The influence of experience on risk taking: results from a common-garden experiment on populations of Eurasian perch

Predation is often thought of as an unforgiving and strong selective force, quickly selecting against maladaptive behaviour in the prey. It is argued that experience is likely to have low influence on the phenotypic response to predation, as failing to react correctly to a predator may mean death to the prey and no second chance to learn and correct the behaviour. Individuals from different populations of Eurasian perch are known to differ in risk-taking behaviour. Variation in predation pressure has been suggested as a key factor causing these differences, but little is known about the underlying mechanism by which predation generates risk-taking phenotypes in perch. We compared the degree of boldness between two natural populations of Eurasian perch, living under different predation regimes, and the same populations hatched and reared under identical conditions, free from predation. By this common-garden approach, we sought to investigate patterns in the influence of inheritance and experience on boldness phenotype. The wild fish differed in risk taking, with fish from the low predation-risk population acting bolder than fish from the high-risk environment. In the reared fish, both populations behaved equally bold. Only the fish originating from the high predation population showed different behaviour when comparing wild and reared ecotypes. Our results suggest that experience has an important impact on the response to predators and that geographic variation in risk taking between populations of Eurasian perch to a high degree is shaped by adjustments to the current environment. Habituation had an effect of risk-taking behaviour over the experimental period, but consistent differences between individuals were also found. Furthermore, we also show, by the estimation of variance components, that the behaviour we observe is affected by a range of random effects, such as aquaria and group membership, that in concert shapes the behaviour of an individual perch.     

The role of ecological context and predation risk-stimuli in revealing the true picture about the genetic basis of boldness evolution in fish

To showcase the importance of genotype × environment interactions and the presence of predation risk in the experimental assessment of boldness in fish, we investigated boldness in terms of feeding behavior and refuge use in two genetically different populations of juvenile carp (Cyprinus carpio) in two replicated experimental conditions in ponds and laboratory tanks. The populations were expected to exhibit genetic differences in boldness due to differential evolutionary adaptation to low-predation-risk pond aquaculture conditions. Boldness was measured in variants of open-field trials with and without implementation of additional predation risk-stimuli by angling on feeding spots. Without explicit implementation of risk, genotypes adapted to low-risk environments, i.e., domesticated mirror carp behaved consistently bolder than their less domesticated scaled conspecifics in the pond environment, but not in the laboratory environment. When we implemented artificial risk-stimuli by angling on previously safe feeding spots, boldness differences among genotypes also emerged in the laboratory environment, indicating strong genotype × environment effects on boldness behavior of carp. The expected genetic basis of boldness differences among genotypes was clearly supported in the pond environment, while the laboratory study revealed these patterns only under inclusion of explicit risk-stimuli. Our study thus underscores that boldness may involve both a basal component that is expressed independently of obvious predation risk (e.g., in open fields) and a component revealed in relation to explicit predation risk, and both dimensions may respond differently in behavioral tests.     

Heritable and experiential effects on boldness in a tropical poeciliid

Consistent differences in human behaviour are often explained with reference to personality traits. Recent evidence suggests that similar traits are widespread across the entire animal kingdom and that they may have substantial fitness consequences. One of the major components of personality is the shyness–boldness continuum. Little is known about the relative contributions of genes and the environment in the development of boldness in wild animal populations. Here, we bred wild-caught fish (Brachyraphis episcopi) collected from regions of high- and low-predation pressure, reared their offspring in the laboratory under varying conditions and tested boldness utilising an open-field paradigm. First-generation laboratory-reared fish showed similar behaviour to their wild parents suggesting that boldness has a heritable component. In addition, repeated chasing with a net increased boldness in both high- and low-predation offspring, showing that boldness is also heavily influenced by life experiences. Differences between males and females were also sustained in the laboratory-reared generation indicating that sex differences in boldness are also heritable. We discuss these results with reference to the potential underlying genetic and hormonal mechanisms as well as the environmental influences that may be responsible for expression of boldness in wild animals.     

Behavioural trait assortment in a social network: patterns and implications

The social fine structure of a population plays a central role in ecological and evolutionary processes. Whilst many studies have investigated how morphological traits such as size affect social structure of populations, comparatively little is known about the influence of behaviours such as boldness and shyness. Using information on social interactions in a wild population of Trinidadian guppies (Poecilia reticulata), we construct a social network. For each individual in the network, we quantify its behavioural phenotype using two measures of boldness, predator inspection tendency, a repeatable and reliably measured behaviour well studied in the context of co-operation, and shoaling tendency. We observe striking heterogeneity in contact patterns, with strong ties being positively assorted and weak ties negatively assorted by our measured behavioural traits. Moreover, shy fish had more network connections than bold fish and these were on average stronger. In other words, social fine structure is strongly influenced by behavioural trait. We assert that such structure will have implications for the outcome of selection on behavioural traits and we speculate that the observed positive assortment may act as an amplifier of selection contributing to the maintenance of co-operation during predator inspection.     

Variation along the shy–bold continuum in extremophile fishes (<Emphasis Type="BoldItalic">Poecilia mexicana</Emphasis>, <Emphasis Type="BoldItalic">Poecilia sulphuraria</Emphasis>)

One potential trade-off that bold individuals face is between increased predation risks and gains in resources. Individuals experiencing high predation and hungry individuals (or individuals with low body condition) are predicted to show increased boldness. We examined one behavioral trait previously reported to be associated with boldness (the time individual fish needed to emerge from shelter) in various populations of mollies (Poecilia spp.). Our study system included several southern Mexican surface streams with high piscine predation and high food availability, sulfidic surface streams with high avian predation, in which the inhabiting fish show reduced body condition, and a sulfidic cave, where predation and body condition are low. Our comparison revealed very short times to emerge from the start box in populations from non-sulfidic streams. In sulfidic habitats (whether surface or cave), it took individual Poecilia mexicana considerably longer to emerge from the start box, and the same difference was also found in an independent comparison between P. mexicana and the closely related, highly sulfide-adapted Poecilia sulphuraria. Fish reared under common garden conditions (in the absence of predators and hydrogen sulfide) showed intermediate boldness scores to the extremes observed in the field. Our data thus indicate that (a) boldness is shaped by environmental conditions/experiential effects, but is not heritable, (b) predation affects boldness in the predicted direction, but (c) low body condition leads to reduced boldness. Extremophile Poecilia spp. spend most of their time surfacing to survive under sulfidic and hypoxic conditions, which exposes them to increased levels of predations, but the fish forage on the bottom. Hence, in this system, increased boldness does not increase foraging success. We argue that energy limitation favors reducing energetically costly behaviors, and exploring novel environments may be just one of them.     

Sex differences in the repeatability of boldness over metamorphosis

Consistent individual differences in boldness have been identified in many species and can have important effects on fitness. In most animals, juveniles face different costs and benefits of risk-taking behavior than do adults. Furthermore, profound changes in hormones, morphology and environment often occur when juveniles become adults. Therefore, the boldness of individuals might change with ontogeny. In field crickets, adult males call to attract sexually receptive females, and male calling increases predation risk. We measured the repeatability of boldness (latency to emerge from a safe refuge) in both male and female crickets. Each cricket was tested once as a small nymph and once as an adult. We found that boldness was repeatable across metamorphosis in females, but not in males. Males became less bold with maturation, a result that we predicted because of the risk associated with calling for mates. We also found that in general, nymphs were bolder than adults and that individuals spent more time immobile in response to a predator cue when they were nymphs, versus when they were adults.     

Personality trait differences between mainland and island populations in the common frog (Rana temporaria)

Understanding and predicting species range expansions is an important challenge in modern ecology because of rapidly changing environments. Recent studies have revealed that consistent within-species variation in behavior (i.e., animal personality) can be imperative for dispersal success, a key process in range expansion. Here we investigate how habitat isolation can mediate differentiation of personality traits between recently founded island populations and the main population. We performed laboratory studies of boldness and exploration across life stages (tadpoles and froglets) using four isolated island populations and four mainland populations of the common frog (Rana temporaria). Both tadpoles and froglets from isolated populations were bolder and more exploratory than conspecifics from the mainland. Although the pattern can be influenced by possible differences in predation pressure, we suggest that this behavioral differentiation might be the result of a disperser-dependent founder effect brought on by an isolation-driven environmental filtering of animal personalities. These findings can have important implications for both species persistence in the face of climate change (i.e., range expansions) and ecological invasions as well as for explaining rapid speciation in isolated patches.     

Balancing the response to predation—the effects of shoal size,predation risk and habituation on behaviour of juvenile perch

Group size, predation risk and habituation are key drivers of behaviour and evolution in gregarious prey animals. However, the extent to which they interact in shaping behaviour is only partially understood. We analyzed their combined effects on boldness and vigilance behaviour in juvenile perch (Perca fluviatilis) by observing individuals in groups of one, two, three and five faced with four different levels of predation risk in a repeated measures design. The perch showed an asymptotic increase in boldness with increasing group size and the highest per capita vigilance in groups of two. With increasing predation risk, individuals reduced boldness and intensified vigilance. The interaction between group size and predation risk influenced vigilance but not boldness. In this context, individuals in groups of two elevated their vigilance compared to individuals in larger groups only when at higher risk of predation. Further, as only group size, they significantly reduced vigilance at the highest level of risk. With increasing habituation, solitary individuals became considerably bolder. Also, predation risk affected boldness only in the more habituated situation. Hence, repeated measures may be essential to correctly interpret certain relationships in behaviour. Our results suggest that perch may adjust boldness behaviour to group size and predation risk independently. This is rather unexpected since in theory, natural selection would strongly favour an interactive adjustment. Finally, vigilance might be particularly effective in groups of two due to the intense monitoring and detailed response to changing levels of risk.     

Are behavioral syndromes invariant? Spatiotemporal variation in shy/bold behavior in squid

Behavioral syndromes are correlated suites of behavior, analogous to human personality traits. Most work to date has been taken from limited “snapshots” in space and time, with the implicit assumption that a behavioral syndrome is an invariant property, fixed by evolutionary constraints or adaptations. However, directional selection on two mechanistically independent traits (selective covariance) could also result in correlated behaviors. Previously, we have shown that shy/bold behavior in Southern dumpling squid (Euprymna tasmanica) across predator encounter and feeding risk contexts is genetically and phenotypically uncoupled, and hence potentially free to vary independently. Here, we collected data on shy/bold behaviors from two independent wild populations of squid in two different years to test whether behavioral correlations across these same two functional contexts vary through time and space. We detected significant influences of population, sex, and body size on the expression of boldness in squid within each functional context, and this was coupled with significant differences in relative population density and adult sex ratio. Despite these changes in behavior and demographic parameters, we found that correlations between boldness scores across the two functional contexts were largely absent in both wild populations of squid in both years. Our work suggests that some animal groups may be largely characterized by context-specific behavioral expression. A theoretical framework which conceptualizes behavioral syndromes resulting from context-specific behavioral rules may be needed to fully understand why behaviors are sometimes correlated, and why sometimes they are not.     

How stable are personalities? A multivariate view of behavioural variation over long and short timescales in the sheepshead swordtail,Xiphophorus birchmanni

Many studies have revealed repeatable (among-individual) variance in behavioural traits consistent with variation in animal personality; however, these studies are often conducted using data collected over single sampling periods, most commonly with short time intervals between observations. Consequently, it is not clear whether population-level patterns of behavioural variation are stable across longer timescales and/or multiple sampling periods or whether individuals maintain consistent ranking of behaviours (and/or personality) over their lifetimes. Here, we address these questions in a captive-bred population of a tropical freshwater poeciliid fish, Xiphophorus birchmanni. Using a multivariate approach, we estimate the among-individual variance-covariance matrix (I), for a set of behavioural traits repeatedly assayed in two different experimental contexts (open-field trials, emergence and exploration trials) over long-term (56 days between observations) and short-term (4-day observation interval) time periods. In both long- and short-term data sets, we find that traits are repeatable and the correlation structure of I is consistent with a latent axis of variation in boldness. While there are some qualitative differences in the way individual traits contribute to boldness and a tendency towards higher repeatabilities in the short-term study, overall, we find that population-level patterns of among-individual behavioural (co)variance to be broadly similar over both time frames. At the individual level, we find evidence that short-term studies can be informative for an individual’s behavioural phenotype over longer (e.g. lifetime) periods. However, statistical support is somewhat mixed and, at least for some observed behaviours, relative rankings of individual performance change significantly between data sets.     

Social influence on the correlation between behaviours in young-of-the-year perch

The connection between risk-taking behaviour and exploratory behaviour in young-of-the-year perch (Perca fluviatilis) was studied in aquarium experiments to see whether individual behaviour patterns could be identified in this species and also to investigate how individual behaviour is influenced by their social environment. Risk-taking was defined as the time spent foraging in an open area vs hiding in the vegetation in the presence of a piscivore. Explorative behaviour was measured as latency to enter a passage leading to an unknown area. Groups of four fish were used for the observations, and both behaviours measured were positively correlated with the mean scores of these behaviours in the other group members. Risk-taking and explorative behaviours were correlated only when data was adjusted for the behaviour of the other group members. Individuals that spent more time in the open than their companions also tended to be faster than the others to enter the passage to the unknown area and vice versa. The results indicate that there are consistent individual differences in boldness in perch, but also that behaviour could be modified according to the behaviour of group members.     

Reproductive Success of Captive-Bred Steelhead Trout in the Wild: Evaluation of Three Hatchery Programs in the Hood River

Abstract:  Population supplementation programs that release captive-bred offspring into the wild to boost the size of endangered populations are now in place for many species. The use of hatcheries for supplementing salmonid populations has become particularly popular. Nevertheless, whether such programs actually increase the size of wild populations remains unclear, and predictions that supplementation fish drag down the fitness of wild fish remain untested. To address these issues, we performed DNA-based parentage analyses on almost complete samples of anadromous steelhead ( Oncorhynchus mykiss ) in the Hood River in Oregon (U.S.A.). Steelhead from a supplementation hatchery (reared in a supplementation hatchery and then allowed to spawn naturally in the wild) had reproductive success indistinguishable from that of wild fish. In contrast, fish from a traditional hatchery (nonlocal origin, multiple generations in hatcheries) breeding in the same river showed significantly lower fitness than wild fish. In addition, crosses between wild fish and supplementation fish were as reproductively successful as those between wild parents. Thus, there was no sign that supplementation fish drag down the fitness of wild fish by breeding with them for a single generation. On the other hand, crosses between hatchery fish of either type (traditional or supplementation) were less fit than expected, suggesting a possible interaction effect. These are the first data to show that a supplementation program with native brood stock can provide a single-generation boost to the size of a natural steelhead population without obvious short-term fitness costs. The long-term effects of population supplementation remain untested.     

Behavioral variation shows heritability in juvenile brown trout Salmo trutta

Animal personalities (sometimes referred also as coping styles) and their fitness consequences are currently among the most intensively explored subjects in behavioral ecology. To estimate the evolvability and adaptability of individually consistent behavioral variation, there is a crucial need to quantify the genetics underlying personality. Here, we experimentally studied the repeatability of various individual behaviors and then estimated heritability of formed boldness, exploration, and aggression components in juvenile brown trout Salmo trutta in standardized laboratory environment. Principal component analysis indicated that individually recorded behaviors were described by two personality axes: the first reflecting boldness, exploration, and aggression and the second tendency to freeze. These personality components, as well as the originally recorded behaviors, were statistically significantly repeatable over time. The latter PC, but not the first one, was statistically significantly heritable, though at low level (h ²?=?0.142?±?0.096). These results suggest that additive genetic variation underlies phenotypically consistent behavioral patterns, proposing that any selection acting on behavior, stress tolerance, or correlated traits has a potential to induce evolution in fish personality.     

Novel methods for discriminating behavioral differences between stickleback individuals and populations in a laboratory shoaling assay

Threespine sticklebacks (Gasterosteus aculeatus) from different habitats have been observed to differ in shoaling behavior, both in the wild and in laboratory studies. In the present study, we surveyed the shoaling behavior of sticklebacks from a variety of marine, lake, and stream habitats throughout the Pacific Northwest. We tested the shoaling tendencies of 113 wild-caught sticklebacks from 13 populations using a laboratory assay that was based on other published shoaling assays in sticklebacks. Using traditional behavioral measures for this assay, such as time spent shoaling and mean position in the tank, we were unable to find population differences in shoaling behavior. However, simple plotting techniques revealed differences in spatial distributions during the assay. When we collapsed individual trials into population-level data sets and applied information theoretic measurements, we found significant behavioral differences between populations. For example, entropy estimates confirm that populations display differences in the extent of clustering at various tank positions. Using log-likelihood analysis, we show that these population-level observations reflect consistent differences in individual behavioral patterns that can be difficult to discriminate using standard measures. The analytical techniques we describe may help improve the detection of potential behavioral differences between fish groups in future studies.     

Habituation to low-risk predators improves body condition in lizards

Habituation to nonlethal predation stimuli may provide benefits for animals living in areas with frequent encounters with low-risk predators. On the other hand, individuals can be very consistent in their antipredator responses, with shy individuals showing greater degree of responsiveness than bold individuals. However, the link between habituation or boldness and individual benefits has not been thoroughly investigated. We established whether and how two behavioral components associated with antipredator responses (habituation and boldness, and their interaction) would influence body condition, which is a parameter related to fitness. We conducted an outdoor semi-natural experiment with Iberian wall lizards (Podarcis hispanica). Individual boldness was consistent across contexts, but we did not find any effect of boldness or the interaction between boldness and habituation on body condition. However, those individuals that habituated more readily to a frequent predatory stimulus were able to increase their body condition more relative to lizards that habituated less. This finding highlights the importance of individual differences in behavioral plasticity, which could influence traits related to fitness. Habituation can provide benefits for individuals exposed to low-risk predators; however, individuals more prone to habituation could also experience mortality costs by wrongly habituating to a dangerous predator.     

A simple model to assess selection for treatment-resistant sea lice

Sea lice are damaging marine copepod parasites that infest wild and farmed salmon. Lice are controlled largely by the application of medicines; however resistance has evolved to several such treatments. A simple model is used to explore situations under which treatment-resistant lice are likely to emerge. The model consists of farmed and wild populations of hosts that are infected with lice that exist in treatment-sensitive and treatment-resistant morphs. Resistance is assumed to impose costs on lice fitness, so the sensitive morphs have a selective advantage in the absence of treatment. Larval lice are exchanged between treated farmed hosts and untreated wild hosts by variable water currents. The model finds that resistance is most strongly selected under moderate levels of treatment on farms. High levels of treatment remove both sensitive and resistant lice from farms and, leave the wild untreated fish as a source of lice. The treatment per fish required to eradicate the resistant morphs increases as hydrodynamic mixing rates increase and so controlling emergence of resistance becomes less cost effective when mixing rates are high.     

Evaluating animal personalities: do observer assessments and experimental tests measure the same thing?

The animal personality literature uses three approaches to assess personality. However, two of these methods, personality ratings and experimentation, have been little compared in captivity and never compared in the wild. We assessed the boldness of wild chacma baboons Papio ursinus using both ratings and experimental methods. Boldness was experimentally assessed when individuals were presented with a novel food item during natural foraging. The boldness of the same individuals was rated on a five-point scale by experienced observers. The ratings and experimental assessments of boldness were found to correlate positively and in a linear fashion. When considered categorically the two approaches showed variable agreement depending on the number of categories assigned and the cut-off criteria adopted. We suggest that the variation between approaches arises because each method captures different aspects of personality; ratings consider personality in absolute terms (using predefined criteria) and multiple contexts, while experimental assessments consider personality in relative terms (using experimental scores relative to the population average) and in limited contexts. We encourage animal personality researchers to consider adopting both methodologies in future studies. We also propose that future studies restrict their analyses to continuous data, since the greatest comparability between methods was found with these data. However, if individuals must be categorised, we suggest that researchers either (a) analyse only those individuals categorised as bold or shy by both ratings and experimental approaches or, if these methods cannot be employed simultaneously, (b) do not use approach-specific criteria but choose a cut-off that can be compared by both approaches.     

Boldness by habituation and social interactions: a model

Most studies of animal personality attribute personality to genetic traits. But a recent study by Magnhagen and Staffan (Behav Ecol Sociobiol 57:295–303, 2005) on young perch in small groups showed that boldness, a central personality trait, is also shaped by social interactions and by previous experience. The authors measured boldness by recording the duration that an individual spent near a predator and the speed with which it fed there. They found that duration near the predator increased over time and was higher the higher the average boldness of other group members. In addition, the feeding rate of shy individuals was reduced if other members of the same group were bold. The authors supposed that these behavioral dynamics were caused by genetic differences, social interactions, and habituation to the predator. However, they did not quantify exactly how this could happen. In the present study, we therefore use an agent-based model to investigate whether these three factors may explain the empirical findings. We choose an agent-based model because this type of model is especially suited to study the relation between behavior at an individual level and behavioral dynamics at a group level. In our model, individuals were either hiding in vegetation or feeding near a predator, whereby their behavior was affected by habituation and by two social mechanisms: social facilitation to approach the predator and competition over food. We show that even if we start the model with identical individuals, these three mechanisms were sufficient to reproduce the behavioral dynamics of the empirical study, including the consistent differences among individuals. Moreover, if we start the model with individuals that already differ in boldness, the behavioral dynamics produced remained the same. Our results indicate the importance of previous experience and social interactions when studying animal personality empirically.     

Effects of relaxed predation pressure on visual predator recognition in the guppy

Many prey species have a genetic predisposition to recognise and respond to predators and can fine-tune their anti-predator behaviour following appropriate experience. Although the Trinidadian guppy ( Poecilia reticulata) has become a model species for the investigation of adaptive behaviour, the extent to which experience mediates predator recognition remains unclear. In this study, we examined the effects of relaxed predation pressure on patterns of anti-predator behaviour in populations differing in evolutionary history. The anti-predator behaviour of wild- and laboratory-born guppies from high- and low-predation localities in Trinidad were compared using three models resembling Crenicichla alta, a dangerous guppy predator, Aequidens pulcher, a less dangerous piscivore, and a snake. Snakes are not known to prey on guppies in Trinidad. Specifically, the following predictions were tested: (1) wild caught fish from the high-predation localities (where guppies co-occur with C. alta and A. pulcher) would respond to the three models according to their perceived level of threat, whereas guppies from the low-predation site would show a reduced response to all of the predator models; (2) high-predation laboratory-reared fish would display a reduced but qualitatively similar response to their wild counterparts; and (3) there would be no behavioural differences between wild- and laboratory-reared low-predation fish. In accordance with these predictions, the results revealed that wild fish originating from high-predation sites responded more strongly to the models than fish from low-predation sites. When reared in the laboratory, guppies from the high-predation population showed a reduced response compared to their wild-caught counterparts, but there was no difference in the behaviour of wild- and laboratory-reared low-predation fish. Model type affected predator inspection behaviour but not schooling tendency, and both wild- and laboratory-reared guppies were more wary of the fish models than the snake. These results suggest that early experience differentially mediates the anti-predator responses of fish from high-risk localities.     

Naturally and hatchery produced European trout Salmo trutta: do their marine survival and dispersal differ?

We tested whether marine survival and migration pattern differed between naturally and hatchery produced European trout Salmo trutta of different origins. The hatchery fish were released 150 m above the river estuary of the southwestern, Norwegian River Imsa, the home of the local population. Recaptures were used as proxy for survival. Wild and local hatchery fish survived better than transplanted hatchery stocks. Trout that were 1 year at release survived less well than 2-year olds, and small individuals less well than larger ones. Relative to their body size at release, populations that originated most distant from the River Imsa, the Baltic River Emån and the Norwegian mountain Lake Tunhovd, exhibited the poorest sea survival. At sea, trout chiefly moved less than 240 km from the river of release, but there were significant differences in dispersal among populations. Hatchery-produced River Emån and Lake Tunhovd trout moved farther from the River Imsa than the south Norwegian sea trout populations, and the marine distributions of the former were similar to that of the natural River Imsa trout. Large fish moved farther from the river than smaller ones. Straying to other rivers was low among wild and local hatchery-produced fish, and significantly lower than among most transplanted populations, and River Emån trout in particular. Thus, the River Imsa trout appeared better adapted to survival under the local conditions than non-local trout with consequences for optimal population management.