Ellis J. G. Langley

Differential participation in cognitive tests is driven by personality, sex, body condition and experience

Failure to participate in a cognitive test may result in sampling biases when measuring inter-individual variation in cognitive performances in both captive and wild populations. This would be problematic if particular classes of individuals consistently fail to participate, skewing data and making generalisations or comparisons difficult. We presented 144 pheasant chicks, raised under standardised conditions, with a battery of cognitive tests to investigate whether sex, body condition or personality traits, measured by differences in latencies to explore a novel object, novel environment or unknown conspecific, predicted individual variation in voluntary participation across 37 test sessions. In general, participation increased across testing sessions, yet patterns of participation differed with sex and body condition. Males with a high body condition were more likely to participate in early test sessions compared to males with a low body condition or females. While participation among males in high body condition was consistent across sessions, males with a low body condition and females, regardless of body condition, were more likely to participate in later, rather than earlier sessions. Individuals also showed repeatable behaviours across time and different contexts, revealing not only that the exploration of novelty, but also that the order that subjects entered the testing arena and their latencies to acquire a freely available meal-worm reward may be considered valid proxies for different personality traits. During each test session, those individuals that were among the first to voluntarily enter the testing arena were more likely to participate in subsequent trials. Moreover, when isolated in the testing arena, individuals that rapidly acquired a freely available meal-worm, positioned on the testing apparatus, were also more likely to participate in a cognitive test. Our findings therefore reveal that sex, body condition and personality traits, along with habituation to the testing paradigms, all play important roles in determining whether or not particular individuals participate in cognitive tests. Sampling biases may therefore misrepresent our understanding of variation in cognitive performance in wild and captive populations, making individual differences in cognition difficult to interpret.

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 individuals prior experience of transparent objects, or their motivation to acquire food, than providing a reliable measure of their inhibitory control.

The repeatability of cognitive performance: a meta-analysis

Behavioural and cognitive processes play important roles in mediating an individuals interactions with its environment. Yet, while there is a vast literature on repeatable individual differences in behaviour, relatively little is known about the repeatability of cognitive performance. To further our understanding of the evolution of cognition, we gathered 44 studies on individual performance of 25 species across six animal classes and used meta-analysis to assess whether cognitive performance is repeatable. We compared repeatability (R) in performance (1) on the same task presented at different times (temporal repeatability), and (2) on different tasks that measured the same putative cognitive ability (contextual repeatability). We also addressed whether R estimates were influenced by seven extrinsic factors (moderators): type of cognitive performance measurement, type of cognitive task, delay between tests, origin of the subjects, experimental context, taxonomic class and publication status. We found support for both temporal and contextual repeatability of cognitive performance, with mean R estimates ranging between 0.15 and 0.28. Repeatability estimates were mostly influenced by the type of cognitive performance measures and publication status. Our findings highlight the widespread occurrence of consistent inter-individual variation in cognition across a range of taxa which, like behaviour, may be associated with fitness outcomes. This article is part of the theme issue ‘Causes and consequences of individual differences in cognitive abilities’.

Males and females differentially adjust vigilance levels as group size increases: effect on optimal group size

A strong motivation for one individual to aggregate with others is to reduce their vigilance because other group members provide coverage and warning of approaching predators. This collective vigilance means that a focal individual is usually less susceptible to predation than when alone. However, individuals differ in their vigilance levels depending on status and context. They may also differ in how they adjust their vigilance levels as group size changes. This flexibility in response means that the collective vigilance of a group, and hence its optimal size, is not intuitive. We demonstrate, in both natural and experimental systems, that male and female pheasants, Phasianus colchicus, in harems differentially adjusted their vigilance levels as harem size changed. Females became less vigilant as harems became larger, and benefited by increasing their foraging time. Conversely, males became more vigilant as harems became larger. We calculated the collective probability that a harem would detect a predator. Within natural harem sizes, a male and two females exhibited the highest probability of collective detection, with decreases as more females joined. This optimal harem size matched the average harem size observed at our study site. Females may join harems for benefits of collective vigilance. Despite both sexes having a shared interest in larger harems for mating benefits, optimal harem size is influenced by trade-offs in a nonsexual behaviour, vigilance. This results in males with relatively small harems, females associating with less preferred males and each male being surrounded by fewer females than he could mate with.

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’.

How does cognition shape social relationships

The requirements of living in social groups, and forming and maintaining social relationships are hypothesized to be one of the major drivers behind the evolution of cognitive abilities. Most empirical studies investigating the relationships between sociality and cognition compare cognitive performance between species living in systems that differ in social complexity. In this review, we ask whether and how individuals benefit from cognitive skills in their social interactions. Cognitive abilities, such as perception, attention, learning, memory, and inhibitory control, aid in forming and maintaining social relationships. We investigate whether there is evidence that individual variation in these abilities influences individual variation in social relationships. We then consider the evolutionary consequences of the interaction between sociality and cognitive ability to address whether bi-directional relationships exist between the two, such that cognition can both shape and be shaped by social interactions and the social environment. In doing so, we suggest that social network analysis is emerging as a powerful tool that can be used to test for directional causal relationships between sociality and cognition. Overall, our review highlights the importance of investigating individual variation in cognition to understand how it shapes the patterns of social relationships. This article is part of the theme issue ‘Causes and consequences of individual differences in cognitive abilities’.

Erratum to: Differences in social preference between the sexes during ontogeny drive segregation in a precocial species

The work was jointly funded by the University of Exeter, the Game and Wildlife Conservation Trust, a Royal Society Small Project Grant awarded to JRM and an ERC Consolidator Grant (616474) awarded to JRM.

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 individuals 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.

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 individuals 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 individuals social environment when attempting to characterize cognitive capacities. It also demonstrates the flexibility of an individuals cognitive performance depending on the social context.

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.