Ella F. Cole

Personality and problem-solving performance explain competitive ability in the wild

Competitive ability is a major determinant of fitness, but why individuals vary so much in their competitiveness remains only partially understood. One increasingly prevalent view is that realized competitive ability varies because it represents alternative strategies that arise because of the costs associated with competitiveness. Here we use a population of great tits (Parus major) to explore whether individual differences in competitive ability when foraging can be explained by two traits that have previously been linked to alternative behavioural strategies: the personality trait ‘exploration behaviour’ and a simple cognitive trait, ‘innovative problem-solving performance’. We assayed these traits under standardized conditions in captivity and then measured competitive ability at feeders with restricted access in the wild. Competitive ability was repeatable within individual males across days and correlated positively with exploration behaviour, representing the first such demonstration of a link between a personality trait and both competitive ability and food intake in the wild. Competitive ability was also simultaneously negatively correlated with problem-solving performance; individuals who were poor competitors were good at problem-solving. Rather than being the result of variation in ‘individual quality’, our results support the hypothesis that individual variation in competitive ability can be explained by alternative behavioural strategies.

Cognitive Ability Influences Reproductive Life History Variation in the Wild

Cognition has been studied intensively for several decades, but the evolutionary processes that shape individual variation in cognitive traits remain elusive [1-3]. For instance, the strength of selection on a cognitive trait has never been estimated in a natural population, and the possibility that positive links with life history variation [1-5] are mitigated by costs [6] or confounded by ecological factors remains unexplored in the wild. We assessed novel problem-solving performance in 468 wild great tits Parus major temporarily taken into captivity and subsequently followed up their reproductive performance in the wild. Problem-solver females produced larger clutches than nonsolvers. This benefit did not arise because solvers timed their breeding better, occupied better habitats, or compromised offspring quality or their own survival. Instead, foraging range size and day length were relatively small and short, respectively, for solvers, suggesting that they were more efficient at exploiting their environment. In contrast to the positive effect on clutch size, problem solvers deserted their nests more often, leading to little or no overall selection on problem-solving performance. Our results are consistent with the idea that variation in cognitive ability is shaped by contrasting effects on different life history traits directly linked to fitness [1, 3].

Individual variation in spontaneous problem-solving performance among wild great tits

Behavioural traits generally and cognitive traits in particular are relatively understudied in an evolutionary ecological context. One reason for this is that such traits are often difficult to characterize among large numbers of individuals, without the influence of diverse environmental effects swamping intrinsic individual differences. We conducted standardized assays on a natural population of great tits, Parus major, to quantify and characterize individual variation in problem-solving performance, a simple cognitive trait often linked to innovative foraging ability. Forty-four per cent of 570 birds solved a food-motivated, lever-pulling problem and this proportion was consistent across three seasons. Individual performance was consistent within and across captivity sessions, across seasons, and between two different problem-solving tasks (lever and string pulling). Problem-solving performance was not explained by differences in latency to approach the empty task, nor latency to feed after human disturbance. Variation was unrelated to body condition, while age and natal origin explained significant but minimal amounts of variation, the importance of which varied between seasons. Problem-solving performance did not covary with exploration behaviour of a novel environment, suggesting that individual differences in problem solving represent an independent source of behavioural variation in our population. Rather than simply reflecting covariance with state or with other behavioural traits, our results suggest that variation in problem-solving performance represents inherent individual differences in the propensity to forage innovatively. We suggest that standardized problem-solving assays may prove ideal for studying the evolutionary ecology of simple cognitive traits.

Personality predicts individual responsiveness to the risks of starvation and predation

Theory suggests that individual personality is tightly linked to individual life histories and to environmental variation. The reactive–proactive axis, for example, is thought to reflect whether individuals prioritize productivity or survival, mutually exclusive options that can be caused by conflicts between foraging and anti-predation behaviour. Evidence for this trade-off hypothesis, however, is limited. Here, we tested experimentally whether exploration behaviour (EB), an assay of proactivity, could explain how great tits (Parus major) respond to changes in starvation and predation risk. Individuals were presented with two feeders, holding good or poor quality food, which interchanged between safe and dangerous positions 10 m apart, across two 24 h treatments. Starvation risk was assumed to be highest in the morning and lowest in the afternoon. The proportion of time spent feeding on good quality food (PTG) rather than poor quality food was repeatable within treatments, but individuals varied in how PTG changed with respect to predation- and starvation-risk across treatments. This individual plasticity variation in foraging behaviour was linked to EB, as predicted by the reactive–proactive axis, but only among individuals in dominant social classes. Our results support the trade-off hypothesis at the level of individuals in a wild population, and suggest that fine-scale temporal and spatial variation may play important roles in the evolution of personality.

Studying the evolutionary ecology of cognition in the wild: a review of practical and conceptual challenges

Cognition is defined as the processes by which animals collect, retain and use information from their environment to guide their behaviour. Thus cognition is essential in a wide range of behaviours, including foraging, avoiding predators and mating. Despite this pivotal role, the evolutionary processes shaping variation in cognitive performance among individuals in wild populations remain very poorly understood. Selection experiments in captivity suggest that cognitive traits can have substantial heritability and can undergo rapid evolution. However only a handful of studies have attempted to explore how cognition influences life‐history variation and fitness in the wild, and direct evidence for the action of natural or sexual selection on cognition is still lacking, reasons for which are diverse. Here we review the current literature with a view to: (i) highlighting the key practical and conceptual challenges faced by the field; (ii) describing how to define and measure cognitive traits in natural populations, and suggesting which species, populations and cognitive traits might be examined to greatest effect; emphasis is placed on selecting traits that are linked to functional behaviour; (iii) discussing how to deal with confounding factors such as personality and motivation in field as well as captive studies; (iv) describing how to measure and interpret relationships between cognitive performance, functional behaviour and fitness, offering some suggestions as to when and what kind of selection might be predicted; and (v) showing how an evolutionary ecological framework, more generally, along with innovative technologies has the potential to revolutionise the study of cognition in the wild. We conclude that the evolutionary ecology of cognition in wild populations is a rapidly expanding interdisciplinary field providing many opportunities for advancing the understanding of how cognitive abilities have evolved.

Shy birds play it safe: personality in captivity predicts risk responsiveness during reproduction in the wild.

Despite a growing body of evidence linking personality to life-history variation and fitness, the behavioural mechanisms underlying these relationships remain poorly understood. One mechanism thought to play a key role is how individuals respond to risk. Relatively reactive and proactive (or shy and bold) personality types are expected to differ in how they manage the inherent trade-off between productivity and survival, with bold individuals being more risk-prone with lower survival probability, and shy individuals adopting a more risk-averse strategy. In the great tit (Parus major), the shy–bold personality axis has been well characterized in captivity and linked to fitness. Here, we tested whether ‘exploration behaviour’, a captive assay of the shy–bold axis, can predict risk responsiveness during reproduction in wild great tits. Relatively slow-exploring (shy) females took longer than fast-exploring (bold) birds to resume incubation after a novel object, representing an unknown threat, was attached to their nest-box, with some shy individuals not returning within the 40 min trial period. Risk responsiveness was consistent within individuals over days. These findings provide rare, field-based experimental evidence that shy individuals prioritize survival over reproductive investment, supporting the hypothesis that personality reflects life-history variation through links with risk responsiveness.

Personality and parasites: sex-dependent associations between avian malaria infection and multiple behavioural traits

The evolution and ecology of consistent behavioural variation, or personality, is currently the focus of much attention in natural populations. Associations between personality traits and parasite infections are increasingly being reported, but the extent to which multiple behavioural traits might be associated with parasitism at the same time is largely unknown. Here, we use a population of great tits, Parus major, to examine whether infection by avian malaria (Plasmodium and Leucocytozoon) is associated with three behavioural traits assayed under standardized conditions. All of these traits are of broad ecological significance and two of them are repeatable or heritable in our population. Here, we show weak correlations between some but not all of these behavioural traits, and sex-dependent associations between all three behavioural traits and parasite infection. Infected males showed increased problem-solving performance whereas infected females showed reduced performance; furthermore, uninfected females were four times more likely to solve problems than uninfected males. Infected females were more exploratory than uninfected females, but infection had no effect on males. Finally, infected males were more risk-averse than uninfected males but females were unaffected. Our results demonstrate the potential for complex interactions between consistent personality variation and parasite infection, though we discuss the difficulty of attributing causality in these associations. Accounting for complex parasite-behaviour associations may prove essential in understanding the evolutionary ecology of behavioural variation and the dynamics of host–parasite interactions.

Scale-dependent phenological synchrony between songbirds and their caterpillar food source.

In seasonal environments, the timing of reproduction has important fitness consequences. Our current understanding of the determinants of reproductive phenology in natural systems is limited because studies often ignore the spatial scale on which animals interact with their environment. When animals use a restricted amount of space and the phenology of resources is spatially variable, selection may favor sensitivity to small-scale environmental variation. Population-level studies of how songbirds track the changing phenology of their food source have been influential in explaining how populations adjust to changing climates but have largely ignored the spatial scale at which phenology varies. We explored whether individual great tits (Parus major) synchronize their breeding with phenological events in their local environment and investigated the spatial scale at which this occurs. We demonstrate marked variation in the timing of food availability, at a spatial scale relevant to individual birds, and that such local variation predicts the breeding phenology of individuals. Using a 45-year data set, we show that measures of vegetation phenology at very local scales are the most important predictors of timing of breeding within years, suggesting that birds can fine-tune their phenology to that of other trophic levels. Knowledge of the determinants of variation in reproductive behavior at different spatial scales is likely to be critical in understanding how selection operates on breeding phenology in natural populations.

Environmental and genetic determinants of innovativeness in a natural population of birds.

Much of the evidence for the idea that individuals differ in their propensity to innovate and solve new problems has come from studies on captive primates. Increasingly, behavioural ecologists are studying innovativeness in wild populations, and uncovering links with functional behaviour and fitness-related traits. The relative importance of genetic and environmental factors in driving this variation, however, remains unknown. Here, we present the results of the first large-scale study to examine a range of causal factors underlying innovative problem-solving performance (PSP) among 831 great tits (Parus major) temporarily taken into captivity. Analyses show that PSP in this population: (i) was linked to a variety of individual factors, including age, personality and natal origin (immigrant or local-born); (ii) was influenced by natal environment, because individuals had a lower PSP when born in poor-quality habitat, or where local population density was high, leading to cohort effects. Links with many of the individual and environmental factors were present only in some years. In addition, PSP (iii) had little or no measurable heritability, as estimated by a Bayesian animal model; and (iv) was not influenced by maternal effects. Despite previous reports of links between PSP and a range of functional traits in this population, the analyses here suggest that innovativeness had weak if any evolutionary potential. Instead most individual variation was caused by phenotypic plasticity driven by links with other behavioural traits and by environmentally mediated developmental stress. Heritability estimates are population, time and context specific, however, and more studies are needed to determine the generality of these effects. Our results shed light on the causes of innovativeness within populations, and add to the debate on the relative importance of genetic and environmental factors in driving phenotypic variation within populations.

Taking the Operant Paradigm into the Field: Associative Learning in Wild Great Tits

Associative learning is essential for resource acquisition, predator avoidance and reproduction in a wide diversity of species, and is therefore a key target for evolutionary and comparative cognition research. Automated operant devices can greatly enhance the study of associative learning and yet their use has been mainly restricted to laboratory conditions. We developed a portable, weatherproof, battery-operated operant device and conducted the first fully automated colour-associative learning experiment using free-ranging individuals in the wild. We used the device to run a colour discrimination task in a monitored population of tits (Paridae). Over two winter months, 80 individuals from four species recorded a total of 5,128 trials. Great tits (Parus major) were more likely than other species to visit the devices and engage in trials, but there were no sex or personality biases in the sample of great tits landing at the devices and registering key pecks. Juveniles were more likely than adults to visit the devices and to register trials. Individuals that were successful at solving a novel technical problem in captivity (lever-pulling) learned faster than non-solvers when at the operant devices in the wild, suggesting cross-contextual consistency in learning performance in very different tasks. There was no significant effect of personality or sex on learning rate, but juveniles’ choice accuracy tended to improve at a faster rate than adults. We discuss how customisable automated operant devices, such as the one described here, could prove to be a powerful tool in evolutionary ecology studies of cognitive traits, especially among inquisitive species such as great tits.