How integrated are behavioral and endocrine stress response traits? A repeated measures approach to testing the stress-coping style model

It is widely expected that physiological and behavioral stress responses will be integrated within divergent stress‐coping styles (SCS) and that these may represent opposite ends of a continuously varying reactive–proactive axis. If such a model is valid, then stress response traits should be repeatable and physiological and behavioral responses should also change in an integrated manner along a major axis of among‐individual variation. While there is some evidence of association between endocrine and behavioral stress response traits, few studies incorporate repeated observations of both. To test this model, we use a multivariate, repeated measures approach in a captive‐bred population of Xiphophorus birchmanni. We quantify among‐individual variation in behavioral stress response to an open field trial (OFT) with simulated predator attack (SPA) and measure waterborne steroid hormone levels (cortisol, 11‐ketotestosterone) before and after exposure. Under the mild stress stimulus (OFT), (multivariate) behavioral variation among individuals was consistent with a strong axis of personality (shy–bold) or coping style (reactive–proactive) variation. However, behavioral responses to a moderate stressor (SPA) were less repeatable, and robust statistical support for repeatable endocrine state over the full sampling period was limited to 11‐ketotestosterone. Although post hoc analysis suggested cortisol expression was repeatable over short time periods, qualitative relationships between behavior and glucocorticoid levels were counter to our a priori expectations. Thus, while our results clearly show among‐individual differences in behavioral and endocrine traits associated with stress response, the correlation structure between these is not consistent with a simple proactive–reactive axis of integrated stress‐coping style. Additionally, the low repeatability of cortisol suggests caution is warranted if single observations (or indeed repeat measures over short sampling periods) of glucocorticoid traits are used in ecological or evolutionary studies focussed at the individual level.     

Lack of social preference between unfamiliar and familiar juvenile Port Jackson sharks Heterodontus portusjacksoni

This study investigated whether captive-reared juvenile Port Jackson sharks Heterodontus portusjacksoni choose to aggregate and if familiarity is one of the mechanisms driving social preference. In a controlled binary-choice experiment, juvenile sharks were given the option to associate or not with unfamiliar conspecifics, or to associate or not with familiar conspecifics. In neither group did juvenile H. portusjacksoni actively choose to associate with conspecifics, but familiarity decreased the proportion of time spent near a conspecific only during the initial phase of the experiment. Treatment (1 or 3 shoal mates), sex and size had no effect on aggregation behaviour. These findings suggest that familiarity is not a driver of social preferences in juvenile H. portusjacksoni, contrary to results in another shark species. Additionally, adult H. portusjacksoni form large aggregations during the breeding season and actively associate with familiar sex and size-matched individuals, thus our results suggest the species undergoes an ontogenetic shift in social behaviour.     

From egg to hatchling: preferential retention of fatty acid biomarkers in young‐of‐the‐year Port Jackson sharks Heterodontus portusjacksoni

The muscle and liver fatty acid composition of young‐of‐the‐year (YOY) Port Jackson sharks Heterodontus portusjacksoni were investigated to determine the effects of a known dietary lipid source v. maternal input as demonstrated by egg yolk fatty acid profiles. Ten Heterodontus portusjacksoni egg yolks were collected in situ and compared with four hatched H. portusjacksoni fed a known diet in a controlled feeding experiment of 185 days. This study demonstrated that fatty acids are probably conservatively transferred from egg yolks to YOY H. portusjacksoni, while diet did not have a large effect on the fatty acid composition of the liver or muscle.     

Does individual personality predict male mating preference for female body size in the Trinidadian guppy?

Within populations, individual animals vary considerably in their behaviour, including mate choice and personality. There is mounting interest in the potential covariation between these two behaviours within individuals, such that personality would influence mate choice. We experimentally tested this proposition under controlled laboratory conditions using male Trinidadian guppies (Poecilia reticulata) as a model study system. We assayed repeatedly the mating preference of individual males for females based on their body size. Additionally, we assayed repeatedly two ecologically relevant personality traits in males, namely exploration of a novel environment and boldness under a simulated predation threat. Finally, we analysed whether male mating preference and personality traits were repeatable, and tested whether the personality of individual males was correlated (covaried) with their mating preference scores. Although all but one of the measures of exploration and boldness behaviour were repeatable over time, male mating preference scores were not repeatable. Measures of male exploration and boldness were not inter-correlated among individuals, suggesting the absence of a behavioural syndrome between exploration and boldness. Unexpectedly, males did not exhibit on average a significant mating preference for larger females over smaller ones; they chose randomly between the paired stimulus females. Overall, we found no compelling evidence for a relationship between individual personality traits and mating preference in male guppies, suggesting that personality does not predict mate choice, at least in our study population and under our experimental conditions. We discuss potential factors, other than male personality and body length, that might maintain inter-individual variation in male mating preferences in the guppy in the wild.     

On the Validity of a Single (Boldness) Assay in Personality Research

A common method to assess behavioral types in personality research involves the use of a single emergence test (employed by researchers working on fish, avian, mammal, amphibian, and invertebrate taxa), whereby a shorter latency to emerge from a holding container into a novel environment is inferred to represent greater ‘boldness’. Although any behavior might be context specific, studies using this single assay type must assume it reflects boldness in other similar contexts, otherwise it cannot reflect personality (defined as consistency across time and/or contexts). We attempted to validate whether a single assay of this type is correlated with other similar assays of boldness under more familiar, and less stressful, situations. We compared single emergence test scores of two species of damselfish (Pomacentrus wardi; P. amboinensis) in a novel environment, with two different behavioral assays of the same fish in subsequent repeated trials in home tanks. Although behavior was highly repeatable in home tanks, we found no correlation between emergence test scores in the novel environment and measures of latency to emerge from shelter following disturbance, or activity levels, on the first, second, or third observations in home tanks; there was also no correlation when we used average home tank scores from mixed models that accounted for individual differences (i.e., plasticity) in the rate of habituation (latency) and acclimation (activity). Our results therefore lead us to question the validity of using this single emergence test assay as a predictor of general boldness and to question the use of any single assay of behavior in personality research.     

Residency and movement patterns of adult Port Jackson sharks (Heterodontus portusjacksoni) at a breeding aggregation site

Examining the movement ecology of mesopredators is fundamental to developing an understanding of their biology, ecology and behaviour, as well as the communities and ecosystems they influence. The limited research on the residency and movements of benthic marine mesopredators has primarily used visual tags, which do not allow for the efficient and accurate monitoring of individual space use. In this study, the authors investigated the residency and movement patterns of Port Jackson sharks Heterodontus portusjacksoni (Meyer 1793) at a breeding aggregation site in Jervis Bay, south-eastern Australia, using passive acoustic telemetry to further our understanding of the movement ecology of these important mesopredators. Between 2012 and 2014, individuals were tagged with acoustic transmitters, and their residency and movements within the bay were monitored for up to 4 years. H. portusjacksoni showed strong preferences for particular reefs within and between breeding seasons. Males had significantly higher residency indices at their favoured sites relative to females, suggesting that males may be engaging in territorial behaviour. Conversely, female H. portusjacksoni exhibited higher roaming indices relative to males indicating that females may move between sites to assess males. Finally, H. portusjacksoni showed temporal variation in movements between reefs with individuals typically visiting more reefs at night relative to the day, dusk and dawn corresponding with their nocturnal habits.     

The blood respiratory, haematological, acid-base and ionic status of the Port Jackson shark, Heterodontusportusjacksoni, during recovery from anaesthesia and surgery: a comparison with sampling by direct caudal puncture

The effects of caudal cannulation on the blood physiology of the Port Jackson shark, Heterodontus portusjacksoni, were investigated in sharks given between 4 and 72 h to recover from surgery. Neither the Pa_O2–Pv_O2 difference nor the Ca_O2–Cv_O2 difference of cannulated sharks fluctuated throughout the sampling period. The plasma acidosis exhibited 4 h after surgery was partially compensated after 24 h by a respiratory (hyperventilatory) alkalosis and after 72 h by a marked metabolic alkalosis. Whilst H. portusjacksoni exhibited some cell swelling after surgery the haematological status of cannulated sharks generally varied little throughout the recovery period. In contrast, marked changes in plasma and erythrocyte ion concentrations were indicative of increased branchial and erythrocyte ion permeability. The blood status of H. portusjacksoni given 72 h to recover from surgery was also compared with sharks sampled by caudal puncture. The respiratory and acid-base status of sharks sampled by caudal puncture was comparable to that of cannulated sharks. In contrast, the plasma ion concentrations of the cannulated sharks were markedly elevated and the erythrocyte ion concentrations concomitantly reduced when compared with punctured sharks. The apparent increase in the water and ion permeability of cannulated sharks was reflected by the reduced [Hb] and mean cell haemoglobin concentrations (MCHC). Blood sampling by caudal puncture appeared to reduce the haematological and ionic perturbations that resulted from surgery and thus provided a less invasive and reliable method for obtaining samples from ‘non-disturbed’ elasmobranchs.     

Linking fearfulness and coping styles in fish

Consistent individual differences in cognitive appraisal and emotional reactivity, including fearfulness, are important personality traits in humans, non-human mammals, and birds. Comparative studies on teleost fishes support the existence of coping styles and behavioral syndromes also in poikilothermic animals. The functionalist approach to emotions hold that emotions have evolved to ensure appropriate behavioral responses to dangerous or rewarding stimuli. Little information is however available on how evolutionary widespread these putative links between personality and the expression of emotional or affective states such as fear are. Here we disclose that individual variation in coping style predicts fear responses in Nile tilapia Oreochromis niloticus, using the principle of avoidance learning. Fish previously screened for coping style were given the possibility to escape a signalled aversive stimulus. Fearful individuals showed a range of typically reactive traits such as slow recovery of feed intake in a novel environment, neophobia, and high post-stress cortisol levels. Hence, emotional reactivity and appraisal would appear to be an essential component of animal personality in species distributed throughout the vertebrate subphylum.     

Patterns of Occurrence of Sharks in Sydney Harbour,a Large Urbanised Estuary

Information about spatial and temporal variability in the distribution and abundance of shark-populations are required for their conservation, management and to update measures designed to mitigate human-shark interactions. However, because some species of sharks are mobile, migratory and occur in relatively small numbers, estimating their patterns of distribution and abundance can be very difficult. In this study, we used a hierarchical sampling design to examine differences in the composition of species, size- and sex-structures of sharks sampled with bottom-set longlines in three different areas with increasing distance from the entrance of Sydney Harbour, a large urbanised estuary. During two years of sampling, we obtained data for four species of sharks (Port Jackson, Heterodontus portusjacksoni; wobbegong, Orectolobus maculatus; dusky whaler, Carcharhinus obscurus and bull shark, Carcharhinus leucas). Only a few O. maculatus and C. obscurus were caught, all in the area closest to the entrance of the Harbour. O. maculatus were caught in all seasons, except summer, while C. obscurus was only caught in summer. Heterodontus portusjacksoni were the most abundant species, caught in the entrance location mostly between July to November, when water temperature was below 21.5°C. This pattern was consistent across both years. C. leucas, the second most abundant species, were captured in all areas of Sydney Harbour but only in summer and autumn when water temperatures were above 23°C. This study quantified, for this first time, how different species utilise different areas of Sydney Harbour, at different times of the year. This information has implications for the management of human-shark interactions, by enabling creation of education programs to modify human behaviour in times of increased risk of potentially dangerous sharks.     

Physiological and genetic correlates of boldness: characterising the mechanisms of behavioural variation in rainbow trout, Oncorhynchus mykiss

Bold, risk-taking animals have previously been putatively linked with a proactive stress coping style whereas it is suggested shyer, risk-averse animals exhibit a reactive coping style. The aim of this study was to investigate whether differences in the expression of bold-type behaviour were evident within and between two lines of rainbow trout, Oncorhynchus mykiss, selectively bred for a low (LR) or high (HR) endocrine response to stress, and to link boldness and stress responsiveness with the expression of related candidate genes. Boldness was determined in individual fish over two trials by measuring the latency to approach a novel object. Differences in plasma cortisol concentrations and the expression of eight novel candidate genes previously identified as being linked with divergent behaviours or stress were determined. Bold and shy individuals, approaching the object within 180 s or not approaching within 300 s respectively, were evident within each line, and this was linked with activity levels in the HR line. Post-stress plasma cortisol concentrations were significantly greater in the HR line compared with the LR line, and six of the eight tested genes were upregulated in the brains of LR fish compared with HR fish. However, no direct relationship between boldness and either stress responsiveness or gene expression was found, although clear differences in stress physiology and, for the first time, gene expression could be identified between the lines. This lack of correlation between physiological and molecular responses and behavioural variation within both lines highlights the complexity of the behavioural-physiological complex.     

Examining the link between personality and laterality in a feral guppy Poecilia reticulata population

This study examined whether variation in the strength and direction of lateralization in a detour task was linked with variation in three common personality measurements: boldness, activity and sociability, in a population of wild guppies Poecilia reticulata. Additionally, the aim was to determine whether any consistent correlations between these behavioural traits, known as behavioural syndromes, were present in the study population. The results revealed that all three personality traits were highly repeatable over time in both sexes. Evidence of a complex syndrome in the form of a correlation between boldness, sociability and activity was found; however, this relationship was only present in males. Males that were more active in a familiar environment emerged more quickly from shelter into a novel environment and were more social. In general, male P. reticulata were bold, active and antisocial compared to females, with these differences probably a reflection of opposing life‐history strategies. Only a weak link between the strength of cerebral lateralisation and personality was discovered and this was mediated by sex.     

Stress coping styles and singing behavior in the short-tailed singing mouse (Scotinomys teguina)

Stress coping styles have been characterized as a proactive/reactive dichotomy in laboratory and domesticated animals. In this study, we examined the prevalence of proactive/reactive stress coping styles in wild-caught short-tailed singing mice (Scotinomys teguina). We compared stress responses to spontaneous singing, a social and reproductive behavior that characterizes this species. To establish proactive/reactive profiles for singing mice, we measured exploratory and anxiety behavior using an open-field behavioral test. We examined correlations between open-field behaviors and fecal corticosterone (CORT) metabolites, baseline plasma CORT, and stress-induced CORT. Mice with proactive behavioral responses in the open-field had higher fecal CORT titers than reactive males, but did not differ in baseline or stress-induced plasma CORT. We suggest that individual differences in CORT metabolism may contribute to this surprising pattern. Males that sang in the open-field were behaviorally proactive and had lower stress-induced CORT, indicating a link between stress responses and singing in this species. Overall, the data demonstrate that singing mice offer an interesting model for exploring how stress reactivity can shape social behaviors.     

Long-term behavioral repeatability in wild adult and captive juvenile turtles (Terrapene carolina): Implications for personality development

Animal personality can be defined as conspecific individuals consistently differing in behavioral tendencies. Personality is typically identified by behavioral repeatability, which occurs when within-individual variance is low relative to among-individual variance in the population. Intraspecific comparisons of behavioral repeatability in juveniles and adults within and across years are rare, but would be useful for testing hypotheses related to origins of animal personality and whether individuals exhibit stable or diverging behavior with ontogeny. To examine within- and across-year behavioral repeatability for eastern box turtles (Terrapene carolina), we assessed boldness (movement latency after brief confinement) of captive-born juveniles twice within three days when eight months old. We then repeated these tests for the same individuals one year later. Juveniles exhibited repeatable boldness within and across years. Although increasing body temperature was slightly associated with decreased movement latency, test year (1 or 2), or housing experience (being raised in an enriched or unenriched condition) had no effects on boldness. We also assessed across-year repeatability of boldness (head emergence from the shell after brief confinement) for wild adults at 1–3 year intervals. Adults also exhibited repeatable across-year boldness that was of similar magnitude to juveniles. We found no indication that sex class or whether adults had been radio-tracked influenced boldness. Our results suggest eastern box turtles demonstrate consistent individuality in boldness from an early age that is largely unaffected by temporal or environmental variation, and these behavioral differences can be maintained for multiple years in captivity and the wild, contrasting with theoretical expectations for personality development. These findings add to recent accumulating evidence demonstrating juvenile and adult box turtles exhibit multiple repeatable behaviors over the short- and long-term. We suggest this species is quickly gaining traction as a model organism for studying the proximate and ultimate causes of personality development within long-lived animals.     

Individually assessed boldness predicts Perca fluviatilis behaviour in shoals,but is not associated with the capture order or angling method

Selectivity of recreational angling on fish behaviour was studied by examining whether capture order or lure type (natural v. artificial bait) in ice‐fishing could explain behavioural variation among perch Perca fluviatilis individuals. It was also tested if individually assessed personality predicts fish behaviour in groups, in the presence of natural predators. Perca fluviatilis showed individually repeatable behaviour both in individual and in group tests. Capture order, capture method, condition factor or past growth rate did not explain variation in individual behaviour. Individually determined boldness as well as fish size, however, were positively associated with first entrance to the predator zone (i.e. initial risk taking) in group behaviour tests. Individually determined boldness also explained long‐term activity and total time spent in the vicinity of predators in the group. These findings suggest that individual and laboratory‐based boldness tests predict boldness of P. fluviatilis in also ecologically relevant conditions, i.e. in shoals and in the presence of natural predators. The present results, however, also indicate that the above‐mentioned two angling methods may not be selective for certain behavioural types in comparison to each other.     

Differences in boldness are repeatable and heritable in a long‐lived marine predator

Animal personalities, composed of axes of consistent individual behaviors, are widely reported and can have important fitness consequences. However, despite theoretical predictions that life‐history trade‐offs may cause and maintain personality differences, our understanding of the evolutionary ecology of personality remains poor, especially in long‐lived species where trade‐offs and senescence have been shown to be stronger. Furthermore, although much theoretical and empirical work assumes selection shapes variation in personalities, studies exploring the genetic underpinnings of personality traits are rare. Here we study one standard axis of personality, the shy–bold continuum, in a long‐lived marine species, the wandering albatross from Possession Island, Crozet, by measuring the behavioral response to a human approach. Using generalized linear mixed models in a Bayesian framework, we show that boldness is highly repeatable and heritable. We also find strong differences in boldness between breeding colonies, which vary in size and density, suggesting birds are shyer in more dense colonies. These results demonstrate that in this seabird population, boldness is both heritable and repeatable and highlights the potential for ecological and evolutionary processes to shape personality traits in species with varying life‐history strategies.     

Boldness as a consistent personality trait in the noble crayfish, <Emphasis Type="Italic">Astacus astacus</Emphasis>

Consistent individual differences in behavioural responses to perceived predation risk may have extensive ecological and evolutionary implications. We studied the repeatability of boldness across time and its relation to resource holding potential in the noble crayfish, Astacus astacus L., using predator-naïve immature individuals. We followed individual’s shelter use both with and without exposure to the chemical and physical cues of predators, and with and without the presence of a conspecific. In addition, we examined if armament, i.e. relative chelae size, would be correlated with individual differences in behaviour. Individuals showed repeatable behaviours across time and context. Individuals that occupied the shelter in competitive dyadic tests also spent more time in the shelter during individual control observations, suggesting that boldness is a personality trait that does not necessarily relate positively to high resource holding potential in the noble crayfish. The relative size of chelae did not correlate with any of the measured behavioural variables. Our results suggest that boldness can be considered as individually consistent and ecologically important personality trait in the noble crayfish.     

Blood cortisol concentrations predict boldness in juvenile mulloway (Argyosomus japonicus)

There is a growing interest in animal personality because individual variation is the substrate of the evolutionary process. Despite revelations that personality traits affect key fitness variables, little is known about the proximate mechanisms generating consistent behavioural differences between individuals. Boldness, the propensity to take risks, is one of the most widely studied aspects of personality in fishes. We assessed the position of juvenile Argyosomus japonicus on the ??boldness?Cshyness?? continuum by repeatedly recording the time taken to exit a refuge and explore a novel environment. Stress-related hormone concentrations after exposure to a mild stressor were analysed 1?month before behavioural assays and found to be significantly linked to boldness scores. Shy fish had significantly higher plasma cortisol concentrations in response to handling stress than bold fish. Spontaneous switching between personality categories occurred between trials, highlighting the importance of repeated testing of personality traits over time to correctly attribute personality.     

Sequential hermaphroditism and personality in a clonal vertebrate: the mangrove killifish

Individuals are regularly documented to consistently differ in their behavioural types (BTs). For example, some individuals are bold whereas others are shy. Within the human personality literature, the big five personality dimensions are commonly documented to be sex-specific with testosterone suggested to underpin traits such as aggressiveness. In non-human animals recent research suggests sex-specific BT expression may be influenced by ecology, mating system and sexual selection. While most research on sex-specific personality has focused on dioecious species, we explore sex differences in BT expression in a sequential hermaphrodite the mangrove killifish. We replicate within 7 isogenic genotypes and investigate sex differences (hermaphrodite and secondary male) in three BTs (exploration, boldness and aggression). This approach allows us to investigate sex differences in BT expression whilst controlling for genetic variation. In this study we find that both secondary males and hermaphrodites are repeatable at the individual level yet there was no difference between the sexes in average BT scores. Furthermore, aggression scores differed between genotypes, and were repeatable at the genotype level, suggesting strong genetic control. Finally, male boldness was significantly more repeatable than hermaphrodites potentially supporting recent proposals relating to sexual selection. We document a behavioural syndrome in male fish with bolder individuals being more aggressive, this behavioural syndrome was not observed however in hermaphrodites. In contrast to a previous developmental study in this species exploration did not correlate with either aggression or boldness in either males or hermaphrodites.     

Stability in Activity and Boldness Across Time and Context in Captive Siberian Dwarf Hamsters

Individual personality is an important source of variation in animal behavior. However, few studies have examined the reliability of individual behaviors across both time and context for even common temperament traits such as boldness, especially in mammals. We tested a laboratory colony of Siberian dwarf hamsters (Phodopus sungorus) in two similar assays, a tunnel maze and an open field, both provisioned with a home nestbox for shelter. Animals were tested in each assay at three ages, beginning at weaning. Principal components analysis on each assay identified an axis of activity level in both tests, boldness and reactivity in the tunnel maze, and nestbox orientation in the open field. All traits were moderately (7–18%) heritable. Individual activity level was the most reliably consistent trait, both within and between tests. Tunnel maze boldness, tunnel maze reactivity, and open field nestbox orientation did not correlate at any age. Correlation between boldness and activity changes from positive to negative as animals age, while reactivity was consistently negatively associated with activity. A negative correlation emerged in adults between open field activity and nestbox orientation. These results suggest that either development or habituation results in different personality trait associations in an individual over time. Individual temperament traits such as general activity level may be quite stable, but caution should be used in generalizing single assays to represent boldness across time and across contexts.