Past threatening experiences, such as exposure to a predator or a capture event, can influence an animal's future behaviour, with profound consequences on its survival and ultimate fitness. We hypothesize that an animal's physiological stress response phenotype modulates the influence of past experiences on future behaviour in the Florida scrub-jay, Aphelocoma coerulescens, a species that exhibits individual physiological stress response phenotypes that are repeatable across a life span. We subjected young, trap-capture-naïve Florida scrub-jays to a standardized capture and restraint protocol to quantify stress-induced levels of circulating glucocorticoids. Twenty-four hours later, we assessed their response to a novel object and compared this measure of neophobia to age-matched individuals that had never been captured in a trap. We predicted that individuals trapped prior to novel object trials would be more neophobic than noncaptured controls. Furthermore, we predicted that scrub-jays with high glucocorticoid responses would be the most neophobic. Indeed, previously captured individuals had longer latencies to approach and enter a novel ring compared to controls. Past trap experience interacted with a bird's physiological phenotype to influence their neophobic behaviour. Contrary to our predictions, trapped birds with a low glucocorticoid response phenotype were more neophobic compared to low response controls, whereas trapped individuals with a high response phenotype where less neophobic compared to high response controls. Our results demonstrate that experience can affect individuals differently depending on their physiological phenotype. This novel finding highlights the need to consider how differential responses to invasive and captive protocols may confound results of behavioural studies involving free-living subjects.

Glucocorticoids are steroid hormones which increase dramatically in response to a physical or perceived stressor. However, developing young of altricial species typically have a damped glucocorticoid stress response. The developmental hypothesis posits that the physiological stress response should develop concurrently with an individual's ability to respond to a challenge. The dampened response may benefit an organism, as chronic exposure to glucocorticoids can have short- and long-term detrimental effects, and altricial young are unable to escape most stressors. However, we do not know if or why species with similar ontogeny vary in their development of the physiological stress response. We assessed levels of baseline and stress-induced corticosterone (the main avian glucocorticoid) in six passerine species with varying life-history strategies, including a brood parasite, the brown-headed cowbird (Molothrus ater). Circulating baseline corticosterone levels increased with nestling age for all species. Stress-induced corticosterone levels sampled at 15-min post-capture significantly increased with nestling age at a similar rate and magnitude in brown-headed cowbirds, eastern phoebes (Sayornis phoebe), hooded warblers (Setophaga citrina), red-winged blackbirds (Agelaius phoeniceus), and song sparrows (Melospiza melodia). However, gray catbird (Dumetella carolinensis) nestlings showed an extremely dampened elevation in corticosterone in response to stress, even near fledge. Gray catbirds are unusual among songbirds, as they are open-ended song learners. Stress during development can profoundly influence avian song learning and performance abilities. However, further study is necessary to determine if there is a relationship between nestling adrenocortical activity and open- versus closed-ended song learning.

Plasma glucocorticoid (CORT) levels collected within 3min of capture are commonly believed to reflect pre-stressor, baseline CORT levels. Differences in these "baseline" values are often interpreted as reflecting differences in health, or the amount of social and environmental stress recently experienced by an individual. When interpreting "baseline" values it is generally assumed that any effect of capture-and-handling during the initial sampling period is small enough and consistent enough among individuals to not obscure pre-capture differences in CORT levels. However, plasma CORT increases in less than 3min post-capture in many free-living, endothermic species in which timing has been assessed. In addition, the rate of CORT secretion and the maximum level attained (i.e., the degree of stress-responsiveness) during a severe stressor often differs among individuals of the same species. In Florida scrub-jays (Aphelocoma coerulescens), an individual's stress-responsiveness during a 30min post-capture stressor is correlated with CORT levels in samples collected within 1.5min of capture, suggesting there is an intrinsic connection between stress-responsiveness and pre-capture CORT levels. Although differences in stress-responsiveness accounted for just 11% of the variance in these samples, on average, higher stress-responsive jays (top third of individuals) had baseline values twice that of lower stress-responsive jays (bottom third). Further, plasma CORT levels begin to increase around 2min post-capture in this species, but the rate of increase between 2 and 3min differs markedly with CORT increasing more rapidly in jays with higher stress-responsiveness. Together, these data indicate that baseline CORT values can be influenced by an individual's stress response phenotype and the differences due to stress-responsiveness can be exaggerated during sample collection. In some cases, the effects of differences in stress-responsiveness and the increase in CORT during sample collection could obscure, or supersede, differences in pre-capture plasma CORT levels that are caused by extrinsic factors.

For decades, scientists have used threat conditioning (traditionally termed 'fear conditioning') to study the link between glucocorticoids and the consolidation of long-term memories (i.e. memories that last hours to weeks) in model organisms in the laboratory. We assessed this relationship in a free-living species, and examined a possible relationship between glucocorticoids and the retention of longlasting memories (i.e. memories that last months to a lifetime). We developed a novel threat-conditioning protocol by which free-living Florida scrub-jays, Aphelocoma coerulescens, were either chased by a novel predator or exposed to a control. We measured flight initiation distance (FID) 48 h, 11 months and 2 years after conditioning or control exposures, and compared these measures to levels of stress-induced glucocorticoids. Conditioned subjects maintained significantly longer FIDs for at least 2 years. Furthermore, the long-term memory consolidation of conditioned subjects positively correlated with their stress-induced glucocorticoid response, similar to results from laboratory studies. Surprisingly, individuals with a moderate stress response exhibited an exaggerated defence response (i.e. FIDs increased) at 11 months and 2 years post-conditioning, whereas low and high stress responders exhibited memory decay or extinction (i.e. FIDs decreased). We speculate that the recently discovered processes of memory reconsolidation and system consolidation may help explain why some Florida scrub-jays exhibit more fearful-like behaviour with time. (C) 2016 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Intraspecies differences are fundamental to natural selection, yet individual differences in cognition in free-living populations have received little attention. Proactive and reactive coping styles describe individual differences in personality and related stress physiology; however, the coping style model can be extended to include predictions regarding measures of cognition. We compared two measures of personality (neophobia and exploratory behaviour) included in the coping style model to cognitive performance on colour-based associative and reversal learning tests in adult Florida scrub-jays, Aphelocoma coerulescens. Also, as exogenous glucocorticoid treatment can affect cognitive performance, we examined whether an individual's naturally occurring physiological phenotype, reflected by corticosterone measures obtained during development and at the time of the learning tests, covaried with learning performance. Performance on associative and reversal learning tests were inversely related. Scrub-jays with low levels of corticosterone as 11-day-old nestlings performed better on an associative learning test as adults, and there was a marginally nonsignificant trend for nestlings with high levels of corticosterone to perform better on a reversal learning test. There was also a marginally nonsignificant trend for neophobic birds to perform better on reversal learning tests. There were no relationships either between adult stress-induced corticosterone levels and learning, or between exploratory behaviour and learning. Our findings provide evidence that variation in sensitivity to environmental conditions, as reflected by an individual's coping style, underlie the specific strategy by which individuals perform cognitive tasks (i.e. cognitive style). Florida scrub-jays experience a trade-off in performance between types of learning that covary with early corticosterone exposure.

We assessed the degree of similarity between signature whistles of mother and offspring pairs in free-living Atlantic spotted dolphins (Stenella frontalis). As a means of qualitative evaluation, judges compared the time-frequency contour patterns of signature whistle spectrograms. We also evaluated quantitative measurements of whistle frequency and duration. All five female offspring produced signature whistles that were similar to their mothers’ whistles by a least one means of comparison, whereas two of the four male offspring produced signature whistles that were dissimilar from their mothers’ by both methods of comparison. However, statistically, male offspring were just as likely to produce signature whistles like their mothers’ as female offspring (p = 0.167). We compared whistle similarity between mothers and offspring to the degree of association for each pair. Offspring that most often associated with their mothers when they were four years of age had whistles that were more similar to their mothers’ whistles both qualitatively (r(4) = 0.92, p = 0.009) and quantitatively (r(4) = 0.92, p = 0.004). Because signature whistles are developed within a dolphin’s first year, our finding likely reflects the level of bond between mother and calf.

Researchers typically study “acute” activation of the hypothalamic–pituitary–adrenal (HPA) axis by measuring levels of circulating glucocorticoids in animals that have been exposed to a predator or a cue from a predator (e.g., odor), or have experienced a standardized capture-and-restraint protocol, all of which are many minutes in duration. However, exposure to predators in the “wild”, either as the subject of an attack or as a witness to an attack, is generally much shorter as most depredation attempts upon free-living animals last <5s. Yet, whether a stimulus lasting only seconds can activate the HPA axis is unknown. To determine if a stimulus of a few seconds triggers a glucocorticoid response, we measured levels of corticosterone (CORT; the primary avian glucocorticoid) in wild-caught European starlings (Sturnus vulgaris) after they witnessed a brief (<2–8s) raptor attack upon a conspecific, a human “attack” (i.e., a researcher handling a conspecific), and an undisturbed control. Witnesses of a raptor attack responded with CORT levels comparable to that induced by a standardized capture-and-restraint protocol. Glucocorticoid levels of individuals following the control treatment were similar to baseline levels, and those that witnessed a human “attack” had intermediate levels. Our results demonstrate that witnessing a predator attack of very brief duration triggers a profound adrenocortical stress response. Given the considerable evidence of a role for glucocorticoids in learning and memory, such a response may affect how individuals learn to recognize and appropriately react to predators.