Aggressive interactions influence cognitive performance in Western Australian magpies.

Extensive research has investigated the relationship between the social environment and cognition, suggesting that social complexity may drive cognitive evolution and development. However, evidence for this relationship remains equivocal. Group size is often used as a measure of social complexity, but this may not capture intraspecific variation in social interactions. Social network analysis can provide insight into the cognitively demanding challenges associated with group living at the individual level. Here, we use social networks to investigate whether the cognitive performance of wild Western Australian magpies (Gymnorhina tibicen dorsalis) is related to group size and individual social connectedness. We quantified social connectedness using four interaction types: proximity, affiliative, agonistic and vocal. Consistent with previous research on this species, individuals in larger groups performed better on an associative learning task. However, social network position was also related to cognitive performance. Individuals receiving aggressive interactions performed better, while those involved in aggressive interactions with more group members performed worse. Overall, this suggests that cognitive performance is related to specific types of social interaction. The findings from this study highlight the value of considering fine-grained metrics of sociality that capture the challenges associated with social life when testing the relationship between the social environment and cognition.

Anthropogenic disturbance affects calling and collective behaviour in corvid roosts.

Acoustic communication plays an important role in coordinating group dynamics and collective movements across a range of taxa. However, anthropogenic disturbance can inhibit the production or reception of acoustic signals. Here, we investigate the effects of noise and light pollution on the calling and collective behaviour of wild jackdaws (Corvus monedula), a highly social corvid species that uses vocalizations to coordinate collective movements at winter roosting sites. Using audio and video monitoring of roosts in areas with differing degrees of urbanization, we evaluate the influence of anthropogenic disturbance on vocalizations and collective movements. We found that when levels of background noise were higher, jackdaws took longer to settle following arrival at the roost in the evening and also called more during the night, suggesting that human disturbance may cause sleep disruption. High levels of overnight calling were, in turn, linked to disruption of vocal consensus decision-making and less cohesive group departures in the morning. These results raise the possibility that, by affecting cognitive and perceptual processes, human activities may interfere with animals' ability to coordinate collective behaviour. Understanding links between anthropogenic disturbance, communication, cognition and collective behaviour must be an important research priority in our increasingly urbanized world. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Heritability of cognitive performance in wild Western Australian magpies.

Individual differences in cognitive performance can have genetic, social and environmental components. Most research on the heritability of cognitive traits comes from humans or captive non-human animals, while less attention has been given to wild populations. Western Australian magpies (Gymnorhina tibicen dorsalis, hereafter magpies) show phenotypic variation in cognitive performance, which affects reproductive success. Despite high levels of individual repeatability, we do not know whether cognitive performance is heritable in this species. Here, we quantify the broad-sense heritability of associative learning ability in a wild population of Western Australian magpies. Specifically, we explore whether offspring associative learning performance is predicted by maternal associative learning performance or by the social environment (group size) when tested at three time points during the first year of life. We found little evidence that offspring associative learning performance is heritable, with an estimated broad-sense heritability of just -0.046 ± 0.084 (confidence interval: -0.234/0.140). However, complementing previous findings, we find that at 300 days post-fledging, individuals raised in larger groups passed the test in fewer trials compared with individuals from small groups. Our results highlight the pivotal influence of the social environment on cognitive development.

Ultimate drivers of forced extra-pair copulations in birds lacking a penis: jackdaws as a case-study.

Forced copulation is common, presumably because it can increase male reproductive success. Forced extra-pair copulation (FEPC) occurs in birds, even though most species lack a penis and are widely thought to require female cooperation for fertilization. How FEPC persists, despite a presumed lack of siring success and likely non-negligible costs to the male, is unknown. Using the jackdaw (Corvus monedula) as a case study, we use SNPs to quantify the extra-pair paternity rate through FEPC and evaluate explanations for the persistence of FEPC in species without a penis. We then collate evidence for FEPC across penis-lacking birds. Combining genetic and behavioural analyses, our study suggests that the most likely explanations for the maintenance of FEPC in jackdaws are that it provides a selective advantage to males or it is a relic. Our literature review shows that across birds lacking a penis, FEPC is taxonomically widespread, and yet, little is known about its evolution. A broader implementation of the approach used here, combining both genetic and behavioural data, may shed light on why this widespread sexual behaviour persists. Additional work is necessary to understand whether a penis is needed for paternity through forced copulation and to quantify the costs of FEPC.

High temperatures during early development reduce adult cognitive performance and reproductive success in a wild animal population.

Global warming is rapidly changing the phenology, distribution, behaviour and demography of wild animal populations. Recent studies in wild animals have shown that high temperatures can induce short-term cognitive impairment, and captive studies have demonstrated that heat exposure during early development can lead to long-term cognitive impairment. Given that cognition underpins behavioural flexibility and can be directly linked to fitness, understanding how high temperatures during early life might impact adult cognitive performance in wild animals is a critical next step to predict wildlife responses to climate change. Here, we investigated the relationship between temperatures experienced during development, adult cognitive performance, and reproductive success in wild southern pied babblers (Turdoides bicolor). We found that higher mean daily maximum temperatures during nestling development led to long-term cognitive impairment in associative learning performance, but not reversal learning performance. Additionally, a higher number of hot days (exceeding 35.5 °C, temperature threshold at which foraging efficiency and offspring provisioning decline) during post-fledging care led to reduced reproductive success in adulthood. We did not find evidence that low reproductive success was linked to impaired associative learning performance: associative learning performance was not related to reproductive success. In contrast, reversal learning performance was negatively related to reproductive success in breeding adults. This suggests that reproduction can carry a cost in terms of reduced performance in cognitively demanding tasks, confirming previous evidence in this species. Taken together, these findings indicate that naturally occurring high temperatures during early development have long-term negative effects on cognition and reproductive success in wild animals. Compounding effects of high temperatures on current nestling mortality and on the long-term cognitive and reproductive performance of survivors are highly concerning given ongoing global warming.

Genetic and context-specific effects on individual inhibitory control performance in the guppy (Poecilia reticulata).

Among-individual variation in cognitive traits, widely assumed to have evolved under adaptive processes, is increasingly being demonstrated across animal taxa. As variation among individuals is required for natural selection, characterizing individual differences and their heritability is important to understand how cognitive traits evolve. Here, we use a quantitative genetic study of wild-type guppies repeatedly exposed to a 'detour task' to test for genetic variance in the cognitive trait of inhibitory control. We also test for genotype-by-environment interactions (GxE) by testing related fish under alternative experimental treatments (transparent vs. semi-transparent barrier in the detour-task). We find among-individual variation in detour task performance, consistent with differences in inhibitory control. However, analysis of GxE reveals that heritable factors only contribute to performance variation in one treatment. This suggests that the adaptive evolutionary potential of inhibitory control (and/or other latent variables contributing to task performance) may be highly sensitive to environmental conditions. The presence of GxE also implies that the plastic response of detour task performance to treatment environment is genetically variable. Our results are consistent with a scenario where variation in individual inhibitory control stems from complex interactions between heritable and plastic components.

High temperatures are associated with reduced cognitive performance in wild southern pied babblers.

Global temperatures are increasing rapidly. While considerable research is accumulating regarding the lethal and sublethal effects of heat on wildlife, its potential impact on animal cognition has received limited attention. Here, we tested wild southern pied babblers (Turdoides bicolor) on three cognitive tasks (associative learning, reversal learning and inhibitory control) under naturally occurring heat stress and non-heat stress conditions. We determined whether cognitive performance was explained by temperature, heat dissipation behaviours, individual and social attributes, or proxies of motivation. We found that temperature, but not heat dissipation behaviours, predicted variation in associative learning performance. Individuals required on average twice as many trials to learn an association when the maximum temperature during testing exceeded 38°C compared with moderate temperatures. Higher temperatures during testing were also associated with reduced inhibitory control performance, but only in females. By contrast, we found no temperature-related decline in performance in the reversal learning task, albeit individuals reached learning criterion in only 14 reversal learning tests. Our findings provide novel evidence of temperature-mediated cognitive impairment in a wild animal and indicate that its occurrence depends on the cognitive trait examined and individual sex.

Cognition mediates response to anthropogenic noise in wild Western Australian magpies (Gmynorhina tibicen dorsalis).

Anthropogenic noise is a pollutant of growing concern, with wide-ranging effects on taxa across ecosystems. Until recently, studies investigating the effects of anthropogenic noise on animals focused primarily on population-level consequences, rather than individual-level impacts. Individual variation in response to anthropogenic noise may result from extrinsic or intrinsic factors. One such intrinsic factor, cognitive performance, varies between individuals and is hypothesised to aid behavioural response to novel stressors. Here, we combine cognitive testing, behavioural focals and playback experiments to investigate how anthropogenic noise affects the behaviour and anti-predator response of Western Australian magpies (Gymnorhina tibicen dorsalis), and to determine whether this response is linked to cognitive performance. We found a significant population-level effect of anthropogenic noise on the foraging effort, foraging efficiency, vigilance, vocalisation rate and anti-predator response of magpies, with birds decreasing their foraging, vocalisation behaviours and anti-predator response, and increasing vigilance when loud anthropogenic noise was present. We also found that individuals varied in their response to playbacks depending on their cognitive performance, with individuals that performed better in an associative learning task maintaining their anti-predator response when an alarm call was played in anthropogenic noise. Our results add to the growing body of literature documenting the adverse effects of anthropogenic noise on wildlife and provide the first evidence for an association between individual cognitive performance and behavioural responses to anthropogenic noise.

Wild jackdaws can selectively adjust their social associations while preserving valuable long-term relationships.

Influential theories of the evolution of cognition and cooperation posit that tracking information about others allows individuals to adjust their social associations strategically, re-shaping social networks to favour connections between compatible partners. Crucially, to our knowledge, this has yet to be tested experimentally in natural populations, where the need to maintain long-term, fitness-enhancing relationships may limit social plasticity. Using a social-network-manipulation experiment, we show that wild jackdaws (Corvus monedula) learned to favour social associations with compatible group members (individuals that provided greater returns from social foraging interactions), but resultant change in network structure was constrained by the preservation of valuable pre-existing relationships. Our findings provide insights into the cognitive basis of social plasticity and the interplay between individual decision-making and social-network structure.

Competition and generalization impede cultural formation in wild jackdaws.

Animal cultures have now been demonstrated experimentally in diverse taxa from flies to great apes. However, experiments commonly use tasks with unrestricted access to equal pay-offs and innovations seeded by demonstrators who are trained to exhibit strong preferences. Such conditions may not reflect those typically found in nature. For example, the learned preferences of natural innovators may be weaker, while competition for depleting resources can favour switching between strategies and generalizing from past experience. Here we show that in experiments where wild jackdaws (Corvus monedula) can freely discover depleting supplies of novel foods, generalization has a powerful effect on learning, allowing individuals to exploit multiple new opportunities through both social and individual learning. Further, in contrast to studies with trained demonstrators, individuals that were first to innovate showed weak preferences. As a consequence, many individuals ate all available novel foods, displaying no strong preference and no group-level culture emerged. Individuals followed a 'learn from adults' strategy, but other demographic factors played a minimal role in shaping social transmission. These results demonstrate the importance of generalization in allowing animals to exploit new opportunities and highlight how natural competitive dynamics may impede the formation of culture.

General cognitive performance declines with female age and is negatively related to fledging success in a wild bird.

Identifying the causes and fitness consequences of intraspecific variation in cognitive performance is fundamental to understand how cognition evolves. Selection may act on different cognitive traits separately or jointly as part of the general cognitive performance (GCP) of the individual. To date, few studies have examined simultaneously whether individual cognitive performance covaries across different cognitive tasks, the relative importance of individual and social attributes in determining cognitive variation, and its fitness consequences in the wild. Here, we tested 38 wild southern pied babblers (Turdoides bicolor) on a cognitive test battery targeting associative learning, reversal learning and inhibitory control. We found that a single factor explained 59.5% of the variation in individual cognitive performance across tasks, suggestive of a general cognitive factor. GCP varied by age and sex; declining with age in females but not males. Older females also tended to produce a higher average number of fledglings per year compared to younger females. Analysing over 10 years of breeding data, we found that individuals with lower general cognitive performance produced more fledglings per year. Collectively, our findings support the existence of a trade-off between cognitive performance and reproductive success in a wild bird.

Velocity correlations in jackdaw flocks in different ecological contexts.

Velocity correlation is an important feature for animal groups performing collective motions. Previous studies have mostly focused on the velocity correlation in a single ecological context. It is unclear whether correlation characteristics vary in a single species in different contexts. Here, we studied the velocity correlations in jackdaw flocks in two different contexts: transit flocks where birds travel from one location to another, and mobbing flocks where birds respond to an external stimulus. We found that in both contexts, although the interaction rules are different, the velocity correlations remain scale-free, i.e. the correlation length (the distance over which the velocity of two individuals is similar) increases linearly with the group size. Furthermore, we found that the correlation length is independent of the group density for transit flocks, but increases with increasing group density in mobbing flocks. This result confirms a previous observation that birds obey topological interactions in transit flocks, but switch to metric interactions in mobbing flocks. Finally, in both contexts, the impact of group polarization on correlation length is not significant. Our results suggest that wild animals are always able to respond coherently to perturbations regardless of context.

Does trappability and self-selection influence cognitive performance?

Recent research has highlighted how trappability and self-selection-the processes by which individuals with particular traits may be more likely to be caught or to participate in experiments-may be sources of bias in studies of animal behaviour and cognition. It is crucial to determine whether such biases exist, and if they do, what effect they have on results. In this study, we investigated if trappability (quantified through 'ringing status'-whether or not a bird had been trapped for ringing) and self-selection are sources of bias in a series of associative learning experiments spanning 5 years in the Western Australian magpie (Gymnorhina tibicen dorsalis). We found no evidence of self-selection, with no biases in task participation associated with sex, age, group size or ringing status. In addition, we found that there was no effect of trappability on cognitive performance. These findings give us confidence in the results generated in the animal cognition literature and add to a growing body of literature seeking to determine potential sources of bias in studies of animal behaviour, and how they influence the generalizability and reproducibility of findings.

Problems with using comparative analyses of avian brain size to test hypotheses of cognitive evolution.

There are multiple hypotheses for the evolution of cognition. The most prominent hypotheses are the Social Intelligence Hypothesis (SIH) and the Ecological Intelligence Hypothesis (EIH), which are often pitted against one another. These hypotheses tend to be tested using broad-scale comparative studies of brain size, where brain size is used as a proxy of cognitive ability, and various social and/or ecological variables are included as predictors. Here, we test how robust conclusions drawn from such analyses may be. First, we investigate variation in brain and body size measurements across >1000 bird species. We demonstrate that there is substantial variation in brain and body size estimates across datasets, indicating that conclusions drawn from comparative brain size models are likely to differ depending on the source of the data. Following this, we subset our data to the Corvides infraorder and interrogate how modelling decisions impact results. We show that model results change substantially depending on variable inclusion, source and classification. Indeed, we could have drawn multiple contradictory conclusions about the principal drivers of brain size evolution. These results reflect concerns from a growing number of researchers that conclusions drawn from comparative brain size studies may not be robust. We suggest that to interrogate hypotheses of cognitive evolution, a fruitful way forward is to focus on testing cognitive performance within and between closely related taxa, with an emphasis on understanding the relationship between informational uncertainty and cognitive evolution.

Long-term repeatability of cognitive performance.

Measures of cognitive performance, derived from psychometric tasks, have yielded important insights into the factors governing cognitive variation. However, concerns remain over the robustness of these measures, which may be susceptible to non-cognitive factors such as motivation and persistence. Efforts to quantify short-term repeatability of cognitive performance have gone some way to address this, but crucially the long-term repeatability of cognitive performance has been largely overlooked. Quantifying the long-term repeatability of cognitive performance provides the opportunity to determine the stability of cognitive phenotypes and the potential for selection to act on them. To this end, we quantified long-term repeatability of cognitive performance in wild Australian magpies over a three-year period. Cognitive performance was repeatable in two out of four cognitive tasks-associative learning and reversal-learning performance was repeatable, but spatial memory and inhibitory control performance, although trending toward significance, was not. Measures of general cognitive performance, obtained from principal components analyses carried out on each cognitive test battery, were highly repeatable. Together, these findings provide evidence that at least some cognitive phenotypes are stable, which in turn has important implications for our understanding of cognitive evolution.

Vocally mediated consensus decisions govern mass departures from jackdaw roosts.

In the early morning, large groups of up to hundreds or even thousands of roosting birds, sometimes comprising the entire roost population, often take off together in sudden mass departures. These departures commonly occur in low-light conditions and structurally complex habitats where access to visual cues is likely to be restricted. Roosting birds are often highly vocal, leading us to hypothesise that vocalisations, which can propagate over large distances, could provide a means of enabling individuals to agree on when to depart - that is to establish a consensus1 - and thus coordinate the timing of mass movements. Investigations of the role of acoustic signals in coordinating collective decisions have been limited to honeybees2 and relatively small vertebrate groups (<50 individuals)3-5 and have rarely included experimental validation2,3. Here, by combining field recordings with a large-scale experimental manipulation, we show that jackdaws (Corvus monedula) use vocalisations to coordinate mass departures from winter roosts. This provides empirical evidence for vocally-mediated consensus decision-making in large vertebrate groups.

Stochastic modelling of bird flocks: accounting for the cohesiveness of collective motion.

Collective behaviour can be difficult to discern because it is not limited to animal aggregations such as flocks of birds and schools of fish wherein individuals spontaneously move in the same way despite the absence of leadership. Insect swarms are, for example, a form of collective behaviour, albeit one lacking the global order seen in bird flocks and fish schools. Their collective behaviour is evident in their emergent macroscopic properties. These properties are predicted by close relatives of Okubo's 1986 [Adv. Biophys.22, 1-94. (doi:10.1016/0065-227X(86)90003-1)] stochastic model. Here, we argue that Okubo's stochastic model also encapsulates the cohesiveness mechanism at play in bird flocks, namely the fact that birds within a flock behave on average as if they are trapped in an elastic potential well. That is, each bird effectively behaves as if it is bound to the flock by a force that on average increases linearly as the distance from the flock centre increases. We uncover this key, but until now overlooked, feature of flocking in empirical data. This gives us a means of identifying what makes a given system collective. We show how the model can be extended to account for intrinsic velocity correlations and differentiated social relationships.

Animal cognition in an urbanised world.

Explaining how animals respond to an increasingly urbanised world is a major challenge for evolutionary biologists. Urban environments often present animals with novel problems that differ from those encountered in their evolutionary past. To navigate these rapidly changing habitats successfully, animals may need to adjust their behaviour flexibly over relatively short timescales. These behavioural changes, in turn, may be facilitated by an ability to acquire, store and process information from the environment. The question of how cognitive abilities allow animals to avoid threats and exploit resources (or constrain their ability to do so) is attracting increasing research interest, with a growing number of studies investigating cognitive and behavioural differences between urban-dwelling animals and their non-urban counterparts. In this review we consider why such differences might arise, focusing on the informational challenges faced by animals living in urban environments, and how different cognitive abilities can assist in overcoming these challenges. We focus largely on birds, as avian taxa have been the subject of most research to date, but discuss work in other species where relevant. We also address the potential consequences of cognitive variation at the individual and species level. For instance, do urban environments select for, or influence the development of, particular cognitive abilities? Are individuals or species with particular cognitive phenotypes more likely to become established in urban habitats? How do other factors, such as social behaviour and individual personality, interact with cognition to influence behaviour in urban environments? The aim of this review is to synthesise current knowledge and identify key avenues for future research, in order to improve our understanding of the ecological and evolutionary consequences of urbanisation.