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.     

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.     

Hunted Woolly Monkeys (Lagothrix poeppigii) Show Threat-Sensitive Responses to Human Presence

Responding only to individuals of a predator species which display threatening behaviour allows prey species to minimise energy expenditure and other costs of predator avoidance, such as disruption of feeding. The threat sensitivity hypothesis predicts such behaviour in prey species. If hunted animals are unable to distinguish dangerous humans from non-dangerous humans, human hunting is likely to have a greater effect on prey populations as all human encounters should lead to predator avoidance, increasing stress and creating opportunity costs for exploited populations. We test the threat sensitivity hypothesis in wild Poeppigi''s woolly monkeys (Lagothrix poeppigii) in Yasuní National Park, Ecuador, by presenting human models engaging in one of three behaviours “hunting”, “gathering” or “researching”. These experiments were conducted at two sites with differing hunting pressures. Visibility, movement and vocalisations were recorded and results from two sites showed that groups changed their behaviours after being exposed to humans, and did so in different ways depending on the behaviour of the human model. Results at the site with higher hunting pressure were consistent with predictions based on the threat sensitivity hypothesis. Although results at the site with lower hunting pressure were not consistent with the results at the site with higher hunting pressure, groups at this site also showed differential responses to different human behaviours. These results provide evidence of threat-sensitive predator avoidance in hunted primates, which may allow them to conserve both time and energy when encountering humans which pose no threat.     

Using social rank as the lens to focus on the neural circuitry driving stress coping styles

Social hierarchy position in humans is negatively correlated with stress-related psychiatric disease risk. Animal models have largely corroborated human studies, showing that social rank can impact stress susceptibility and is considered to be a major risk factor in the development of psychiatric illness. Differences in stress coping style is one of several factors that mediate this relationship between social rank and stress susceptibility. Coping styles encompass correlated groupings of behaviors associated with differential physiological stress responses. Here, we discuss recent insights from animal models that highlight several neural circuits that can contribute to social rank–associated differences in coping style.     

Loss of gene function and evolution of human phenotypes

Humans have acquired many distinct evolutionary traits after the human-chimpanzee divergence. These phenotypes have resulted from genetic changes that occurred in the human genome and were retained by natural selection. Comparative primate genome analyses reveal that loss-of-function mutations are common in the human genome. Some of these gene inactivation events were revealed to be associated with the emergence of advantageous phenotypes and were therefore positively selected and fixed in modern humans (the “less-ismore” hypothesis). Representative cases of human gene inactivation and their functional implications are presented in this review. Functional studies of additional inactive genes will provide insight into the molecular mechanisms underlying acquisition of various human-specific traits. [BMB Reports 2015; 48(7): 373-379]     

Are behavioral responses to eyespots in sticklebacks influenced by the visual environment? An experimental examination

Eyespots are taxonomically widespread color patterns consisting of large concentric rings that are commonly assumed to protect prey by influencing the behaviors of predators. Although there is ample experimental evidence supporting an anti‐predator function of eyespots in terrestrial animals, whether eyespots have a similar deterring function in aquatic animals remains unclear. Furthermore, studies in terrestrial systems suggest that the protective function of eyespots depends on ambient light conditions where predators encounter them, but this effect has never been tested in aquatic environments. Here, we examine how eyespots influence behavioral responses in an aquatic environment under different visual environments, using laboratory‐reared three‐spined sticklebacks (Gasterosteus aculeatus) as model predators. Specifically, we experimentally examined behavioral responses of sticklebacks toward artificial prey patterns (control vs. eyespots) under two different light environment treatments (low vs. high). We found that eyespots did not postpone attacks from sticklebacks. However, sticklebacks approaching eyespots stopped more frequently than sticklebacks approaching prey items with a control pattern. Sticklebacks were (marginally) slower to attack prey in the low‐light treatment, but the light level did not influence stickleback behavioral responses toward eyespots. We conclude that eyespots can modulate some behaviors of an aquatic predator, albeit with a different functional role from that previously demonstrated in terrestrial species.     

Exposure to a contextually neutral stressor potentiates fear conditioning in juvenile rainbow trout,Oncorhynchus mykiss

Organisms faced with stressors deploy a suite of adaptive responses in the form of behavioral, physiological and cognitive modifications to overcome the challenge. Interactive effects of these responses are known to influence learning and memory processes and facilitation is thought to be dependent, in part, upon contextual relevance of the stressor to the learning task. Predation is one such stressor for prey animals, and their ability to manage reliable information about predators is essential for adaptive antipredator strategies. Here, we investigated (i) the influence cortisol has on the ability of juvenile rainbow trout to learn and retain conditioned antipredator responses to predatory cues, and (ii) whether conditioned behavioral and physiological responses to predator cues are fixed or deployed in a threat-sensitive manner. Trout were fed cortisol-coated pellets minutes prior to a conditioning event where they were exposed to novel predator odor paired with chemical alarm cues (unconditioned stimulus). We tested for conditioned responses by exposing trout to predator cues after 2, 4 or 10 days and subsequently documented physiological and behavioral responses. Both control and cortisol-fed trout learned the predator odor and responded 2 and 4 days post conditioning. However, at 10 days only cortisol-fed trout maintained strong behavioral responses to predator cues. Interestingly, we failed to find conditioned physiological responses to predator odor despite the presence of threat-sensitive cortisol responses to the unconditioned stimulus. Our findings suggest cortisol exposure prior to predator-learning may enhance retention of conditioned responses, even without a contextual link between stressor source and learning task.     

Do Naïve Primates Recognize the Vocalizations of Felid Predators?

Traits that were adaptive under previous conditions may no longer have fitness benefits. However, some species still retain appropriate antipredator behaviors even though they do not coexist with the predators that their ancestors once faced. Studies have examined the responses of a variety of naïve species to these predators, but none have specifically investigated whether naïve primates retain antipredator behaviors against felid predators. We studied the pig‐tailed langur (Simias concolor) to determine whether it still recognizes felids as predators even though dangerous felids do not exist on the islands on which it inhabits. The responses of the langurs to the playbacks of the vocalizations of felids (an ancestral predator), elephants (an unknown animal but not a predator), humans (a known predator) and, pigs and birds (known animals but not predators) were compared. Langurs fled more slowly and looked at the speaker less in response to the felid and elephant calls than they did in response to the human voices. Similar numbers of langurs fled in response to all playback treatments except the pig and bird. The results suggest that langurs are afraid of novel vocalizations but have not retained specific acoustic knowledge of felid predator vocalizations. For long‐lived species that have extended periods of learning, being able to modify general behavioral responses, such as antipredator behaviors, based on individual experiences may be more adaptive than having fixed behavioral strategies.     

Model vs. playback experiments: The impact of sensory mode on predator-specific escape responses in saki monkeys

Although experimentally simulating predator presence helps improve sample sizes in studies of free-ranging animals, few studies have examined whether auditory playbacks and visual models produce similar results. Additionally, it is unclear if anti-predator strategies are specific to predator hunting styles in understudied Neotropical pitheciid primates, limiting what we can generalize about this phenomenon across this taxonomic order. We conducted predator simulation experiments to assess whether wild Rylands' bald-faced saki monkeys (Pithecia rylandsi) recognize predators based solely on acoustic cues, exhibit predator-specific responses to different predator types, and vary responses to presentations in different sensory modes. In our playback experiments, sakis had weak responses to non-predator control vocalizations compared to jaguar growls and harpy eagle shrieks. In most predator playbacks, subjects' first glance corresponded to the direction from which simulated predators would typically attack (above vs. below). However, although sakis exhibited appropriate movement responses to harpy playbacks (i.e., descending canopy), they exhibited no clear movement patterns when presented with jaguar playbacks. In contrast, jaguar model experiments consistently elicited fast approaches, mobbing-style responses, and long alarm calling bouts. Thus, if we had relied on playbacks alone, we might have concluded that sakis have only generalized responses to terrestrial ambush predators. In fact, in all variables measured (e.g., latency, number of calls, and response duration), models of both predator species elicited stronger reactions than playbacks. Results indicate that bald-faced sakis can identify predators based solely on vocalizations, but do not exhibit predator-specific escape responses to terrestrial predators based on acoustic cues alone. The differential response to playbacks and models calls into question the reliability of using acoustic-only stimuli to assess the specificity of anti-predator behavior to predator hunting styles in some primate species.     

Urbanization and biological invasion shape animal personalities

Novel selective pressures derived from human activities challenge the persistence of animal populations worldwide. Behavior is expected to be a major factor driving animals’ responses to global change because it largely determines how animals interact with the environment. However, the role of individual variation in behavior to facilitate the persistence of animals in changing environments remains poorly understood. Here, we adopted an animal personality approach to investigate whether different behavioral traits allow animals to deal with two major components of global change: urbanization and biological invasions. By studying six populations of Anolis sagrei lizards, we found for the first time that anoles vary consistently in their behavior across different times and contexts. Importantly, these animal personalities were consistent in the wild and in captivity. We investigated whether behavioral traits are pulled in different directions by different components of global change. On the one hand, we found that lizards from urban areas differ from nearby forest lizards in that they were more tolerant of humans, less aggressive, bolder after a simulated predator attack, and they spent more time exploring new environments. Several of these risk‐taking behaviors constituted a behavioral syndrome that significantly differed between urban and forest populations. On the other hand, the behavior of urban A. sagrei coexisting with the invasive predatory lizard Leiocephalus carinatus was associated with dramatic changes in their foraging niche. Overall, we provide evidence that differences in animal personalities facilitate the persistence of animals under novel selective regimes by producing adaptive behaviors relevant to their ecology such as predator avoidance. Our results suggest that natural selection can favor certain behaviors over others when animals are confronted with different ecological challenges posed by global change. Therefore, we underscore the need to incorporate behavioral ecology into the study of how animals adaptively respond to human‐induced environmental changes.     

Hormone‐mediated foraging strategies in an uncertain environment: Insights into the at‐sea behavior of a marine predator

1. Hormones are extensively known to be physiological mediators of energy mobilization and allow animals to adjust behavioral performance in response to their environment, especially within a foraging context.
2. Few studies, however, have narrowed focus toward the consistency of hormonal patterns and their impact on individual foraging behavior. Describing these relationships can further our understanding of how individuals cope with heterogeneous environments and exploit different ecological niches.
3. To address this, we measured between‐ and within‐individual variation of basal cortisol (CORT), thyroid hormone T3, and testosterone (TEST) levels in wild adult female Galápagos sea lions (Zalophus wollebaeki) and analyzed how these hormones may be associated with foraging strategies. In this marine predator, females exhibit one of three spatially and temporally distinct foraging patterns (i.e., “benthic,” “pelagic,” and “night” divers) within diverse habitat types.
4. Night divers differentiated from other strategies by having lower T3 levels. Considering metabolic costs, night divers may represent an energetically conservative strategy with shorter dive durations, depths, and descent rates to exploit prey which migrate up the water column based on vertical diel patterns.
5. Intriguingly, CORT and TEST levels were highest in benthic divers, a strategy characterized by congregating around limited, shallow seafloors to specialize on confined yet reliable prey. This pattern may reflect hormone‐mediated behavioral responses to specific risks in these habitats, such as high competition with conspecifics, prey predictability, or greater risks of predation.
6. Overall, our study highlights the collective effects of hormonal and ecological variation on marine foraging. In doing so, we provide insights into how mechanistic constraints and environmental pressures may facilitate individual specialization in adaptive behavior in wild populations.

     

Ontogeny of behavioral traits in commercial sows

As the number of gestating sows reared in group housing increases, a better understanding of behavioral traits needed to negotiate these more complex social interactions promises to increase animal welfare and productivity. However, little is known about different behavioral strategies or coping styles in sows, and even less is understood about their ontogeny. To study the development of coping styles in adult gestating sows, 36 sows from the same sire line and same commercial maternal genetics were followed from birth through their second parity. Each animal was observed in a battery of stress-related behavioral tests at 5 weeks, and 3 months of age as well as 24 h postpartum as a parity 1 sow, and during introduction to subsequent gestation period in group housing. The tests at different ages included response to handling, open field exploration, human interaction, litter handling and social interactions with conspecifics. Many of the observed behaviors were correlated during the same period of the animal’s life and provided the motivation for a principal component analysis by age. Using principal component analysis, multiple traits were determined at each age point; at 5 weeks old: active, non-exploratory and cautious explained 82.5% of the variance; at 3 months of age: active, non-exploratory and low fear of humans explained 87.7% of the variance; and as primiparous sows: active, aggressive/dominant and submissive explained 82.0% of the variance. Several individual juvenile behaviors were associated with adult behavioral traits. For instance, the response to handling at 5 weeks was significantly predictive (β=0.4; P<0.05) of the aggressive/dominant trait of parity 1 sows. Taken together results presented here suggest that early behavioral responses of prepuberal gilts during specific instances of elevated environmental or social stress can predict future behavioral response as gestating sows.     

Human activity helps prey win the predator-prey space race

Predator-prey interactions, including between large mammalian wildlife species, can be represented as a "space race", where prey try to minimize and predators maximize spatial overlap. Human activity can also influence the distribution of wildlife species. In particular, high-human disturbance can displace large carnivore predators, a trait-mediated direct effect. Predator displacement by humans could then indirectly benefit prey species by reducing predation risk, a trait-mediated indirect effect of humans that spatially decouples predators from prey. The purpose of this research was to test the hypothesis that high-human activity was displacing predators and thus indirectly creating spatial refuge for prey species, helping prey win the "space race". We measured the occurrence of eleven large mammal species (including humans and cattle) at 43 camera traps deployed on roads and trails in southwest Alberta, Canada. We tested species co-occurrence at camera sites using hierarchical cluster and nonmetric multidimensional scaling (NMS) analyses; and tested whether human activity, food and/or habitat influenced predator and prey species counts at camera sites using regression tree analysis. Cluster and NMS analysis indicated that at camera sites humans co-occurred with prey species more than predator species and predator species had relatively low co-occurrence with prey species. Regression tree analysis indicated that prey species were three times more abundant on roads and trails with >32 humans/day. However, predators were less abundant on roads and trails that exceeded 18 humans/day. Our results support the hypothesis that high-human activity displaced predators but not prey species, creating spatial refuge from predation. High-human activity on roads and trails (i.e., >18 humans/day) has the potential to interfere with predator-prey interactions via trait-mediated direct and indirect effects. We urge scientist and managers to carefully consider and quantify the trait-mediated indirect effects of humans, in addition to direct effects, when assessing human impacts on wildlife and ecosystems.     

哺乳动物的生理应激反应及其生态适应性

应激反应是哺乳动物的基本生理现象之一。目前,与应激有关的研究主要来自生物医学和神经内分泌学。虽然Hans Selye 提出了个体对应激的普遍性适应综合症概念,但目前的研究还主要集中于应激对个体的负效应以及与应激相关的疾病研究。然而,从进化角度似乎很难理解在数亿年的进化过程中,动物应激反应仅简单地
进化为影响个体健康并导致个体患病的一种生理过程。本文从进化的角度,综述了应激反应与动物繁殖对策的关系以及个体对环境应激源的应对类型,并阐述了动物应激反应的适应和进化意义。     

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.     

Predator-Induced Changes in Metabolism Cannot Explain the Growth/Predation Risk Tradeoff

Defence against predators is usually accompanied by declining rates of growth or development. The classical growth/predation risk tradeoff assumes reduced activity as the cause of these declines. However, in many cases these costs cannot be explained by reduced foraging effort or enhanced allocation to defensive structures under predation risk. Here, we tested for a physiological origin of defence costs by measuring oxygen consumption in tadpoles (Rana temporaria) exposed to predation risk over short and long periods of time. The short term reaction was an increase in oxygen consumption, consistent with the “fight-or-flight” response observed in many organisms. The long term reaction showed the opposite pattern: tadpoles reduced oxygen consumption after three weeks exposure to predators, which would act to reduce the growth cost of predator defence. The results point to an instantaneous and reversible stress response to predation risk. This suggests that the tradeoff between avoiding predators and growing rapidly is not caused by changes in metabolic rate, and must be sought in other behavioural or physiological processes.     

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.     

Failure of captive-born greater rheas (Rhea americana, Rheidae, Aves) to discriminate between predator and nonpredator models

The capacity to recognize and respond to predators can be lost by captive animals. Habituation to humans caused by the captive environment can be transferred to other stimuli, such as predators, a situation that conservation biologists wish to avoid. Greater rheas are threatened South American birds, for which there are plans for reintroduction programs in Brazil. The goal of this study was to evaluate the behavioral responses of captive-born greater rheas to different models of predators and nonpredators. Seventeen captive-born greater rheas, divided into four groups, from the Belo Horizonte Zoo, Brazil were studied. Three predator and three nonpredator models were presented to the birds and their behavioral responses recorded. Predators versus nonpredator models and the behavior of rheas in three experimental phases (baseline, models, and postmodels) were analyzed. Captive-born greater rheas modified their behaviors in the presence of both predator/nonpredator models, increasing alert and wary behaviors (alert, observing, and pacing behaviors: P?<?0.01), showing some degree of antipredator behavior persistence, but they were unable to discriminate between predator and nonpredator models (all behaviors: P?>?0.05). In conclusion, antipredator training should be implemented to develop the expression of this behavior before reintroductions are attempted.     

Costs and benefits of defences induced by predators differing in dangerousness

While theoretical studies predict that inducible defences should be fine-tuned according to the qualities of the predator, very few studies have investigated how dangerousness of predators, i.e. the rate at which predators kill prey individuals, affects the strength of phenotypic responses and resulting benefits and costs of induced defences. We performed a comprehensive study on fitness consequences of predator-induced responses by involving four predators (leech, water scorpion, dragonfly larva and newt), evaluating costs and benefits of responses, testing differences in dangerousness between predators and measuring responses in several life history traits of prey. We raised Rana dalmatina tadpoles in the presence of free-ranging predators, in the presence of caged predators, and exposed naive and experienced tadpoles to free-ranging predators. Tadpoles adjusted the intensities of their behavioural and morphological defences to predator dangerousness. Survival was lower in the nonlethal presence of the most dangerous predator, while we could not detect costs of induced defences at or after metamorphosis. When exposed to free-ranging predators, small, but not large, tadpoles benefited from exhibiting an induced phenotype in terms of elevated survival when compared to naive tadpoles, but we did not observe higher survival either in tadpoles exhibiting more extreme phenotypes or in tadpoles exposed to the type of predator they were raised with. These results indicate that while predator-induced defences can mirror dangerousness of predators, costs and benefits do not necessarily scale to the magnitude of plastic responses.