Can We Predict Personality in Fish? Searching for Consistency over Time and across Contexts

The interest in animal personality, broadly defined as consistency of individual behavioural traits over time and across contexts, has increased dramatically over the last years. Individual differences in behaviour are no longer recognised as noise around a mean but rather as adaptive variation and thus, essentially, raw material for evolution. Animal personality has been considered evolutionary conserved and has been shown to be present in all vertebrates including fish. Despite the importance of evolutionary and comparative aspects in this field, few studies have actually documented consistency across situations in fish. In addition, most studies are done with individually housed fish which may pose additional challenges when interpreting data from social species. Here, we investigate, for the first time in fish, whether individual differences in behavioural responses to a variety of challenges are consistent over time and across contexts using both individual and grouped-based tests. Twenty-four juveniles of Gilthead seabream Sparus aurata were subjected to three individual-based tests: feed intake recovery in a novel environment, novel object and restraining and to two group-based tests: risk-taking and hypoxia. Each test was repeated twice to assess consistency of behavioural responses over time. Risk taking and escape behaviours during restraining were shown to be significantly consistent over time. In addition, consistency across contexts was also observed: individuals that took longer to recover feed intake after transfer into a novel environment exhibited higher escape attempts during a restraining test and escaped faster from hypoxia conditions. These results highlight the possibility to predict behaviour in groups from individual personality traits.     

Dimensions of Animal Personalities in Guinea Pigs

Behavioural phenotypes can be studied from a variety of perspectives. Recent developments have focused on the individual, seeking patterns of behaviour that are stable over time and/or across different contexts (animal personalities). This study applied this method of understanding individual behavioural variability to domestic guinea pigs. Two behavioural domains were investigated: emotionality and social behaviour. Additionally, individual cortisol–stress reactivity and dominance status were examined. Adult male domestic guinea pigs living in large mixed‐sex colonies were subjected to a series of behavioural and physiological tests twice with an intertest interval of 8 wk. Individual consistency over time was found regarding social behaviour, cortisol reactivity and dominance status, whereas no stability regarding emotional behaviour was detected. Furthermore, no stability over contexts was found. Our results suggest that the concept of animal personality is applicable to domestic guinea pigs. The ecological relevance of these data is underscored by the fact that they were obtained in animals from a very rich, socially complex scenario. Moreover, our study highlights that behaviour alone is not sufficient to describe individual phenotypic consistency. Physiological parameters such as stress reactivity should be included in animal personality research. Furthermore dominance – a relative measure which is not an absolute attribute of individuals – proved to be stable over time and thus also shed light on individuality.     

Sex and the Syndrome: Individual and Population Consistency in Behaviour in Rock Pool Prawn Palaemon elegans

Animal personality has been widely documented across a range of species. The concept of personality is composed of individual behavioural consistency across time and between situations, and also behavioural trait correlations known as behavioural syndromes. Whilst many studies have now investigated the stability of individual personality traits, few have analysed the stability over time of entire behavioural syndromes. Here we present data from a behavioural study of rock pool prawns. We show that prawns are temporally consistent in a range of behaviours, including activity, exploration and boldness, and also that a behavioural syndrome is evident in this population. We find correlations between many behavioural traits (activity, boldness, shoaling and exploration). In addition, behavioural syndrome structure was consistent over time. Finally, few studies have explicitly studied the role of sex differences in personality traits, behavioural consistency and syndrome structure. We report behavioural differences between male and female prawns but no differences in patterns of consistency. Our study adds to the growing literature on animal personality, and provides evidence showing that syndromes themselves can exhibit temporal consistency.     

An explanatory framework for adaptive personality differences

We develop a conceptual framework for the understanding of animal personalities in terms of adaptive evolution. We focus on two basic questions. First, why do behavioural types exhibit limited behavioural plasticity, that is, behavioural correlations both across contexts and over time? Second, how can multiple behavioural types coexist within a single population? We emphasize differences in 'state' among individuals in combination with state-dependent behaviour. Some states are inherently stable and individual differences in such states can explain stable differences in suites of behaviour if it is adaptive to make behaviour in various contexts dependent on such states. Behavioural stability and cross-context correlations in behaviour are more difficult to explain if individual states are potentially more variable. In such cases stable personalities can result from state-dependent behaviour if state and behaviour mutually reinforce each other by feedback mechanisms. We discuss various evolutionary mechanisms for the maintenance of variation (in states and/or behaviour), including frequency-dependent selection, spatial variation with incomplete matching between habitat and phenotype, bet-hedging in a temporally fluctuating environment, and non-equilibrium dynamics. Although state differences are important, we also discuss how social conventions and social signalling can give rise to adaptive personality differences in the absence of state differences.     

Personality Predicts Social Dominance in Male Domestic Fowl

Individuals in social species commonly form dominance relationships, where dominant individuals enjoy greater access to resources compared to subordinates. A range of factors such as sex, age, body size and prior experiences has to varying degrees been observed to affect the social status an individual obtains. Recent work on animal personality (i.e. consistent variation in behavioural responses of individuals) demonstrates that personality can co-vary with social status, suggesting that also behavioural variation can play an important role in establishment of status. We investigated whether personality could predict the outcome of duels between pairs of morphologically matched male domestic fowl (Gallus gallus domesticus), a species where individuals readily form social hierarchies. We found that males that more quickly explored a novel arena, or remained vigilant for a longer period following the playback of a warning call were more likely to obtain a dominant position. These traits were uncorrelated to each other and were also uncorrelated to aggression during the initial part of the dominance-determining duel. Our results indicate that several behavioural traits independently play a role in the establishment of social status, which in turn can have implications for the reproductive success of different personality types.     

Assessing Short‐ and Long‐Term Repeatability and Stability of Personality in Captive Zebra Finches Using Longitudinal Data

Assessing behavioural consistency is crucial to understand the evolution of personality traits. In the present study, we examined the short‐ and long‐term repeatability and stability of two unrelated personality traits – exploratory tendencies and struggling rate – using captive female zebra finches ( Taeniopygia guttata). We performed two experimental sessions of behavioural tests with a 7‐mo interval, which represents up to one quarter of a zebra finch's life expectancy. We showed that, overall, exploratory tendencies and struggling rate were significantly repeatable in the short term. However, only exploratory tendencies were repeatable in the long term. We found interindividual differences in short‐term stability of exploratory tendencies, but not struggling rate, providing evidence for differences in intraindividual variability. In the long term, struggling rate significantly decreased between the two experimental sessions, whereas exploratory tendencies remained stable. Finally, the amount of interindividual variation measured at both sessions did not differ. Our results suggest that short‐ and long‐term repeatability and stability of personality may vary between individuals, depending on the behavioural trait under scrutiny. As a consequence, deducing personality from measures realized earlier in a subject's life should be performed with caution. We discuss the implications of inter‐ and intraindividual variation in personality consistency on individual fitness.     

What's your move? Movement as a link between personality and spatial dynamics in animal populations

Recent studies have established the ecological and evolutionary importance of animal personalities. Individual differences in movement and space‐use, fundamental to many personality traits (e.g. activity, boldness and exploratory behaviour) have been documented across many species and contexts, for instance personality‐dependent dispersal syndromes. Yet, insights from the concurrently developing movement ecology paradigm are rarely considered and recent evidence for other personality‐dependent movements and space‐use lack a general unifying framework. We propose a conceptual framework for personality‐dependent spatial ecology. We link expectations derived from the movement ecology paradigm with behavioural reaction‐norms to offer specific predictions on the interactions between environmental factors, such as resource distribution or landscape structure, and intrinsic behavioural variation. We consider how environmental heterogeneity and individual consistency in movements that carry‐over across spatial scales can lead to personality‐dependent: (1) foraging search performance; (2) habitat preference; (3) home range utilization patterns; (4) social network structure and (5) emergence of assortative population structure with spatial clusters of personalities. We support our conceptual model with spatially explicit simulations of behavioural variation in space‐use, demonstrating the emergence of complex population‐level patterns from differences in simple individual‐level behaviours. Consideration of consistent individual variation in space‐use will facilitate mechanistic understanding of processes that drive social, spatial, ecological and evolutionary dynamics in heterogeneous environments.     

Extending the Functionality of Behavioural Change-Point Analysis with k-Means Clustering: A Case Study with the Little Penguin (Eudyptula minor)

We present a simple framework for classifying mutually exclusive behavioural states within the geospatial lifelines of animals. This method involves use of three sequentially applied statistical procedures: (1) behavioural change point analysis to partition movement trajectories into discrete bouts of same-state behaviours, based on abrupt changes in the spatio-temporal autocorrelation structure of movement parameters; (2) hierarchical multivariate cluster analysis to determine the number of different behavioural states; and (3) k-means clustering to classify inferred bouts of same-state location observations into behavioural modes. We demonstrate application of the method by analysing synthetic trajectories of known ‘artificial behaviours’ comprised of different correlated random walks, as well as real foraging trajectories of little penguins (Eudyptula minor) obtained by global-positioning-system telemetry. Our results show that the modelling procedure correctly classified 92.5% of all individual location observations in the synthetic trajectories, demonstrating reasonable ability to successfully discriminate behavioural modes. Most individual little penguins were found to exhibit three unique behavioural states (resting, commuting/active searching, area-restricted foraging), with variation in the timing and locations of observations apparently related to ambient light, bathymetry, and proximity to coastlines and river mouths. Addition of k-means clustering extends the utility of behavioural change point analysis, by providing a simple means through which the behaviours inferred for the location observations comprising individual movement trajectories can be objectively classified.     

Social familiarity modulates personality trait in a cichlid fish

Personality traits, such as exploration–avoidance, are expected to be adaptive in a given context (e.g. low-risk environment) but to be maladaptive in others (e.g. high-risk environment). Therefore, it is expected that personality traits are flexible and respond to environmental fluctuations, given that consistency across different contexts is maintained, so that the relative individual responses in relation to others remains the same (i.e. although the magnitude of the response varies the differences between high and low responders are kept). Here, we tested the response of male cichlid fish (Oreochromis mossambicus) to a novel object (NO) in three different social contexts: (i) social isolation, (ii) in the presence of an unfamiliar conspecific, and (iii) in the presence of a familiar conspecific. Males in the familiar treatment exhibited more exploratory behaviour and less neophobia than males in either the unfamiliar or the social isolation treatments. However, there were no overall correlations in individual behaviour across the three treatments, suggesting a lack of consistency in exploration–avoidance as measured by the NO test in this species. Moreover, there were no differences in cortisol responsiveness to an acute stressor between the three treatments. Together, these results illustrate how behavioural traits usually taken as measures of personality may exhibit significant flexibility and lack the expected consistency across different social contexts.     

Individual Variation in Behavioural Reactions to Unfamiliar Conspecific Vocalisation and Hormonal Underpinnings in Male Chimpanzees

It has been established that various species exhibit personality, defined as intra‐individual consistency and inter‐individual variation in behavioural phenotypes. For example, certain individuals may demonstrate consistently greater behavioural reactions and elevated stress responses. We conducted playback experiments and hormonal analyses on male chimpanzees (Pan troglodytes) in captivity to investigate the patterns and proximate mediators of individual variations in behavioural reactions. We found intra‐individual consistency and inter‐individual variation in behavioural reactions (intensive vigilance towards the direction of speakers) to vocalisations by unfamiliar chimpanzees. This behavioural reaction was positively correlated with changes in salivary cortisol concentration, suggesting that stress is a proximate factor mediating the variation in behavioural reactions. The males who were highly responsive to the conspecific vocalisation also exhibited high behavioural reactions towards the neutral broadcast stimulus (the jungle crow’s Corvus macrorhynchos ‘ka’ vocalisation). This observation is consistent with the notion that male chimpanzees vary in intrinsic behavioural tendency to different stimuli.     

What can whole genome expression data tell us about the ecology and evolution of personality?

Consistent individual differences in behaviour, aka personality, pose several evolutionary questions. For example, it is difficult to explain within-individual consistency in behaviour because behavioural plasticity is often advantageous. In addition, selection erodes heritable behavioural variation that is related to fitness, therefore we wish to know the mechanisms that can maintain between-individual variation in behaviour. In this paper, we argue that whole genome expression data can reveal new insights into the proximate mechanisms underlying personality, as well as its evolutionary consequences. After introducing the basics of whole genome expression analysis, we show how whole genome expression data can be used to understand whether behaviours in different contexts are affected by the same molecular mechanisms. We suggest strategies for using the power of genomics to understand what maintains behavioural variation, to study the evolution of behavioural correlations and to compare personality traits across diverse organisms.     

Context Matters: Multiple Novelty Tests Reveal Different Aspects of Shyness-Boldness in Farmed American Mink (Neovison vison)

Animal personality research is receiving increasing interest from related fields, such as evolutionary personality psychology. By merging the conceptual understanding of personality, the contributions to both fields of research may be enhanced. In this study, we investigate animal personality based on the definition of personality traits as underlying dispositional factors, which are not directly measurable, but which predispose individuals to react through different behavioural patterns. We investigated the shyness-boldness continuum reflected in the consistency of inter-individual variation in behavioural responses towards novelty in 47 farmed American mink (Neovison vison), which were raised in identical housing conditions. Different stages of approach behaviour towards novelty, and how these related within and across contexts, were explored. Our experimental design contained four tests: two novel object tests (non-social contexts) and two novel animated stimuli tests (social contexts). Our results showed consistency in shyness measures across multiple tests, indicating the existence of personality in farmed American mink. It was found that consistency in shyness measures differs across non-social and social contexts, as well as across the various stages in the approach towards novel objects, revealing that different aspects of shyness exist in the farmed American mink. To our knowledge this is the first study to reveal aspects of the shyness-boldness continuum in the American mink. Since the mink were raised in identical housing conditions, inherited factors may have been important in shaping the consistent inter-individual variation. Body weight and sex had no effect on the personality of the mink. Altogether, our results suggest that the shyness-boldness continuum cannot be explained by a simple underlying dispositional factor, but instead encompasses a broader term of hesitating behaviour that might comprise several different personality traits.     

Behaviour in captivity predicts some aspects of natural behaviour,but not others,in a wild cricket population

Examining the relevance of ‘animal personality’ involves linking consistent among- and within-individual behavioural variation to fitness in the wild. Studies aiming to do this typically assay personality in captivity and rely on the assumption that measures of traits in the laboratory reflect their expression in nature. We examined this rarely tested assumption by comparing laboratory and field measurements of the behaviour of wild field crickets (Gryllus campestris) by continuously monitoring individual behaviour in nature, and repeatedly capturing the same individuals and measuring their behaviour in captivity. We focused on three traits that are frequently examined in personality studies: shyness, activity and exploration. All of them showed repeatability in the laboratory. Laboratory activity and exploration predicted the expression of their equivalent behaviours in the wild, but shyness did not. Traits in the wild were predictably influenced by environmental factors such as temperature and sunlight, but only activity showed appreciable within-individual repeatability. This suggests that some behaviours typically studied as personality traits can be accurately assayed in captivity, but the expression of others may be highly context-specific. Our results highlight the importance of validating the relevance of laboratory behavioural assays to analogous traits measured in the wild.     

Evidence of social niche construction: persistent and repeated social interactions generate stronger personalities in a social spider

While there are now a number of theoretical models predicting how consistent individual differences in behaviour may be generated and maintained, so far, there are few empirical tests. The social niche specialization hypothesis predicts that repeated social interactions among individuals may generate among-individual differences and reinforce within-individual consistency through positive feedback mechanisms. Here, we test this hypothesis using groups of the social spider Stegodyphus mimosarum that differ in their level of familiarity. In support of the social niche specialization hypothesis, individuals in groups of spiders that were more familiar with each other showed greater repeatable among-individual variation in behaviour. Additionally, individuals that were more familiar with each other exhibited lower within-individual variation in behaviour, providing one of the first examples of how the social environment can influence behavioural consistency. Our study demonstrates the potential for the social environment to generate and reinforce consistent individual differences in behaviour and provides a potentially general mechanism to explain this type of behavioural variation in animals with stable social groups.     

Animal personality as a cause and consequence of contest behaviour

We review the evidence for a link between consistent among-individual variation in behaviour (animal personality) and the ability to win contests over limited resources. Explorative and bold behaviours often covary with contest behaviour and outcome, although there is evidence that the structure of these ‘behavioural syndromes'' can change across situations. Aggression itself is typically repeatable, but also subject to high within-individual variation as a consequence of plastic responses to previous fight outcomes and opponent traits. Common proximate mechanisms (gene expression, endocrine control and metabolic rates) may underpin variation in both contest behaviour and general personality traits. Given the theoretical links between the evolution of fighting and of personality, we suggest that longitudinal studies of contest behaviour, combining behavioural and physiological data, would be a useful context for the study of animal personalities.     

Behavioural plasticity in a native species may be related to foraging resilience in the presence of an aggressive invader

Competition between invasive and native species can result in the exploitation of resources by the invader, reducing foraging rates of natives. However, it is increasingly recognized that multiple factors can enhance the resilience of native species competing for limiting resources with invaders. Although extensively studied in terrestrial species, little research has focused on behavioural plasticity in aquatic ecosystems and how this influences native species resilience. Here, we examined the role of behavioural plasticity in interactions between a native Australian fish, Pseudomugil signifer, and a widespread invasive fish, Gambusia holbrooki. To determine whether P. signifer displays behavioural plasticity that may mitigate competition with G. holbrooki, we first quantified social behaviours (aggression, submission and affiliation) and shoal cohesion for each species in single- and mixed-species groups. Second, we compared the feeding rates of both species in these groups to ascertain if any modulation of social behaviours and cohesion related to foraging success. We found that aggressive and submissive behaviours of G. holbrooki and P. signifer showed plasticity in the presence of heterospecifics, but social affiliation, shoaling and, most importantly, foraging, remained inflexible. This variation in the degree of plasticity highlights the complexity of the behavioural response of a native species and suggests that both behavioural modulation and consistency may be related to sustaining foraging efficiency in the presence of an invader.     

Socially Driven Consistent Behavioural Differences during Development in Common Ravens and Carrion Crows

Consistent individual differences in behaviour, or ‘personality’, are likely to be influenced by development, social context, and species ecology, though few comparative, longitudinal studies exist. Here, we investigated the role of development and social context on personality variation in two identically reared, social corvids: common ravens and carrion crows. We repeatedly presented subjects with a variety of novel food and objects, while alone and in a primarily sibling subgroup, from fledging to sub-adulthood. We predicted that consistent individual differences would emerge later in development, and that conspecific presence would facilitate behavioural similarities. In contrast to our predictions, we found that individuals of both species were highly inconsistent in their behavioural responses throughout the development period. In line with our predictions, though in the ravens only, conspecific presence promoted behavioural similarities as individuals were strongly shaped by their subgroup, and it is likely that these effects were driven by social context rather than relatedness. We discuss these findings in relation to developmental steps and the role of social relations in these species. Overall, our findings highlight that these two species are highly adaptable in their behaviour, and the ravens in particular are strongly influenced by their social environment, which may facilitate cooperation and social learning.     

The influence of mitonuclear genetic variation on personality in seed beetles

There is a growing awareness of the influence of mitochondrial genetic variation on life-history phenotypes, particularly via epistatic interactions with nuclear genes. Owing to their direct effect on traits such as metabolic and growth rates, mitonuclear interactions may also affect variation in behavioural types or personalities (i.e. behavioural variation that is consistent within individuals, but differs among individuals). However, this possibility is largely unexplored. We used mitonuclear introgression lines, where three mitochondrial genomes were introgressed into three nuclear genetic backgrounds, to disentangle genetic effects on behavioural variation in a seed beetle. We found within-individual consistency in a suite of activity-related behaviours, providing evidence for variation in personality. Composite measures of overall activity of individuals in behavioural assays were influenced by both nuclear genetic variation and by the interaction between nuclear and mitochondrial genomes. More importantly, the degree of expression of behavioural and life-history phenotypes was correlated and mitonuclear genetic variation affected expression of these concerted phenotypes. These results show that mitonuclear genetic variation affects both behavioural and life-history traits, and they provide novel insights into the maintenance of genetic variation in behaviour and personality.     

Absence of a Context‐General Behavioural Syndrome in a Solitary Predator

The correlation of seemingly unrelated behaviours into behavioural syndromes has been established in a wide range of species and taxa. However, most studies report on short‐term behavioural correlations without insight into individual consistency or temporal stability of the behavioural syndrome. Here, we examine the individual repeatability of single behaviours, and the presence and temporal stability of a context‐general behavioural syndrome in a solitary piscivorous predator, the pike (Esox lucius). Behavioural measurements on the same individuals were quantified independently through time and across three contexts: activity in the presence of a competitor, exploration of a novel environment and boldness under predation risk. There was no indication of a temporally stable behavioural syndrome, consisting of boldness, activity and exploration, nor were individuals consistent in the separate behaviours, contradicting the general assertion of its taxonomic prevalence. Furthermore, the study did not provide support for size or growth‐dependent behaviour in this size‐dimorphic species in conditions of limited food availability. The study highlights the importance of independent multiple observations of individual behaviour across time or contexts when measuring behavioural repeatability and covariation.     

Sexual selection and animal personality

Consistent individual behavioural tendencies, termed “personalities”, have been identified in a wide range of animals. Functional explanations for personality have been proposed, but as yet, very little consideration has been given to a possible role for sexual selection in maintaining differences in personality and its stability within individuals. We provide an overview of the available literature on the role of personality traits in intrasexual competition and mate choice in both human and non‐human animals and integrate this into a framework for considering how sexual selection can generate and maintain personality. For this, we consider the evolution and maintenance of both main aspects of animal personality: inter‐individual variation and intra‐individual consistency.