The relation between dominance and exploratory behavior is context-dependent in wild great tits

Individual differences in personality affect behavior in novelor challenging situations. Personality traits may be subjectto selection because they affect the ability to dominate others.We investigated whether dominance rank at feeding tables inwinter correlated with a heritable personality trait (as measuredby exploratory behavior in a novel environment) in a naturalpopulation of great tits, Parus major. We provided clumped resourcesat feeding tables and calculated linear dominance hierarchieson the basis of observations between dyads of color-ringed individuals,and we used an experimental procedure to measure individualexploratory behavior of these birds. We show that fast-exploringterritorial males had higher dominance ranks than did slow-exploringterritorial males in two out of three samples, and that dominancerelated negatively to the distance between the site of observationand the territory. In contrast, fast-exploring nonterritorialjuveniles had lower dominance ranks than did slow-exploringnonterritorial juveniles, implying that the relation betweendominance and personality is context-dependent in the wild.We discuss how these patterns in dominance can explain earlierreported effects of avian personality on natal dispersal andfitness.     

Animal personality: what are behavioural ecologists measuring?

The discovery that an individual may be constrained, and even behave sub‐optimally, because of its personality type has fundamental implications for understanding individual‐ to group‐level processes. Despite recent interest in the study of animal personalities within behavioural ecology, the field is fraught with conceptual and methodological difficulties inherent in any young discipline. We review the current agreement of definitions and methods used in personality studies across taxa and systems, and find that current methods risk misclassifying traits. Fortunately, these problems have been faced before by other similar fields during their infancy, affording important opportunities to learn from past mistakes. We review the tools that were developed to overcome similar methodological problems in psychology. These tools emphasise the importance of attempting to measure animal personality traits using multiple tests and the care that needs to be taken when interpreting correlations between personality traits or their tests. Accordingly, we suggest an integrative theoretical framework that incorporates these tools to facilitate a robust and unified approach in the study of animal personality.     

Genetics of personalities: no simple answers for complex traits

Identifying the genes that underlie phenotypic variation in natural populations, and assessing the consequences of polymorphisms at these loci for individual fitness are major objectives in evolutionary biology. Yet, with the exception of a few success stories, little progress has been made, and our understanding of the link between genotype and phenotype is still in its infancy. For example, although body length in humans is largely genetically determined, with heritability estimates greater than 0.8, massive genome‐wide association studies (GWAS) have only been able to account for a very small proportion of this variation ( Gudbjartsson et al. 2008 ). If it is so difficult to explain the genetics behind relatively ‘simple’ traits, can we envision that it will at all be possible to find genes underlying complex behavioural traits in wild non‐model organisms? Some notable examples suggest that this can indeed be a worthwhile endeavour. Recently, the circadian rhythm gene Clock has been associated with timing of breeding in a wild blue tit population ( Johnsen et al. 2007 ; Liedvogel et al. 2009 ) and the Pgi gene to variation in dispersal and flight endurance in Glanville fritillary butterflies ( Niitepold et al. 2009 ). A promising candidate gene for influencing complex animal personality traits, also known as behavioural syndromes ( Sih et al. 2004 ), is the dopamine receptor D4 (DRD4) gene. Within the last decade, polymorphisms in this gene have been associated with variation in novelty seeking and exploration behaviour in a range of species, from humans to great tits ( Schinka et al. 2002 ; Fidler et al. 2007 ). In this issue, Korsten et al. (2010) attempt to replicate this previously observed association in wild‐living birds, and test for the generality of the association between DRD4 and personality across a number of European great tit populations.     

Speed of exploration and risk-taking behavior are linked to corticosterone titres in zebra finches

The existence of consistent individual differences in behavioral strategies ("personalities" or coping styles) has been reported in several animal species. Recent work in great tits has shown that such traits are heritable and exhibit significant genetic variation. Free-living birds respond to environmental stresses by up-regulating corticosterone production. Behavior during mild stress can occur in accordance to two types of coping styles, i.e. active and passive. Using artificially selected lines of zebra finches that vary in the amount of corticosterone produced in response to a manual restraint stressor we ran three "personality" experiments. We show that birds in the different corticosterone lines differ in their exploratory and risk-taking behaviors. There was an increase in exploratory behavior as corticosterone titre increased but only in the low corticosterone line. Birds in high corticosterone line showed greater risk-taking behavior than birds in the other lines. Thus, in general, higher levels of circulating corticosterone following a mild stress result in greater exploratory behavior and greater risk taking. This study shows that lines of animals selected for endocrine hormonal responses differ in their "coping" styles or "personalities".     

Predation risk and abiotic habitat parameters affect personality traits in extremophile populations of a neotropical fish (Poecilia vivipara)

Understanding whether and how ambient ecological conditions affect the distribution of personality types within and among populations lies at the heart of research on animal personality. Several studies have focussed on only one agent of divergent selection (or driver of plastic changes in behavior), considering either predation risk or a single abiotic ecological factor. Here, we investigated how an array of abiotic and biotic environmental factors simultaneously shape population differences in boldness, activity in an open‐field test, and sociability/shoaling in the livebearing fish Poecilia vivipara from six ecologically different lagoons in southeastern Brazil. We evaluated the relative contributions of variation in predation risk, water transparency/visibility, salinity (ranging from oligo‐ to hypersaline), and dissolved oxygen. We also investigated the role played by environmental factors for the emergence, strength, and direction of behavioral correlations. Water transparency explained most of the behavioral variation, whereby fish from lagoons with low water transparency were significantly shyer, less active, and shoaled less than fish living under clear water conditions. When we tested additional wild‐caught fish from the same lagoons after acclimating them to homogeneous laboratory conditions, population differences were largely absent, pointing toward behavioral plasticity as a mechanism underlying the observed behavioral differences. Furthermore, we found correlations between personality traits (behavioral syndromes) to vary substantially in strength and direction among populations, with no obvious associations with ecological factors (including predation risk). Altogether, our results suggest that various habitat parameters simultaneously shape the distribution of personality types, with abiotic factors playing a vital (as yet underestimated) role. Furthermore, while predation is often thought to lead to the emergence of behavioral syndromes, our data do not support this assumption.     

Individual variation in behavioural plasticity: direct and indirect effects of boldness,exploration and sociability on habituation to predators in lizards

Little is known about the factors causing variation in behavioural plasticity and the interplay between personality and plasticity. Habituation to predators is a special case of behavioural plasticity. We investigated the direct and indirect effects of boldness, exploration and sociability traits on the habituation ability of Iberian wall lizards, considering exposure and sex effects. Individual boldness was consistent across several non-habituation contexts, but it did not significantly affect habituation. Exploration had a strong direct effect on habituation, with more exploratory individuals being able to habituate faster than less exploratory ones, probably because of their ability to assess risk better. Individual variation in habituation was also affected by sociability, but this was an indirect effect mediated by exposure to the predator. Less social individuals avoided refuges with conspecific cues, increasing exposure to the predator and eventually habituation. Finally, the direct effects of sex (females habituated faster than males) were opposite to its indirect effects through exposure. We conclude that risk assessment, instead of the proactivity–reactivity gradient usually considered in the literature, can affect behavioural plasticity through complex interactions between direct and indirect effects, including exploratory behaviour, degree of exposure to the predator and sex, which represent novel mechanisms generating inter-individual variation in plasticity.     

Growth-mortality tradeoffs and 'personality traits' in animals

Consistent individual differences in boldness, reactivity, aggressiveness, and other 'personality traits' in animals are stable within individuals but vary across individuals, for reasons which are currently obscure. Here, I suggest that consistent individual differences in growth rates encourage consistent individual differences in behavior patterns that contribute to growth-mortality tradeoffs. This hypothesis predicts that behavior patterns that increase both growth and mortality rates (e.g. foraging under predation risk, aggressive defense of feeding territories) will be positively correlated with one another across individuals, that selection for high growth rates will increase mean levels of potentially risky behavior across populations, and that within populations, faster-growing individuals will take more risks in foraging contexts than slower-growing individuals. Tentative empirical support for these predictions suggests that a growth-mortality perspective may help explain some of the consistent individual differences in behavioral traits that have been reported in fish, amphibians, reptiles, and other animals with indeterminate growth.     

Plastic proteans: reduced predictability in the face of predation risk in hermit crabs

Variation in behaviour occurs at multiple levels, including between individuals (personality) and between situations (plasticity). Behaviour also varies within individuals, and intra-individual variation (IIV) in behaviour describes within-individual residual variance in behaviour that remains after the effects of obvious external and internal influences on behaviour have been accounted for. IIV thus describes how predictable an individual''s behaviour is. Differences in predictability, between individuals and between situations, might be biologically significant. For example, behaving unpredictably under predation threat might reduce the chance of capture. Here, we investigated the duration of startle responses in hermit crabs, in the presence and absence of a predator cue. Individuals differed in startle response duration (personality) and while individuals also varied in their sensitivity to risk, mean response time was greater in the presence of a predator (plasticity). Moreover, IIV was greater in the presence of a predator, providing some of the first evidence that the facultative injection of unpredictability into behaviour might represent a strategy for dealing with risk.     

Long-term repeatability and stability of three personality traits in meadow voles

Consistency of animal personality traits is expected. Mounting evidence suggests that animal personalities will change with time and major life events. Research into this phenomenon is often limited to span only short periods of time in the animals’ life or have few measures across their life. We measured Exploration, Activity and Boldness of litters of meadow voles, Microtus pennsylvanicus, in a pair of novel object tests six times over a year, representing a large proportion of the lifespan of the vole. Our null hypothesis was that the personality traits would not change, and our first alternative hypothesis was that personality traits would change equally for all individuals as they aged. Neither was supported. The data support our third hypothesis that traits would change and change unequally. Activity and Boldness were consistent across time. However, Exploratory behaviour increased with the vole's age. The supported models show that personality traits change consistently for related individuals, but the litters differ in their change with age. This suggests that meadow vole life history affects how personality traits develop, but not necessarily their magnitudes. We also tested the repeatability of traits across the testing intervals. We discovered that the repeatability of these three personality traits varied across time, depending on the trait. Activity was repeatable equally across ages. Exploration became more repeatable and Boldness became less so. Thus, personality traits may be more malleable than supposed, especially over long periods of time.     

Behavioral syndromes and the evolution of correlated behavior in zebrafish

Studies of "behavioral syndromes" in different populations andspecies of animals can be used to shed light on the underlyingmechanisms of evolution. For example, some personality syndromessuggest the existence of an underlying hormonal link, whereasother relationships between boldness and aggression appear tobe the result of similar selective pressures. Here, we used1 wild-derived and 2 laboratory strains of zebrafish (Daniorerio) to examine relationships among 5 behavioral measures:shoaling, activity level, predator approaches, latency to feedafter a disturbance, and biting to a mirror stimulus. We foundevidence of an activity syndrome, as if underlying metaboliccosts influence variation in multiple forms of behavior. Evidencefor a relationship between boldness and aggression was alsoapparent but depended both on strain and which specific behaviorpatterns were identified as measures of "boldness." Althoughsome comparisons of laboratory and wild-derived strains wereconsistent with a domestication syndrome, others were not. Mostobserved relationships were relatively weak and occasionallyinconsistent, arguing against strong underlying genetic linkagesor pleiotropic effects relating any of the behavioral measures.Instead, it may be more important to study the details of selectivecontext or the long-term impact of linkages between some, butnot all, of a large set of genes influencing complex behavioraltraits. We found profound differences among strains in mostbehavior patterns, but few sex differences. One strain (TM1)was consistently different from the others (SH and Nadia) beingmore social, more likely to approach predators, and taking lesstime to recover from disturbance than were the other 2 strains.     

The influence of predation risk on threat display in great tits

In wintering birds, conflicts over food are often resolved bythreat displays. For displays to be effective, there oughtto be a cost associated with displaying. We investigated whetherincreased vulnerability to predators due to reduced vigilancecould be such a cost. Conflicts ought then to be resolved usingfewer or less intense displays in conditions of high risk. We also looked for differences between dominants and subordinatesin their reaction to risk. Because there is considerable evidencethat subordinate wintering birds forage in riskier places thandominants, one might expect dominants to be less successfulin conflicts under high predation risk. In our experiment,nine flocks of four or five wintering male great tits were keptin outdoor aviaries. In the predation risk treatment, a stuffedpygmy owl was briefly shown before birds were allowed accessto a feeder. In the control treatment the owl did not appear.The predator presentation caused a reduction in the amountof aggression shown by subordinates, whereas for dominants there was no statistically significant change. Dominants were at leastas successful in subduing subordinates under high risk as underlow risk. A possible interpretation is that our experimentreflected a natural foraging situation for great tits, whereephemeral resources can appear unpredictably. In such situations,dominants may need to be bold to gain priority of access even under increased risk of predation, whereas a subordinate wouldgain little by risking a conflict with small chances of winning.     

Comparing the strength of behavioural plasticity and consistency across situations: animal personalities in the hermit crab Pagurus bernhardus

Many phenotypic traits show plasticity but behaviour is often considered the 'most plastic' aspect of phenotype as it is likely to show the quickest response to temporal changes in conditions or 'situation'. However, it has also been noted that constraints on sensory acuity, cognitive structure and physiological capacities place limits on behavioural plasticity. Such limits to plasticity may generate consistent differences in behaviour between individuals from the same population. It has recently been suggested that these consistent differences in individual behaviour may be adaptive and the term 'animal personalities' has been used to describe them. In many cases, however, a degree of both behavioural plasticity and relative consistency is probable. To understand the possible functions of animal personalities, it is necessary to determine the relative strength of each tendency and this may be achieved by comparison of statistical effect sizes for tests of difference and concordance. Here, we describe a new statistical framework for making such comparisons and investigate cross-situational plasticity and consistency in the duration of startle responses in the European hermit crab Pagurus bernhardus, in the field and the laboratory. The effect sizes of tests for behavioural consistency were greater than for tests of behavioural plasticity, indicating for the first time the presence of animal personalities in a crustacean model.     

Innovation as part of a wider behavioural syndrome in the guppy: The effect of sex and body size

Recent work on animal personalities has shown that individuals within populations often differ consistently in various types of behaviour and that many of these behaviours correlate among individuals to form behavioural syndromes. Individuals of certain species have also been shown to differ in their rate of behavioural innovation in arriving at novel solutions to new and existing problems (e.g., mazes, novel foods). Here, we investigate whether behaviours traditionally studied in personality research are correlated with individual rates of innovation as part of a wider behavioural syndrome. Guppies (Poecilia reticulata) of both sexes from three different wild population sources were assessed: (a) exploration of an open area; (b) speed through a three‐dimensional maze; (c) investigation of a novel object; and (d) attraction to a novel food. The covariance structure (syndrome structure) was examined using structural equation modelling. The best model separated behaviours relating to activity in all contexts from rates of exploration/investigation and innovation. Innovative behaviour (utilizing new food and moving through a novel area) in these fish therefore forms part of the same syndrome as the traditional shy‐bold continuum (exploration of an open area and investigation of a novel object) found in many animal personality studies. There were no clear differences in innovation or syndrome structure between the sexes, or between the three different populations. However, body size was implicated as part of the behavioural syndrome structure, and because body size is highly correlated with age in guppies, this suggests that individual behavioural differences in personality/innovation in guppies may largely be driven by developmental state.     

The Personality Behind Cheating: Behavioural Types and the Feeding Ecology of Cleaner Fish

The complex mutualistic relationship between the cleaner fish (Labroides dimidiatus) and their ‘clients’ in many reef systems throughout the world has been the subject of debate and research interest for decades. Game‐theory models have long struggled with explaining how the mixed strategies of cheating and honesty might have evolved in such a system and while significant efforts have been made theoretically, demonstrating the nature of this relationship empirically remains an important research challenge. Using the experimental framework of behavioural syndromes, we sought to quantitatively assess the relationship between personality and the feeding ecology of cleaner fish to provide novel insights into the underlying mechanistic basis of cheating in cleaner‐client interactions. First, we observed and filmed cleaner fish interactions with heterospecifics, movement patterns and general feeding ecology in the wild. We then captured and measured all focal individuals and tested them for individual consistency in measures of activity, exploration and risk taking (boldness) in the laboratory. Our results suggest a syndrome incorporating aspects of personality and foraging effort are central components of the behavioural ecology of L. dimidiatus on the Great Barrier Reef. We found that individuals that exhibited greater feeding effort tended to cheat proportionately less and move over smaller distances relative to bolder more active, exploratory individuals. Our study demonstrates for the first time that individual differences in personality might be mechanistically involved in explaining how the mixed strategies of cheating and honesty persist in cleaner fish mutualisms.     

Energy expenditure, nestling age, and brood size: an experimental study of parental behavior in the great tit Parus major

A brood manipulation experiment on great tits Parus major was performedto study the effects of nestling age and brood size on parentalcare and offspring survival. Daily energy expenditure (DEE)of females feeding nestlings of 6 and 12 days of age was measuredusing the doubly-labeled water technique. Females adjusted theirbrooding behavior to the age of the young. The data are consistentwith the idea that brooding behavior was determined primarilyby the thermoregulatory requirements of the brood. Female DEEdid not differ with nestling age; when differences in body masswere controlled for, it was lower during the brooding periodthan later. In enlarged broods, both parents showed significantlyhigher rates of food provisioning to the brood. Female DEE wasaffected by brood size manipulation, and it did not level offwith brood size. There was no significant effect of nestlingage on the relation between DEE and manipulation. Birds wereable to raise a larger brood than the natural brood size, althoughlarger broods suffered from increased nestling mortality ratesduring the peak demand period of the nestlings. Offspring conditionat fledging was negatively affected by brood size manipulation,but recruitment rate per brood was positively related to broodsize, suggesting that the optimal brood size exceeds the naturalbrood size in this population.     

The function of extrapair paternity in blue tits and great tits: good genes or fertility insurance?

DNA fingerprinting of an island population of blue tits andgreat tits in southeast Norway revealed that extrapair paternityaccounted for 36% (17/47) and 27% (15/55) of broods and for7% (31/466) and 8% (33/408) of young in the two species, respectively.Cuckolded males did not differ from noncuckolded males withrespect to morphology, age, or survival. There was no seasonalpattern in the frequency of extrapair paternity, and males showedno individual consistency in paternity loss over multiple broods.Extrapair offspring did not grow faster, they did not fledgewith a higher body mass, and they did not show a higher localsurvival rate than their half siblings. Hence, there was noevidence of any association between extrapair paternity andmale phenotypic or genotypic quality. Extrapair offspring wererandomly distributed among broods, with the only exceptionsof one blue tit and two great tit broods in which all young(six to nine) were sired by an extrapair male. This patternis best explained by a small proportion of males (2%–4%)being infertile and by most females performing a few extrapaircopulations as insurance against laying infertile eggs. We concludethat the results suggest a role for fertility insurance butthat alternative functional explanations to extrapair paternityin these populations cannot yet be ruled out.     

Poor nutritional condition promotes high-risk behaviours: a systematic review and meta-analysis

Animal behaviour can lead to varying levels of risk, and an individual's physical condition can alter the potential costs and benefits of undertaking risky behaviours. How risk-taking behaviour depends on condition is subject to contrasting hypotheses. The asset protection principle proposes that individuals in better condition should be more risk averse, as they have higher future reproductive potential (i.e. more to lose). The state-dependent safety hypothesis proposes that high-condition individuals that are more likely to survive and maximise the benefits of risky situations may make apparently riskier choices, as their individual risk is in fact lower. We systematically searched for studies that experimentally manipulated animals’ nutritional or energetic condition through diet treatments, and subsequently measured risk-taking behaviour in contexts relating to predation, novelty and exploration. Our meta-analysis quantified condition effects on risk-taking behaviour at both the mean and variance level. We preregistered our methods and hypotheses prior to conducting the study. Phylogenetic multilevel meta-analysis revealed that the lower-nutritional-condition individuals showed on average ca. 26% greater tendency towards risk than high-condition individuals (95% confidence interval: 15–38%; N = 126 studies, 1297 effect sizes). Meta-regressions revealed several factors influencing the overall effect, such as the experimental context used to measure risk-taking behaviour, and the life stage when condition was manipulated. Meta-analysis of variance revealed no clear overall effect of condition on behavioural variance (on average ca. 3% decrease in variance in low- versus high-condition groups; 95% confidence interval: −8 to 3%; N = 119 studies, 1235 effect sizes), however, the experimental context was an important factor influencing the strength and direction of the variance effect. Our comprehensive systematic review and meta-analysis provide insights into the roles of state dependency and plasticity in intraspecific behavioural variation. While heterogeneity among effect sizes was high, our results show that poor nutritional state on average increases risk taking in ecological contexts involving predation, novelty and exploration.     

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.