Early-life diet does not affect preference for fish in herring gulls (Larus argentatus).

Urban populations of herring gulls (Larus argentatus) are increasing and causing human-wildlife conflict by exploiting anthropogenic resources. Gulls that breed in urban areas rely on varying amounts of terrestrial anthropogenic foods (e.g., domestic refuse, agricultural and commercial waste) to feed themselves. However, with the onset of hatching, many parent gulls switch to sourcing more marine than anthropogenic or terrestrial foods to provision their chicks. Although anthropogenic foods may meet chick calorific requirements for growth and development, some such foods (e.g., bread) may have lower levels of protein and other key nutrients compared to marine foods. However, whether this parental switch in chick diet is driven by chicks' preference for marine foods, or whether chicks' food preferences are shaped by the food types provisioned by their parents, remains untested. This study tests whether chick food preferences can be influenced by their provisioned diet by experimentally manipulating the ratio of time for which anthropogenic and marine foods were available (80:20 and vice versa) in the rearing diets of two treatment groups of rescued herring gull chicks. Each diet was randomly assigned to each of the 27 captive-reared chicks for the duration of the study. We tested chicks' individual food preferences throughout their development in captivity using food arrays with four food choices (fish, cat food, mussels and brown bread). Regardless of the dietary treatment group, we found that all chicks preferred fish and almost all refused to eat most of the bread offered. Our findings suggest that early-life diet, manipulated by the ratio of time the different foods were available, did not influence gull chicks' food preferences. Instead, chicks developed a strong and persistent preference for marine foods, which appears to match adult gulls' dietary switch to marine foods upon chick hatching and may reinforce the provisioning of marine foods during chick development. However, whether chicks in the wild would refuse provisioned foods, and to a sufficient extent to influence parental provisioning, requires further study. Longitudinal studies of urban animal populations that track wild individuals' food preferences and foraging specialisations throughout life are required to shed light on the development and use of anthropogenic resource exploitation.

Familiarity, personality, and foraging performance in three-spined sticklebacks.

Animals can gain large benefits from living in groups but must coordinate with their groupmates in order to do so. Social interactions between groupmates drive overall group coordination and are influenced by the characteristics of individual group members. In particular, consistent inter-individual differences in behaviour (e.g. boldness) and familiarity between individuals in groups profoundly affect the individual interactions that mediate group coordination. However, the effects of boldness and familiarity have mostly been studied in isolation. Here we describe how familiarity and boldness interact to affect individual performance, leadership, and group coordination in small shoals of three-spined sticklebacks (Gasterosteus aculeatus) solving a novel foraging task. Groups of higher average boldness were less cohesive, but only when group members were familiar with one another. Familiarity affected shy and bold individuals' foraging performance and leadership tendencies differently depending on group characteristics: the shyest group member experienced declining foraging success and leadership with increased group boldness in familiar groups, but experienced the opposite effect on foraging and no effect on leadership in unfamiliar groups. The boldest group member, in contrast, exhibited the opposite pattern: leading and eating more with increasing group boldness in familiar groups, but eating less with increasing group boldness in unfamiliar groups. These results suggest that both boldness and familiarity are important for establishing group behaviour and coordination, and that consistent inter-individual differences in behaviour may primarily impact group coordination once familiarity has been established.

Links between personality traits and problem-solving performance in zebra finches (Taeniopygia guttata).

Consistent individual differences in behaviour across time or contexts (i.e. personality types) have been found in many species and have implications for fitness. Likewise, individual variation in cognitive abilities has been shown to impact fitness. Cognition and personality are complex, multidimensional traits. However, previous work has generally examined the connection between a single personality trait and a single cognitive ability, yielding equivocal results. Links between personality and cognitive ability suggest that behavioural traits coevolved and highlight their nuanced connections. Here we examined individuals' performance on multiple personality tests and repeated problem-solving tests (each measuring innovative performance). We assessed behavioural traits (dominance, boldness, activity, risk-taking, aggressiveness and obstinacy) in 41 captive zebra finches. Birds' scores for boldness and obstinacy were consistent over two years. We also examined whether personality correlated with problem-solving performance on repeated tests. Our results indicate that neophobia, dominance and obstinacy were related to successful solving, and less dominant, more obstinate birds solved the tasks quicker on average. Our results indicate the importance of examining multiple measures over a long period. Future work that identifies links between personality and innovation in non-model organisms may elucidate the coevolution of these two forms of individual differences.

Captive Asian short-clawed otters (Aonyx cinereus) learn to exploit unfamiliar natural prey.

Foraging plays a vital role in animal life histories, and learning whether unfamiliar food items are palatable is a key part of this process. Animals that engage in extractive foraging must also learn how to overcome the protective measures of their prey. While otters (subfamily Lutrinae) are a taxon known for their extractive foraging behaviour, how they learn about prey palatability and acquire extractive foraging techniques remains poorly understood. Here we investigated (i) how captive Asian short-clawed otters (Aonyx cinereus) learned to interact with, and extract meat from, unfamiliar natural prey and (ii) how their exploitation of such prey compared to their ability to overcome artificial foraging tasks containing familiar food rewards. Network-based diffusion analysis showed that otters learned to interact with unfamiliar natural prey by observing their group mates. However, once interacting with the prey, they learned to extract the meat mainly asocially. In addition, otters took longer to overcome the protective measures of unfamiliar natural prey than those of extractive food puzzles. Asian short-clawed otter populations are declining in the wild. Increasing our understanding of how they learn to overcome novel foraging challenges could help develop pre-release training procedures as part of reintroduction programmes for otter conservation.

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.

Predator or provider? How wild animals respond to mixed messages from humans.

Wild animals encounter humans on a regular basis, but humans vary widely in their behaviour: whereas many people ignore wild animals, some people present a threat, while others encourage animals' presence through feeding. Humans thus send mixed messages to which animals must respond appropriately to be successful. Some species appear to circumvent this problem by discriminating among and/or socially learning about humans, but it is not clear whether such learning strategies are actually beneficial in most cases. Using an individual-based model, we consider how learning rate, individual recognition (IR) of humans, and social learning (SL) affect wild animals' ability to reach an optimal avoidance strategy when foraging in areas frequented by humans. We show that 'true' IR of humans could be costly. We also find that a fast learning rate, while useful when human populations are homogeneous or highly dangerous, can cause unwarranted avoidance in other scenarios if animals generalize. SL reduces this problem by allowing conspecifics to observe benign interactions with humans. SL and a fast learning rate also improve the viability of IR. These results provide an insight into how wild animals may be affected by, and how they may cope with, contrasting human behaviour.

How feedback and feed-forward mechanisms link determinants of social dominance.

In many animal societies, individuals differ consistently in their ability to win agonistic interactions, resulting in dominance hierarchies. These differences arise due to a range of factors that can influence individuals' abilities to win agonistic interactions, spanning from genetically driven traits through to individuals' recent interaction history. Yet, despite a century of study since Schjelderup-Ebbe's seminal paper on social dominance, we still lack a general understanding of how these different factors work together to determine individuals' positions in hierarchies. Here, we first outline five widely studied factors that can influence interaction outcomes: intrinsic attributes, resource value asymmetry, winner-loser effects, dyadic interaction-outcome history and third-party support. A review of the evidence shows that a variety of factors are likely important to interaction outcomes, and thereby individuals' positions in dominance hierarchies, in diverse species. We propose that such factors are unlikely to determine dominance outcomes independently, but rather form part of feedback loops whereby the outcomes of previous agonistic interactions (e.g. access to food) impact factors that might be important in subsequent interactions (e.g. body condition). We provide a conceptual framework that illustrates the multitude potential routes through which such feedbacks can occur, and how the factors that determine the outcomes of dominance interactions are highly intertwined and thus rarely act independently of one another. Further, we generalise our framework to include multi-generational feed-forward mechanisms: how interaction outcomes in one generation can influence the factors determining interaction outcomes in the next generation via a range of parental effects. This general framework describes how interaction outcomes and the factors determining them are linked within generations via feedback loops, and between generations via feed-forward mechanisms. We then highlight methodological approaches that will facilitate the study of feedback loops and dominance dynamics. Lastly, we discuss how our framework could shape future research, including: how feedbacks generate variation in the factors discussed, and how this might be studied experimentally; how the relative importance of different feedback mechanisms varies across timescales; the role of social structure in modulating the effect of feedbacks on hierarchy structure and stability; and the routes of parental influence on the dominance status of offspring. Ultimately, by considering dominance interactions as part of a dynamic feedback system that also feeds forward into subsequent generations, we will understand better the factors that structure dominance hierarchies in animal groups.

Costs dictate strategic investment in dominance interactions.

Dominance is important for access to resources. As dominance interactions are costly, individuals should be strategic in whom they interact with. One hypothesis is that individuals should direct costly interactions towards those closest in rank, as they have most to gain-in terms of attaining or maintaining dominance-from winning such interactions. Here, we show that male vulturine guineafowl (Acryllium vulturinum), a gregarious species with steep dominance hierarchies, strategically express higher-cost aggressive interactions towards males occupying ranks immediately below themselves in their group's hierarchy. By contrast, lower-cost aggressive interactions are expressed towards group members further down the hierarchy. By directly evaluating differences in the strategic use of higher- and lower-cost aggressive interactions towards competitors, we show that individuals disproportionately use highest-cost interactions-such as chases-towards males found one to three ranks below themselves. Our results support the hypothesis that the costs associated with different interaction types can determine their expression in social groups with steep dominance hierarchies. 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'.

Group size and modularity interact to shape the spread of infection and information through animal societies.

Social interactions between animals can provide many benefits, including the ability to gain useful environmental information through social learning. However, these social contacts can also facilitate the transmission of infectious diseases through a population. Animals engaging in social interactions therefore face a trade-off between the potential informational benefits and the risk of acquiring disease. Theoretical models have suggested that modular social networks, associated with the formation of groups or sub-groups, can slow spread of infection by trapping it within particular groups. However, these social structures will not necessarily impact the spread of information in the same way if its transmission follows a "complex contagion", e.g. through individuals disproportionally copying the majority (conformist learning). Here we use simulation models to demonstrate that modular networks can promote the spread of information relative to the spread of infection, but only when the network is fragmented and group sizes are small. We show that the difference in transmission between information and disease is maximised for more well-connected social networks when the likelihood of transmission is intermediate. Our results have important implications for understanding the selective pressures operating on the social structure of animal societies, revealing that highly fragmented networks such as those formed in fission-fusion social groups and multilevel societies can be effective in modulating the infection-information trade-off for individuals within them. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00265-021-03102-4.

Phthalate diversity in eggs and associations with oxidative stress in the European herring gull (Larus argentatus).

Phthalates are plastic-derived contaminants that are ubiquitous in natural environments and function as pro-oxidants. The extent to which phthalates bioaccumulate in wild animals and associations with oxidative stress are poorly understood. Here, we describe relationships between maternally-derived phthalates, lipid peroxidation (malondialdehyde, MDA) and the dietary antioxidant α-tocopherol in eggs of European herring gulls (Larus argentatus) in Cornwall, UK. Up to six phthalate parent compounds and four phthalate metabolites were detected. Egg concentrations of MDA were positively associated with dicyclohexyl phthalate (DCHP) and negatively associated with α-tocopherol, suggesting that DCHP is associated with oxidative stress in gulls. The consequences of phthalate exposure in ovo for offspring development warrants study.

Effects of food type and abundance on begging and sharing in Asian small-clawed otters (Aonyx cinereus).

Begging for food, a conspicuous solicitation display, is common in a variety of taxa, and it has received extensive research attention in a parent-offspring context. Both theoretical models and empirical evidence suggest that offspring begging can be an honest signal of hunger or a mediator of competition between siblings. At a behavioural mechanistic level, begging for food can be a form of harassment aimed at persuading those in possession of food to share. Food sharing, defined as the transfer of a defendable food item from one individual to another, can vary considerably between species, age-classes and food type and abundance. We investigated the determinants of begging and food-sharing behaviours in Asian small-clawed otters (Aonyx cinereus), a group-living species that commonly exhibits begging in captivity. We presented two captive otter populations with three food types that varied in exploitation complexity, in three different abundances. We predicted that begging rates would be highest when food was in lowest abundance and hardest to exploit, and that increased begging would lead to increased food sharing. We found that, over time, increased begging rates were indeed correlated with increased food transfers, but neither food type complexity nor abundance affected begging or sharing rates. However, age category was significantly associated with begging and food sharing rates: juvenile otters begged more and shared less than adult otters. The results from this first experimental study on begging and food sharing within the Mustelid family begin to reveal some of the drivers of these behaviours.

The Role of Animal Cognition in Human-Wildlife Interactions.

Humans have a profound effect on the planet's ecosystems, and unprecedented rates of human population growth and urbanization have brought wild animals into increasing contact with people. For many species, appropriate responses toward humans are likely to be critical to survival and reproductive success. Although numerous studies have investigated the impacts of human activity on biodiversity and species distributions, relatively few have examined the effects of humans on the behavioral responses of animals during human-wildlife encounters, and the cognitive processes underpinning those responses. Furthermore, while humans often present a significant threat to animals, the presence or behavior of people may be also associated with benefits, such as food rewards. In scenarios where humans vary in their behavior, wild animals would be expected to benefit from the ability to discriminate between dangerous, neutral and rewarding people. Additionally, individual differences in cognitive and behavioral phenotypes and past experiences with humans may affect animals' ability to exploit human-dominated environments and respond appropriately to human cues. In this review, we examine the cues that wild animals use to modulate their behavioral responses toward humans, such as human facial features and gaze direction. We discuss when wild animals are expected to attend to certain cues, how information is used, and the cognitive mechanisms involved. We consider how the cognitive abilities of wild animals are likely to be under selection by humans and therefore influence population and community composition. We conclude by highlighting the need for long-term studies on free-living, wild animals to fully understand the causes and ecological consequences of variation in responses to human cues. The effects of humans on wildlife behavior are likely to be substantial, and a detailed understanding of these effects is key to implementing effective conservation strategies and managing human-wildlife conflict.

The drivers and functions of rock juggling in otters.

Object play refers to the seemingly non-functional manipulation of inanimate items when in a relaxed state. In juveniles, object play may help develop skills to aid survival. However, why adults show object play remains poorly understood. We studied potential drivers and functions of the well-known object play behaviour of rock juggling in Asian small-clawed (Aonyx cinereus) and smooth-coated (Lutrogale perspicillata) otters. These are closely related species, but Asian small-clawed otters perform extractive foraging movements to exploit crabs and shellfish while smooth-coated otters forage on fish. We thus predicted that frequent rock jugglers might be better at solving extractive foraging puzzles in the first species, but not the latter. We also assessed whether species, age, sex and hunger correlated with rock juggling frequency. We found that juvenile and senior otters juggled more than adults. However, rock juggling frequency did not differ between species or sexes. Otters juggled more when 'hungry', but frequent jugglers did not solve food puzzles faster. Our results suggest that rock juggling may be a misdirected behaviour when hungry and may facilitate juveniles' motor development, but it appears unrelated to foraging skills. We suggest future studies to reveal the ontogeny, evolution and welfare implications of this object play behaviour.

Urban herring gulls use human behavioural cues to locate food.

While many animals are negatively affected by urbanization, some species appear to thrive in urban environments. Herring gulls (Larus argentatus) are commonly found in urban areas and often scavenge food discarded by humans. Despite increasing interactions between humans and gulls, little is known about the cognitive underpinnings of urban gull behaviour and to what extent they use human behavioural cues when making foraging decisions. We investigated whether gulls are more attracted to anthropogenic items when they have been handled by a human. We first presented free-living gulls with two identical food objects, one of which was handled, and found that gulls preferentially pecked at the handled food object. We then tested whether gulls' attraction to human-handled objects generalizes to non-food items by presenting a new sample of gulls with two non-food objects, where, again, only one was handled. While similar numbers of gulls approached food and non-food objects in both experiments, they did not peck at handled non-food objects above chance levels. These results suggest that urban gulls generally show low levels of neophobia, but that they use human handling as a cue specifically in the context of food. These behaviours may contribute to gulls' successful exploitation of urban environments.

Learning strategies and long-term memory in Asian short-clawed otters (Aonyx cinereus).

Social learning, where information is acquired from others, is taxonomically widespread. There is growing evidence that animals selectively employ 'social learning strategies', which determine e.g. when to copy others instead of learning asocially and whom to copy. Furthermore, once animals have acquired new information, e.g. regarding profitable resources, it is beneficial for them to commit it to long-term memory (LTM), especially if it allows access to profitable resources in the future. Research into social learning strategies and LTM has covered a wide range of taxa. However, otters (subfamily Lutrinae), popular in zoos due to their social nature and playfulness, remained neglected until a recent study provided evidence of social learning in captive smooth-coated otters (Lutrogale perspicillata), but not in Asian short-clawed otters (Aonyx cinereus). We investigated Asian short-clawed otters' learning strategies and LTM performance in a foraging context. We presented novel extractive foraging tasks twice to captive family groups and used network-based diffusion analysis to provide evidence of a capacity for social learning and LTM in this species. A major cause of wild Asian short-clawed otter declines is prey scarcity. Furthering our understanding of how they learn about and remember novel food sources could inform key conservation strategies.

Coping with strangers: how familiarity and active interactions shape group coordination in Corydoras aeneus.

Social groups composed of familiar individuals exhibit better coordination than unfamiliar groups; however, the ways familiarity contributes to coordination are poorly understood. Prior social experience probably allows individuals to learn the tendencies of familiar group-mates and respond accordingly. Without prior experience, individuals would benefit from strategies for enhancing coordination with unfamiliar others. We used a social catfish, Corydoras aeneus, that uses discrete, observable tactile interactions to assess whether active interactions could facilitate coordination, and how their role might be mediated by familiarity. We describe this previously understudied physical interaction, 'nudges', and show it to be associated with group coordination and cohesion. Furthermore, we investigated nudging and coordination in familiar/unfamiliar pairs. In all pairs, we found that nudging rates were higher during coordinated movements than when fish were together but not coordinating. We observed no familiarity-based difference in coordination or cohesion. Instead, unfamiliar pairs exhibited significantly higher nudging rates, suggesting that unfamiliar pairs may be able to compensate for unfamiliarity through increased nudging. By contrast, familiar individuals coordinated with comparatively little nudging. Second, we analysed nudging and cohesion within triplets of two familiar and one unfamiliar individual (where familiar individuals had a choice of partner). Although all individuals nudged at similar rates, the unfamiliar group-mate was less cohesive than its familiar group-mates and spent more time alone. Unfamiliar individuals that nudged their group-mates more frequently exhibited higher cohesion, indicating that nudging may facilitate cohesion for the unfamiliar group-mate. Overall, our results suggest that nudges can mitigate unfamiliarity, but that their usage is reduced in the case of familiar individuals, implying a cost is associated with the behaviour.

Herring gulls respond to human gaze direction.

Human-wildlife conflict is one of the greatest threats to species populations worldwide. One species facing national declines in the UK is the herring gull (Larus argentatus), despite an increase in numbers in urban areas. Gulls in urban areas are often considered a nuisance owing to behaviours such as food-snatching. Whether urban gull feeding behaviour is influenced by human behavioural cues, such as gaze direction, remains unknown. We therefore measured the approach times of herring gulls to a food source placed in close proximity to an experimenter who either looked directly at the gull or looked away. We found that only 26% of targeted gulls would touch the food, suggesting that food-snatching is likely to be conducted by a minority of individuals. When gulls did touch the food, they took significantly longer to approach when the experimenter's gaze was directed towards them compared with directed away. However, inter-individual behaviour varied greatly, with some gulls approaching similarly quickly in both treatments, while others approached much more slowly when the experimenter was looking at them. These results indicate that reducing human-herring gull conflict may be possible through small changes in human behaviour, but will require consideration of behavioural differences between individual gulls.

Animal Cognition: The Benefits of Remembering.

How cognitive abilities evolve through natural selection is poorly understood. Two new studies show that a good spatial memory helps birds that hide their food to survive and produce more offspring.

Measuring and understanding individual differences in cognition.

Individuals vary in their cognitive performance. While this variation forms the foundation of the study of human psychometrics, its broader importance is only recently being recognized. Explicitly acknowledging this individual variation found in both humans and non-human animals provides a novel opportunity to understand the mechanisms, development and evolution of cognition. The papers in this special issue highlight the growing emphasis on individual cognitive differences from fields as diverse as neurobiology, experimental psychology and evolutionary biology. Here, we synthesize this body of work. We consider the distinct challenges in quantifying individual differences in cognition and provide concrete methodological recommendations. In particular, future studies would benefit from using multiple task variants to ensure they target specific, clearly defined cognitive traits and from conducting repeated testing to assess individual consistency. We then consider how neural, genetic, developmental and behavioural factors may generate individual differences in cognition. Finally, we discuss the potential fitness consequences of individual cognitive variation and place these into an evolutionary framework with testable hypotheses. We intend for this special issue to stimulate researchers to position individual variation at the centre of the cognitive sciences.This article is part of the theme issue 'Causes and consequences of individual differences in cognitive abilities'.

Stress hormones, social associations and song learning in zebra finches.

The use of information provided by others is a common short-cut adopted to inform decision-making. However, instead of indiscriminately copying others, animals are often selective in what, when and whom they copy. How do they decide which 'social learning strategy' to use? Previous research indicates that stress hormone exposure in early life may be important: while juvenile zebra finches copied their parents' behaviour when solving novel foraging tasks, those exposed to elevated levels of corticosterone (CORT) during development copied only unrelated adults. Here, we tested whether this switch in social learning strategy generalizes to vocal learning. In zebra finches, juvenile males often copy their father's song; would CORT-treated juveniles in free-flying aviaries switch to copying songs of other males? We found that CORT-treated juveniles copied their father's song less accurately as compared to control juveniles. We hypothesized that this could be due to having weaker social foraging associations with their fathers, and found that sons that spent less time foraging with their fathers produced less similar songs. Our findings are in line with a novel hypothesis linking early-life stress and social learning: early-life CORT exposure may affect social learning indirectly as a result of the way it shapes social affiliations.This article is part of the theme issue 'Causes and consequences of individual differences in cognitive abilities'.