in periods of weather instability but depleted when high livestock numbers lead to overgrazing. In addition, increasing vulture population numbers also negatively affect body mass suggesting density-dependent competition for food. Interestingly, the relative strength of individual, population and resource availability factors on body mass changed with age and territorial status, a pattern presumably shaped by differences in competitive abilities and/or age-dependent environmental knowledge and foraging skills. Our study supports that individual plastic traits may be extremely reliable tools to better understand the response of secondary consumers to current and future natural and human-induced environmental changes.

Food predictability and social status drive individual resource specializations in a territorial vulture.

Despite increasing work detailing the presence of foraging specializations across a range of taxa, limited attention so far has been given to the role of spatiotemporal variation in food predictability in shaping individual resource selection. Here, we studied the exploitation of human-provided carrion resources differing in predictability by Canarian Egyptian vultures (Neophron percnopterus majorensis). We focussed specifically on the role of individual characteristics and spatial constraints in shaping patterns of resource use. Using high-resolution GPS data obtained from 45 vultures tracked for 1 year, we show that individual vultures were repeatable in both their monthly use of predictable and semi-predicable resources (feeding station vs. farms) and monthly levels of mobility (home range size and flight activity). However, individual foraging activities were simultaneously characterized by a high degree of (temporal) plasticity in the use of the feeding station in specific months. Individual rank within dominance hierarchy revealed sex-dependent effects of social status on resource preference in breeding adults, illustrating the potential complex social mechanisms underpinning status-dependent resource use patterns. Our results show that predictable food at feeding stations may lead to broad-scale patterns of resource partitioning and affect both the foraging and social dynamics within local vulture populations.

Seasonal- and sex-specific correlations between dispersal and exploratory behaviour in the great tit.

While the importance of personality in explaining individual dispersal strategies is increasingly recognized, limited information is still available on how patterns of personality-dependent dispersal may develop, hampering our understanding of the ecological significance of behavioural dispersal syndromes. Here, we examine the relative importance of personality at different stages of dispersal in the great tit, by analysing the sex-specific relationship between exploratory behaviour (EB; quantified in a novel environment) and dispersal distances in different seasons over the course of the first year of life (summer, autumn, winter, and until the first breeding attempt). In females, we found that EB was an important predictor of dispersal distances in summer and autumn, but only a weak to moderate correlation remained for females captured in winter or for natal dispersal distances based on first breeding records. We obtained a contrasting pattern at the population level, whereby male (but not female) immigrants captured in summer and autumn had higher EB scores than locally born birds, while this was not the case in birds captured in winter and those recruited as breeders into the population. In addition to providing further evidence for the existence of a behaviour dispersal syndrome in birds, our results show that correlations between EB and dispersal appear strongest at the early stages of the dispersal process, rather than being developed gradually. These findings show the importance of analysing the effect of phenotypic attributes on dispersal across different stages of the dispersal phenomenon and in each sex separately.

Genetic integration of local dispersal and exploratory behaviour in a wild bird.

Dispersal is a major determinant of the ecological and evolutionary dynamics of natural populations. Individuals differ greatly in the likelihood and distance of dispersal, but it is generally unclear to what extent intrinsic, possibly genetic, differences contribute. Here we present the first explicit empirical evidence for genetic coupling of local dispersal and exploratory behaviour, a key 'animal personality' trait. Using relatedness data from a multi-generation pedigree of free-living great tits (Parus major), we find quantitative genetic variation for both the distance of local dispersal within our study area and the rate at which individuals explore a novel environment. Moreover, we find a strongly positive genetic correlation between local dispersal distance and exploration rate, despite a weak and non-significant phenotypic correlation. These findings demonstrate a potentially important behavioural mechanism underlying heritable differences in local dispersal and highlight the potential for concerted evolution of dispersal and animal personality in response to selection.

Haplotype structure, adaptive history and associations with exploratory behaviour of the DRD4 gene region in four great tit (Parus major) populations.

The assessment of genetic architecture and selection history in genes for behavioural traits is fundamental to our understanding of how these traits evolve. The dopamine receptor D4 (DRD4) gene is a prime candidate for explaining genetic variation in novelty seeking behaviour, a commonly assayed personality trait in animals. Previously, we showed that a single nucleotide polymorphism in exon 3 of this gene is associated with exploratory behaviour in at least one of four Western European great tit (Parus major) populations. These heterogeneous association results were explained by potential variable linkage disequilibrium (LD) patterns between this marker and the causal variant or by other genetic or environmental differences among the populations. Different adaptive histories are further hypothesized to have contributed to these population differences. Here, we genotyped 98 polymorphisms of the complete DRD4 gene including the flanking regions for 595 individuals of the four populations. We show that the LD structure, specifically around the original exon 3 SNP is conserved across the four populations and does not explain the heterogeneous association results. Study-wide significant associations with exploratory behaviour were detected in more than one haplotype block around exon 2, 3 and 4 in two of the four tested populations with different allele effect models. This indicates genetic heterogeneity in the association between multiple DRD4 polymorphisms and exploratory behaviour across populations. The association signals were in or close to regions with signatures of positive selection. We therefore hypothesize that variation in exploratory and other dopamine-related behaviour evolves locally by occasional adaptive shifts in the frequency of underlying genetic variants.

Personality and information gathering in free-ranging great tits.

One aspect of animal personality that has been well described in captivity, but received only little attention in studies in the wild, is that personality types may vary in their behavioural flexibility towards environmental changes. A fundamental factor underlying such differences is believed to be the degree to which individual behavior is guided by environmental stimuli. We tested this hypothesis in the wild using free-ranging great tits. Personality variation was quantified using exploratory behaviour in a novel environment, which has previously been shown to be repeatable and correlated with other behaviours in this and other populations of the same species. By temporarily removing food at feeding stations we examined whether birds with different personality differed in returning to visit empty feeders as this may provide information on how birds continue to sample their environment after a sudden change in conditions. In two summer experiments, we found that fast-exploring juveniles visited empty feeders less often compared to slow-exploring juveniles. In winter, sampling behaviour was sex dependent but not related to personality. In both seasons, we found that birds who sampled empty feeders more often were more likely to rediscover food after we again re-baited the feeding stations, but there was no effect of personality. Our results show that personality types may indeed differ in ways of collecting environmental information, which is consistent with the view of personalities as different styles of coping with environmental changes. The adaptive value of these alternative behavioural tactics, however, needs to be further explored.

Variation in personality and behavioural plasticity across four populations of the great tit Parus major.

1. Interest in the evolutionary origin and maintenance of individual behavioural variation and behavioural plasticity has increased in recent years. 2. Consistent individual behavioural differences imply limited behavioural plasticity, but the proximate causes and wider consequences of this potential constraint remain poorly understood. To date, few attempts have been made to explore whether individual variation in behavioural plasticity exists, either within or between populations. 3. We assayed 'exploration behaviour' among wild-caught individual great tits Parus major when exposed to a novel environment room in four populations across Europe. We quantified levels of individual variation within and between populations in average behaviour, and in behavioural plasticity with respect to (i) repeated exposure to the room (test sequence), (ii) the time of year in which the assays were conducted and (iii) the interval between successive tests, all of which indicate habituation to novelty and are therefore of functional significance. 4. Consistent individual differences ('I') in behaviour were present in all populations; repeatability (range: 0.34-0.42) did not vary between populations. Exploration behaviour was also plastic, increasing with test sequence - but less so when the interval between subsequent tests was relatively large - and time of year; populations differed in the magnitude of plasticity with respect to time of year and test interval. Finally, the between-individual variance in exploration behaviour increased significantly from first to repeat tests in all populations. Individuals with high initial scores showed greater increases in exploration score than individuals with low initial scores; individual by environment interaction ('I × E') with respect to test sequence did not vary between populations. 5. Our findings imply that individual variation in both average level of behaviour and behavioural plasticity may generally characterize wild great tit populations and may largely be shaped by mechanisms acting within populations. Experimental approaches are now needed to confirm that individual differences in behavioural plasticity (habituation) - not other hidden biological factors - caused the observed patterns of I × E. Establishing the evolutionary causes and consequences of this variation in habituation to novelty constitutes an exciting future challenge.

Association between DRD4 gene polymorphism and personality variation in great tits: a test across four wild populations.

Polymorphisms in the dopamine receptor D4 gene (DRD4) have been related to individual variation in novelty-seeking or exploratory behaviour in a variety of animals, including humans. Recently, the human DRD4 orthologue was sequenced in a wild bird, the great tit (Parus major) and a single nucleotide polymorphism in exon 3 of this gene (SNP830) was shown to be associated with variation in exploratory behaviour of lab-raised individuals originating from a single wild population. Here we test the generality of this finding in a large sample of free-living individuals from four European great tit populations, including the originally sampled population. We demonstrate that the association between SNP830 genotype and exploratory behaviour also exists in free-living birds from the original population. However, in the other three populations we found only limited evidence for an association: in two populations the association appeared absent; while in one there was a nonsignificant tendency. We could not confirm a previously demonstrated interaction with another DRD4 polymorphism, a 15 bp indel in the promoter region (ID15). As yet unknown differences in genetic or environmental background could explain why the same genetic polymorphism (SNP830) has a substantial effect on exploratory behaviour in one population, explaining 4.5-5.8% of the total variance-a large effect for a single gene influencing a complex behavioural trait-but not in three others. The confirmation of an association between SNP830 genotype and personality-related behaviour in a wild bird population warrants further research into potential fitness effects of the polymorphism, while also the population differences in the strength of the association deserve further investigation. Another important future challenge is the identification of additional loci influencing avian personality traits in the wild.

Family movements before independence influence natal dispersal in a territorial songbird.

Dispersal behaviour in territorial species is typically assumed to be independent of parental behaviour except for the possible role of parental eviction from the natal territory. Great tits defend exclusive territories at the onset of breeding but after fledging undertake substantial excursions with dependent offspring, sometimes covering distances equivalent to ten or more breeding territories and even moving across open spaces into neighbouring woodlots. We show that postfledging family movements are significantly associated with subsequent dispersal directions of recruits by comparing observed angles of movement with a simulated distribution taking into account the patchy nature of the landscape. However, the extent of family movements did not predict dispersal distances. Our findings provide an explanation for previously observed similarities in dispersal direction between siblings in the same study population, as well as for effects of nest site location on dispersal. More generally we show the existence of a novel mechanism for parents to influence dispersal and fine-scale kinship structure among their offspring.

Personality predicts spatial responses to food manipulations in free-ranging great tits (Parus major).

Personality differences measured under standardized lab-conditions are assumed to reflect differences in the way individuals cope with spatio-temporal changes in their natural environment, but few studies have examined how these are expressed in the field. We tested whether exploratory behaviour in a novel environment predicts how free-living individual great tits (Parus major) react to a change in food supply. We temporarily removed food at feeding stations during two summers and recorded the behavioural response of juvenile birds to these food manipulations using radio-tracking. When challenged by an abrupt change in food supply, fast-exploring individuals more rapidly switched to different foraging areas at longer distances from the feeder. This study is the first to show that personality traits predict the spatial response to experimentally induced changes in their natural environment.