Behavioural Flexibility and Personality in Zebra Finches

Consistent individual differences in behaviour of animals, that is, personalities, are both widespread and widely studied, but very few studies also include cognitive traits in this context. Animal personality has recently been integrated into the pace‐of‐life‐syndrome hypothesis, relating individual behavioural traits to life history. Variation in cognitive traits could be explained well by this theoretical framework. A risk‐reward trade‐off might lead to different cognitive types: Active birds that learn fast, take risks and probably have a fast lifestyle and less active, slow learning birds that are risk averse but thereby perform better in reversal learning as they probably pay more attention to external cues. We investigated the performance of zebra finches (Taeniopygia guttata) in a cognitively challenging reversal learning task and linked this to two personality traits: activity and fearfulness. Male birds were better in reversal learning than females. While no personality‐related differences occurred in the initial learning of our task, more active and fearful birds relearned the cue–reward association faster. While birds of different sex might have revealed different risk‐taking strategies in the training, our findings do not reveal the expected direction of a risk‐reward trade‐off in the reversal learning. It seems likely that a more general and personality‐related cognitive ability might improve performance across different tasks. The linkage between personality and cognition documented here could hence suggest that cognitive traits are indeed part of an overall pace‐of‐life syndrome.     

ARTIFICIAL SELECTION ON RELATIVE BRAIN SIZE REVEALS A POSITIVE GENETIC CORRELATION BETWEEN BRAIN SIZE AND PROACTIVE PERSONALITY IN THE GUPPY

Animal personalities range from individuals that are shy, cautious, and easily stressed (a “reactive” personality type) to individuals that are bold, innovative, and quick to learn novel tasks, but also prone to routine formation (a “proactive” personality type). Although personality differences should have important consequences for fitness, their underlying mechanisms remain poorly understood. Here, we investigated how genetic variation in brain size affects personality. We put selection lines of large‐ and small‐brained guppies (Poecilia reticulata), with known differences in cognitive ability, through three standard personality assays. First, we found that large‐brained animals were faster to habituate to, and more exploratory in, open field tests. Large‐brained females were also bolder. Second, large‐brained animals excreted less cortisol in a stressful situation (confinement). Third, large‐brained animals were slower to feed from a novel food source, which we interpret as being caused by reduced behavioral flexibility rather than lack of innovation in the large‐brained lines. Overall, the results point toward a more proactive personality type in large‐brained animals. Thus, this study provides the first experimental evidence linking brain size and personality, an interaction that may affect important fitness‐related aspects of ecology such as dispersal and niche exploration.     

Risk‐taking behaviour variation over time in sea bass Dicentrarchus labrax: effects of day–night alternation,fish phenotypic characteristics and selection for growth

Differences in bold and shy personality on sea bass Dicentrarchus labrax were investigated between a population (wild) produced from wild‐brood fish and a population (selected) produced from selected‐brood fish. During the experiment (112 days), fish were reared under self‐feeding condition to characterize the feeding behaviour of each individual fish. Three risk‐taking tests (T1, T2 and T3 of 24 h with day–night alternation) were carried out at > 1 month intervals on 180 fish of each strain in order to monitor D. labrax behaviour over time and in relation to the light:dark period. A risk‐taking score was evaluated via a preference choice between a safe zone (without food) and a risky zone (potentially with food) by recording the number and the duration of individual passages through an opening in an opaque divider. Results showed that fish performed passages preferentially during the night period and that wild fish were generally bolder than selected fish during T1 and T2 but showed a decrease in risk taking during T3, contrary to selected fish which showed a constant increase in their risk‐taking behaviour. The phenotypic characteristics of the bold fish were different in the two strains: wild bold fish were the smallest within the wild strain and selected bold fish presented the higher growth rate within the selected strain. For both strains, these bold fish were also generally characterized by a high feed‐demand activity. Fish hunger state thus seemed to be the highest motivation for risk‐taking behaviour under the present conditions. Furthermore, behavioural variations over tests such as higher risk taking (number of passages) and faster exploratory responses (higher score emergence) could be interpreted as relevant indicators of the learning process and habituation. According to the results, however, no real difference in coping strategy between strains could be observed at this first stage of domestication and selection.     

Depth distribution of Daphnia in response to a deep-water algal maximum: the effect of body size and temperature gradient

1. In the absence of fish predation, Daphnia exploiting a deep‐water algal maximum are faced with a trade‐off. They can either dwell in the epilimnion where development in the warm water is fast, but food shortage causes low egg production, or in the hypolimnion, where food availability is high but development is slow because of low temperatures. 2. We tested the hypotheses that (i) depth distributions of various ontogenetic stages (size classes and egg‐bearing females) differ because daphnids react to light with size‐specific diel vertical migration (DVM) even in the absence of fish (residual predator avoidance hypothesis) and (ii) differently sized daphnids select different depths because the relative importance of temperature and food varies for ontogenetic stages (physiological hypothesis). We used large indoor mesocosms (Plankton Towers) to test these hypotheses experimentally. 3. Temperature was the strongest factor governing the distribution, with larger proportions of the population dwelling in the food‐rich hypolimnion if the temperature gradient was shallow. There were small but significant differences between ontogenetic stages during the day, but not at night. This suggested the existence of a ‘residual’ effect of light on depth distribution in the absence of a fish cue. 4. Although large individuals exhibited greater amplitude of DVM, the physiological hypothesis had to be rejected. A stage‐specific physiological effect is unlikely to be directly triggered by light, hence vertical movement of the individuals should not be synchronised. Rather, being forced into deeper layers by the residual light response during the day, large and egg‐bearing females experience a lower average temperature during day than juveniles. They probably compensate for this by spending longer time periods in warm waters at night.     

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.     

An approach to incorporate individual personality in modeling fish dispersal across in‐stream barriers

Animal personalities are an important factor that affects the dispersal of animals. In the context of aquatic species, dispersal modeling needs to consider that most freshwater ecosystems are highly fragmented by barriers reducing longitudinal connectivity. Previous research has incorporated such barriers into dispersal models under the neutral assumption that all migrating animals attempt to ascend at all times. Modeling dispersal of animals that do not perform trophic or reproductive migrations will be more realistic if it includes assumptions of which individuals attempt to overcome a barrier. We aimed to introduce personality into predictive modeling of whether a nonmigratory invasive freshwater fish (the round goby, Neogobius melanostomus) will disperse across an in‐stream barrier. To that end, we experimentally assayed the personalities of 259 individuals from invasion fronts and established round goby populations. Based on the population differences in boldness, asociability, and activity, we defined a priori thresholds with bolder, more asocial, and more active individuals having a higher likelihood of ascent. We then combined the personality thresholds with swimming speed data from the literature and in situ measurements of flow velocities in the barrier. The resulting binary logistic regression model revealed probabilities of crossing a barrier which depended not only on water flow and fish swimming speed but also on animal personalities. We conclude that risk assessment through predictive dispersal modeling across fragmented landscapes can be advanced by including personality traits as parameters. The inclusion of behavior into modeling the spread of invasive species can help to improve the accuracy of risk assessments.     

State dependence,personality, and plants: light‐foraging decisions in Mimosa pudica (L.)

Plants make foraging decisions that are dependent on ecological conditions, such as resource availability and distribution. Despite the field of plant behavioral ecology gaining momentum, ecologists still know little about what factors impact plant behavior, especially light‐foraging behavior. We made use of the behavioral reaction norm approach to investigate light foraging in a plant species that exhibits rapid movement: Mimosa pudica. We explored how herbivore avoidance behavior in M. pudica (which closes its leaflets temporarily when disturbed) is affected by an individual's energy state and the quality of the current environment and also repeatedly tested the behavior of individuals from two seed sources to determine whether individuals exhibit a “personality” (i.e., behavioral syndrome). We found that when individuals are in a low‐energy state, they adopt a riskier light‐foraging strategy, opening leaflets faster, and not closing leaflets as often in response to a disturbance. However, when plants are in a high‐energy state, they exhibit a plastic light‐foraging strategy dependent on environment quality. Although we found no evidence that individuals exhibit behavioral syndromes, we found that individuals from different seed sources consistently behave differently from each other. Our results suggest that plants are capable of making state‐dependent decisions and that plant decision making is complex, depending on the interplay between internal and external factors.     

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.     

Picking personalities apart: estimating the influence of predation,sex and body size on boldness in the guppy Poecilia reticulata

Predation is a strong selective force in most natural systems, potentially fueling evolutionary changes in prey morphology, life history and behaviour. Recent work has suggested that contrasting predation pressures may lead to population differentiation in personality traits. However, there are indications that these personality traits also differ between sexes and not necessarily in a consistent way between populations. We used an integrative approach to quantify boldness (latency to emerge from a shelter) in wild‐caught guppies in relation to predation pressure, population origin, sex and size. In addition we quantified the repeatability of these personality traits. We show that predation regime had significant effects on emergence time. In general, fish from high predation localities emerged sooner from the shelter compared to those from low predation localities. We found strong sex differences; males were significantly bolder than females. The relationship between emergence time and body size was non‐significant in all populations. We discuss what responses to expect from predator‐naïve versus predator‐experienced individuals and how this can be linked to the shyness–boldness continuum.     

Personality interacts with habitat quality to govern individual mortality and dispersal patterns

Individual phenotypic differences are increasingly recognized as key drivers of ecological processes. However, studies examining the relative importance of these differences in comparison with environmental factors or how individual phenotype interacts across different environmental contexts remain lacking. We performed two field experiments to assess the concurrent roles of personality differences and habitat quality in mediating individual mortality and dispersal. We quantified the predator avoidance response of mud crabs, Panopeus herbstii, collected from low‐ and high‐quality oyster reefs and measured crab loss in a caging experiment. We simultaneously measured the distance crabs traveled as well as the stability of personalities across reef quality in a separate reciprocal transplant experiment. Habitat quality was the primary determinant of crab loss, although the distance crabs traveled was governed by personality which interacted with habitat quality to control the fate of crabs. Here, crabs on low‐quality reefs rapidly emigrated, starting with the boldest individuals, and experienced modest levels of predation regardless of personality. In contrast, both bold and shy crabs would remain on high‐quality reefs for months where bolder individuals experienced higher predation risk. These findings suggest that personalities could produce vastly different population dynamics across habitat quality and govern community responses to habitat degradation.     

Boldness and Information Use in Three‐Spined Sticklebacks

In foraging groups, individuals may utilise information from their social environment to aid decision making when choosing where to search for food. Little work has looked at the costs or benefits of behavioural differences, such as consistent individual variation in boldness, with respect to learning ability. Here, we investigate the response of three‐spined stickleback (Gasterosteus aculeatus) to ‘social cues’, ‘local enhancement’ and ‘public information’ during foraging tasks. Our results confirm previous work suggesting that this species responds to social cues and local enhancement but not public information. Variation in boldness did not affect the use of different types of information. However, time taken to make a choice and reach a patch varied between fish with different levels of boldness. Contrary to expectation, shy fish were the more variable individuals, having a greater range of reaction times when responding to the tasks. This suggests that individual behavioural differences still play a role when utilising information obtained from the environment and may influence the relative benefits that could result in different contexts.     

The presence of a conspecific induces risk-taking behaviour and enlargement of somata size of dopaminergic neurons in the brain of male medaka fish

Boldness and risk-taking behaviours in animals are important traits to obtain advantages such as habitation, food resources, reproductive success and social dominance. Risk-taking behaviour is influenced by physiological and environmental conditions; however, whether individual fish become bolder by the presence of conspecifics remains unknown. In this study, a light–dark preference test was conducted using medaka fish (Oryzias latipes) with or without a neighbouring conspecific. It was found that individual medaka male fish preferred a light environment and avoided a dark environment, whereas the display of a neighbouring conspecific enhanced the time the male spent in the dark environment (i.e., this condition encouraged risk-taking). The blood glucose level increased in fish confined to the dark condition but did not increase in light-preferring fish and risk-taking fish. Large somata expressing tyrosine hydroxylase, which is the rate-limiting enzyme in dopamine synthesis, were detected in the telencephalic and diencephalic brain regions in risk-taking medaka, whereas large somata were detected in the diencephalic region in medaka confined to the dark condition. These findings indicated that medaka is a good fish model to explore the central roles of dopaminergic neurons in the telencephalon and the diencephalon, which regulate risk-taking behaviour.     

Olfactory learning and behaviour are ‘insulated’ against visual processing in larval Drosophila

We investigate the organization of behaviour across sensory modalities, using larval Drosophila melanogaster. We ask whether olfactory learning and behaviour are affected by visual processing. We find that: (1) Visual choice does not affect concomitant odour choice. (2) Visual context does not influence odour learning, nor do changes of visual context between training and test affect retrieval of odour memory. (3) Larvae cannot solve a biconditional discrimination task, despite generally permissive conditions. In this task, larvae are required to establish conditional associations: in light, one odour is rewarded and the other one is not, whereas in dark the opposite contingency is established. After such training, choice between the two odours is equal under light and dark testing conditions, suggesting that larvae do not establish odour memories specifically for one visual context only. Together, these data suggest that, in larval Drosophila, olfactory learning and behaviour are ‘insulated’ against visual processing.     

The effect of boldness on decision-making in barnacle geese is group-size-dependent

In group-living species, decisions made by individuals may result in collective behaviours. A central question in understanding collective behaviours is how individual variation in phenotype affects collective behaviours. However, how the personality of individuals affects collective decisions in groups remains poorly understood. Here, we investigated the role of boldness on the decision-making process in different-sized groups of barnacle geese. Naive barnacle geese, differing in boldness score, were introduced in a labyrinth in groups with either one or three informed demonstrators. The demonstrators possessed information about the route through the labyrinth. In pairs, the probability of choosing a route prior to the informed demonstrator increased with increasing boldness score: bolder individuals decided more often for themselves where to go compared with shyer individuals, whereas shyer individuals waited more often for the demonstrators to decide and followed this information. In groups of four individuals, however, there was no effect of boldness on decision-making, suggesting that individual differences were less important with increasing group size. Our experimental results show that personality is important in collective decisions in pairs of barnacle geese, and suggest that bolder individuals have a greater influence over the outcome of decisions in groups.     

Express your personality or go along with the group: what determines the behaviour of shoaling perch?

Behavioural syndromes, defined as correlated behaviours in different contexts, have been studied across species and taxa including humans as part of a personality concept. While most studies have focused on solitary individuals, less is known on how shoaling fish compromise between own personality and group behaviour. Risk-taking behaviour in 1-year-old perch (Perca fluviatilis) was observed to compare individual behaviour when in a group and when alone. An experimental design gave the fish the choice between foraging in an open area in the presence of a piscivore and hiding in the vegetation. We quantified the variation accountable by the effect of individuals being in a group, individuals alone and repeated measurements, using hierarchical mixed effects models. Within-group variances were low, but when individuals were later tested alone, individual differences explained most of the variation. Still, the individual best linear unbiased predictors (BLUPs) of time spent in the open area, extracted from the random effects of the mixed effects model, were positively correlated with the corresponding BLUPs when alone. The results indicate that individual behavioural traits are to some degree expressed also within groups. Most fish showed a shyer behaviour when alone, but bolder individuals changed less between treatments than did shyer ones, suggesting a more influential role of bold fish in the group.     

A Comparison of Blue Light and Caffeine Effects on Cognitive Function and Alertness in Humans

The alerting effects of both caffeine and short wavelength (blue) light have been consistently reported. The ability of blue light to enhance alertness and cognitive function via non-image forming neuropathways have been suggested as a non-pharmacological countermeasure for drowsiness across a range of occupational settings. Here we compare and contrast the alerting and psychomotor effects of 240 mg of caffeine and a 1-h dose of ~40 lx blue light in a non-athletic population. Twenty-one healthy subjects performed a computer-based psychomotor vigilance test before and after each of four randomly assigned trial conditions performed on different days: white light/placebo; white light/240 mg caffeine; blue light/placebo; blue light/240 mg caffeine. The Karolinska Sleepiness Scale was used to assess subjective measures of alertness. Both the caffeine only and blue light only conditions enhanced accuracy in a visual reaction test requiring a decision and an additive effect was observed with respect to the fastest reaction times. However, in a test of executive function, where a distraction was included, caffeine exerted a negative effect on accuracy. Furthermore, the blue light only condition consistently outperformed caffeine when both congruent and incongruent distractions were presented. The visual reactions in the absence of a decision or distraction were also enhanced in the blue light only condition and this effect was most prominent in the blue-eyed participants. Overall, blue light and caffeine demonstrated distinct effects on aspects of psychomotor function and have the potential to positively influence a range of settings where cognitive function and alertness are important. Specifically, despite the widespread use of caffeine in competitive sporting environments, the possible impact of blue light has received no research attention.     

Taking the Operant Paradigm into the Field: Associative Learning in Wild Great Tits

Associative learning is essential for resource acquisition, predator avoidance and reproduction in a wide diversity of species, and is therefore a key target for evolutionary and comparative cognition research. Automated operant devices can greatly enhance the study of associative learning and yet their use has been mainly restricted to laboratory conditions. We developed a portable, weatherproof, battery-operated operant device and conducted the first fully automated colour-associative learning experiment using free-ranging individuals in the wild. We used the device to run a colour discrimination task in a monitored population of tits (Paridae). Over two winter months, 80 individuals from four species recorded a total of 5,128 trials. Great tits (Parus major) were more likely than other species to visit the devices and engage in trials, but there were no sex or personality biases in the sample of great tits landing at the devices and registering key pecks. Juveniles were more likely than adults to visit the devices and to register trials. Individuals that were successful at solving a novel technical problem in captivity (lever-pulling) learned faster than non-solvers when at the operant devices in the wild, suggesting cross-contextual consistency in learning performance in very different tasks. There was no significant effect of personality or sex on learning rate, but juveniles’ choice accuracy tended to improve at a faster rate than adults. We discuss how customisable automated operant devices, such as the one described here, could prove to be a powerful tool in evolutionary ecology studies of cognitive traits, especially among inquisitive species such as great tits.     

Individual‐ and population‐level personalities in a floriphilic katydid

Behaviour, including personality, informs us about the response of animals towards their changing environment. Despite the widespread occurrence of florivorous insects and the important but often underrated ecological roles that they play, the study of florivore behaviour is neglected relative to that of pollinators and other herbivores. Specifically, we do not know how different personality types can develop among florivores and enable them to persist in habitats with an ephemeral and dynamic availability of food resources. To address this knowledge gap, we investigated the following questions: whether the (a) inter‐individual differences of exploration and boldness are consistent; (b) inter‐population differences of exploration and boldness are consistent; (c) exploration and boldness are correlated. We collected individuals of the polyphagous floriphilic katydid, Phaneroptera brevis from four populations from wasteland sites in Singapore and performed a personality assay conducted in an insectary to investigate the exploratory and boldness levels of the individuals and populations. The major novel finding was that the floriphilic P. brevis katydids exhibit population‐level personality types for boldness, but not for exploration. Some katydid individuals were consistently more exploratory and bolder than other individuals. However, contrary to our predictions, we did not find any evidence of behavioural syndromes in the katydid individuals, as the boldness level for individuals was not significantly correlated with exploration for individuals. This suggests that an individual which is more exploratory may not be equally keen to take risks and consume novel food that it encounters. Our findings also suggest that boldness and exploration are linked to ecologically important behaviours, but more studies are needed to better understand population‐level personality and how and why natural selection may favour the evolution of personality in certain populations.     

Effects of light or dark phase testing on behavioural and cognitive performance in DBA mice

Behavioural experiments in mice are often carried out during the resting phase of these nocturnal animals. Ignoring the fact that mice are more active during the dark period, results from resting-phase testing has also been used to characterize these animals. Since the influence of the light/dark cycle on testing is likely to be a relevant factor for the analysis of behavioural results, the aim of this study was to evaluate the effects of the relative time of the day as well as light conditions during testing on behavioural and cognitive performance in inbred mice. Na?ve DBA/2N (DBA) mice were tested in the modified hole board (mHB) either during the dark phase under red light or during the light phase under white light. Different behavioural dimensions and cognitive functions were evaluated in parallel. Depending on the testing conditions, the results showed significant differences in behavioural activity, with DBA mice being less inhibited during dark phase. The same experimental group made fewer memory errors in a visuo-spatial task and showed a faster habituation compared with the group tested during the dark phase. From the results we conclude that testing during the light phase induces a pronounced behavioural inhibition as well as a cognitive disruption in DBA mice, which should be taken into account when cognitively testing these animals.     

One cost of being gold: selective predation and implications for the maintenance of the Midas cichlid colour polymorphism (Perciformes: Cichlidae)

In the colour‐polymorphic Midas cichlid fish species complex (Amphilophus citrinellus spp.), gold morphs occur at much lower frequencies (< 10%) than dark individuals. This might be surprising because gold coloration is dominant and coded for by a single Mendelian locus. Furthermore, gold individuals are considered to be competitively advantaged over dark ones because they grow faster and win aggressive encounters more often compared to dark individuals of equal size. However, one might expect a cost of being gold in terms of natural selection as a result of predation. We tested whether the Jaguar cichlid (Parachromis managuensis), a major fish predator of Midas cichlids, preys differentially on colour variants of goldfish (Carassius auratus auratus), which were used as a proxy for Midas cichlids because of their similarity in colour. Size‐matched pairs of prey fish (gold and dark) were offered to the predator and the time until the fish were attacked was recorded. The gold morph was attacked first more often (approximately 70%) but not faster than the dark morph. This suggests that the predator perceives the gold individual first, and/or that the predator exhibits a preference or higher motivation to attack the gold prey fish. The increased risk of predation of gold prey fish suggests for the Midas cichlid system that being gold may carry significant costs in terms of natural selection as a result of its major piscivorous predator. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 350–358.