Spatial memory predicts home range size and predation risk in pheasants.

Most animals confine their activities to a discrete home range, long assumed to reflect the fitness benefits of obtaining spatial knowledge about the landscape. However, few empirical studies have linked spatial memory to home range development or determined how selection operates on spatial memory via the latter's role in mediating space use. We assayed the cognitive ability of juvenile pheasants (Phasianus colchicus) reared under identical conditions before releasing them into the wild. Then, we used high-throughput tracking to record their movements as they developed their home ranges, and determined the location, timing and cause of mortality events. Individuals with greater spatial reference memory developed larger home ranges. Mortality risk from predators was highest at the periphery of an individual's home range in areas where they had less experience and opportunity to obtain spatial information. Predation risk was lower in individuals with greater spatial memory and larger core home ranges, suggesting selection may operate on spatial memory by increasing the ability to learn about predation risk across the landscape. Our results reveal that spatial memory, determined from abstract cognitive assays, shapes home range development and variation, and suggests predation risk selects for spatial memory via experience-dependent spatial variation in mortality.

Big-data approaches lead to an increased understanding of the ecology of animal movement.

Understanding animal movement is essential to elucidate how animals interact, survive, and thrive in a changing world. Recent technological advances in data collection and management have transformed our understanding of animal "movement ecology" (the integrated study of organismal movement), creating a big-data discipline that benefits from rapid, cost-effective generation of large amounts of data on movements of animals in the wild. These high-throughput wildlife tracking systems now allow more thorough investigation of variation among individuals and species across space and time, the nature of biological interactions, and behavioral responses to the environment. Movement ecology is rapidly expanding scientific frontiers through large interdisciplinary and collaborative frameworks, providing improved opportunities for conservation and insights into the movements of wild animals, and their causes and consequences.

Hot-headed peckers: thermographic changes during aggression among juvenile pheasants (Phasianus colchicus).

In group-living vertebrates, dominance status often covaries with physiological measurements (e.g. glucocorticoid levels), but it is unclear how dominance is linked to dynamic changes in physiological state over a shorter, behavioural timescale. In this observational study, we recorded spontaneous aggression among captive juvenile pheasants (Phasianus colchicus) alongside infrared thermographic measurements of their external temperature, a non-invasive technique previously used to examine stress responses in non-social contexts, where peripheral blood is redirected towards the body core. We found low but highly significant repeatability in maximum head temperature, suggesting individually consistent thermal profiles, and some indication of lower head temperatures in more active behavioural states (e.g. walking compared to resting). These individual differences were partly associated with sex, females being cooler on average than males, but unrelated to body size. During pairwise aggressive encounters, we observed a non-monotonic temperature change, with head temperature dropping rapidly immediately prior to an attack and increasing rapidly afterwards, before returning to baseline levels. This nonlinear pattern was similar for birds in aggressor and recipient roles, but aggressors were slightly hotter on average. Our findings show that aggressive interactions induce rapid temperature changes in dominants and subordinates alike, and highlight infrared thermography as a promising tool for investigating the physiological basis of pecking orders in galliforms. This article is part of the theme issue 'The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies'.

Spatial cognitive ability is associated with transitory movement speed but not straightness during the early stages of exploration.

Memories about the spatial environment, such as the locations of foraging patches, are expected to affect how individuals move around the landscape. However, individuals differ in the ability to remember spatial locations (spatial cognitive ability) and evidence is growing that these inter-individual differences influence a range of fitness proxies. Yet empirical evaluations directly linking inter-individual variation in spatial cognitive ability and the development and structure of movement paths are lacking. We assessed the performance of young pheasants (Phasianus colchicus) on a spatial cognition task before releasing them into a novel, rural landscape and tracking their movements. We quantified changes in the straightness and speed of their transitory paths over one month. Birds with better performances on the task initially made slower transitory paths than poor performers but by the end of the month, there was no difference in speed. In general, birds increased the straightness of their path over time, indicating improved efficiency independent of speed, but this was not related to performance on the cognitive task. We suggest that initial slow movements may facilitate more detailed information gathering by better performers and indicates a potential link between an individual's spatial cognitive ability and their movement behaviour.

Is habitat selection in the wild shaped by individual-level cognitive biases in orientation strategy?

Cognitive biases for encoding spatial information (orientation strategies) in relation to self (egocentric) or landmarks (allocentric) differ between species or populations according to the habitats they occupy. Whether biases in orientation strategy determine early habitat selection or if individuals adapt their biases following experience is unknown. We determined orientation strategies of pheasants, Phasianus colchicus, using a dual-strategy maze with an allocentric probe trial, before releasing them (n = 20) into a novel landscape, where we monitored their movement and habitat selection. In general, pheasants selected for woodland over non-woodland habitat, but allocentric-biased individuals exhibited weaker avoidance of non-woodland habitat, where we expected allocentric navigation to be more effective. Sex did not influence selection but was associated with speed and directional persistence in non-woodland habitat. Our results suggest that an individual's habitat selection is associated with inherent cognitive bias in early life, but it is not yet clear what advantages this may offer.

Heritability and correlations among learning and inhibitory control traits.

To understand the evolution of cognitive abilities, we need to understand both how selection acts upon them and their genetic (co)variance structure. Recent work suggests that there are fitness consequences for free-living individuals with particular cognitive abilities. However, our current understanding of the heritability of these abilities is restricted to domesticated species subjected to artificial selection. We investigated genetic variance for, and genetic correlations among four cognitive abilities: inhibitory control, visual and spatial discrimination, and spatial ability, measured on >450 pheasants, Phasianus colchicus, over four generations. Pheasants were reared in captivity but bred from adults that lived in the wild and hence, were subject to selection on survival. Pheasant chicks are precocial and were reared without parents, enabling us to standardize environmental and parental care effects. We constructed a pedigree based on 15 microsatellite loci and implemented animal models to estimate heritability. We found moderate heritabilities for discrimination learning and inhibitory control (h2 = 0.17-0.23) but heritability for spatial ability was low (h2 = 0.09). Genetic correlations among-traits were largely positive but characterized by high uncertainty and were not statistically significant. Principle component analysis of the genetic correlation matrix estimate revealed a leading component that explained 69% of the variation, broadly in line with expectations under a general intelligence model of cognition. However, this pattern was not apparent in the phenotypic correlation structure which was more consistent with a modular view of animal cognition. Our findings highlight that the expression of cognitive traits is influenced by environmental factors which masks the underlying genetic structure.

Early-life learning ability predicts adult social structure, with potential implications for fitness outcomes in the wild.

Social environments influence important ecological processes and can determine how selection acts on traits. Cognitive abilities can shape these social environments and in turn, affect individuals' fitness. To understand how cognitive abilities evolve, we need to understand the complex interplay between an individual's cognitive abilities, the social environment that they inhabit and the fitness consequences of these relationships. We measured the associative learning ability of pheasant chicks, Phasianus colchicus, then released them into the wild where we quantified their social position by observing their associations at feeding stations and monitored the number of days survived. We observed disassortative mixing by learning performance at the population level, and poor learners had more associates than good learners. Learning was beneficial for survival when focal individuals had fewer than four associates, but survival probability across learning abilities equalized for individuals with more than four associates. While the mechanisms underlying these relationships remain to be determined, the patterns of association exhibited by pheasants at feeders can be predicted by individual variation in cognitive performances and we suspect these patterns are related to differences in information use. Critically, these resulting patterns of association have fitness consequences for individuals that cannot be explained directly by their cognitive ability, but which could mediate selection on cognition.

No evidence that footedness in pheasants influences cognitive performance in tasks assessing colour discrimination and spatial ability.

The differential specialization of each side of the brain facilitates the parallel processing of information and has been documented in a wide range of animals. Animals that are more lateralized as indicated by consistent preferential limb use are commonly reported to exhibit superior cognitive ability as well as other behavioural advantages. We assayed the lateralization of 135 young pheasants (Phasianus colchicus), indicated by their footedness in a spontaneous stepping task, and related this measure to individual performance in either 3 assays of visual or spatial learning and memory. We found no evidence that pronounced footedness enhances cognitive ability in any of the tasks. We also found no evidence that an intermediate footedness relates to better cognitive performance. This lack of relationship is surprising because previous work revealed that pheasants have a slight population bias towards right footedness, and when released into the wild, individuals with higher degrees of footedness were more likely to die. One explanation for why extreme lateralization is constrained was that it led to poorer cognitive performance, or that optimal cognitive performance was associated with some intermediate level of lateralization. This stabilizing selection could explain the pattern of moderate lateralization that is seen in most non-human species that have been studied. However, we found no evidence in this study to support this explanation.

The inhibitory control of pheasants (Phasianus colchicus) weakens when previously learned environmental information becomes unpredictable.

Inhibitory control (IC) is the ability to intentionally restrain initial, ineffective responses to a stimulus and instead exhibit an alternative behaviour that is not pre-potent but which effectively attains a reward. Individuals (both humans and non-human animals) differ in their IC, perhaps as a result of the different environmental conditions they have experienced. We experimentally manipulated environmental predictability, specifically how reliable information linking a cue to a reward was, over a very short time period and tested how this affected an individual's IC. We gave 119 pheasants (Phasianus colchicus) the opportunity to learn to associate a visual cue with a food reward in a binary choice task. We then perturbed this association for half the birds, whereas control birds continued to be rewarded when making the correct choice. We immediately measured all birds' on a detour IC task and again 3 days later. Perturbed birds immediately performed worse than control birds, making more unrewarded pecks at the apparatus than control birds, although this effect was less for individuals that had more accurately learned the initial association. The effect of the perturbation was not seen 3 days later, suggesting that individual IC performance is highly plastic and susceptible to recent changes in environmental predictability. Specifically, individuals may perform poorly in activities requiring IC immediately after information in their environment is perturbed, with the perturbation inducing emotional arousal. Our finding that recent environmental changes can affect IC performance, depending on how well an animal has learned about that environment, means that interpreting individual differences in IC must account for both prior experience and relevant individual learning abilities.

Response learning confounds assays of inhibitory control on detour tasks.

The ability to inhibit prepotent actions towards rewards that are made inaccessible by transparent barriers has been considered to reflect capacities for inhibitory control (IC). Typically, subjects initially reach directly, and incorrectly, for the reward. With experience, subjects may inhibit this action and instead detour around barriers to access the reward. However, assays of IC are often measured across multiple trials, with the location of the reward remaining constant. Consequently, other cognitive processes, such as response learning (acquisition of a motor routine), may confound accurate assays of IC. We measured baseline IC capacities in pheasant chicks, Phasianus colchicus, using a transparent cylinder task. Birds were then divided into two training treatments, where they learned to access a reward placed behind a transparent barrier, but experienced differential reinforcement of a particular motor response. In the stationary-barrier treatment, the location of the barrier remained constant across trials. We, therefore, reinforced a fixed motor response, such as always go left, which birds could learn to aid their performance. Conversely, we alternated the location of the barrier across trials for birds in the moving-barrier treatment and hence provided less reinforcement of their response learning. All birds then experienced a second presentation of the transparent cylinder task to assess whether differences in the training treatments influenced their subsequent capacities for IC. Birds in the stationary-barrier treatment showed a greater improvement in their subsequent IC performance after training compared to birds in the moving-barrier treatment. We, therefore, suggest that response learning aids IC performance on detour tasks. Consequently, non-target cognitive processes associated with different neural substrates appear to underlie performances on detour tasks, which may confound accurate assays of IC. Our findings question the construct validity of a commonly used paradigm that is widely considered to assess capacities for IC in humans and other animals.

Unpredictable environments enhance inhibitory control in pheasants.

The ability to control impulsive actions is an important executive function that is central to the self-regulation of behaviours and, in humans, can have important implications for mental and physical health. One key factor that promotes individual differences in inhibitory control (IC) is the predictability of environmental information experienced during development (i.e. reliability of resources and social trust). However, environmental predictability can also influence motivational and other cognitive abilities, which may therefore confound interpretations of the mechanisms underlying IC. We investigated the role of environmental predictability, food motivation and cognition on IC. We reared pheasant chicks, Phasianus colchicus, under standardised conditions, in which birds experienced environments that differed in their spatial predictability. We systematically manipulated spatial predictability during their first 8 weeks of life, by either moving partitions daily to random locations (unpredictable environment) or leaving them in fixed locations (predictable environment). We assessed motivation by presenting pheasants with two different foraging tasks that measured their dietary breadth and persistence to acquire inaccessible food rewards, as well as recording their latencies to acquire a freely available baseline worm positioned adjacent to each test apparatus, their body condition (mass/tarsus3) and sex. We assessed cognitive performance by presenting each bird with an 80-trial binary colour discrimination task. IC was assessed using a transparent detour apparatus, which required subjects to inhibit prepotent attempts to directly acquire a visible reward through the barrier and instead detour around a barrier. We found greater capacities for IC in pheasants that were reared in spatially unpredictable environments compared to those reared in predictable environments. While IC was unrelated to individual differences in cognitive performance on the colour discrimination task or motivational measures, we found that environmental predictability had differential effects on sex. Males reared in an unpredictable environment, and all females regardless of their rearing environment, were less persistent than males reared in a predictable environment. Our findings, therefore, suggest that an individual's developmental experience can influence their performance on IC tasks.

A single factor explanation for associative learning performance on colour discrimination problems in common pheasants (Phasianus colchicus).

It remains unclear whether performance of non-human animals on cognitive test batteries can be explained by domain general cognitive processes, as is found in humans. The persistence of this dispute is likely to stem from a lack of clarity of the psychological or neural processes involved. One broadly accepted cognitive process, that may predict performance in a range of psychometric tasks, is associative learning. We therefore investigated intra-individual performances on tasks that incorporate processes of associative learning, by assessing the speed of acquisition and reversal learning in up to 187 pheasants (Phasianus colchicus) on four related binary colour discrimination tasks. We found a strong, positive significant bivariate relationship between an individual's acquisition and reversal learning performances on one cue set. Weak, positive significant bivariate relationships were also found between an individual's performance on pairs of reversal tasks and between the acquisition and reversal performances on different cue sets. A single factor, robust to parallel analysis, explained 36% of variation in performance across tasks. Inter-individual variation could not be explained by differential prior experience, age, sex or body condition. We propose that a single factor explanation, which we call 'a', summarises the covariance among scores obtained from these visual discrimination tasks, as they all assess capacities for associative learning. We argue that 'a' may represent an underlying cognitive ability exhibited by an individual, which manifests across a variety of tasks requiring associative processes.

The relationship between social rank and spatial learning in pheasants, Phasianus colchicus: cause or consequence?

Individual differences in performances on cognitive tasks have been found to differ according to social rank across multiple species. However, it is not clear whether an individual's cognitive performance is flexible and the result of their current social rank, modulated by social interactions (social state dependent hypothesis), or if it is determined prior to the formation of the social hierarchy and indeed influences an individual's rank (prior attributes hypothesis). We separated these two hypotheses by measuring learning performance of male pheasants, Phasianus colchicus, on a spatial discrimination task as chicks and again as adults. We inferred adult male social rank from observing agonistic interactions while housed in captive multi-male multi-female groups. Learning performance of adult males was assayed after social rank had been standardised; by housing single males with two or four females. We predicted that if cognitive abilities determine social rank formation we would observe: consistency between chick and adult performances on the cognitive task and chick performance would predict adult social rank. We found that learning performances were consistent from chicks to adults for task accuracy, but not for speed of learning and chick learning performances were not related to adult social rank. Therefore, we could not support the prior attributes hypothesis of cognitive abilities aiding social rank formation. Instead, we found that individual differences in learning performances of adults were predicted by the number of females a male was housed with; males housed with four females had higher levels of learning performance than males housed with two females; and their most recent recording of captive social rank, even though learning performance was assayed while males were in a standardized, non-competitive environment. This does not support the hypothesis that direct social pressures are causing the inter-individual variation in learning performances that we observe. Instead, our results suggest that there may be carry-over effects of aggressive social interactions on learning performance. Consequently, whether early life spatial learning performances influence social rank is unclear but these performances are modulated by the current social environment and a male's most recent social rank.

Size dimorphism and sexual segregation in pheasants: tests of three competing hypotheses.

Fine scale sexual segregation outside of the mating season is common in sexually dimorphic and polygamous species, particularly in ungulates. A number of hypotheses predict sexual segregation but these are often contradictory with no agreement as to a common cause, perhaps because they are species specific. We explicitly tested three of these hypotheses which are commonly linked by a dependence on sexual dimorphism for animals which exhibit fine-scale sexual segregation; the Predation Risk Hypothesis, the Forage Selection Hypothesis, and the Activity Budget Hypothesis, in a single system the pheasant, Phasianus colchicus; a large, sedentary bird that is predominantly terrestrial and therefore analogous to ungulates rather than many avian species which sexually segregate. Over four years we reared 2,400 individually tagged pheasants from one day old and after a period of 8-10 weeks we released them into the wild. We then followed the birds for 7 months, during the period that they sexually segregate, determined their fate and collected behavioural and morphological measures pertinent to the hypotheses. Pheasants are sexually dimorphic during the entire period that they sexually segregate in the wild; males are larger than females in both body size and gut measurements. However, this did not influence predation risk and predation rates (as predicted by the Predation Risk Hypothesis), diet choice (as predicted by the Forage Selection Hypothesis), or the amount of time spent foraging, resting or walking (as predicted by the Activity Budget Hypothesis). We conclude that adult sexual size dimorphism is not responsible for sexual segregation in the pheasant in the wild. Instead, we consider that segregation may be mediated by other, perhaps social, factors. We highlight the importance of studies on a wide range of taxa to help further the knowledge of sexual segregation.

Low survival of strongly footed pheasants may explain constraints on lateralization.

Brain lateralization is considered adaptive because it leads to behavioral biases and specializations that bring fitness benefits. Across species, strongly lateralized individuals perform better in specific behaviors likely to improve survival. What constrains continued exaggerated lateralization? We measured survival of pheasants, finding that individuals with stronger bias in their footedness had shorter life expectancies compared to individuals with weak biases. Consequently, weak, or no footedness provided the highest fitness benefits. If, as suggested, footedness is indicative of more general brain lateralization, this could explain why continued brain lateralization is constrained even though it may improve performance in specific behaviors.

Intra-individual variation in performance on novel variants of similar tasks influences single factor explanations of general cognitive processes.

Intra-individual variation in performance within and across cognitive domains may confound interpretations of both domain-general and domain-specific abilities. Such variation is rarely considered in animal test batteries. We investigate individual consistency in performance by presenting pheasant chicks (n = 31), raised under standardized conditions, with nine different cognitive tasks. Among these tasks were two replicated novel variants of colour learning and colour reversal problems, tests of positional learning and memory, as well as two different tasks that captured multiple putative measures of inhibitory control and motor-related performance. These task variants were also used to compare subjects' performance on alternative test batteries comprised of different task combinations. Subjects' performance improved with experience, yet we found relatively little consistency in their performance, both within similar tasks using different paradigms and across different tasks. Parallel analysis revealed non-significant factors when all nine tasks were included in a principal axis factor analysis. However, when different combinations of six of the nine tasks were included in principal axis factoring, 14 of 84 combinations revealed significant main factors, explaining between 28 and 35% of the variance in task performance. While comparable findings have been suggested to reflect domain-general intelligence in other species, we found no evidence to suggest that a single factor encompassed a diverse range of cognitive abilities in pheasants. Instead, we reveal how single factor explanations of cognitive processes can be influenced by test battery composition and intra-individual variation in performance across tasks. Our findings highlight the importance of conducting multiple tests within specific domains to ensure robust cognitive measures are obtained.

The quick are the dead: pheasants that are slow to reverse a learned association survive for longer in the wild.

Cognitive abilities probably evolve through natural selection if they provide individuals with fitness benefits. A growing number of studies demonstrate a positive relationship between performance in psychometric tasks and (proxy) measures of fitness. We assayed the performance of 154 common pheasant (Phasianus colchicus) chicks on tests of acquisition and reversal learning, using a different set of chicks and different set of cue types (spatial location and colour) in each of two years and then followed their fates after release into the wild. Across all birds, individuals that were slow to reverse previously learned associations were more likely to survive to four months old. For heavy birds, individuals that rapidly acquired an association had improved survival to four months, whereas for light birds, slow acquirers were more likely to be alive. Slow reversers also exhibited less exploratory behaviour in assays when five weeks old. Fast acquirers visited more artificial feeders after release. In contrast to most other studies, we showed that apparently 'poor' cognitive performance (slow reversal speed suggesting low behavioural flexibility) correlates with fitness benefits in at least some circumstances. This correlation suggests a novel mechanism by which continued exaggeration of cognitive abilities may be constrained.This article is part of the theme issue 'Causes and consequences of individual differences in cognitive abilities'.

Individuals in larger groups are more successful on spatial discrimination tasks.

To understand how natural selection may act on cognitive processes, it is necessary to reliably determine interindividual variation in cognitive abilities. However, an individual's performance in a cognitive test may be influenced by the social environment. The social environment explains variation between species in cognitive performances, with species that live in larger groups purportedly demonstrating more advanced cognitive abilities. It also explains variation in cognitive performances within species, with larger groups more likely to solve novel problems than smaller groups. Surprisingly, an effect of group size on individual variation in cognitive performance has rarely been investigated and much of our knowledge stems from impaired performance of individuals reared in isolation. Using a within-subjects design we assayed individual learning performance of adult female pheasants, Phasianus colchicus, while housed in groups of three and five. Individuals experienced the group sizes in a different order, but were presented with two spatial discrimination tasks, each with a distinct cue set, in a fixed order. We found that across both tasks individuals housed in the large groups had higher levels of success than individuals housed in the small groups. Individuals had higher levels of success on their second than their first task, irrespective of group size. We suggest that the expression of individual learning performance is responsive to the current social environment but the mechanisms underpinning this relationship require further investigation. Our study demonstrates that it is important to account for an individual's social environment when attempting to characterize cognitive capacities. It also demonstrates the flexibility of an individual's cognitive performance depending on the social context.

Group social rank is associated with performance on a spatial learning task.

Dominant individuals differ from subordinates in their performances on cognitive tasks across a suite of taxa. Previous studies often only consider dyadic relationships, rather than the more ecologically relevant social hierarchies or networks, hence failing to account for how dyadic relationships may be adjusted within larger social groups. We used a novel statistical method: randomized Elo-ratings, to infer the social hierarchy of 18 male pheasants, Phasianus colchicus, while in a captive, mixed-sex group with a linear hierarchy. We assayed individual learning performance of these males on a binary spatial discrimination task to investigate whether inter-individual variation in performance is associated with group social rank. Task performance improved with increasing trial number and was positively related to social rank, with higher ranking males showing greater levels of success. Motivation to participate in the task was not related to social rank or task performance, thus indicating that these rank-related differences are not a consequence of differences in motivation to complete the task. Our results provide important information about how variation in cognitive performance relates to an individual's social rank within a group. Whether the social environment causes differences in learning performance or instead, inherent differences in learning ability predetermine rank remains to be tested.

Do detour tasks provide accurate assays of inhibitory control?

Transparent Cylinder and Barrier tasks are used to purportedly assess inhibitory control in a variety of animals. However, we suspect that performances on these detour tasks are influenced by non-cognitive traits, which may result in inaccurate assays of inhibitory control. We therefore reared pheasants under standardized conditions and presented each bird with two sets of similar tasks commonly used to measure inhibitory control. We recorded the number of times subjects incorrectly attempted to access a reward through transparent barriers, and their latencies to solve each task. Such measures are commonly used to infer the differential expression of inhibitory control. We found little evidence that their performances were consistent across the two different Putative Inhibitory Control Tasks (PICTs). Improvements in performance across trials showed that pheasants learned the affordances of each specific task. Critically, prior experience of transparent tasks, either Barrier or Cylinder, also improved subsequent inhibitory control performance on a novel task, suggesting that they also learned the general properties of transparent obstacles. Individual measures of persistence, assayed in a third task, were positively related to their frequency of incorrect attempts to solve the transparent inhibitory control tasks. Neophobia, Sex and Body Condition had no influence on individual performance. Contrary to previous studies of primates, pheasants with poor performance on PICTs had a wider dietary breadth assayed using a free-choice task. Our results demonstrate that in systems or taxa where prior experience and differences in development cannot be accounted for, individual differences in performance on commonly used detour-dependent PICTS may reveal more about an individual's prior experience of transparent objects, or their motivation to acquire food, than providing a reliable measure of their inhibitory control.