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.

Repeatable group differences in the collective behaviour of stickleback shoals across ecological contexts.

Establishing how collective behaviour emerges is central to our understanding of animal societies. Previous research has highlighted how universal interaction rules shape collective behaviour, and that individual differences can drive group functioning. Groups themselves may also differ considerably in their collective behaviour, but little is known about the consistency of such group variation, especially across different ecological contexts that may alter individuals' behavioural responses. Here, we test if randomly composed groups of sticklebacks differ consistently from one another in both their structure and movement dynamics across an open environment, an environment with food, and an environment with food and shelter. Based on high-resolution tracking data of the free-swimming shoals, we found large context-associated changes in the average behaviour of the groups. But despite these changes and limited social familiarity among group members, substantial and predictable behavioural differences between the groups persisted both within and across the different contexts (group-level repeatability): some groups moved consistently faster, more cohesively, showed stronger alignment and/or clearer leadership than other groups. These results suggest that among-group heterogeneity could be a widespread feature in animal societies. Future work that considers group-level variation in collective behaviour may help understand the selective pressures that shape how animal collectives form and function.

The evolution of self-control.

Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.

Developmental stress predicts social network position.

The quantity and quality of social relationships, as captured by social network analysis, can have major fitness consequences. Various studies have shown that individual differences in social behaviour can be due to variation in exposure to developmental stress. However, whether these developmental differences translate to consistent differences in social network position is not known. We experimentally increased levels of the avian stress hormone corticosterone (CORT) in nestling zebra finches in a fully balanced design. Upon reaching nutritional independence, we released chicks and their families into two free-flying rooms, where we measured daily social networks over five weeks using passive integrated transponder tags. Developmental stress had a significant effect on social behaviour: despite having similar foraging patterns, CORT chicks had weaker associations to their parents than control chicks. Instead, CORT chicks foraged with a greater number of flock mates and were less choosy with whom they foraged, resulting in more central network positions. These findings highlight the importance of taking developmental history into account to understand the drivers of social organization in gregarious species.

Developmental programming: cumulative effects of increased pre-hatching corticosterone levels and post-hatching unpredictable food availability on physiology and behaviour in adulthood.

Prolonged exposure to stress during development can have long-term detrimental effects on health and wellbeing. However, the environmental matching hypothesis proposes that developmental stress programs physiology and behaviour in an adaptive way that can enhance fitness if early environments match those experienced later in life. Most research has focused on the harmful effects that stress during a single period in early life may exert in adulthood. In this study, we tested the potential additive and beneficial effects that stress experienced during both pre- and post-hatching development may have on adult physiology and behaviour. Japanese quail experienced different stress-related treatments across two developmental life stages: pre-hatching corticosterone (CORT) injection, post-hatching unpredictable food availability, both pre- and post-hatching treatments, or control. In adulthood, we determined quails' acute stress response, neophobia and novel environment exploration. The pre-hatching CORT treatment resulted in attenuated physiological responses to an acute stressor, increased activity levels and exploration in a novel environment. Post-hatching unpredictable food availability decreased adults' latency to feed. Furthermore, there were cumulative effects of these treatments across the two developmental stages: quail subjected to both pre- and post-hatching treatments were the most explorative and risk-taking of all treatment groups. Such responses to novel environments could enhance survival in unpredictable environments in later life. Our data also suggest that these behavioural responses may have been mediated by long-term physiological programming of the adrenocortical stress response, creating phenotypes that could exhibit fitness-enhancing behaviours in a changing environment.

Pre- and post-natal stress have opposing effects on social information use.

Theoretical models of social learning predict that animals should copy others in variable environments where resource availability is relatively unpredictable. Although short-term exposure to unpredictable conditions in adulthood has been shown to encourage social learning, virtually nothing is known concerning whether and how developmental conditions affect social information use. Unpredictable food availability increases levels of the stress hormone corticosterone (CORT). In birds, CORT can be transferred from the mother to her eggs, and have downstream behavioural effects. We tested how pre-natal CORT elevation through egg injection, and chick post-natal development in unpredictable food conditions, affected social information use in adult Japanese quail (Coturnix japonica). Pre-natal CORT exposure encouraged quail to copy the foraging decisions of demonstrators in video playbacks, whereas post-natal food unpredictability led individuals to avoid the demonstrated food source. An individual's exposure to stress and uncertainty during development can thus affect its use of social foraging information in adulthood. However, the stressor's nature and developmental timing determine whether an adult will tend to copy conspecifics or do the opposite. Developmental effects on social information use might thus help explain individual differences in social foraging tactics and leadership.

Brain size and morphology of the brood-parasitic and cerophagous honeyguides (Aves: Piciformes).

Honeyguides (Indicatoridae, Piciformes) are unique among birds in several respects. All subsist primarily on wax, are obligatory brood parasites and one species engages in 'guiding' behavior in which it leads human honey hunters to bees' nests. This unique life history has likely shaped the evolution of their brain size and morphology. Here, we test that hypothesis using comparative data on relative brain and brain region size of honeyguides and their relatives: woodpeckers, barbets and toucans. Honeyguides have significantly smaller relative brain volumes than all other piciform taxa. Volumetric measurements of the brain indicate that honeyguides have a significantly larger cerebellum and hippocampal formation (HF) than woodpeckers, the sister clade of the honeyguides, although the HF enlargement was not significant across all of our analyses. Cluster analyses also revealed that the overall composition of the brain and telencephalon differs greatly between honeyguides and woodpeckers. The relatively smaller brains of the honeyguides may be a consequence of brood parasitism and cerophagy ('wax eating'), both of which place energetic constraints on brain development and maintenance. The inconclusive results of our analyses of relative HF volume highlight some of the problems associated with comparative studies of the HF that require further study.

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.

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.

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.

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.

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'.

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.

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.

Detecting social transmission in networks.

In recent years researchers have drawn attention to a need for new methods with which to identify the spread of behavioural innovations through social transmission in animal populations. Network-based analyses seek to recognise diffusions mediated by social learning by detecting a correspondence between patterns of association and the flow of information through groups. Here we introduce a new order of acquisition diffusion analysis (OADA) and develop established time of acquisition diffusion analysis (TADA) methods further. Through simulation we compare the merits of these and other approaches, demonstrating that OADA and TADA have greater power and lower Type I error rates than available alternatives, and specifying when each approach should be deployed. We illustrate the new methods by applying them to reanalyse an established dataset corresponding to the diffusion of foraging innovations in starlings, where OADA and TADA detect social transmission that hitherto had been missed. The methods are potentially widely applicable by researchers wishing to detect social learning in natural and captive populations of animals, and to facilitate this we provide code to implement OADA and TADA in the statistical package R.

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.

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.