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.     

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.     

Nymphal density, behavioral development, and life history in a field cricket

Population density regulates the strength of intraspecific competition and may thereby be reflected in life-history variables, such as development time, growth rate, or investment in immune defense. However, population density may also affect the fitness payoffs of different behaviors and consequently shape the development of personality. Here we studied if population density during nymphal development (one, four, or ten individuals raised together) affects the level of boldness, measured as the latency time to recover from freezing and emerge from a shelter, aggressiveness towards conspecifics or their correlation at the adult stage in the field crickets, Gryllus integer. In addition, we tested if individuals invest more resources in immune function or speed up their development in response to a high conspecifics density during ontogeny. Nymphal density did not affect adult boldness or aggressiveness towards conspecific males per se, but these variables showed a negative association, i.e., indicated an unconventional behavioral syndrome in the highest density treatment. Supporting the effectiveness of density treatments in inducing plastic responses, individuals reached maturity sooner and invested more resources in immune function in the highest nymphal density group compared to groups consisting of one or four individuals. Our results suggest that population density may play an important role in shaping both the realized life history and development of behavioral syndromes.     

Causes and consequences of contest outcome: aggressiveness, dominance and growth in the sheepshead swordtail, Xiphophorus birchmanni

Although our understanding of how animal personality affects fitness is incomplete, one general hypothesis is that personality traits (e.g. boldness and aggressiveness) contribute to competitive ability. If so, then under resource limitation, personality differences will generate variation in life history traits crucial to fitness, like growth. Here, we test this idea using data from same-sex dyadic interaction trials of sheepshead swordtails (Xiphophorus birchmanni). In males, there was evidence of repeatable variation across a suite of agonistic contest behaviours, while repeatable opponent effects on focal behaviour were also detected. A single vector explains 80 % of the among-individual variance in multivariate phenotype and can be viewed as aggressiveness. We also find that aggressiveness predicts dominance—the repeatable tendency to win food in competition—and dominant individuals show faster post-trial weight gain (independently of initial size). In females, a dominance hierarchy predictive of weight gain was also found, but there was no evidence of variation in aggressiveness. While size often predicts contest outcome, our results show that individuals may sometimes grow larger because they are behaviourally dominant rather than vice versa. When resources are limited, personality traits such as aggression can influence growth, life history, and fitness through impacts on resource acquisition.     

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.     

The scale and cause of spatial heterogeneity in strength of temporal density dependence

The importance of density dependence in natural communities continues to spark much debate because it is fundamental to population regulation. We used temporal manipulations of density to explore potentially stabilizing density dependence in early survivorship among six local populations of a tropical damselfish (Dascyllus flavicaudus). Specifically, we tested the premise that spatial heterogeneity in the strength of temporal density dependence would reflect variation in density of predators, the agent of mortality. Our field manipulations revealed that mortality among successive cohorts of young fishes was density dependent at each reef, but that its strength varied by approximately 1.5 orders of magnitude. This spatial heterogeneity was well predicted by variation among the six reefs in the density of predatory fishes that consume juvenile damselfishes. Because density dependence arose from competition for enemy-free space within a shelter coral, the mortality consequence of the competition depended on the neighborhood density of predators. Thus, the scale of heterogeneity in the density dependence largely reflected attributes of the environment that shaped the local abundance of predators. These results have important implications for how ecologists explore regulatory processes in nature. Failure to account for spatial variation could frequently yield misleading conclusions regarding density dependence as a stabilizing process, obscure underlying mechanisms influencing its strength, and provide no insight into the spatial scale of the heterogeneity. Further, models of population dynamics will be improved when experimental approaches better estimate the magnitude and causes of variation in strength of stabilizing density dependence.     

Chihuahuan Desert kangaroo rats: nonlinear effects of population dynamics, competition, and rainfall

Using long-term data on two kangaroo rats in the Chihuahuan Desert of North America, we fitted logistic models including the exogenous effects of seasonal rainfall patterns. Our aim was to test the effects of intraspecific interactions and seasonal rainfall in explaining and predicting the numerical fluctuations of these two kangaroo rats. We found that logistic models fit both data sets quite well; Dipodomys merriami showed lower maximum per capita growth rates than Dipodomys ordii, and in both cases logistic models were nonlinear. Summer rainfall appears to be the most important exogenous effect for both rodent populations; models including this variable were able to predict independent data better than models including winter rainfall. D. merriami was also negatively affected by another kangaroo rat (Dipodomys spectabilis), consistent with previous experimental evidence. We hypothesized that summer rainfall influences the carrying capacity of the environment by affecting seed availability and the intensity of intraspecific competition.     

Do brain parasites alter host personality? — Experimental study in minnows

Despite that the existence of animal personalities is widely recognized, no consensus has been reached on the relative importance of different ecological factors behind their expression. Recently, it has been suggested that parasites may have a crucial role in shaping animal personalities, but only a very few studies have experimentally tested the idea. We infected Eurasian minnows (Phoxinus phoxinus) with the brain-encysted trematode parasite, Diplostomum phoxini, and studied whether infection could modify the personality of their hosts. Our results show that D. phoxini infection did not affect the mean levels of boldness, activity or exploration, but infected minnows showed higher repeatability in boldness and activity, and reduced repeatability in exploration. We also found that D. phoxini may be able to break the associations (behavioral syndromes) between behavioral traits, but that this effect may be dependent on parasite intensity. Furthermore, the effect of D. phoxini infection on personality of the hosts was found to be nonlinearly dependent on infection intensity. Taken together, our results suggest that D. phoxini parasites may shape the personality of their hosts, but that behavioral consequences of ecologically relevant infection levels may be rather subtle and easily remain undetected if only the mean trait expressions are compared.     

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.     

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.     

Boldness is influenced by sublethal interactions with predators and is associated with successful harem infiltration in Madagascar hissing cockroaches

One of the contemporary challenges of the behavioral syndromes literature is to identify how individual variation in behavior is determined, and whether this variation impacts ecological success. Although variation in experience is an obvious potential driver of intraspecific behavioral variation, predicting the impact of experience on suites of correlated behavioral traits is less intuitive. Specifically, if experience impacts traits that shape individuals' success in multiple contexts (e.g., foraging and anti-predator behavior), then experience could generate cross-contextual performance trade-offs associated with behavioral spillover. In the present study, we explore how sublethal experience with predators impacts various aspects of male behavioral tendencies in the Madagascar hissing cockroach, Gromphadorhina portentosa. First, we found that males' activity level and boldness were correlated together in the form of a behavioral syndrome. Second, we found that repeated sublethal interactions with predators shifted male boldness but not activity level, thus suggesting that the syndrome's constituent traits can respond to experience at least semi-independently. Third, we discovered that although predator exposure only influenced boldness, we found that boldness was highly correlated with males' ability to obtain rewarding positions in the harems of rival males. Taken together, our data suggest (but do not yet confirm) that although sublethal exposure to predators influences only a narrow subset of male's behavioral tendencies, these effects could still have nonintuitive consequences for males' success in functionally dissimilar ecological contexts (i.e., social and sexual encounters).     

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.     

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.     

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.     

Laterality is linked to personality in the black-lined rainbowfish,Melanotaenia nigrans

Emotions such as fear in vertebrates are often strongly lateralised, that is, a single cerebral hemisphere tends to be dominant when processing emotive stimuli. Boldness is a measure of an individual’s propensity to take risks and it has obvious connections with fear responses. Given the emotive nature of this well-studied personality trait, there is good reason to suspect that it is also likely to be expressed in a single hemisphere. Here, we examined the link between laterality and boldness in wild and captive-reared rainbowfish, Melanotaenia nigrans. We found that fish from the wild were bolder than those from captivity, which might be a reflection of the differences in the level of predation pressure experienced by the two populations. Secondly, we found that non-lateralised fish were bolder than strongly lateralised fish. In addition, differences in boldness scores between left- and right-biased fish were revealed. We suggest that variation in cerebral lateralisation contributes to the persistence of individual differences in boldness scores in animal populations.     

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.     

Genetic structure of the subtidal red alga Delisea pulchra

We used random amplified polymorphic DNA (RAPDs) to examine small-scale spatial genetic structure in the red alga Delisea pulchra (Greville) Montagne at two locations near Sydney, Australia. We examined genetic structure among plants at four spatial scales ranging from 2 km apart down to <50 cm apart between locations, among sites within locations, among quadrats within sites, and among plants within quadrats. Haploid stages of D. pulchra were absent from the populations studied, suggesting that they are maintained through asexual reproduction of diploid plants. Consistent with this, we found that 19 RAPD phenotypes scored in this study had multiple individuals, indicating the presence of clones in these populations. However, there were no RAPD phenotypes common to two locations separated by only 2 km. Analysis of molecular variance revealed that strong genetic differences occurred between plants from these two locations, with 46.3% of the total genetic variation occurring at this scale, most probably reflecting limited gene flow. Within each location, <25% of the genetic variation was attributable to differences among sites or quadrats, indicating gene flow at those smaller scales. Most of the variation within each location occurred at the smallest spatial scale, among plants within 0.25 m² quadrats. Nonetheless, some pairwise genetic distances (φST) between sites or quadrats within locations were large, indicating some genetic divergence on smaller scales. Genetic distance was independent of spatial distance within both locations, suggesting that fine-scale differences within locations were most probably caused by variation in fine-scale patterns of water movement or fine-scale natural selection. We assessed the impact of one potential selective agent, grazing sea urchins, on the fine-scale genetic structure of D. pulchra. There was no evidence that grazing by sea urchins affected the genetic structure of D. pulchra. In combination with demographic data, our results indicated that local populations of D. pulchra within locations were relatively open and that fine-scale genetic structure was probably constrained by gene flow. At the larger scale however, strong genetic differentiation indicated little gene flow between locations and restricted dispersal of spores. Received: 22 April 1999 / Accepted: 29 November 1999     

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.     

Terrestrial habitat selection and strong density-dependent mortality in recently metamorphosed amphibians

To predict the effects of terrestrial habitat change on amphibian populations, we need to know how amphibians respond to habitat heterogeneity, and whether habitat choice remains consistent throughout the life-history cycle. We conducted four experiments to evaluate how the spatial distribution of juvenile wood frogs, Rana sylvatica (including both overall abundance and localized density), was influenced by habitat choice and habitat structure, and how this relationship changed with spatial scale and behavioral phase. The four experiments included (1) habitat manipulation on replicated 10-ha landscapes surrounding breeding pools; (2) short-term experiments with individual frogs emigrating through a manipulated landscape of 1 m wide hexagonal patches; and habitat manipulations in (3) small (4-m2); and (4) large (100-m2) enclosures with multiple individuals to compare behavior both during and following emigration. The spatial distribution of juvenile wood frogs following emigration resulted from differences in the scale at which juvenile amphibians responded to habitat heterogeneity during active vs. settled behavioral phases. During emigration, juvenile wood frogs responded to coarse-scale variation in habitat (selection between 2.2-ha forest treatments) but not to fine-scale variation. After settling, however, animals showed habitat selection at much smaller scales (2-4 m2). This resulted in high densities of animals in small patches of suitable habitat where they experienced rapid mortality. No evidence of density-dependent habitat selection was seen, with juveniles typically choosing to remain at extremely high densities in high-quality habitat, rather than occupying low-quality habitat. These experiments demonstrate how prediction of the terrestrial distribution of juvenile amphibians requires understanding of the complex behavioral responses to habitat heterogeneity. Understanding these patterns is important, given that human alterations to amphibian habitats may generate extremely high densities of animals, resulting in high density-dependent mortality.