What's in a mate? Social pairing decisions and spatial cognitive ability in food-caching mountain chickadees.

While researchers have investigated mating decisions for decades, gaps remain in our understanding of how behaviour influences social mate choice. We compared spatial cognitive performance and food caching propensity within social pairs of mountain chickadees inhabiting differentially harsh winter climates to understand how these measures contribute to social mate choice. Chickadees rely on specialized spatial cognitive abilities to recover food stores and survive harsh winters, and females can discriminate among males with varying spatial cognition. Because spatial cognition and caching propensity are critical for survival and likely heritable, pairing with a mate with such enhanced traits may provide indirect benefits to offspring. Comparing the behaviour of social mates, we found that spatial cognitive performance approached a significant correlation within pairs at low, but not at high elevation. We found no correlation within pairs in spatial reversal cognitive performance at either elevation; however, females at high elevation tended to perform better than their social mates. Finally, we found that caching propensity correlated within pairs at low, while males cached significantly more food than their social mates at high elevations. These results suggest that cognition and caching propensity may influence social mating decisions, but only in certain environments and for some aspects of cognition.

Food-caching chickadees with specialized spatial cognition do not use scrounging as a stable strategy when learning a spatial task.

Social animals may use alternative strategies when foraging, with producer-scrounger being one stable dichotomy of strategies. While 'producers' search and discover new food sources, 'scroungers' obtain food discovered by producers. Previous work suggests that differences in cognitive abilities may influence tendencies toward being either a producer or a scrounger, but scrounging behaviour in the context of specialized cognitive abilities is less understood. We investigated whether food-caching mountain chickadees, which rely on spatial cognition to retrieve food caches, engage in scrounging when learning a spatial task. We analysed data from seven seasons of spatial cognition testing, using arrays of radio frequency identification-enabled bird feeders, to identify and quantify potential scrounging behaviour. Chickadees rarely engaged in scrounging, scrounging was not repeatable within individuals and nearly all scrounging events occurred before the bird learned the 'producer' strategy. Scrounging was less frequent in harsher winters, but adults scrounged more than juveniles, and birds at higher elevations scrounged more than chickadees at lower elevations. There was no clear association between spatial cognitive abilities and scrounging frequency. Overall, our study suggests that food-caching species with specialized spatial cognition do not use scrounging as a stable strategy when learning a spatial task, instead relying on learning abilities.

Natural variation in developmental condition has limited effect on spatial cognition in a wild food-caching bird.

Laboratory studies show that increased physiological burden during development results in cognitive impairment. In the wild, animals experience a wide range of developmental conditions, and it is critical to understand how variation in such conditions affects cognitive abilities later in life, especially in species that strongly depend on such abilities for survival. We tested whether variation in developmental condition is associated with differences in spatial cognitive abilities in wild food-caching mountain chickadees. Using tail feathers grown during development in juvenile birds, we measured feather corticosterone (Cortf) levels and growth rates and tested these birds during their first winter on two spatial learning tasks. In only 1 of the 3 years, higher feather Cortf was negatively associated with memory acquisition. No significant associations between feather Cortf and any other measurement of spatial cognition were detected in the other 2 years of the study or between feather growth rate and any measurement of cognition during the entire study. Our results suggest that in the wild, naturally existing variation in developmental condition has only a limited effect on spatial cognitive abilities, at least in a food-caching species. This suggests that there may be compensatory mechanisms to buffer specialized cognitive abilities against developmental perturbations.

Environmental, individual and social traits of free-ranging raccoons influence performance in cognitive testing.

Cognitive abilities, such as learning and flexibility, are hypothesized to aid behavioral adaptation to urbanization. Although growing evidence suggests that cognition may indeed facilitate persistence in urban environments, we currently lack knowledge of the cognitive abilities of many urban taxa. Recent methodological advances, including radio frequency identification (RFID), have extended automated cognitive testing into the field but have yet to be applied to a diversity of taxa. Here, we used an RFID-enabled operant conditioning device to assess the habituation, learning and cognitive flexibility of a wild population of raccoons (Procyon lotor). We examined how several biological and behavioral traits influenced participation and performance in testing. We then compared the cognitive performance of wild raccoons tested in natural conditions with that of wild-caught raccoons tested in captivity from a previous study. In natural conditions, juvenile raccoons were more likely to habituate to the testing device, but performed worse in serial reversal learning, compared with adults. We also found that docile raccoons were more likely to learn how to operate the device in natural conditions, which suggests a relationship between emotional reactivity and cognitive ability in raccoons. Although raccoons in both captive and natural conditions demonstrated rapid associative learning and flexibility, raccoons in captive conditions generally performed better, likely owing to the heightened vigilance and social interference experienced by raccoons in natural conditions. Our results have important implications for future research on urban carnivores and cognition in field settings, as well as our understanding of behavioral adaptation to urbanization and coexistence with urban wildlife.

Food discovery is associated with different reliance on social learning and lower cognitive flexibility across environments in a food-caching bird.

Social learning is a primary mechanism for information acquisition in social species. Despite many benefits, social learning may be disadvantageous when independent learning is more efficient. For example, searching independently may be more advantageous when food sources are ephemeral and unpredictable. Individual differences in cognitive abilities can also be expected to influence social information use. Specifically, better spatial memory can make a given environment more predictable for an individual by allowing it to better track food sources. We investigated how resident food-caching chickadees discovered multiple novel food sources in both harsher, less predictable high elevation and milder, more predictable low elevation winter environments. Chickadees at high elevation were faster at discovering multiple novel food sources and discovered more food sources than birds at low elevation. While birds at both elevations used social information, the contribution of social learning to food discovery was significantly lower at high elevation. At both elevations, chickadees with better spatial cognitive flexibility were slower at discovering food sources, likely because birds with lower spatial cognitive flexibility are worse at tracking natural resources and therefore spend more time exploring. Overall, our study supported the prediction that harsh environments should favour less reliance on social learning.

Social dominance has limited effects on spatial cognition in a wild food-caching bird.

Social dominance has long been used as a model to investigate social stress. However, many studies using such comparisons have been performed in captive environments. These environments may produce unnaturally high antagonistic interactions, exaggerating the stress of social subordination and any associated adverse consequences. One such adverse effect concerns impaired cognitive ability, often thought to be associated with social subordination. Here, we tested whether social dominance rank is associated with differences in spatial learning and memory, and in reversal spatial learning (flexibility) abilities in wild food-caching mountain chickadees at different montane elevations. Higher dominance rank was associated with higher spatial cognitive flexibility in harsh environments at higher elevations, but not at lower, milder elevations. By contrast, there were no consistent differences in spatial learning and memory ability associated with dominance rank. Our results suggest that spatial learning and memory ability in specialized food-caching species is a stable trait resilient to social influences. Spatial cognitive flexibility, on the other hand, appears to be more sensitive to environmental influences, including social dominance. These findings contradict those from laboratory studies and suggest that it is critical to investigate the biological consequences of social dominance under natural conditions.

Specialized spatial cognition is associated with reduced cognitive senescence in a food-caching bird.

Senescence, the gradual reduction and loss of function as organisms age, is a widespread process that is especially pronounced in cognitive abilities. Senescence appears to have a genetic basis and can be affected by evolutionary processes. If cognitive senescence is shaped by natural selection, it may be linked with selection on cognitive abilities needed for survival and reproduction, such that species where fitness is directly related to cognitive abilities should evolve delayed cognitive senescence likely resulting in higher lifetime fitness. We used wild food-caching mountain chickadees, which rely on specialized spatial cognition to recover thousands of food caches annually, to test for cognitive senescence in spatial learning and memory and reversal spatial learning and memory abilities. We detected no signs of age-related senescence in spatial cognitive performance on either task in birds ranging from 1 to 6 years old; older birds actually performed better on spatial learning and memory tasks. Our results therefore suggest that cognitive senescence may be either delayed (potentially appearing after 6 years) or negligible in species with strong selection on cognitive abilities and that food-caching species may present a useful model to investigate mechanisms associated with cognitive senescence.

Variation in reversal learning by three generalist mesocarnivores.

Urbanization imposes novel challenges for wildlife, but also provides new opportunities for exploitation. Generalist species are commonly found in urban habitats, but the cognitive mechanisms facilitating their successful behavioral adaptations and exploitations are largely under-investigated. Cognitive flexibility is thought to enable generalists to be more plastic in their behavior, thereby increasing their adaptability to a variety of environments, including urban habitats. Yet direct measures of cognitive flexibility across urban wildlife are lacking. We used a classic reversal-learning paradigm to investigate the cognitive flexibility of three generalist mesocarnivores commonly found in urban habitats: striped skunks (Mephitis mephitis), raccoons (Procyon lotor), and coyotes (Canis latrans). We developed an automated device and testing protocol that allowed us to administer tests of reversal learning in captivity without extensive training or experimenter involvement. Although most subjects were able to rapidly form and reverse learned associations, we found moderate variation in performance and behavior during trials. Most notably, we observed heightened neophobia and a lack of habituation expressed by coyotes. We discuss the implications of such differences among generalists with regard to urban adaptation and we identify goals for future research. This study is an important step in investigating the relationships between cognition, generalism, and urban adaptation.

Testing the greater male variability phenomenon: male mountain chickadees exhibit larger variation in reversal learning performance compared with females.

The greater male variability phenomenon predicts that males exhibit larger ranges of variation in cognitive performance compared with females; however, support for this pattern has come exclusively from studies of humans and lacks mechanistic explanation. Furthermore, the vast majority of the literature assessing sex differences in cognition is based on studies of humans and a few other mammals. In order to elucidate the underpinnings of cognitive variation and the potential for fitness consequences, we must investigate sex differences in cognition in non-mammalian systems as well. Here, we assess the performance of male and female food-caching birds on a spatial learning and memory task and a reversal spatial task to address whether there are sex differences in mean cognitive performance or in the range of variation in performance. For both tasks, male and female mean performance was similar across four years of testing; however, males did exhibit a wider range of variation in performance on the reversal spatial task compared with females. The implications for mate choice and sexual selection of cognitive abilities are discussed and future directions are suggested to aid in the understanding of sex-related cognitive variation.

Light-level geolocator analyses: A user's guide.

Light-level geolocator tags use ambient light recordings to estimate the whereabouts of an individual over the time it carried the device. Over the past decade, these tags have emerged as an important tool and have been used extensively for tracking animal migrations, most commonly small birds. Analysing geolocator data can be daunting to new and experienced scientists alike. Over the past decades, several methods with fundamental differences in the analytical approach have been developed to cope with the various caveats and the often complicated data. Here, we explain the concepts behind the analyses of geolocator data and provide a practical guide for the common steps encompassing most analyses - annotation of twilights, calibration, estimating and refining locations, and extraction of movement patterns - describing good practices and common pitfalls for each step. We discuss criteria for deciding whether or not geolocators can answer proposed research questions, provide guidance in choosing an appropriate analysis method and introduce key features of the newest open-source analysis tools. We provide advice for how to interpret and report results, highlighting parameters that should be reported in publications and included in data archiving. Finally, we introduce a comprehensive supplementary online manual that applies the concepts to several datasets, demonstrates the use of open-source analysis tools with step-by-step instructions and code and details our recommendations for interpreting, reporting and archiving.

Smart is the new sexy: female mountain chickadees increase reproductive investment when mated to males with better spatial cognition.

Understanding the evolution of inter and intraspecific variation in cognitive abilities is one of the main goals in cognitive ecology. In scatter-caching species, spatial memory is critical for the recovery of food caches and overwinter survival, but its effects on reproduction are less clear. Better spatial cognition may improve pre-breeding condition allowing for earlier reproduction. Alternatively, when mated to males with better spatial memory, females may be able to invest more in reproduction which may allow increased offspring survival and hence higher fitness. Using wild food-caching mountain chickadees, we found that when environmental conditions were favourable for breeding, females mated to males with better spatial cognition laid larger clutches and fledged larger broods than females mated to males with worse cognitive performance. Our results support the hypothesis that females may increase their reproductive investment to gain indirect, genetic benefits when mated to high-quality males with better spatial cognitive abilities.

Assessing Behavioral Associations in a Hybrid Zone through Social Network Analysis: Complex Assortative Behaviors Structure Associations in a Hybrid Quail Population.

Behavior can strongly influence rates and patterns of hybridization between animal populations and species. Yet few studies have examined reproductive behaviors in natural hybrid zones within the fine-scale social context in which they naturally occur. We use radio-frequency identification tags with social network analyses to test whether phenotypic similarity in plumage and mass correlate with social behavior throughout a breeding season in a California and Gambel's quail hybrid zone. We use a novel approach to partition phenotypic variation in a way that does not confound differences between sexes and species, and we illustrate the complex ways that phenotype and behavior structure the social environment, mating opportunities, and male-male associations. Associations within the admixed population were random with respect to species-specific plumage but showed strong patterns of assortment based on sexually dimorphic plumage, monomorphic plumage, and mass. Weak behavioral reproductive isolation in this admixed population may be the result of complex patterns of phenotypic assortment based on multiple traits rather than a lack of phenotypic discrimination. More generally, our results support the utility of social network analyses for analyzing behavioral factors affecting genetic exchange between populations and species.

A range-wide domino effect and resetting of the annual cycle in a migratory songbird.

Latitudinal differences in timing of breeding are well documented but how such differences carry over to influence timing of events in the annual cycle of migratory birds is not well understood. We examined geographical variation in timing of events throughout the year using light-level geolocator tracking data from 133 migratory tree swallows ( Tachycineta bicolor) originating from 12 North American breeding populations. A swallow's breeding latitude influenced timing of breeding, which then carried over to affect breeding ground departure. This resulted in subsequent effects on the arrival and departure schedules at autumn stopover locations and timing of arrival at non-breeding locations. This 'domino effect' between timing events was no longer apparent by the time individuals departed for spring migration. Our range-wide analysis demonstrates the lasting impact breeding latitude can have on migration schedules but also highlights how such timing relationships can reset when individuals reside at non-breeding sites for extended periods of time.

Stress-responsiveness influences baseline glucocorticoid levels: Revisiting the under 3min sampling rule.

Plasma glucocorticoid (CORT) levels collected within 3min of capture are commonly believed to reflect pre-stressor, baseline CORT levels. Differences in these "baseline" values are often interpreted as reflecting differences in health, or the amount of social and environmental stress recently experienced by an individual. When interpreting "baseline" values it is generally assumed that any effect of capture-and-handling during the initial sampling period is small enough and consistent enough among individuals to not obscure pre-capture differences in CORT levels. However, plasma CORT increases in less than 3min post-capture in many free-living, endothermic species in which timing has been assessed. In addition, the rate of CORT secretion and the maximum level attained (i.e., the degree of stress-responsiveness) during a severe stressor often differs among individuals of the same species. In Florida scrub-jays (Aphelocoma coerulescens), an individual's stress-responsiveness during a 30min post-capture stressor is correlated with CORT levels in samples collected within 1.5min of capture, suggesting there is an intrinsic connection between stress-responsiveness and pre-capture CORT levels. Although differences in stress-responsiveness accounted for just 11% of the variance in these samples, on average, higher stress-responsive jays (top third of individuals) had baseline values twice that of lower stress-responsive jays (bottom third). Further, plasma CORT levels begin to increase around 2min post-capture in this species, but the rate of increase between 2 and 3min differs markedly with CORT increasing more rapidly in jays with higher stress-responsiveness. Together, these data indicate that baseline CORT values can be influenced by an individual's stress response phenotype and the differences due to stress-responsiveness can be exaggerated during sample collection. In some cases, the effects of differences in stress-responsiveness and the increase in CORT during sample collection could obscure, or supersede, differences in pre-capture plasma CORT levels that are caused by extrinsic factors.

Are invasive fire ants kept in check by native aerial insectivores?

Aerial predator-prey interactions may impact populations of many terrestrial species. Here, we use altitude loggers to study aerial foraging in a native insectivore, the purple martin (Progne subis), in the southern USA. Purple martins fed primarily on mating queens and males of the invasive red imported fire ant (Solenopsis invicta), and doubled their foraging efficiency by doing so. Across the USA, purple martins likely eat billions of fire ant queens each year, potentially impacting the spread of this species. Alternatively, predation on fire ants may help sustain populations of purple martins and other aerial insectivores.

Differential gene expression in seasonal sympatry: mechanisms involved in diverging life histories.

In an era of climate change, understanding the genetic and physiological mechanisms underlying flexibility in phenology and life history has gained greater importance. These mechanisms can be elucidated by comparing closely related populations that differ in key behavioural and physiological traits such as migration and timing of reproduction. We compared gene expression in two recently diverged dark-eyed Junco ( Junco hyemalis) subspecies that live in seasonal sympatry during winter and early spring, but that differ in behaviour and physiology, despite exposure to identical environmental cues. We identified 547 genes differentially expressed in blood and pectoral muscle. Genes involved in lipid transport and metabolism were highly expressed in migrant juncos, while genes involved in reproductive processes were highly expressed in resident breeders. Seasonal differences in gene expression in closely related populations residing in the same environment provide significant insights into mechanisms underlying variation in phenology and life history, and have potential implications for the role of seasonal timing differences in gene flow and reproductive isolation.

Is extinction forever?

Mistrust of science has seeped into public perception of the most fundamental aspect of conservation-extinction. The term ought to be straightforward, and yet, there is a disconnect between scientific discussion and public views. This is not a mere semantic issue, rather one of communication. Within a population dynamics context, we say that a species went locally extinct, later to document its return. Conveying our findings matters, for when we use local extinction, an essentially nonsensical phrase, rather than extirpation, which is what is meant, then we contribute to, if not create outright, a problem for public understanding of conservation, particularly as local extinction is often shortened to extinction in media sources. The public that receives the message of our research void of context and modifiers comes away with the idea that extinction is not forever or, worse for conservation as a whole, that an extinction crisis has been invented.

Stable Isotopes Suggest Low Site Fidelity in Bar-headed Geese (Anser indicus) in Mongolia: Implications for Disease Transmission.

Population connectivity is an important consideration in studies of disease transmission and biological conservation, especially with regard to migratory species. Determining how and when different subpopulations intermingle during different phases of the annual cycle can help identify important geographical regions or features as targets for conservation efforts and can help inform our understanding of continental-scale disease transmission. In this study, stable isotopes of hydrogen and carbon in contour feathers were used to assess the degree of molt-site fidelity among Bar-headed Geese (Anser indicus) captured in north-central Mongolia. Samples were collected from actively molting Bar-headed Geese (n = 61), and some individual samples included both a newly grown feather (still in sheath) and an old, worn feather from the bird's previous molt (n = 21). Although there was no difference in mean hydrogen isotope ratios for the old and new feathers, the isotopic variance in old feathers was approximately three times higher than that of the new feathers, which suggests that these birds use different and geographically distant molting locations from year to year. To further test this conclusion, online data and modeling tools from the isoMAP website were used to generate probability landscapes for the origin of each feather. Likely molting locations were much more widespread for old feathers than for new feathers, which supports the prospect of low molt-site fidelity. This finding indicates that population connectivity would be greater than expected based on data from a single annual cycle, and that disease spread can be rapid even in areas like Mongolia where Bar-headed Geese generally breed in small isolated groups.

Dynamic change in spring habitat use by the brown eared pheasant (Crossptilon mantchuricum) in the Huanglong mountains, Yanan City, Shaanxi Province, China.

Characterization of foraging-site preferences of threatened and endangered species is a key component of effective habitat conservation. We studied foraging-site selection by the brown eared pheasant (Crossoptilon mantchuricum) in the Huanglongshan Nature Reserve, Yanan City, Shaanxi Province, China, from early February to end of May 2011. We identified feeding sites by locating tracks and scratches characteristic of the birds, and compared habitat characteristics at these sites to those at randomly selected sites across the study area. During the pre-breeding season, the birds tended to be found in the areas characterized by gullies within mixed forests with intermediate sun exposure on gentle slopes (< 10°), and close to water and footpaths. The sites utilized by the birds also featured greater tree diameter, lower shrub density, lower grass cover, and lower altitude than random sites. During the breeding season, the birds tended to be found in the areas of slightly higher altitude, more shrubs, moderately steep slopes (10°-20°), and farther from water and paths. These patterns were consistent with seasonal changes in vegetation and food-resource availability in the study area. Management of brown eared pheasants' populations for conservation must account for these seasonal shifts in habitat requirements.

Bird Migration and Avian Influenza: A Comparison of Hydrogen Stable Isotopes and Satellite Tracking Methods.

Satellite-based tracking of migratory waterfowl is an important tool for understanding the potential role of wild birds in the long-distance transmission of highly pathogenic avian influenza. However, employing this technique on a continental scale is prohibitively expensive. This study explores the utility of stable isotope ratios in feathers in examining both the distances traveled by migratory birds and variation in migration behavior. We compared the satellite-derived movement data of 22 ducks from 8 species captured at wintering areas in Bangladesh, Turkey, and Hong Kong with deuterium ratios (δD) of these and other individuals captured at the same locations. We derived likely molting locations from the satellite tracking data and generated expected isotope ratios based on an interpolated map of δD in rainwater. Although δD was correlated with the distance between wintering and molting locations, surprisingly, measured δD values were not correlated with either expected values or latitudes of molting sites. However, population-level parameters derived from the satellite-tracking data, such as mean distance between wintering and molting locations and variation in migration distance, were reflected by means and variation of the stable isotope values. Our findings call into question the relevance of the rainfall isotope map for Asia for linking feather isotopes to molting locations, and underscore the need for extensive ground truthing in the form of feather-based isoscapes. Nevertheless, stable isotopes from feathers could inform disease models by characterizing the degree to which regional breeding populations interact at common wintering locations. Feather isotopes also could aid in surveying wintering locations to determine where high-resolution tracking techniques (e.g. satellite tracking) could most effectively be employed. Moreover, intrinsic markers such as stable isotopes offer the only means of inferring movement information from birds that have died as a result of infection. In the absence of feather based-isoscapes, we recommend a combination of isotope analysis and satellite-tracking as the best means of generating aggregate movement data for informing disease models.