Learning rate and temperament in a high predation risk environment

Living in challenging environments can influence the behavior of animals in a number of ways. For instance, populations of prey fish that experience frequent, nonlethal interactions with predators have a high proportion of individuals that express greater reaction to risk and increased activity and exploration—collectively known as temperament traits. Temperament traits are often correlated, such that individuals that are risk-prone also tend to be active and explore more. Spatial learning, which requires the integration of many sensory cues, has also been shown to vary in fish exposed to different levels of predation threat. Fish from areas of low predation risk learn to solve spatial tasks faster than fish from high predation areas. However, it is not yet known whether simpler forms of learning, such as learning associations between two events, are similarly influenced. Simple forms of associative learning are likely to be affected by temperament because a willingness to approach and explore novel situations could provide animals with a learning advantage. However, it is possible that routine-forming and inflexible traits associated with risk-prone and increased exploratory behavior may act in the opposite way and make risk-prone individuals poorer at learning associations. To investigate this, we measured temperament in Panamanian bishop fish (Brachyrhaphis episcopi) sampled from a site known to contain many predators. The B. episcopi were then tested with an associative learning task. Within this population, fish that explored more were faster at learning a cue that predicted access to food, indicating a link between temperament and basic learning abilities.     

Behavioral Syndromes Break Down in Urban Song Sparrow Populations

Animals in urban habitats face a number of unique stresses, including the necessity of dealing with high levels of human activity. Growing research suggests that: (1) inherent traits, as opposed to learned behavior, influence which species invade urban habitats, and (2) individuals exhibit behavioral syndromes that limit behavioral flexibility. As a result, perhaps only animals with inherently bold personalities successfully settle in areas of high human activity, and such animals may also exhibit correlated variation in other behavioral traits, such as territorial aggression. In this study, we examine boldness and aggression in several urban and rural populations of song sparrows (Melospiza melodia). We found that urban birds were both bolder toward humans and also showed higher levels of aggression. We found a correlation between boldness and aggression in all populations combined, but no correlation within urban populations. Our results agree with other recent studies of song sparrow behavior, suggesting that greater boldness and aggression are general features of urban song sparrow populations, and a lack of a correlation between boldness and aggression in urban habitats is a general phenomenon as well. Urban habitats may select for bold and aggressive birds, and yet the traits can vary independently. These results add to a small number of studies which find that behavioral syndromes break down in potentially high quality habitats.     

Differences in aggression,activity and boldness between native and introduced populations of an invasive crayfish

Aggressiveness, along with foraging voracity and boldness, are key behavioral mechanisms underlying the competitive displacement and invasion success of exotic species. However, do aggressiveness, voracity and boldness of the invader depend on the presence of an ecologically similar native competitor in the invaded community? We conducted four behavioral assays to compare aggression, foraging voracity, threat response and boldness to forage under predation risk of multiple populations of exotic signal crayfish Pacifastacus leniusculus across its native and invaded range with and without a native congener, the Shasta crayfish P. fortis. We predicted that signal crayfish from the invaded range and sympatric with a native congener (IRS) should be more aggressive to outcompete a close competitor than populations from the native range (NR) or invaded range and allopatric to a native congener (IRA). Furthermore, we predicted that IRS populations of signal crayfish should be more voracious, but less bold to forage under predation risk since native predators and prey likely possess appropriate behavioral responses to the invader. Contrary to our predictions, results indicated that IRA signal crayfish were more aggressive towards conspecifics and more voracious and active foragers, yet also bolder to forage under predation risk in comparison to NR and IRS populations, which did not differ in behavior. Higher aggression/voracity/boldness was positively correlated with prey consumption rates, and hence potential impacts on prey. We suggest that the positive correlations between aggression/voracity/boldness are the result of an overall aggression syndrome. Results of stream surveys indicated that IRA streams have significantly lower prey biomass than in IRS streams, which may drive invading signal crayfish to be more aggressive/voracious/bold to acquire resources to establish a population.     

Correlation between boldness and body mass in natural populations of the poeciliid Brachyrhaphis episcopi

The boldness of individual Brachyrhaphis episcopi , collected from regions of high and low predation, was investigated using two independent assays: (1) the time to emerge from cover and (2) the propensity to leave shoal mates and investigate a novel object. A strong correlation between the two assays was revealed such that fish that emerged from shelter sooner were also more likely to approach a novel object. This is indicative of a boldness personality axis acting across both behavioural contexts. Fish from high-predation areas were bolder than those from low-predation areas and males were bolder than females. A significant correlation between body mass, standard length ( L _S) and boldness score was also found. In general, bold fish had a greater body mass at a given L _S than shy fish. These results suggest that personality traits are strongly influenced by population-specific ecological variables and may have fitness consequences in wild populations.     

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.     

Growth-mortality tradeoffs and 'personality traits' in animals

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

Environmental and genetic effects shape the development of personality traits in the mangrove killifish Kryptolebias marmoratus

Consistent individual differences in behaviour are well documented, for example, individuals can be defined as consistently bold or consistently shy. To date our understanding of the mechanisms underpinning consistent individual differences in behaviour (also termed behavioural types (BTs)) remains limited. Theoretical work suggests life‐history tradeoffs drive BT variation, however, empirical support is scarce. Moreover, whilst life‐history is known to be phenotypically plastic in response to environmental conditions during ontogeny, the extent to which such plasticity drives plasticity in behavioural traits and personality remains poorly understood. Using a natural clonal vertebrate, Kryptolebias marmoratus, we control for genetic variation and investigate developmental plasticity in life‐history and three commonly studied behavioural traits (exploration, boldness, aggression) in response to three ecologically relevant environments; conspecific presence, low food and perceived risk. Simulated predation risk was the only treatment that generated repeatable behaviour i.e. personality during ontogeny. Treatments differed in their effects on mean life‐history and behavioural scores. Specifically, low food fish exhibited reduced growth rate and exploration but did not differ from control fish in their boldness or aggression scores. Conspecific presence resulted in a strong negative effect on mean aggression, boldness and exploration during ontogeny but had minimal effect on life‐history traits. Simulated predation risk resulted in increased reproductive output but had minimal effect upon average behavioural scores. Together these results suggest that life‐history plasticity/variation may be insufficient in driving variation in personality during development. Finally, using offspring derived from each rearing environment we investigate maternal effects and find strong maternal influence upon offspring size, but not behaviour. These results highlight and support the current understanding that risk perception is important in shaping personality, and that social experience during ontogeny is a major influence upon behavioural expression.     

Behavioural Syndromes in Urban and Rural Populations of Song Sparrows

Animals in urban habitats are often noticeably bold in the presence of humans. Such boldness may arise due to habituation, as urban animals learn, through repeated exposure, that passing humans do not represent a threat. However, there is growing research suggesting that: (1) inherent traits, as opposed to learned behaviour, influence which species invade urban habitats, and (2) individuals exhibit individual personality traits that limit behavioural flexibility, with the possible result that not all individuals would be able to demonstrate an appropriate level of boldness in urban environments. As a result, perhaps only birds with inherently bold personalities could successfully settle in an area of high human disturbance, and further, we might also expect to see the existence of behavioural syndromes, where boldness is correlated with variation in other behavioural traits such as aggression. In this study, we examined boldness and territorial aggression in urban and rural populations of song sparrows. We found that urban birds were bolder towards humans and that urban birds also showed higher levels of territorial aggression. We also found an overall correlation between boldness and territorial aggression, suggesting that urban boldness may be part of a behavioural syndrome. However, we see no correlation between boldness and aggression in the urban population, and thus, more work is needed to determine the mechanisms accounting for high levels of boldness and aggression urban song sparrows.     

Maladaptive behavior reinforces a recruitment bottleneck in newly settled fishes

Settlement from the plankton ends the major dispersive stage of life for many marine organisms and exposes them to intense predation pressure in juvenile habitats. This predation mortality represents a life-history bottleneck that can determine recruitment success. At the level of individual predator–prey interactions, prey survival depends upon behavior, specifically how behavior affects prey conspicuousness and evasive ability. We conducted an experiment to identify behavioral traits and performance levels that are important determinants of which individuals survive or die soon after settlement. We measured a suite of behavioral traits on late stage, pre-settlement Ward's damsel (Pomacentrus wardi) collected using light traps. These behavioral traits included two measures of routine swimming (indicators of conspicuousness) and eight measures of escape performance to a visual startle stimulus. Fish were then released onto individual patch reefs, where divers measured an additional behavioral trait (boldness). We censused each patch reef until approximately 50% of the fish were missing (~24 h), which we assumed to be a result of predation. We used classification tree analysis to discriminate survivors from fish presumed dead based on poor behavioral performance. The classification tree revealed that individuals displaying the maladaptive combination of low escape response speed, low boldness on the reef, and high routine swimming speed were highly susceptible to predation (92.4% with this combination died within 24 h). This accounted for 55.2% of all fish that died. Several combinations of behavioral traits predicted likely survival over 24 h, but there was greater uncertainty about that prediction than there was for fish that were predicted to die. Thus maladaptive behavioral traits were easier to identify than adaptive traits.     

Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus)

A perplexing new question that has emerged from the recent surge of interest in behavioural syndromes or animal personalities is – why do individual animals behave consistently when behavioural flexibility is advantageous? If individuals have a tendency to be generally aggressive, then a relatively aggressive individual might be overly aggressive towards offspring, mates or even predators. Despite these costs, studies in several taxa have shown that individuals that are more aggressive are also relatively bold. However, the behavioural correlation is not universal; even within a species, population comparisons have shown that boldness and aggressiveness are correlated in populations of sticklebacks that are under strong predation pressure, but not in low predation populations. Here, we provide the first demonstration that an environmental factor can induce a correlation between boldness and aggressiveness. Boldness under predation risk and aggressiveness towards a conspecific were measured before and after sticklebacks were exposed to predation by trout, which predated half the sticklebacks. Exposure to predation generated the boldness–aggressiveness behavioural correlation. The behavioural correlation was produced by both selection by predators and behavioural plasticity. These results support the hypothesis that certain correlations between behaviours might be adaptive in some environments.     

Effects of predation pressure on the cognitive ability of the poeciliid Brachyraphis episcopi

Variable levels of predation pressure are known to have significantimpacts on the evolutionary ecology of different populationsand can affect life-history traits, behavior, and morphology.To date, no studies have directly investigated the impact ofpredation pressure on cognitive ability. Here we use a systemof replicate rivers, each with sites of high- and low-predationpressure, to investigate how this ecological variable affectslearning ability in a tropical poeciliid, Brachyraphis episcopi.We used a spatial task to assess the cognitive ability of eightpopulations from four independent streams (four high- and fourlow-predation populations). The fish were required to locatea foraging patch in one of four compartments by utilizing spatialcues. Fish from areas of low-predation pressure had shorterforaging latencies, entered fewer compartments before discoveringthe reward patch and navigated more actively within the maze,than fish from high-predation sites. The difference in performanceis discussed with reference to forage patch predictability,inter- and intraspecific foraging competition, geographic variationin predation pressure, boldness–shyness traits, and brainlateralization.     

How the cascading effects of a single behavioral trait can generate personality

Individuals from the same population generally vary in suites of correlated behavioral traits: personality. Yet, the strength of the behavioral correlations sometimes differs among populations and environmental conditions, suggesting that single underlying mechanisms, such as genetic constraints, cannot account for them. We propose, instead, that such suites of correlated traits may arise when a single key behavior has multiple cascading effects on several other behaviors through affecting the range of options available. For instance, an individual's shyness can constrain its habitat choice, which, in turn, could restrict the expression of other behavioral traits. We hypothesize that shy individuals should be especially restrained in their choice of habitat when the risk of predation is high, which then canalizes them into different behavioral options making them appear behaviorally distinct from bolder individuals. We test this idea using an individual‐based simulation model. Our results show that individual differences in boldness can be sufficient, under high predation pressure, to generate behavioral correlations between boldness and both the tendency to aggregate and the propensity to use social information. Thus, our findings support the idea that some behavioral syndromes can be, at least to some extent, labile. Our model further predicts that such cascading effects should be more pronounced in populations with a long history of predation, which are expected to exhibit a low average boldness level, compared with predator‐naïve populations.     

Behavioral Plasticity in Response to Environmental Manipulation among Zebrafish (Danio rerio) Populations

Plastic responses can have adaptive significance for organisms occurring in unpredictable environments, migratory species and organisms occupying novel environments. Zebrafish (Danio rerio) occur in a wide range of habitats and environments that fluctuate frequently across seasons and habitats. We expect wild populations of fish to be behaviorally more flexible than fish reared in conventional laboratory and hatchery environments. We measured three behavioral traits among 2 wild (U and PN) and 1 laboratory bred (SH) zebrafish populations in four environments differing in water flow and vegetation regimes. We found that the degree of plasticity varied with the type of behavior and also among populations. In general, vegetation increased aggression and water flow decreased latency to feed after a disturbance, but the patterns were population dependent. For example, while wild U fish fed more readily after a disturbance in vegetated and/or flowing habitats, fish from the wild PN population and lab-reared SH strain showed little variation in foraging across different environmental conditions. Zebrafish from all the three populations were more aggressive when tested in an arena with vegetation. In contrast, while there was an inter- population difference in shoaling distances, variation in shoaling distance across environmental conditions within populations was not significant. These results suggest that both foraging and aggression in zebrafish are more plastic and influenced by immediate context than is shoaling distance, which may have a stronger genetic basis. Our findings point to different underlying mechanisms influencing the expression of these traits and warrants further investigations.     

Ecological consequences of the bold–shy continuum: the effect of predator boldness on prey risk

Although the existence of different personality traits within and between animal populations has been relatively well established, the ecological implications of this variation remain neglected. In this study we tested whether differences in the boldness of pairs of three-spined sticklebacks led to differential predation risk in their prey, Chironomidae larvae. Bolder pairs, those that left a refuge and crossed the tank mid-line sooner, ate a greater proportion of prey in 10 min than less bold fish (therefore prey were at a greater per capita risk). Fish crossed the mid-line more rapidly when a larger number of prey were presented, suggesting they accepted greater risk in return for a larger foraging reward. Perception of predation risk also affected the differences between fish in boldness, as larger fish crossed the mid-line sooner after leaving the refuge (larger fish are less at risk from predation). Hence, an interesting trophic interaction occurs, where the risk experienced by the chironomid larvae is determined by the risk perceived by their predators. Through the variation generated by boldness, a form of behaviourally mediated trophic cascade can occur within (as well as between) communities.     

Behavioural variation in Eurasian perch populations with respect to relative catchability

Animal personalities, i.e. consistent individual differences in behaviour, are currently of high interest among behavioural and evolutionary biologists. The topic has received increasing attention also in fisheries science because selective harvesting of certain behavioural types might impose fishing-induced selection on personality. Here, we ice-fished wild Eurasian perch (Perca fluviatilis) from three native populations and investigated whether differences in relative catchability would explain behavioural differences observed in experimental conditions. We inferred relative catchability differences indirectly by fishing each location first with generally inefficient artificial bait and then by more efficient natural bait. The captured, individually tagged fish were tested in groups for their exploration tendency, activity and boldness under authentic predation risk in semi-natural stream channels. Fish that were easily captured first with artificial bait expressed fast exploration and acute activity, whereas the fish captured with natural bait showed less active and explorative behaviour. Differences in relative catchability did not explain variation in boldness or body size. In conclusion, we found that (1) Eurasian perch differing in relative catchability differ in certain behavioural traits, (2) fast explorers are more common among fish that get easily caught compared to fish that are more difficult to catch, (3) relative catchability explains more behavioural variation in a novel environment than in a familiar one and (4) selectivity of recreational angling on fish behaviour may depend on applied angling method and the effort spent on each location.     

Increased exposure to predators increases both exploration and activity level in Brachyrhaphis episcopi

Two temperament traits, tendency to explore and activity level, were measured in a tropical poeciliid fish, the Panamanian bishop Brachyrhaphis episcopi. Open-field arena tests were used to quantify how predation pressure shapes activity levels and exploratory behaviours. Fish behaviour differed between high and low-predation populations. Fish that experienced higher levels of predation were both more explorative and more active. There were also some individual differences within populations; fish varied in their levels of exploration and activity in a novel open arena, but these differences were not related to sex or size. Together with previous studies on this species, these results indicate that there is a behavioural syndrome associated with predation pressure. Fish from high-predation populations are bolder, more explorative and more active than those from low-predation populations.     

Sex-Specific Aggression and Antipredator Behaviour in Young Brown Trout

Sex differences in adult behaviour are often interpreted as consequences of sexual selection and/or different reproductive roles in males and females. Sex-specific juvenile behaviour, however, has received less attention. Adult brown trout males are more aggressive than females during spawning and juvenile aggression may be genetically correlated with adult aggression in fish. We therefore tested the prediction that immature brown trout males are more aggressive and bolder than immature females. Because previous work has suggested that precocious maturation increases dominance in salmonids, we included precocious males in the study to test the prediction that early sexual maturation increase male aggression and boldness. Aggression and dominance relations were estimated in dyadic contests, whereas boldness was measured as a response to simulated predation risk using a model heron. Independent of maturity state, males initiated more than twice as many agonistic interactions as females in intersexual contests. However, males were not significantly more likely to win these contests than females. The response to a first predator attack did not differ between sex categories, but males reacted less to a second predator attack than females. Sexual maturity did not affect the antipredator response in males. Since there is no evidence from field studies that stream-living immature male and female salmonids differ in growth rate, it appears unlikely that the sex differences demonstrated are behavioural consequences of sex-specific investment in growth. It seems more likely that sex-specific behaviour arises as a correlated response to sexually selected gene actions promoting differential behaviour in adult males and females during reproduction. Alternatively, sex differences may develop gradually during juvenile life, because a gradual developmental program should be less costly than a sudden behavioural change at the onset of sexual maturity.     

Differences in Aggressiveness in the Midas Cichlid Fish (Cichlasoma citrinellum) in Relation to Sex,Reproductive State and the Individual

The Midas cichlid, Cichlasoma citrinellum, is monogamous and biparental. Because of competition for limited spawning sites and intense predation on their young, vigorous defense of their territory is essential. Although both sexes engage in defense, they differ in aggressiveness. The aggressive responses of both sexes were measured by counting the number of bites and bumps each fish directed toward its own mirror image. The size of the fish's genital papilla was also recorded to estimate its reproductive state. Compared with females, males had higher median mirror scores with greater variance. The scores of individual males were also more consistent through time than were those of females. Females close to spawning had the highest mirror scores, whereas male scores were highest early in the reproductive cycle. Selection has apparently favored aggressiveness in both sexes. We argue, however, that differences in aggression are the result of selection acting dissimilarly on the two sexes.     

Interpopulation Differences in Shoaling Behaviour in Guppies (Poecilia reticulata): Roles of Social Environment and Population Origin

In Trinidad, guppies (Poecilia reticulata) in high‐predation localities show more cohesive shoaling behaviour than those living with less dangerous predators in low‐predation sites. We evaluated the relative contributions of population origin (i.e. genetic and/or maternal effects) and social environment on the expression of shoaling by assessing the behaviour of juveniles reared in a range of social conditions. Focal individuals, offspring of guppies from populations from high‐ or low‐predation localities, were reared in a multifactorial experiment; we created four different social conditions by manipulating the source and demography of the conspecific residents with whom focal individuals interacted. We found that high‐predation fish displayed a stronger propensity to shoal than low‐predation ones. Our results also suggest a role for interactions between the source of the focal individuals, the demography of the group in which they were reared and the origin of the guppies with whom they were reared. Depending on their origin (high‐ vs. low‐ predation) and rearing density, our focal fish were more likely to shoal if they were reared with high‐predation residents. Learning from high‐predation residents, aggressive interactions with low‐predation residents and/or phenotype matching could have played a role in driving this effect of social environment. This effect of the phenotype of conspecifics on shoaling development would enhance heritable differences in shoaling propensity such that both could contribute to the well‐documented difference in shoaling behaviour of high‐ and low‐predation guppies in natural populations.     

Geographic variation in multiple paternity within natural populations of the guppy (Poecilia reticulata)

Mating can increase an individual''s risk of mortality by predation. In response to predation hazards, males in some species court females less often, but alternatively engage in coerced copulations more frequently and females become less selective. Such predator-mediated shifts in mating tactics may result in higher levels of multiple inseminations in females and, thus, in greater frequencies of females with broods of mixed paternity. We tested this hypothesis using two polymorphic microsatellite loci to estimate conservatively multiple paternity in broods of female guppies (Poecilia reticulata) originating from ten natural populations that have evolved under different fish predation regimes in Trinidad. The frequency of broods that were multiply sired was significantly greater on average in populations experiencing high predation pressure compared to populations experiencing a relatively low predation risk. These results suggest that the intensity of male sperm competition covaries geographically with predation pressure in this species and that the local risk of predation mediates the opportunity for sexual selection within populations.