The building-up of social relationships: behavioural types, social networks and cooperative breeding in a cichlid

Consistent individual differences in behavioural types may not only cause variation in life-history decisions, but may also affect the choice of social partners and sociality in general. Here, we tested whether and how behavioural type influences the establishment of social ties using the cooperatively breeding cichlid, Neolamprologus pulcher. In a habitat saturation experiment with individuals pre-tested for behavioural type, we first analysed whether behavioural type affected the likelihood of settlement (i.e. social status), group sizes, and the types of dominant and subordinate individuals accepted as group members. Corrected for effects of body size and sex, the behavioural type did not affect settlement. However, bold dominant males only accepted smaller females, and grouped with bold subordinates, while shy dominant males accepted larger females than themselves, and grouped with shy subordinates. Second, we analysed the relationships between behavioural type and the aggressiveness or affiliation social network. Behavioural type significantly affected the number and quality of connections within the two networks. We show that behavioural types affect group composition, social networks and status achieved, in interaction with body size. Thus, the interactions within groups may depend not only on age, size and sex, but also on the behavioural type of the individuals involved.     

Shoal composition determines foraging success in the guppy

The composition of an animal group can impact greatly on thesurvival and success of its individual members. Much recentwork has concentrated on behavioral variation within animalpopulations along the bold/shy continuum. Here, we screenedindividual guppies, Poecilia reticulata, for boldness usingan overhead fright stimulus. We created groups consisting of4 bold individuals (bold shoals), 4 shy individuals (shy shoals),or 2 bold and 2 shy individuals (mixed shoals). The performanceof these different shoal types was then tested in a novel foragingscenario. We found that both bold and mixed shoals approacheda novel feeder in less time than shy shoals. Interestingly,we found that more fish from mixed shoals fed than in eitherbold or shy shoals. We suggest that this can be explained bythe fact that nearly all the cases where one fish was followedinto the feeder by another occurred within mixed shoals andthat it was almost always a shy fish following a bold one. Theseresults suggest clear foraging benefits to shy individuals throughassociating with bold ones. Surprisingly, our results also suggestpotential foraging benefits to bold individuals through associatingwith shy individuals. This study highlights a possible mechanismby which interindividual variation in behavioral types is maintainedin a population.     

Express yourself: bold individuals induce enhanced morphological defences

Organisms display an impressive array of defence strategies in nature. Inducible defences (changes in morphology and/or behaviour within a prey''s lifetime) allow prey to decrease vulnerability to predators and avoid unnecessary costs of expression. Many studies report considerable interindividual variation in the degree to which inducible defences are expressed, yet what underlies this variation is poorly understood. Here, we show that individuals differing in a key personality trait also differ in the magnitude of morphological defence expression. Crucian carp showing risky behaviours (bold individuals) expressed a significantly greater morphological defence response when exposed to a natural enemy when compared with shy individuals. Furthermore, we show that fish of different personality types differ in their behavioural plasticity, with shy fish exhibiting greater absolute plasticity than bold fish. Our data suggest that individuals with bold personalities may be able to compensate for their risk-prone behavioural type by expressing enhanced morphological defences.     

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.     

The non-consumptive effects of predators and personality on prey growth and mortality

Individual organisms vary in personality, and the ecological consequences of that variation can affect the strength of predator–prey interactions. Prey with bolder tendencies can mitigate the strength of species interactions by altering growth and initiating ontogenetic niche shifts (ONS). While the link between personality and growth has been established, recent research has highlighted the important interplay between ONS and predator cues in community ecology. The objective of this study was to evaluate the effects of prey personality and predator cues on prey growth and ONS. We predicted growth–mortality trade-offs among personalities with higher survival, larger size, and accelerated ONS for bold individuals in comparison with shy individuals. To evaluate this objective, we conducted behavioral assays and a mesocosm experiment to test how southern leopard frog (Rana sphenocephala) tadpole personality and predatory fish (bluegill, Lepomis macrochirus) cues affects tadpole growth and metamorphosis. On average, bold tadpoles had higher mortality across all treatments in comparison with shy tadpoles. The effects of fish cues were dependent on tadpole personality with shy tadpoles metamorphosing significantly later than bold tadpoles. Bold tadpoles were larger than shy tadpoles at metamorphosis; however, that pattern reversed with fish cues as shy individuals metamorphosed larger than bold individuals. Our results suggest personality may be useful for predicting growth and life history for some prey species with predators. Specifically, the threat of predation can interact with personality to incur a benefit (earlier ONS) while also incurring a cost (size at metamorphosis). Hence by incorporating predator cues with personality, ecologists will be able to elucidate growth–mortality trade-offs mediated by personality.     

Personality and Affinities Play a Key Role in the Organisation of Collective Movements in a Group of Domestic Horses

Understanding how groups of individuals with different motives come to daily decisions about the exploitation of their environment is a key question in animal behaviour. While interindividual differences are often seen only as a threat to group cohesion, growing evidence shows that they may to some extent facilitate effective collective action. Recent studies suggest that personality differences influence how individuals are attracted to conspecifics and affect their behaviour as an initiator or a follower. However, most of the existing studies are limited to a few taxa, mainly social fish and arthropods. Horses are social herbivores that live in long‐lasting groups and show identifiable personality differences between individuals. We studied a group of 38 individuals living in a 30‐ha hilly pasture. Over 200 h, we sought to identify how far individual differences such as personality and affinity distribution affect the dynamic of their collective movements. First, we report that individuals distribute their relationships according to similar personality and hierarchical rank. This is the first study that demonstrates a positive assortment between unrelated individuals according to personality in a mammal species. Second, we measured individual propensity to initiate and found that bold individuals initiated more often than shy individuals. However, their success in terms of number of followers and joining duration did not depend on their individual characteristics. Moreover, joining process is influenced by social network, with preferred partners following each other and bolder individuals being located more often at the front of the movement. Our results illustrate the importance of taking into account interindividual behavioural differences in studies of social behaviours.     

Plasticity of boldness in rainbow trout,Oncorhynchus mykiss: do hunger and predation influence risk-taking behaviour?

Boldness, a measure of an individual's propensity for taking risks, is an important determinant of fitness but is not necessarily a fixed trait. Dependent upon an individual's state, and given certain contexts or challenges, individuals may be able to alter their inclination to be bold or shy in response. Furthermore, the degree to which individuals can modulate their behaviour has been linked with physiological responses to stress. Here we attempted to determine whether bold and shy rainbow trout, Oncorhynchus mykiss, can exhibit behavioural plasticity in response to changes in state (nutritional availability) and context (predation threat). Individual trout were initially assessed for boldness using a standard novel object paradigm; subsequently, each day for one week fish experienced either predictable, unpredictable, or no simulated predator threat in combination with a high (2% body weight) or low (0.15%) food ration, before being reassessed for boldness. Bold trout were generally more plastic, altering levels of neophobia and activity relevant to the challenge, whereas shy trout were more fixed and remained shy. Increased predation risk generally resulted in an increase in the expression of three candidate genes linked to boldness, appetite regulation and physiological stress responses - ependymin, corticotrophin releasing factor and GABA(A) - but did not produce a significant increase in plasma cortisol. The results suggest a divergence in the ability of bold and shy trout to alter their behavioural profiles in response to internal and exogenous factors, and have important implications for our understanding of the maintenance of different behavioural phenotypes in natural populations.     

Consistency in Context-specific Measures of Shyness and Boldness in Rainbow Trout, Oncorhynchus mykiss

Shyness and boldness has been considered a fundamental axis of human behavioural variation. At the extreme ends of this behavioural continuum subjects vary from being bold and assertive to shy and timid. Analogous patterns of individual variation have been noted in a number of species including fish. There has been debate on the nature of this continuum as to whether it depends on context. That is, whether it is domain‐general (as in humans), or context‐specific. The purpose of our study was to test if shyness and boldness depends on context in rainbow trout, Oncorhynchus mykiss and to this end we estimated boldness in five different situations. Our data provide evidence of a shy–bold behavioural syndrome in rainbow trout. Bold trout tended to be bold in four situations when the context was similar (when the context concerned foraging). However, in a different context, exploring a swim flume, the ranking was entirely different. We suggest that shyness and boldness depends on context in rainbow trout.     

Personality-dependent inter- and intraspecific foraging competition in the invasive round goby,Neogobius melanostomus

This study examines the impact of boldness on foraging competition of the highly invasive round goby Neogobius melanostomus Pallas 1815. Individual risk tolerance, or boldness, was measured as the time to resume movement after a simulated predation strike. Fish that resumed movement faster were categorized as “bold,” fish that took more time to resume movement were categorized as “shy” and those that fell in between these two categories were determined to have “intermediate” boldness. Competitive impacts of boldness in N. melanostomus were determined in a laboratory foraging experiment in which interspecific (juvenile Atlantic cod Gadus morhua Linnaeus 1758) and intraspecific (intermediate N. melanostomus) individuals were exposed to either bold or shy N. melanostomus competitors. G. morhua consumed fewer prey when competing with bold N. melanostomus than when competing with shy N. melanostomus, whereas intermediately bold N. melanostomus foraging was not affected by competitor boldness. Bold and shy N. melanostomus consumed similar amounts of prey, and the number of interactions between paired fish did not vary depending on the personality of N. melanostomus individuals. Therefore, intraspecific foraging competition was not found to be personality dependent. This study provides evidence that individual differences in boldness can mediate competitive interactions in N. melanostomus; nonetheless, results also show that competition is also governed by other mechanisms that require further study.     

Social heterosis and the maintenance of genetic diversity

Genetic diversity in species is often high in spite of directional selection or strong genetic drift. One resolution to this paradox may be through fitness benefits arising from interactions of genetically diverse individuals. Advantageous phenotypes that are impossible in single individuals (e.g. being simultaneously bold and shy) can be expressed by groups composed of genetically different individuals. Genetic diversity, therefore, can produce mutualistic benefits shared by all group members. We define this effect as 'social heterosis', and mathematically demonstrate maintenance of allelic diversity when diverse groups or neighbourhoods are more reproductively successful than homogenous ones. Through social heterosis, genetic diversity persists without: frequency dependence within groups, migration, balancing selection, genetic linkages, overdominance, antagonistic pleiotropy or nonrandom allele assortment. Social heterosis may also offer an alternative evolutionary pathway to cooperation that does not require clustering of related individuals, nepotistic favouritism towards kin, or overt reciprocity.     

Offspring social network structure predicts fitness in families

Social structures such as families emerge as outcomes of behavioural interactions among individuals, and can evolve over time if families with particular types of social structures tend to leave more individuals in subsequent generations. The social behaviour of interacting individuals is typically analysed as a series of multiple dyadic (pair-wise) interactions, rather than a network of interactions among multiple individuals. However, in species where parents feed dependant young, interactions within families nearly always involve more than two individuals simultaneously. Such social networks of interactions at least partly reflect conflicts of interest over the provision of costly parental investment. Consequently, variation in family network structure reflects variation in how conflicts of interest are resolved among family members. Despite its importance in understanding the evolution of emergent properties of social organization such as family life and cooperation, nothing is currently known about how selection acts on the structure of social networks. Here, we show that the social network structure of broods of begging nestling great tits Parus major predicts fitness in families. Although selection at the level of the individual favours large nestlings, selection at the level of the kin-group primarily favours families that resolve conflicts most effectively.     

Personality composition is more important than group size in determining collective foraging behaviour in the wild

Describing the factors that shape collective behaviour is central to our understanding of animal societies. Countless studies have demonstrated an effect of group size in the emergence of collective behaviours, but comparatively few have accounted for the composition/diversity of behavioural phenotypes, which is often conflated with group size. Here, we simultaneously examine the effect of personality composition and group size on nest architecture and collective foraging aggressiveness in the social spider Stegodyphus dumicola. We created colonies of two different sizes (10 or 30 individuals) and four compositions of boldness (all bold, all shy, mixed bold and shy, or average individuals) in the field and then measured their collective behaviour. Larger colonies produced bigger capture webs, while colonies containing a higher proportion of bold individuals responded to and attacked prey more rapidly. The number of attackers during collective foraging was determined jointly by composition and size, although composition had an effect size more than twice that of colony size: our results suggest that colonies of just 10 bold spiders would attack prey with as many attackers as colonies of 110 ‘average’ spiders. Thus, personality composition is a more potent (albeit more cryptic) determinant of collective foraging in these societies.     

Individual personality and the spatial distribution of groups of grazing animals: An example with sheep

Impacts of individual personality on group distribution were investigated using sheep (Ovis aries) as a model. In an indoor exploration test, individuals who visited <4 (out of 6) objects in a novel environment were classified as ‘shy’ (n = 10), and those who visited 5 or 6 objects were classified as ‘bold’ (n = 10). Nine weeks later, using a series of groups (n = 40) of either 5 shy or 5 bold sheep, we measured distribution at pasture and responses to disturbance and the approach of a human handler. When grazing undisturbed, the mean nearest neighbour distance and spread (minimum convex hull area) of shy groups were less than those of bold groups, with shy individuals moving towards one another more often. Shy groups explored a smaller area than bold groups. When disturbed, shy sheep were more likely to stop grazing and move closer together. Shy sheep kept further away from the handler and moved faster when driven. The results demonstrate a link between personality and group distribution, suggesting that our ‘shy’ and ‘bold’ individuals may occupy different positions on the shy-bold continuum documented for other species. We discuss implications for diet composition and impacts on vegetation grazed by animals with different personalities.     

Zebrafish Danio rerio shows behavioural cross-context consistency at larval and juvenile stages but no consistency between stages

Coping style is defined as a set of individual physiological and behavioural characteristics that are consistent across time and context. In the zebrafish Danio rerio, as well as in many other animals, several covariations have been established among behavioural, physiological and molecular responses. Nonetheless, not many studies have addressed the consistency in behavioural responses over time starting at the larval stage. Therefore, this study aimed to improve the understanding of behavioural consistency across contexts and over time in zebrafish from the larval to juvenile stages. Two distinct experiments were conducted: a larval stage experiment (from 8 to 21 days post fertilization, dpf) and a juvenile stage experiment (from 21 to 60 dpf). On one hand, the larval experiment allows to focus on the transition between 8 and 21 dpf, marked by significant morphological changes related to the end of larval stage and initiation of metamorphosis. On the other hand, the juvenile experiment allows to properly cover the period extending from the end of larval stage to the juvenile stage (60 dpf), including metamorphosis which is itself completed around 45 dpf. Within each experiment, boldness was determined using a group risk-taking test to identify bold and shy individuals. A novel environment test was then performed at the same age to evaluate consistency across contexts. Groups of fish (either bold or shy) were bathed in an alizarin red S solution for later identification of their initially determined coping style to evaluate behavioural consistency over time. Fish were then reared under common garden conditions and challenged again with the same behavioural tests at a later age (21 and 60 dpf in the larval and juvenile experiments, respectively). Behavioural consistency was observed across contexts, with bold fish being more active and expressing higher thigmotaxis regardless of age. There was, however, little behavioural consistency over age, suggesting behavioural plasticity during development. Moreover, the use of alizarin red S to conduct this experiment provides new perspectives for the further study of the longitudinal evolution of various traits, including behaviour, over life stages in fish.     

Social structure modulates the evolutionary consequences of social plasticity: A social network perspective on interacting phenotypes

Organisms express phenotypic plasticity during social interactions. Interacting phenotype theory has explored the consequences of social plasticity for evolution, but it is unclear how this theory applies to complex social structures. We adapt interacting phenotype models to general social structures to explore how the number of social connections between individuals and preference for phenotypically similar social partners affect phenotypic variation and evolution. We derive an analytical model that ignores phenotypic feedback and use simulations to test the predictions of this model. We find that adapting previous models to more general social structures does not alter their general conclusions but generates insights into the effect of social plasticity and social structure on the maintenance of phenotypic variation and evolution. Contribution of indirect genetic effects to phenotypic variance is highest when interactions occur at intermediate densities and decrease at higher densities, when individuals approach interacting with all group members, homogenizing the social environment across individuals. However, evolutionary response to selection tends to increase at greater network densities as the effects of an individual's genes are amplified through increasing effects on other group members. Preferential associations among similar individuals (homophily) increase both phenotypic variance within groups and evolutionary response to selection. Our results represent a first step in relating social network structure to the expression of social plasticity and evolutionary responses to selection.     

Japanese Macaques Depend not Only on Neighbours but also on More Distant Members for Group Cohesion

A well‐known behavioural model for group aggregation is that an individual depends on a few neighbouring individuals to adjust its movement, such as departure (repulsion) from and approach (attraction) to neighbours. However, an individual may rely not only on a few closest neighbours, but also on more distant individuals, in a group of stable membership. We measured temporal changes in the local density of individuals around a focal individual and changes in distance to other focal individuals in a group of wild Japanese macaques to determine whether the macaques depended only on a few neighbours or also on more distant individuals for adjustments in cohesiveness. We used simultaneous focal animal sampling, with two observers recording the individuals' locations using a global positioning system (GPS), over three seasons. Numbers of individuals within 20 m from an animal tended to increase after 10 min when there were a small number of individuals around the animal. However, the number tended to decrease when there was a larger number of individuals. It remained similar when there were an intermediate number of individuals. The two focal animals tended to separate after 10 min when the interindividual distance was short. However, they tended to move closer when far apart. They remained a similar distance apart when they were at an intermediate distance. Contact calls, which are suggested to function as locating group members and keeping cohesiveness, were emitted more frequently when the distance between the two focal animals was very large in two seasons. However, the rate of contact calls was not influenced by the number of individuals within 20 m from an animal. These results suggest that individual Japanese macaques do not only rely on a few closest neighbours, but also rely on more distant group members. Japanese macaques may know the general whereabouts of the whole group, and when they stay at the periphery of the group, they may emit contact calls frequently and move towards the central zone so as not to become separated from the group.     

Turning Shy on a Winter's Day: Effects of Season on Personality and Stress Response in Microtus arvalis

Animal personalities are by definition stable over time, but to what extent they may change during development and in adulthood to adjust to environmental change is unclear. Animals of temperate environments have evolved physiological and behavioural adaptations to cope with the cyclic seasonal changes. This may also result in changes in personality: suites of behavioural and physiological traits that vary consistently among individuals. Winter, typically the adverse season challenging survival, may require individuals to have shy/cautious personality, whereas during summer, energetically favourable to reproduction, individuals may benefit from a bold/risk‐taking personality. To test the effects of seasonal changes in early life and in adulthood on behaviours (activity, exploration and anxiety), body mass and stress response, we manipulated the photoperiod and quality of food in two experiments to simulate the conditions of winter and summer. We used the common voles (Microtus arvalis) as they have been shown to display personality based on behavioural consistency over time and contexts. Summer‐born voles allocated to winter conditions at weaning had lower body mass, a higher corticosterone increase after stress and a less active, more cautious behavioural phenotype in adulthood compared to voles born in and allocated to summer conditions. In contrast, adult females only showed plasticity in stress‐induced corticosterone levels, which were higher in the animals that were transferred to the winter conditions than to those staying in summer conditions. These results suggest a sensitive period for season‐related behavioural plasticity in which juveniles shift over the bold–shy axis.     

The Influence of Personality on a Group‐Level Process: Shy Hermit Crabs Make Longer Vacancy Chains

Animal personality has been investigated in a variety of contexts but few studies have investigated the effects of individual‐level traits on processes that occur at the group or population level. Vacancy chains describe sequences of linked vacancy moves in systems where individuals use discrete and reuseable resource units. When a new resource unit becomes available, this can cause a cascade of moves between resource units, beyond the first individual that encounters the new unit. Thus, vacancy chains can drive the distribution of resources through a population. Here, I investigate the effect of variation in boldness on movements between vacant gastropod shells in the hermit crab Pagurus bernhardus. Boldness was quantified using the duration of a startle response, which varied consistently between individuals. In groups of five crabs, introduction of a single new shell led to aggregate benefits, in terms of improving shell quality, across all group members. Boldness did not influence the extent of these benefits or the extent to which they were distributed between crabs of different sizes. Initially, vacancy chains were longer, indicating that more individuals moved between shells, for bold groups compared with shy groups. After 24 h, however, the chain length was longer for shy groups. Thus, although participation in a vacancy chain may lead to similar benefits, these could be more widespread for groups comprising shy individuals that show long startle responses, low inquisitiveness and low aggression. Similar effects on resource acquisition could be present in other examples of animals that utilise reusable resource units and show consistent between‐individual differences in behaviour.     

Opposite selection on behavioural types by active and passive fishing gears in a simulated guppy Poecilia reticulata fishery

This study assessed whether fishing gear was selective on behavioural traits, such as boldness and activity, and how this was related with a productivity trait, growth. Female guppies Poecilia reticulata were screened for their behaviour on the shy–bold axis and activity, and then tested whether they were captured differently by passive and active fishing gear, here represented by a trap and a trawl. Both gears were selective on boldness; bold individuals were caught faster by the trap, but escaped the trawl more often. Boldness and gear vulnerability showed weak correlations with activity and growth. The results draw attention to the importance of the behavioural dimension of fishing: selective fishing on behavioural traits will change the trait composition of the population, and might eventually affect resilience and fishery productivity.     

Group chorusing as an intragroup signal in the greater ani,a communally breeding bird

Group living often requires maintaining dynamic and varied relationships with fellow group members, while simultaneously monitoring and interacting with external competitors. Group members in many social species vocalize together to produce duets or choruses—coordinated, often conspicuous vocal displays—that may play a role in these interactions. Compared with male–female duets, however, relatively little research exists on the function and adaptive significance of group choruses, which involve three or more individuals. Here we investigate chorusing behavior in the greater ani (Crotophaga major), a communally breeding cuckoo that nests in stable social groups of four to eight unrelated individuals. Groups may remain together for several years on the same nesting territory, and groups occasionally destroy each other's clutches in conflicts over high-quality territories. We asked whether the raucous, highly stereotyped choruses performed by ani groups are primarily used for intra- or intergroup communication, and whether they contain information about the identity of the social group and the number of birds vocalizing. Behavioral observations and acoustic recordings from three breeding seasons revealed that choruses typically occurred during social interactions within the group (78% of choruses) or in response to a predator or extra-group individual (17%) and only rarely in intergroup interactions (4%). Consistent with this finding, choruses did not reliably reflect the number of birds vocalizing, and we found only limited evidence for group-specific acoustic signatures (driven by a single group whose choruses were highly distinct). These results suggest that group choruses play an important role in intra-group signaling, potentially in contexts such as group formation, reinforcement of social bonds within the group, and/or collective decision-making, and they motivate new research questions about the role of collective signaling in social evolution.