Three different coping styles in police dogs exposed to a short-term challenge

According to some researchers, animals show different coping styles to deal with stressful situations. In the case of social carnivores, social stress is a substantial part of the overall stress load. Previous research has established two extreme (proactive and reactive) coping styles in several animal species, but means of coping with social stress has not yet been investigated in the case of dogs. The aim of this current study was to examine whether (1) experienced working police dogs adopt different coping strategies during a short-term unexpected social challenge presented by a threatening human, (2) whether this affects post-encounter cortisol levels, and (3) whether there is an association between the cortisol response and the behavior (coping strategy) displayed during the threatening approach. Using factor analysis, we have identified three different group of dogs which were characterized by either fearfulness, aggressiveness, or ambivalence and in parallel showed specific differences in their reaction norm when threatened by an approaching stranger. This grouping also allowed to draw possible parallels between aggressiveness and the proactive behavior style and fearfulness and reactive coping style, respectively. In addition, we have revealed a third group of animals which show ambivalent behavior in a social threatening situation.     

Three different coping styles in police dogs exposed to a short-term challenge

According to some researchers, animals show different coping styles to deal with stressful situations. In the case of social carnivores, social stress is a substantial part of the overall stress load. Previous research has established two extreme (proactive and reactive) coping styles in several animal species, but means of coping with social stress has not yet been investigated in the case of dogs. The aim of this current study was to examine whether (1) experienced working police dogs adopt different coping strategies during a short-term unexpected social challenge presented by a threatening human, (2) whether this affects post-encounter cortisol levels, and (3) whether there is an association between the cortisol response and the behavior (coping strategy) displayed during the threatening approach. Using factor analysis, we have identified three different group of dogs which were characterized by either fearfulness, aggressiveness, or ambivalence and in parallel showed specific differences in their reaction norm when threatened by an approaching stranger. This grouping also allowed to draw possible parallels between aggressiveness and the proactive behavior style and fearfulness and reactive coping style, respectively. In addition, we have revealed a third group of animals which show ambivalent behavior in a social threatening situation.     

Stress coping style predicts aggression and social dominance in rainbow trout

Social stress is frequently used as a model for studying the neuroendocrine mechanisms underlying stress-induced behavioral inhibition, depression, and fear conditioning. It has previously been shown that social subordination may result in increased glucocorticoid release and changes in brain signaling systems. However, it is still an open question which neuroendocrine and behavioral differences are causes, and which are consequences of social status. Using juvenile rainbow trout of similar size and with no apparent differences in social history, we demonstrate that the ability to win fights for social dominance can be predicted from the duration of a behavioral response to stress, in this case appetite inhibition after transfer to a new environment. Moreover, stress responsiveness in terms of confinement-induced changes in plasma cortisol was negatively correlated to aggressive behavior. Fish that exhibited lower cortisol responses to a standardized confinement test were markedly more aggressive when being placed in a dominant social position later in the study. These findings support the view that distinct behavioral-physiological stress coping styles are present in teleost fish, and these coping characteristics influence both social rank and levels of aggression.     

Genetic differences in coping strategies in response to prolonged and repeated restraint in Japanese quail divergently selected for long or short tonic immobility

Exposure to fearful situations elicits behavioral and Hypothalamic–Pituitary–Adrenal (HPA) axis responses characteristic of the coping response of individual animals to counteract environmental challenges. The aim of this study was to investigate behavioral and corticotropic responses concomitantly following prolonged or repeated restraint stress by placing two genotypes of Japanese quail divergently selected for long (LTI) or short (STI) duration of tonic immobility (TI) in a crush cage. In our study, STI quail exhibited higher corticosterone (CORT) levels than LTI quail in response to prolonged restraint. STI quail struggled sooner and much more than LTI quail, and struggling behavior in STI quail progressively decreased during the course of restraint whereas LTI quail displayed very little struggling behavior in the crush cage. LTI quail are thus more likely to adopt a passive behavior coping strategy upon exposure to threat whereas STI quail behave more as active copers. The corticosterone responses shown by LTI and STI quail under restraint stress suggest that adrenocortical correlates of coping behavior in these genotypes of quail may be different from the coping styles previously described in other species. Repeated restraint slightly decreased CORT responses to stress in all experimental groups, but more markedly in male STI quail, whereas adrenal sensitivity and maximum adrenal corticosterone response capacity did not change in any group. On the other hand, neither behavioral habituation nor sensitization processes occurred in the context of repeated restraint in female and male LTI quail and female STI quail, whereas the decreases observed in some behavioral responses were interpreted to be the result of a habituation process in male STI quail.     

Genetic differences in coping strategies in response to prolonged and repeated restraint in Japanese quail divergently selected for long or short tonic immobility

Exposure to fearful situations elicits behavioral and Hypothalamic–Pituitary–Adrenal (HPA) axis responses characteristic of the coping response of individual animals to counteract environmental challenges. The aim of this study was to investigate behavioral and corticotropic responses concomitantly following prolonged or repeated restraint stress by placing two genotypes of Japanese quail divergently selected for long (LTI) or short (STI) duration of tonic immobility (TI) in a crush cage. In our study, STI quail exhibited higher corticosterone (CORT) levels than LTI quail in response to prolonged restraint. STI quail struggled sooner and much more than LTI quail, and struggling behavior in STI quail progressively decreased during the course of restraint whereas LTI quail displayed very little struggling behavior in the crush cage. LTI quail are thus more likely to adopt a passive behavior coping strategy upon exposure to threat whereas STI quail behave more as active copers. The corticosterone responses shown by LTI and STI quail under restraint stress suggest that adrenocortical correlates of coping behavior in these genotypes of quail may be different from the coping styles previously described in other species. Repeated restraint slightly decreased CORT responses to stress in all experimental groups, but more markedly in male STI quail, whereas adrenal sensitivity and maximum adrenal corticosterone response capacity did not change in any group. On the other hand, neither behavioral habituation nor sensitization processes occurred in the context of repeated restraint in female and male LTI quail and female STI quail, whereas the decreases observed in some behavioral responses were interpreted to be the result of a habituation process in male STI quail.     

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.     

Effects of aversive experience on the behavior within a custom-made plus maze in the short-tailed fruit bat, Carollia perspicillata

Stress exposure evokes a variety of physiological and behavioral responses in an organism, enabling it to cope with stressful situations and changes in the environment. In a previous study, we found that subjecting individuals of Carollia perspicillata to a chronic immobilization stress paradigm resulted in a significant increase of fecal cortisol concentrations. In the present study, we investigated the influence of stress on the behavior of C. perspicillata, by adapting a commonly used behavioral paradigm for characterizing coping styles of animals (i.e., the elevated-plus maze) to bats. Adult bats were subjected 1?h/day to immobilization over a period of 10?days. On the subsequent day, the behavior of each animal was analyzed in a custom-made plus maze, consisting of four arms (two open and two enclosed ones) and designed 3D because of the bats' ability to fly. In this newly invented design, we compared the behaviors of stressed animals and controls. Changes in locomotor and exploratory behavior suggest two divergent adaptive behaviors in C. perspicillata following the chronic stress paradigm, possibly indicating different stress coping styles.     

Effects of predictable and unpredictable food restriction on the stress response in molting and non-molting European starlings (Sturnus vulgaris)

This study tested whether an ethologically relevant stressor, a three-week period of food restriction where food was unavailable for four hours a day, caused chronic stress in molting and non-molting captive European starlings. Although all birds increased weight during the Food Restriction period, only non-molting birds increased food intake. Morning baseline heart rates increased during the Food Restriction period and all birds showed a decrease in heart rate when food was absent from the cage. In non-molting birds, there were no differences in either baseline or stress-induced corticosterone (CORT) concentrations, whereas molting birds showed attenuated baseline CORT, stress-induced CORT, and fecal glucocorticoid metabolite levels over the Food Restriction period. Although several parameters, such as increased morning heart rate, are consistent with chronic stress, the majority of these data suggest that restricting food availability is not chronically stressful. Furthermore, making the timing of food removal less predictable by randomizing when food was removed during the day did not enhance any of the above responses, but did alter the frequency of maintenance and feeding behaviors. In conclusion, starlings appear resistant to developing symptoms of chronic stress from repeated food restriction.     

Effects of maternal stress coping style on offspring characteristics in rainbow trout (Oncorhynchus mykiss)

Maternal size, age, and allostatic load influence offspring size, development, and survival. Some of these effects have been attributed to the release of glucocorticoids, and individual variation in these stress hormones is related to a number of traits. Correlated traits are often clustered and used to define the proactive and reactive stress coping styles. Although stress coping styles have been identified in a number of animal groups, little is known about the coupling between stress coping style and offspring characteristics. In the present study, plasma cortisol levels in ovulated mothers and cortisol levels in non-fertilized eggs from two rainbow trout (Oncorhynchus mykiss) strains selected for high (HR) and low (LR) post-stress plasma cortisol levels were compared. Offspring characteristics such as egg size, larval growth, and energy reserves also were compared between the two strains. Maternal plasma and egg cortisol levels were correlated, but no difference between the HR and LR strains was detected in either parameter. LR females produced larger eggs, and larvae with larger yolk sacs compared to HR females, however no differences in larval body size (excluding the yolk) was detected between strains. Considering that the HR and LR strains have a number of correlated behavioral and physiological traits that resemble the reactive and proactive stress coping styles, respectively, the results suggest that proactive mothers invest more energy into their offspring, producing larvae with larger energy reserves. It is possible that larger energy reserves in proactive larvae support the energy requirement for establishing and defending territory in salmonid fish. Furthermore, in the present study we found a positive relationship between mother plasma cortisol and egg cortisol; however neither mother plasma cortisol nor egg cortisol differed between strains. These results indicate that cortisol endowment from the mother to the offspring plays a minor role in the transfer of the behavioral and physiological traits which separates these strains.     

Behavioral and adrenocortical responses to mate separation and reunion in the zebra finch

The adaptive value of social affiliation has been well established. It is unclear, however, what endogenous mechanisms may mediate affiliative behavior. The Australian zebra finch (Taeniopygia guttata) breeds colonially and adults maintain lifelong pair bonds that may be disrupted in the wild due to high mortality rates. Many of its natural, social behaviors are maintained in laboratory conditions, making this species well suited for studying the mechanisms of affiliation. This study examines the behavioral and neuroendocrine responses to pair mate separation and reunion in zebra finches. We measured plasma corticosterone (CORT) and behavioral changes following separation from a pair bonded mate, and again upon reintroducing the mate or an opposite-sex cagemate. Plasma CORT concentrations were: (1). elevated during pair mate separation, even in the presence of other same-sex individuals, and (2). reduced to baseline upon reunion with the pair mate but not upon re-pairing with a new opposite-sex partner. These findings show that zebra finches exhibit hormonal responses to separation and reunion specifically with a bonded pair mate and not with other familiar conspecifics. In addition, alterations in behavior during separation and reunion are consistent with monogamous pair bond maintenance. This study presents evidence for adrenocortical involvement in avian pair bonding, and for hypothalamic-pituitary-adrenal activation in response to an ecologically relevant social stressor.     

Interaction effects of corticosterone and experience on aggressive behavior in the green anole lizard

Aggressive encounters are accompanied by a release of stress hormone, and this corticosterone (CORT) secretion could influence aggressive behavior in subsequent encounters. We investigated the modulating effects of CORT on aggressive behavior in the context of a 5-day social experience in male green anole lizards. In Experiment 1, we measured plasma CORT levels in animals that were exposed for different times to aggressive males. In Experiment 2, using metyrapone, a CORT synthesis blocker, we tested whether CORT secretion in response to the aggressive stimulus plays a role in experience-dependent facilitation of aggressive behavior. We hypothesized that aggressive encounters would increase plasma CORT levels, and that blocking CORT synthesis with metyrapone treatment during the aggressive encounter would cause an animal to become more aggressive. We also tested whether blocking CORT would interfere with the influence of 5-day social experience on animals' behavior in a subsequent aggressive encounter. Animals that were exposed to another male showed higher plasma CORT levels immediately after the 10 min encounter than animals exposed to the non-social video, and this high level was maintained through day 5. Within the aggressive video groups, in Experiment 2, there was a distinctly different pattern in displays depending on drug condition: vehicle-injected animals showed gradual increases followed by decreases in aggressive behavioral responses to the video as the five days proceeded (habituation), while animals injected with metyrapone started out with high aggressive behavior and did not decrease behavioral responses at later trials (no habituation). Finally, when tested with a novel conspecific on day 6, animals previously injected with metyrapone showed no higher aggression than did animals previously injected with vehicle and exposed to the aggressive video. These results suggest that blocking CORT synthesis during the exposure to the aggressive video induced animals to remain aggressive toward the repetitive stimulus without habituating, while not becoming more aggressive than controls toward a novel challenger.     

Variation in singing style use in the reed bunting Emberiza schoeniclus: influencing factors and possible functions

The two main functions of bird song are territory defence and mate attraction. Considerable progress has been made in understanding how species adjust the use of songs to serve these and other (presumed) functions of bird song, but the striking variety of singing behavior observable in wild birds remains enigmatic. Some species make do with simple songs and small repertoires, while others show large, complex repertoires and still others have evolved several distinct singing styles. In most species with distinct singing styles, however, the functions of singing styles are poorly understood. Two distinct singing styles (type I and II, respectively) have long been known in the reed bunting Emberiza schoeniclus, while a new third one has recently been reported to exist. We first quantitatively investigated the evidence for the existence of three singing styles. Then, we tested predictions of the mate attraction hypothesis, the mate guarding hypothesis and the territory defence hypothesis by examining the relations between singing style use with social and temporal factors. Cluster and discriminant analyses supported the existence of three (instead of two) singing styles, which could be differentiated based on four variables referring to song structure and complexity. Use of singing styles was related to male mating status (consistent with the mate attraction hypothesis), but not to female breeding stage (no support for the mate guarding hypothesis). Finally, use of singing styles differed in relation to time of day, with the dawn chorus of paired reed buntings consisting almost exclusively of songs of the recently discovered type III singing style and daytime singing primarily consisting of songs of long‐known type I (in unpaired males) or II singing styles (in paired males). Our findings suggest that one singing style (type I) primarily serves to attract a social mate, although an additional territorial function of this singing style cannot be dismissed. The function(s) of the other two singing styles, both only sung by paired males, are not related to attraction of a social mate or to the own female's fertility, but appear to be important in the context of territory defence and extra‐pair matings.     

Human protection drives the emergence of a new coping style in animals

Wild animals face novel environmental threats from human activities that may occur along a gradient of interactions with humans. Recent work has shown that merely living close to humans has major implications for a variety of antipredator traits and physiological responses. Here, we hypothesize that when human presence protects prey from their genuine predators (as sometimes seen in urban areas and at some tourist sites), this predator shield, followed by a process of habituation to humans, decouples commonly associated traits related to coping styles, which results in a new range of phenotypes. Such individuals are characterized by low aggressiveness and physiological stress responses, but have enhanced behavioral plasticity, boldness, and cognitive abilities. We refer to these individuals as “preactive,” because their physiological and behavioral coping style falls outside the classical proactive/reactive coping styles. While there is some support for this new coping style, formal multivariate studies are required to investigate behavioral and physiological responses to anthropogenic activities.

This Essay hypothesizes that when human presence protects wild animals from their natural predators, this predator shield decouples commonly associated traits, resulting in a new range of coping phenotypes, dubbed “preactive.”     

Speed of exploration and risk-taking behavior are linked to corticosterone titres in zebra finches

The existence of consistent individual differences in behavioral strategies ("personalities" or coping styles) has been reported in several animal species. Recent work in great tits has shown that such traits are heritable and exhibit significant genetic variation. Free-living birds respond to environmental stresses by up-regulating corticosterone production. Behavior during mild stress can occur in accordance to two types of coping styles, i.e. active and passive. Using artificially selected lines of zebra finches that vary in the amount of corticosterone produced in response to a manual restraint stressor we ran three "personality" experiments. We show that birds in the different corticosterone lines differ in their exploratory and risk-taking behaviors. There was an increase in exploratory behavior as corticosterone titre increased but only in the low corticosterone line. Birds in high corticosterone line showed greater risk-taking behavior than birds in the other lines. Thus, in general, higher levels of circulating corticosterone following a mild stress result in greater exploratory behavior and greater risk taking. This study shows that lines of animals selected for endocrine hormonal responses differ in their "coping" styles or "personalities".     

Ventilation rates indicate stress-coping styles in Nile tilapia

Behavioural responses to stress can form distinct profiles in a wide range of animals: proactive and reactive profiles or coping styles. Stress responsiveness can also differentiate between the behavioural profiles. The tendency to regain feed intake following transfer to a novel social-isolation tank (the speed of acclimation) can discriminate between proactive or reactive profiles. Consequently, differential stress responsiveness can be linked to this feeding behaviour trait. This study shows that ventilation rates of Nile tilapia, Oreochromis niloticus (L.), correlate with the rate of feeding resumption, following transfer to a novel social-isolation aquarium. Therefore, ventilation rate (VR) indicates coping styles; consequently, VR is a proxy for the way fish will deal with environmental challenges.     

Behavioral and physiological adjustments to new predators in an endemic island species,the Galápagos marine iguana

For the past 5 to 15 million years, marine iguanas (Amblyrhynchus cristatus), endemic to the Galápagos archipelago, experienced relaxed predation pressure and consequently show negligible anti-predator behavior. However, over the past few decades introduced feral cats and dogs started to prey on iguanas on some of the islands. We investigated experimentally whether behavioral and endocrine anti-predator responses changed in response to predator introduction. We hypothesized that flight initiation distances (FID) and corticosterone (CORT) concentrations should increase in affected populations to cope with the novel predators. Populations of marine iguanas reacted differentially to simulated predator approach depending on whether or not they were previously naturally exposed to introduced predators. FIDs were larger at sites with predation than at sites without predation. Furthermore, the occurrence of new predators was associated with increased stress-induced CORT levels in marine iguanas. In addition, age was a strong predictor of variation in FID and CORT levels. Juveniles, which are generally more threatened by predators compared to adults, showed larger FIDs and higher CORT baseline levels as well as higher stress-induced levels than adults. The results demonstrate that this naive island species shows behavioral and physiological plasticity associated with actual predation pressure, a trait that is presumably adaptive. However, the adjustments in FID are not sufficient to cope with the novel predators. We suggest that low behavioral plasticity in the face of introduced predators may drive many island species to extinction.     

Personality and innate immune defenses in a wild bird: Evidence for the pace-of-life hypothesis

We tested the two main evolutionary hypotheses for an association between immunity and personality. The risk-of-parasitism hypothesis predicts that more proactive (bold, exploratory, risk-taking) individuals have more vigorous immune defenses because of increased risk of parasite exposure. In contrast, the pace-of-life hypothesis argues that proactive behavioral styles are associated with shorter lifespans and reduced investment in immune function. Mechanistically, associations between immunity and personality can arise because personality differences are often associated with differences in condition and stress responsiveness, both of which are intricately linked with immunity. Here we investigate the association between personality (measured as proactive exploration of a novel environment) and three indices of innate immune function (the non-specific first line of defense against parasites) in wild superb fairy-wrens Malurus cyaneus. We also quantified body condition, hemoparasites (none detected), chronic stress (heterophil:lymphocyte ratio) and circulating corticosterone levels at the end of the behavioral test (CORT, in a subset of birds). We found that fast explorers had lower titers of natural antibodies. This result is consistent with the pace-of-life hypothesis, and with the previously documented higher mortality of fast explorers in this species. There was no interactive effect of exploration score and duration in captivity on immune indices. This suggests that personality-related differences in stress responsiveness did not underlie differences in immunity, even though behavioral style did modulate the effect of captivity on CORT. Taken together these results suggest reduced constitutive investment in innate immune function in more proactive individuals.     

Stress responses of testosterone and corticosterone-binding globulin in a multi-brooded species,Eurasian Tree Sparrows (Passer montanus): Does CBG function as a mediator?

In avian plasma, testosterone (T) and corticosterone (CORT) compete to bind with corticosterone-binding globulin (CBG). Elevation of CBG may function to "buffer" the tissues against high circulating levels of T and stress-induced levels of CORT. To demonstrate the effects of acute stress on CBG and T levels and their biological functions, we investigated seasonal changes of baseline and stress-induced T and CBG levels in Eurasian Tree Sparrows (Passer montanus) during different life stages using the capture-handling-restraint stress method. Our results show that (1) male sparrows had significantly higher baseline T levels and CBG capacities during the nest building, the first egg-laying, and the first nestling stages, and significantly decreased stress-induced T levels only during the nest building and the first egg-laying stages. They also expressed significantly increased stress-induced CBG capacities during the second nestling stage. (2) Females showed significantly higher baseline CBG capacities but significantly decreased stress-induced CBG capacities during the nest building stage, and females also showed significantly increased stress-induced CBG capacities during the second egg-laying and the second nestling stages. Therefore, the seasonal fluctuations of baseline CBG in both sexes and baseline T in males reflect their adaptive strategies for optimizing their physiological and behavioral states to the life history cycle. The different patterns of stress-induced CBG in females suggest CBG functions as an essential mediator in regulating stress response to unpredictable perturbations. Our results highlight the need for future studies of stress-induced CBG and T levels on a wide range of vertebrate species that vary in different life history stages to gain a full understanding of the mechanisms that underlie biological functions of CBG and T for unpredictable stressors.     

Behavioral and physiological adjustments to new predators in an endemic island species, the Galápagos marine iguana

For the past 5 to 15 million years, marine iguanas (Amblyrhynchus cristatus), endemic to the Galápagos archipelago, experienced relaxed predation pressure and consequently show negligible anti-predator behavior. However, over the past few decades introduced feral cats and dogs started to prey on iguanas on some of the islands. We investigated experimentally whether behavioral and endocrine anti-predator responses changed in response to predator introduction. We hypothesized that flight initiation distances (FID) and corticosterone (CORT) concentrations should increase in affected populations to cope with the novel predators. Populations of marine iguanas reacted differentially to simulated predator approach depending on whether or not they were previously naturally exposed to introduced predators. FIDs were larger at sites with predation than at sites without predation. Furthermore, the occurrence of new predators was associated with increased stress-induced CORT levels in marine iguanas. In addition, age was a strong predictor of variation in FID and CORT levels. Juveniles, which are generally more threatened by predators compared to adults, showed larger FIDs and higher CORT baseline levels as well as higher stress-induced levels than adults. The results demonstrate that this naive island species shows behavioral and physiological plasticity associated with actual predation pressure, a trait that is presumably adaptive. However, the adjustments in FID are not sufficient to cope with the novel predators. We suggest that low behavioral plasticity in the face of introduced predators may drive many island species to extinction.