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Glucocorticoids enhance and suppress heart rate and behaviour in time dependent manner in greylag geese (Anser anser)
Abstract
Stress responses involve autonomic, endocrine and behavioural changes. Each of these responses has been studied thoroughly in avian species, but hardly in an integrative way, in free-living birds. This is necessary to reveal the temporal dynamics of the stress response. Towards that goal, we recorded heart rate (HR) and behaviour in free-ranging male greylag geese (Anser anser) simultaneously over 2h. The geese were subjected to (a) unmanipulated control condition, (b) capture, handling and injection of ACTH, and (c) capture, handling and injection of a saline solution (SHAM). Fecal samples for the non-invasive determination of immuno-reactive glucocorticoid metabolite (BM) concentrations were collected for 7h thereafter. The SHAM control caused a significant BM increase, a transient increase in HR, an initial increase of preening behaviour and a delay in feeding. ACTH treatment, relative to SHAM, produced significantly higher BM concentrations, and activation of "displacement behaviours" such as wing flapping, body shaking and preening. Also, feeding activity as well as resting was postponed and/or lower for a longer period of time after ACTH than after SHAM. ACTH injection had a greater effect than SHAM injection on HR increase in the first hour, but particularly on HR decline in the second hour following the injection. Hence, glucocorticoids had time- and dose-dependent stimulatory and suppressive effects on cardiovascular activity and behaviour. HR dynamics after ACTH actually matched with behavioural dynamics: both were first enhanced and later suppressed, which is in alignment with adaptive stress management involving the fight-flight response and recovery from stress, respectively.
... To do so, we experimentally increased levels of circulating CORT in chick-rearing male Adélie penguins and ilmed the birds to determine their detailed activity budget on the nest. Physiologically relevant changes induced by the CORT-treatment could include a redirection of behaviour from chick care (Almasi et al. 2008;Silverin, 1986) to comfort behaviour (Ainley 1974;Kralj-Fišer et al. 2010) or agonistic (Holmes, 2007) behaviour. Captive Adélie penguins treated with similar CORT pellets were shown to increase their locomotor activity (Spée et al. 2011b). ...
... he treatment decreased nest attentiveness, and increased vocalisations, positive social interactions, and comfort behaviours in CORT-treated birds when compared to controls. Our observations are in agreement with the fact that greylag geese (Anser anser) injected with adrenocorticotrophic hormone (ACTH), which stimulates GC synthesis and secretion, spent more time body-shaking, wing-lapping, and preening than sham-treated birds (Kralj-Fišer et al. 2010). When approached by humans, Adélie penguins shook their head and stretched their body (Ainley 1974) and magellanic penguins (Spheniscus magellanicus) showed increases in defensive head turns (Walker et al. 2006). he behavioural responses of chick-rearing gentoo (Pygoscelis papua), royal (Eudyptes schlegeli), and king penguins (Aptenodytes patagonicus) to pedestrian visitation, which are associated with increased CORT secretion (Fowler 1999; but see Walker et al. 2006), included increased vigilance and agonistic interactions (Holmes 2007). ...
Studying endocrine mechanisms is of particular interest because of the major role played by hormones in mediating interactions between an animal’s physiology, its behaviour, and both predictable and unpredictable regimes of environmental variation. During this PhD, I have investigated the relationships between endocrine status, reproductive performance, and reproductive output in a long-lived polar seabird, the Adélie penguin Pygoscelis adeliae, while integrating environmental parameters for some of the studies. The endocrine status of male penguins was experimentally modified using subcutaneous self-degradable pellets, which released either the hormone or an inhibitor of its secretion. The effects of changes in the levels of several hormones on the parental investment during incubation were assessed, using direct observations and dummy eggs to record incubation parameters. The levels of corticosterone – the so-called stress hormone, prolactin – the parental care hormone, and testosterone – the sexual behaviour and aggressiveness hormone, were manipulated. The effects of increased corticosterone levels on reproductive performance and output were also evaluated during the chick-rearing period. Finally, the behavioural consequences of a moderate elevation of corticosterone levels during the whole breeding cycle were assessed. On the whole, an increase in corticosterone levels decreased reproductive performances and output. Changes in prolactin or testosterone levels affected incubation duration and egg temperature, suggesting a role for these hormones in the control of the timing of breeding. The results prevented in this PhD highlight the fact that the relationship between endocrine status and reproductive performance is dose-, state-, and context-dependant. Our results illustrate the major role of the hormones considered in our studies in the regulation of reproductive effort. They also underline the importance of considering the interactions of organisms with their environment in studies of animal behaviour and ecophysiology.
... Repeatability can provide evidence that among-individual variation is caused by factors intrinsic to the individual (Réale et al. 2007), and thus can help determine whether eider FID is a valid personality trait (e.g., Seltmann et al. 2012Seltmann et al. , 2014, or whether heart rate and FID are phenotypically related to proactive or reactive coping styles in eiders (Koolhaas et al. 1999). In line with this, several studies have related individual variation in circulating corticosterone (CORT) to antipredator responses in waterfowl, and determined that CORT may differentially mediate physiological and behavioral responses to threats, and may therefore create inter-individual variation in sensitivity to threats (Kralj-Fišer et al. 2010, Seltmann et al. 2012. These different coping styles offer different adaptive value, and individuals with highly plastic capacities, such as reactive phenotypes, are predicted to perform better to changes in their environment than proactive phenotypes (characterized as being less flexible; B. Sadoul et al., unpublished manuscript). ...
Predator-prey dynamics in the Arctic are being altered with changing sea ice phenology. The increasing frequency of predation on colonial nesting seabirds and their eggs by the polar bear (Ursus maritimus) is a consequence of bears shifting to terrestrial food resources through a shortened seal-hunting season. We examined antipredator responses in a colony of nesting Common Eiders (Somateria mollissima) on East Bay Island, Nunavut, Canada, which is exposed to established nest predators, such as arctic fox (Vulpes lagopus), but also to recent increases in polar bear nest predation due to the bears’ lost on-ice hunting opportunities. Given eiders’ limited eco-evolutionary experience with bears, we aimed to experimentally contrast eider responses to the recent predation pressure by polar bears to those induced by their more traditional mammalian predator, the arctic fox. Our goal was to characterize whether this population of eiders was vulnerable to a changing predator regime. Using simulated approaches of visual stimuli of both predator types, we measured eider heart rate and flight initiation distance as physiological and behavioral metrics, respectively, to characterize the perceived risk of and subsequent response to imminent threat posed by these two predators that differ in historical encounter rates. Eider heart rates were more responsive to impending visual cues of arctic foxes compared to polar bears, but birds responded behaviorally to all simulated threats with similar flight initiation distances. Results suggest eiders may not perceive the full risk that bears pose as egg and adult predators, and are therefore expected to suffer negative fitness consequences from this ongoing and increasing interaction. Eiders may therefore require conservation intervention to aid in their management.
... Higher preening rates are usually present when birds are experiencing disturbances (Delius, 1988) cases (De Almeida et al., 2018). Moreover, preening behaviour correlates with increased MGC levels in some bird species, such as the goose (Anser anser), where geese subjected to handling stress showed increased and longer preening bouts (Kralj-Fiser et al., 2010). Conversely, in other species, such as captive European starlings (Sturnus vulgaris), preening actually decreased after acute stressors (Nephew and Romero, 2003). ...
Glucocorticoids mediate physiological processes to obtain energy, presenting daily variation in basal levels that may be related to behavioural activity pattern. Identification of plasticity in the secretion of these hormones is essential to understand their effects on physiology and behaviour of wild birds and, therefore, their success in their natural or artificial environment. Serial endocrine evaluations are facilitated by implementing non-invasive methodologies that minimize possible effects of manipulation on the animal’s physiological variables. However, non-invasive endocrine-behavioural studies in nocturnal birds, such as owls, are immature. The present work aimed to validate an enzyme immunoassay (EIA) to quantify glucocorticoid metabolites (MGC) in Megascops choliba as well as to evaluate differences in their production at the individual, sexual or daily level. We recorded the behaviour of nine owls during three continuous days to establish activity budget under captive conditions and aiming to correlate with daily MGC variation. The EIA proved to be effective in analytical assays and in pharmacological testing with synthetic ACTH, validating this immunoassay for the species. Additionally, individual differences in MGC production were confirmed in relation to the time of day, especially at 1700 and 2100, but not in relation to sex. During night hours, the owls showed greater behavioural activity, positively related to MGC values. Higher MGC concentrations were significantly related to greater expressions of active behaviours, such as maintenance, while lower MGC concentrations were recorded during moments of higher alertness and resting. The results presented show daily MGC variation to be inversed in this nocturnal species. Our findings can aid future theoretical studies of daily rhythm and evaluations of challenging and/or disturbing situations that result in changes in behaviour or hormonal cascades of these changes in ex situ populations of owls.
... As such, drone surveys of eiders occurring during the final phase of incubation and fasting should be studied, particularly if a project intends to carry out repeated flights throughout the breeding period (e.g., colony formation mapping 12 ). Next, individual variation in circulating corticosterone may differentially mediate physiological and behavioural responses to threats, e.g., 41,65 , and may therefore create inter-eider variation in sensitivity to drones. Finally, for nesting eiders in our study area, the threat of avian predators comes primarily from herring gulls that commonly consume eider eggs and ducklings, but pose little threat to adult eiders. ...
Aerial drones are increasingly being used as tools for ecological research and wildlife monitoring in hard-to-access study systems, such as in studies of colonial-nesting birds. Despite their many advantages over traditional survey methods, there remains concerns about possible disturbance effects that standard drone survey protocols may have on bird colonies. There is a particular gap in the study of their influence on physiological measures of stress. We measured heart rates of incubating female common eider ducks (Somateria mollissima) to determine whether our drone-based population survey affected them. To do so, we used heart-rate recorders placed in nests to quantify their heart rate in response to a quadcopter drone flying transects 30 m above the nesting colony. Eider heart rate did not change from baseline (measured in the absence of drone survey flights) by a drone flying at a fixed altitude and varying horizontal distances from the bird. Our findings suggest that carefully planned drone-based surveys of focal species have the potential to be carried out without causing physiological impacts among colonial-nesting eiders.
... However, encountering a stressful situation induced by a competitor or predator can elevate the occurrence of these activity patterns (Delius, 1967(Delius, , 1988Fernández-Juricic et al., 2004;Wittek et al., 2021). Similarly, preening rates also increase after injections of dopamine or adrenocorticotropic hormone, with the latter also showing increased head shaking (Delius et al., 1976;Delius, 1988;Acerbo, 2001;Kralj-Fiser et al., 2010). Thus, these actions can serve as a behavioral readout of social conflicts and/or neural processes. ...
Manual behavioral observations have been applied in both environment and laboratory experiments in order to analyze and quantify animal movement and behavior. Although these observations contributed tremendously to ecological and neuroscientific disciplines, there have been challenges and disadvantages following in their footsteps. They are not only time-consuming, labor-intensive, and error-prone but they can also be subjective, which induces further difficulties in reproducing the results. Therefore, there is an ongoing endeavor towards automated behavioral analysis, which has also paved the way for open-source software approaches. Even though these approaches theoretically can be applied to different animal groups, the current applications are mostly focused on mammals, especially rodents. However, extending those applications to other vertebrates, such as birds, is advisable not only for extending species-specific knowledge but also for contributing to the larger evolutionary picture and the role of behavior within. Here we present an open-source software package as a possible initiation of bird behavior classification. It can analyze pose-estimation data generated by established deep-learning-based pose-estimation tools such as DeepLabCut for building supervised machine learning predictive classifiers for pigeon behaviors, which can be broadened to support other bird species as well. We show that by training different machine learning and deep learning architectures using multivariate time series data as input, an F1 score of 0.874 can be achieved for a set of seven distinct behaviors. In addition, an algorithm for further tuning the bias of the predictions towards either precision or recall is introduced, which allows tailoring the classifier to specific needs.
... Indeed, when birds are exposed to a competitor or a potential predator, they show higher activity levels and especially elevated levels of preening and other kinds of displacement behaviors (Delius, 1967(Delius, , 1988Lima, 1995;Roberts, 1996;Fernández-Juricic et al., 2004). The same is true when they receive an injection of adrenocorticotropic hormone (ACTH) to induce stress (Delius et al., 1976;Kralj-Fiser et al., 2010) or an injection of dopamine (Acerbo, 2001). Indeed, the presence of a competitor in the next compartment increases the uncertainty to obtain food, a factor known to boost corticosterone and dopamine release in birds and mammals (e.g., Fiorillo et al., 2003;Hart et al., 2015;Marasco et al., 2015). ...
Spontaneous mirror self-recognition is achieved by only a limited number of species, suggesting a sharp “cognitive Rubicon” that only few can pass. But is the demarcation line that sharp? In studies on monkeys, who do not recognize themselves in a mirror, animals can make a difference between their mirror image and an unknown conspecific. This evidence speaks for a gradualist view of mirror self-recognition. We hypothesize that such a gradual process possibly consists of at least two independent aptitudes, the ability to detect synchronicity between self- and foreign movement and the cognitive understanding that the mirror reflection is oneself. Pigeons are known to achieve the first but fail at the second aptitude. We therefore expected them to treat their mirror image differently from an unknown pigeon, without being able to understand that the mirror reflects their own image. We tested pigeons in a task where they either approached a mirror or a Plexiglas barrier to feed. Behind the Plexiglas an unknown pigeon walked at the same time toward the food bowl. Thus, we pitched a condition with a mirror-self and a foreign bird against each other, with both of them walking close toward the food bowl. By a detailed analysis of a whole suit of behavioral details, our results make it likely that the foreign pigeon was treated as a competitor while the mirror image caused hesitation as if being an uncanny conspecific. Our results are akin to those with monkeys and show that pigeons do not equal their mirror reflection with a conspecific, although being unable to recognize themselves in the mirror.
... This indicates a stronger immunosuppressive effect in more infested individuals, which were more challenged from the onset. In previous studies on the influence of aggressive interactions on adrenocortical activity and heart rate in Greylag geese (Frigerio et al., 2003;Scheiber et al., 2005b;Wascher et al., 2012aWascher et al., , 2012b it remained unclear if the observed responses, such as an increase in CORT and heart rate (Kralj-Fišer et al., 2010), were adaptive or rather indicative for negative effects. Our results provide evidence for the latter, as an increase in parasite product excretion can be considered costly. ...
The presence of a social partner may significantly contribute to coping with stressful events, whereas dyadic separation generally increases glucocorticoid levels and, thereby, might also affect immune function and health. To study the covariation between social factors, immuno-reactive corticosterone metabolites, haematology and parasite product excretion patterns in a free-living, long-term monogamous bird, we separated pair mates in Greylag geese (Anser anser). We isolated the males of eight pairs for 48 hours to examine behavioural, adrenocortical, haematological and parasitological responses to mate removal in the female partners, and to social isolation in the males. Females showed no elevated levels of corticosterone metabolites in their droppings, but their haematocrit decreased during mate removal, whereas leucocyte number and heterophil/lymphocyte (H/L) ratio remained unchanged. In contrast, the socially isolated males excreted significantly elevated levels of corticosterone metabolites compared to baseline and showed a decrease in haematocrit as well as elevated leucocyte number and H/L ratio. In both sexes, the excretion of coccidian oocysts increased within 48 hours of the start of the separation, remained high one week after separation, and returned to baseline four weeks later. Described effects were generally more pronounced in males than in females. Our results suggest relatively swift potential health effects of mate loss and social isolation in an unfamiliar confinement in free-living geese.
... We investigated variation in haematocrit and blood leucocytes in relation to endogenous (age, sex) and exogenous factors (social status, season) in a free living and individually marked population of the socially complex greylag geese, Anser anser (Lorenz, 1988; Kotrschal, Hemetsberger & Weiß, 2006; Kotrschal, Scheiber & Hirschenhauser, 2010; Hemetsberger, Scheiber & Weiß, 2013). Social context is known to be among the strongest modulators of the physiological stress responses in greylag geese (e.g., Wascher, Scheiber & Kotrschal, 2008; Wascher, Arnold & Kotrschal, 2008; Wascher et al., 2009; Kralj-Fiser et al., 2010), which in turn are alleviated via emotional social support by partners (Frigerio, et al., 2003; Scheiber et al., 2005; Wascher et al., 2012). Across seasons, males and females are faced with different demands (Kotrschal, Scheiber & Hirschenhauser, 2010); consequently, physiological changes, such as levels of corticosterone, co-vary with seasonal variation in behaviour (Hirschenhauser, Moestl & Kotrschal, 1999a; Hirschenhauser, Moestl & Kotrschal, 1999b; Frigerio et al., 2004a). ...
Background
Blood parameters such as haematocrit or leucocyte counts are indicators of immune status and health, which can be affected, in a complex way, by exogenous as well as endogenous factors. Additionally, social context is known to be among the most potent stressors in group living individuals, therefore potentially influencing haematological parameters. However, with few exceptions, this potential causal relationship received only moderate scientific attention.
Methods
In a free-living and individually marked population of the highly social and long-lived Greylag goose, Anser anser, we relate variation in haematocrit (HCT), heterophils to lymphocytes ratio (H/L) and blood leucocyte counts to the following factors: intrinsic (sex, age, raising condition, i.e. goose- or hand-raised), social (pair-bond status, pair-bond duration and parental experience) and environmental (biologically relevant periods, ambient temperature) factors. Blood samples were collected repeatedly from a total of 105 focal birds during three biologically relevant seasons (winter flock, mating season, summer).
Results
We found significant relationships between haematological parameters and social as well as environmental factors. During the mating season, unpaired individuals had higher HCT compared to paired and family individuals and this pattern reversed in fall. Similarly, H/L ratio was positively related to pair-bond status in a seasonally dependent way, with highest values during mating and successful pairs had higher H/L ratio than unsuccessful ones. Also, absolute number of leucocytes tended to vary depending on raising condition in a seasonally dependent way.
Discussion
Haematology bears a great potential in ecological and behavioural studies on wild vertebrates. In sum, we found that HTC, H/L ratio and absolute number of leucocytes are modulated by social factors and conclude that they may be considered valid indicators of individual stress load.
... Circulating basal glucocorticoids are important for maintaining organismal homeostasis and in addition are thought to have permissive effects: at basal levels, glucocorticoids help the organism prepare for subsequent energetic challenges and potentially enhance the initial response to future stressors (Munck and Tóth 1994; Sapolsky et al. 2000). The effects of glucocorticoids are time, dose, and context dependent (Munck and Náray-Fejes- Tó th 1992; Øverli et al. 2002; Mikics et al. 2007; Kralj-Fišer et al. 2010), pointing to the importance of distinguishing between basal (including both the nadir and the peak of the circadian rhythm) and poststress hormone levels. Numerous studies have examined the relationships among glucocorticoid levels, metabolism, and whole-organism behavior and performance (Sinervo and Calsbeek 2003; Miles et al. 2007; Breuner et al. 2008; Campbell et al. 2009; Careau and Garland 2012). ...
Abstract The glucocorticoid hormones corticosterone (CORT) and cortisol influence numerous physiological, morphological, and behavioral functions. However, few studies have addressed possible relationships between individual differences in glucocorticoid concentrations and whole-animal performance or metabolism. Because CORT is important in glucose regulation and energy metabolism and can influence activity levels, we hypothesized that individual variation in baseline circulating CORT levels would correlate with individual differences in energy expenditure (routine and maximal), aerobic physiology, voluntary exercise on wheels, and organ masses. We tested this hypothesis in the California mouse (Peromyscus californicus). We collected data from 54 adult, colony-bred mice on baseline CORT levels (measured near both the circadian peak and the circadian trough), voluntary wheel running and its energetic costs, maximal oxygen consumption during forced treadmill exercise ([Formula: see text]), basal metabolic rate, and relative organ masses. We found surprisingly few statistically significant relationships among CORT, energy metabolism, behavior, and organ masses, and these relationships appeared to differ between males and females. These findings suggest that individual differences in baseline CORT levels are not an important determinant of voluntary activity levels or aerobic performance in California mice.
Updated tables, figures and references of Palme, 2019,
and the respective supplements (Date: 2nd January 2025)
Over the last decade, several theoretical models have been put forth to describe how animals respond to adverse environments and how this response changes under different physiological demands across life history stages. These models capture the context- and condition-dependent nature of stress responses. Yet, application of the models has been limited thus far in part because each model addresses different aspects of the problems facing the field of stress biology. Thus, there is a need for a unifying theoretical model that incorporates changes in physiological demand with life history stages and age, intricate relationships among physiological systems, and biphasic nature of stress responses. Here, I propose a new integrative framework, the Damage-Fitness Model. In this model, regulators, such as DNA repair mechanisms and glucocorticoids, work together as anti-damage mechanisms to minimize damage at both the cellular and organismal level. When the anti-damage regulators are insufficient or inappropriate, persistent damage accumulates. Previous studies indicate that these damage directly impact reproductive performance, disease risk, and survival. The types of regulators, the threshold at which they are initiated, and the magnitude of the responses are shaped by developmental and current environments. This model unites existing theoretical models by shifting our focus from physiological responses to downstream consequences of the stress responses, circumventing context specificity. Discussions include (1) how the proposed model relates to existing models, (2) steps to test the new model, and (3) how this model can be used to better assess the health of individuals and a population.
Lay summary
The field of stress physiology faces a challenge of characterizing dynamic cellular, physiological, and behavioral responses when animals encounter a stressor. This paper proposes a new theoretical model which links stress avoidance, damage repair and accumulation, and fitness components.
Glucocorticoid hormones (GCs) are important mediators of physiological and behavioral responses to stress. While many studies have evaluated the environmental, behavioral, or physiological correlates of GCs and their effects on reproductive performances, further work is needed to clarify the relationship between GCs and fitness. Assessing the effects of increased GC levels on specific behaviors of breeding animals should improve our understanding of how GCs affect parental care. In this experimental study, we measured the effects of an experimental increase in corticosterone (CORT, the main avian GC) levels on the behavior of free-living male Ad,lie penguins (Pygoscelis adeliae) within the colony, their reproductive output, and the indirect consequences of both on the behavior of their partners. We show that increased CORT levels in males decreased their foraging time at sea while increased their attendance at the nest, although their attentiveness toward the nest itself decreased. In addition, treated males spent more time on comfort behaviors (e.g., preening), vocalizing, and engaging in positive social interactions relative to controls. Treatment further affected the behavior of their partners, but not chick begging and feeding rates. Penguins with increased CORT levels also exhibited decreased reproductive output. Previous studies of Ad,lie penguins in different life history stages and environmental conditions suggest that the consequences of CORT treatment on reproductive performance are context-dependent. In addition to the potential delay in the effects of increased CORT levels on reproduction, this context dependence should be taken into account when studying the behavior of free-living animals in relation to stress-inducing situations.
The flock of greylag geese established by Konrad Lorenz in Austria in 1973 has become an influential model animal system and one of the few worldwide with compelte life history data spanning several decades. Based on the unique records of almost 1000 free-living greylag geese, this is a synthesis of more than 20 years of behavioural research. It provides a comprehensive overview of a complex bird society, placing it in an evolutionary framework and drawing on a range of approaches, including behavioural (personality, aggression, pair bonding and clan formation), physiological, cognitive and genetic. With contributions from leading researchers, the chapters provide valuable insights into historical and recent research on the social behaviour of geese. All aspects of goose and bird sociality are discussed in the context of parallels with mammalian social organisation, making this a fascinating resource for anyone interested in integrative approaches to vertebrate social systems.
Corticosterone (B) may play a direct role in the promotion of feeding behavior under conditions of nutritional stress. However, effects of exogenous B and nutritional stress in passerines indicate a complex relationship of fed state, perceived or anticipated nutritional stress, and previous history. In a series of investigations on caged White-crowned Zonotrichia leucophrys and Song Sparrows Z. melodia, foraging behaviors and feeding rates were unaffected by exogenous B in fed birds. When food was returned, birds implanted with B refed for longer and with greater intensity following the 24 hour fast. Additionally, B-implanted birds showed lower activity (perch hopping) than controls when fed ad libitum, but when fasted this trend reversed with B-implanted birds showing increased activity and apparent escape behavior. In a second study, small flocks of Pine Siskins Carduelis pinus and Dark-eyed Juncos Junco hyemalis held in aviaries and fasted for 24 hours had higher plasma levels of B than similar flocks that had been allowed to refeed for 1 hour after fasting. However, the highest levels of B in fasted birds were still lower than in free-living conspecifics exposed to capture stress. This low amplitude modulation of plasma B levels in relation to fed state was corroborated by results from free-living Pine Siskins and Lapland Longspurs Calcarius lapponicus captured during snow storms. In spite of unusually high feeding intensities during the storm, individuals of only some Pine Siskins and no Lapland Longspurs had elevated circulating levels of B. In the latter species, serial samples revealed very high levels of B within 15 minutes of capture suggesting enhanced adrenal secretory activity as a result of the storm. Finally, in White-crowned Sparrows, exogenous B substantially reduced overnight metabolic expenditure by reducing the frequency and amplitude of arousal bouts during the night. This suggested a possible energy savings effect of B during the hours when foraging was impossible and, possibly, insurance that the individual will retain sufficient resources to seek food the following day. Taken together, our data suggest that B may be important for initiation of food-searching during periods of food deprivation. Only small increases in B secretion appear to be required thus facilitating a rapid return to homeostasis after food is located. Although under prolonged nutritional stress the basal levels of B remained low, adrenal potential to secrete B in response to further stress increased dramatically.
We investigated the reliability of the non-invasive approach of measuring steroid hormones from feces in the domestic goose
(Anser domesticus), a mainly herbivorous bird with a short gut passage time (2–3 h). Groups of eight outdoor-housed male domestic geese were
subjected to three different experiments, injection of either GnRH analogue or ACTH, or ”social stimulation” by confrontation
with two alien males or females. These experiments were replicated in three different seasons, in spring, during peak reproductive
activity, in summer, during long-day photorefractoriness and postnuptial molt, and in fall, during sexual reactivation. GnRH
stimulation resulted in significant increases of mean response and peak fecal testosterone metabolites (TM) in spring and
fall. Response TM concentrations excreted in spring were generally higher than in summer and fall. Social confrontation with
two females, but not with two males, increased mean and peak TM in all seasons. In general, ACTH treatment resulted in a proportionally
higher increase of fecal corticosterone metabolites (BM) than GnRH did in fecal TM (80- to 140-fold vs 6- to 8-fold). ACTH
significantly increased mean and peak BM in all seasons. Social confrontation with two males significantly increased fecal
BM in spring, but confrontation with two females increased fecal BM in fall. Our results indicate that determining steroids
from feces is a generally valid approach. However, the sensitivity of the method may vary between different hormones and results
may differ between seasons. BM results seemed more sensitive and seasonally robust than did TM.
Displacement activities are behaviour patterns (mostly body care activities) characterized by their apparent irrelevance to the situation in which they appear. Scratching, autogrooming, yawning and body shaking are among the most commonly reported displacement activities in non-human primates. A review of the primate literature indicates that displacement activities tend to occur in situations of psychosocial stress and that their frequency of occurrence is affected by anxiogenic and anxiolytic drugs. In the light of this evidence, it is suggested that displacement activities can be used as indicators of emotional states arising in a variety of primate social interactions. Methodological problems associated with such a use are discussed. The hypothesis that displacement activities may also have a communicative function in non-human primates is not supported adequately by available data.
Steroids may rapidly alter neuronal function and behavior through poorly characterized, direct actions on neuronal membranes. The membrane-bound receptors mediating these behavioral responses have not been identified. [3H]Corticosterone labels a population of specific, high-affinity recognition sites (dissociation constant = 0.51 nanomolar) in synaptic membranes from an amphibian brain. These binding sites were localized by receptor autoradiography in the neuropil, outside the regions of perikarya. The affinities of corticoids for this [3H]corticosterone binding site were linearly related to their potencies in rapidly suppressing male reproductive behavior. Thus, it appears that brain membranes contain a corticosteroid receptor that could participate in the regulation of behavior.
Basal levels of glucocorticoids maintained by negative feedback regulation are known to modulate a wide range of physiological processes, through a variety of effects such as those on carbohydrate metabolism and “permissive” actions on effects of other hormones. Glucocorticoid levels increase sharply in response to the stress of any kind of threat to homeostasis. The increased levels have traditionally been ascribed the function of enhancing the organism’s resistance to stress. How known physiological and pharmacological effects of high levels of glucocorticoids might accomplish this function, however, has been a mystery.
A generalization that is beginning to emerge is that many of these effects may be secondary to modulation by glucocorticoids of the actions of numerous intercellular mediators, including established hormones, prostanoids, neutral proteinases, and cytokines such as interferon. These mediators participate in physiological mechanisms — endocrine, renal, immune, neural, etc. — that mount a first line of defense against such challenges to homeostasis as hemorrhage, metabolic disturbances, infection, anxiety, and others.
Contrary to the traditional view that the role of glucocorticoids in stress is to enhance these defense mechanisms, it has become increasingly clear that glucocorticoids at moderate to high levels generally suppress them. This paradox first emerged when glucocorticoids were discovered to be antiinflammatory agents, and had remained a major obstacle to a unified picture of glucocorticoid function.
We have suggested that stress-induced increases in glucocorticoid levels protect not against the source of stress itself but rather against the body’s normal reactions to stress, preventing those reactions from overshooting and themselves threatening homeostasis. This hypothesis, the seeds of which are to be found in many earlier discussions of glucocorticoid effects, immediately accounts for the paradox noted above, and provides glucocorticoid physiology with a unified conceptual framework that can accommodate such apparently unrelated physiological and pharmacological effects as those on carbohydrate metabolism, inflammatory processes, shock and water balance. It also leads us to propose that some enzymes rapidly induced by glucocorticoids detoxify mediators released during stress-induced activation of primary defense mechanisms; those mediators could themselves cause damage if left unchecked.
Glucocorticoids modulate brain function and behaviour through different mechanisms. Although classical effects are mediated through intracellular receptors that modulate gene transcription, recent evidence supports the existence of rapid, nongenomic steroid effects through the neuronal membrane. In this study, we explored possible rapid behavioural effects of corticosterone in the rat, which could provide a model to characterize further the mechanisms involved in rapid corticosteroid nongenomic actions. We found that a corticosterone injection, at doses (2.5 or 5 mg/kg) that mimic plasma concentrations produced by substantial stress, rapidly increases (within 7.5 min of its systemic administration) the locomotor response displayed by rats in a novel environment (activity cage). A lower dose of 1 mg/kg failed to induce this effect. In addition, corticosterone failed to increase locomotion when administered to rats that had been previously exposed to the activity cage. Corticosterone-induced increased locomotion in a novelty situation was not counteracted by either the intracerebroventricular administration of the protein synthesis inhibitor cycloheximide, or by the intracerebroventricular administration of specific antagonists for each type of intracellular corticosteroid receptor, i.e. RU28318, a mineralocorticoid receptor antagonist and RU38486, a glucocorticoid receptor antagonist. Further studies supported the viability of the receptor antagonists to display an anti-corticosteroid action interfering, as previously reported, with the behavioural &winning test. Therefore, the rapid actions of corticosterone in locomotor activity described here, which appear to be nongenomic, might provide a model for future research on the elucidation of the mechanisms involved in steroid-membrane interactions.
Studies of captive animals have suggested that social stress affects subdominants, whereas recent data from the wild have revealed that stress mainly affects dominants. We used a non-invasive approach to investigate, for the first time in a social bird, the circannual stress-dominance relationships between low-ranking single males, intermediately positioned paired ganders without offspring and high-ranking paired males with offspring from a flock of semi-tame, free-ranging greylag geese, Anser anser. We collected 933 faecal samples from 43 individuals, 12 singletons, 18 paired males without offspring and 13 paired males with offspring over an entire year and analysed them for corticosterone metabolites by enzyme immunoassay. During the mating season (February-April), singletons had marginally higher corticosterone than paired males (P<0.1), whereas during the parental season (May-January), the paired males with offspring had significantly higher corticosterone than both paired males without offspring and singletons. All three male categories had significantly higher corticosterone during the mating season than during the rest of the year. These results suggest that social stress in ganders is caused mainly by competition between males and by constrained access to females during the mating season, but by parental commitment during the rest of the year. We suggest that dominance per se may not be a direct cause of stress. Rather, the amount of social stress may co-vary with the behavioural investment individuals need to make to optimize their fitness and with the relationship between such demands and the individuals' rank positions. This relationship seems to be seasonal in geese. Copyright 1998 The Association for the Study of Animal Behaviour.
The secretion of glucocorticoids (GCs) is a classic endocrine response to stress. Despite that, it remains controversial as to what purpose GCs serve at such times. One view, stretching back to the time of Hans Selye, posits that GCs help mediate the ongoing or pending stress response, either via basal levels of GCs permitting other facets of the stress response to emerge efficaciously, and/or by stress levels of GCs actively stimulating the stress response. In contrast, a revisionist viewpoint posits that GCs suppress the stress response, preventing it from being pathologically overactivated. In this review, we consider recent findings regarding GC action and, based on them, generate criteria for determining whether a particular GC action permits, stimulates, or suppresses an ongoing stress-response or, as an additional category, is preparative for a subsequent stressor. We apply these GC actions to the realms of cardiovascular function, fluid volume and hemorrhage, immunity and inflammation, metabolism, neurobiology, and reproductive physiology. We find that GC actions fall into markedly different categories, depending on the physiological endpoint in question, with evidence for mediating effects in some cases, and suppressive or preparative in others. We then attempt to assimilate these heterogeneous GC actions into a physiological whole.
There is accumulating evidence for rapid, non-genomic behavioral effects of various steroids including that of the glucocorticoid, corticosterone. Using an odor preference test, the responses of which are indicative of mate preferences and sexual interest, we examined the effects of acute corticosterone on the responses of oestrous female mice to male odors. Control female mice displayed an overwhelming preference for the odors of male mice. Peripheral administration of corticosterone elicited a significant dose-related (1.0-5.0 mg/kg) decrease in female preference for male odors at 10 min, but not at 60 min, after administration. These inhibitory effects of corticosterone on odor preferences were significantly reduced by the competitive NMDA antagonist, NPC 12626, and enhanced by the GABA antagonist bicuculline. This indicates that corticosterone has rapid inhibitory effects on olfactory mediated female mate preferences and responses to male odor that in part involve interactions with NMDA and GABA receptor mechanisms.
Captive European starlings (Sturnus vulgaris) were subjected to five acute stressors: a visual stressor (strobe light), an auditory stressor (music), and disturbance by three different humans; their accustomed caretaker, an antagonist (the experimenter), and a novel human. Heart rate (HR), behavioral, and corticosterone (CORT) responses to each stressor were simultaneously recorded. The visual stressor elicited a significantly lower maximal HR response [approximately 550 beats per minute (bpm)] that returned to basal levels (335 bpm) more quickly than the HR increases elicited by any of the four other stressors (approximately 700 bpm). These data suggest that the degree of novelty may alter the magnitude and duration of the HR response. Behaviorally, both the auditory stressor and the human antagonist caused a significant decrease in preening behavior without subsequent increases in activity, beak wiping (a behavioral indicator of displaced aggression), or bouts of feeding and/or drinking. In contrast to the stressor-specific differences in HR and behavior, all five acute stressors elicited similar sub-maximal CORT responses, suggesting the presence of a standardized CORT response to sudden, acute stimuli in wild captive starlings. The data indicate that starlings modulate HR, CORT, and behavioral responses depending upon the stressor, but that these three pathways are regulated independently.
One potential stressor to vertebrates both in the wild and in captivity is the presence of numerous individuals in a confined space. To examine the effects of increased conspecific density in birds, we simultaneously measured cardiac, behavioral, and endocrine responses of European starlings (Sturnus vulgaris) to acute crowding. A cage containing a resident bird was outfitted with a trap door that allowed for the introduction of intruder birds (one, three, or five birds) without human interference. The resident bird was implanted with a subcutaneous heart rate (HR) transmitter, behavior was videotaped through a two-way mirror, and blood samples were taken at the end of each treatment to determine plasma corticosterone (CORT) concentrations. Resident starlings significantly increased both general activity and aggressive behaviors while decreasing preening following the initiation of elevated conspecific density. Intruder starlings increased feeding, drinking, and aggressive pecking rates, but postintrusion feeding rates decreased as intruder number increased. Preening decreased in both residents and intruders following the intrusion. HR increased in the resident starlings at the time of intruder introduction, with an increase in the magnitude of this response directly correlating with increasing intruder number. The CORT response to increased density was dependent on social role (resident or intruder), since increasing density did not alter CORT levels in resident birds, but resulted in elevated CORT 30 min following the five-intruder introduction in the intruder birds. Together, these data suggest that increased conspecific density is a significant acute stressor in starlings which is capable of inducing aggression in both residents and intruders. Furthermore, it elicits different responses from different physiological and behavioral systems, and behavioral responses such as feeding and general activity may be density-dependent. The data specifically illustrate that cardiac and behavioral activation can be independent of CORT release, and the CORT response of starlings to increased conspecific density is dependent on social role and degree of the increase in density.
Previous studies in European starlings have concluded that conspecific crowding can be a significant stressor that is capable of simultaneously altering behavior, heart rate, and corticosterone (CORT) concentrations. It was hypothesized that the peptide hormone arginine vasotocin (AVT) has a role in the regulation of these three types of responses to crowding. Four male and four female resident starlings were submitted to nine combinations of 3 crowding treatments (0, 1, or 5 intruder starlings) and 3 subcutaneous injections (1, 4 microg AVT, and saline control). Resident starlings were given a treatment injection, their heart rate and behavior were monitored for 30 min, 0, 1, or 5 intruder Starlings were allowed to enter the residents cage, and HR and behavior were monitored for another 30 min. Blood samples were taken before and after all treatments to assess CORT concentrations. Exogenous AVT decreased the frequency of maintenance behaviors (feeding, drinking, preening, and beak wiping), as well as activity in resident starlings. Although aggressive behaviors upright posture, head feather expansion, and pecking) increased during crowding, these increases were significantly attenuated by AVT. Heart rate was significantly lower during these behavioral effects, and the CORT data indicate that the cardiovascular and behavioral effects are not dependent on significant increases in CORT. These data support the hypothesis that AVT's attenuation of general behavior and crowding induced aggression are modulated by a cardiovascular mechanism.
Elevated levels of circulating corticosterone commonly occur in response to stressors in wild vertebrates. A rise in corticosterone, usually in animals of subordinate rank, results in a variety of effects on behavior and physiology. Behavioral and physiological responses to short-term increases in corticosterone are well studied. In contrast, the effects of chronic elevated levels of corticosterone are poorly understood, particularly in lizards. Here, we examined the long-term effects of exogenous corticosterone on locomotor performance, resting and active metabolic rate, and hematocrit in male side-blotched lizards Uta stansburiana. Corticosterone implantation resulted in higher levels of stamina relative to sham-surgery controls. In addition, lizards with elevated corticosterone exhibited lower resting metabolic rates relative to controls. Corticosterone had no effect on peak activity metabolism but did result in faster recovery times following exhaustive exercise. We suggest that elevated levels of corticosterone in response to dominance interactions promote enhanced locomotor abilities, perhaps as a flight response to avoid agonistic interactions. Furthermore, stressed lizards are characterized by lower resting metabolic rates, which may serve as strategy to conserve energy stores and enhance survival.
Physical activity is generally considered as most relevant for modulating heart rate (HR). The authors show here that HR is not only modulated by physical activity but even more by social contexts. HR modulation in three free-ranging, socially embedded, male greylag geese fitted with implanted radiotransmitters was investigated. Measured HR ranged from 40 beats per minute (bpm) during rest to a maximum over 400 bpm during takeoff. Almost the same maximum HRs (400 bpm) were reached during social interactions, which however, generally require less bodily action. Mean HR during social interactions (agonistic interactions, vocalizations) was significantly higher than during behaviors with a less obvious social context (e.g., resting, comfort or feeding behavior), but with comparable physical activity involved. The authors also found significant and consistent differences in HR between the three focal individuals, probably because of individual behavioral phenotype. Our results show that social context has a strong modulatory effect on the sympathico-adrenergic activity in a social bird and conclude that particularly the latter may pose considerable energetic costs. (PsycINFO Database Record (c) 2008 APA, all rights reserved).
Some investigators have argued that emotions, especially animal emotions, are illusory concepts outside the realm of scientific inquiry. With advances in neurobiology and neuroscience, however, researchers are proving this position wrong while moving closer to understanding the biology and psychology of emotion. In Affective Neuroscience, Jaak Panksepp argues that emotional systems in humans, as well as other animals, are necessarily combinations of innate and learned tendencies; there are no routine and credible ways to really separate the influences of nature and nurture in the control of behavior. The book shows how to move toward a new understanding by taking a psychobiological approach to the subject, examining how the neurobiology and neurochemistry of the mammalian brain shape the psychological experience of emotion. It includes chapters on sleep and arousal, pleasure and pain systems, the sources of rage and anger, and the neural control of sexuality. The book will appeal to researchers and professors in the field of emotion.
Field and laboratory investigations were conducted to assess the effects of selected stressors on White-crowned Sparrows (Zonotrichia leucophrys gambelii and Z. l. pugetensis). Within a few minutes after capture during the non-breeding winter phase, the birds' plasma corticosterone increased, whereas their already low levels of luteinizing hormone (LH) and dihydrotesterone (DHT) declined further. In contrast, in the summer, or breeding phase, corticosterone levels increased much more slowly (sometimes not at all in females) during the first hour after capture. Plasma levels of LH in breeding birds were unaffected by capture and handling, as were levels of DHT in males and estrogen in females. In some cases, however, circulating levels of testosterone declined in males. In photostimulated, caged, male Z. l. gambelii circulating levels of corticosterone, LH, and DHT appeared to be unaffected by ambient temperatures between 5° and 32°C, but the level of testosterone was significantly depressed at 32°C. Capture, transport for 250 km, and subsequent caging of male and female Z. l. gambelii in autumn and winter within 24 h increased plasma corticosterone, and decreased LH and DHT. As the birds acclimated to captivity, a decrease in levels of corticosterone was followed by transient elevations of LH and DHT after which concentrations of these hormones stabilized at capture levels. Males transferred from outdoor aviaries and held one, two, or three per cage on short days also developed elevated concentrations of corticosterone and depressed levels of LH and DHT. Corticosterone decreased within two weeks in birds held one or two per cage, and within three weeks in those housed three per cage. As corticosterone levels decreased, transient increases occurred in LH and DHT, with the highest levels in birds held three per cage.
Amid the deleterious consequences of prolonged stress, there is tremendous variability in how readily various stressors provoke stress responses in different individuals. This review covers some of the underpinnings of such differences, heavily emphasizing adrenocortical secretion of glucocorticoids during stress, and responsiveness to psychological, rather than physical stressors. Psychological stress is shown to involve loss of control or of predictability, an absence of outlets for frustration, an absence of social support, and a perception of events worsening; some powerful studies show that the physiological and pathophysiological responses to identical physical stressors will vary dramatically as a result of manipulating some of those psychological variables. Those findings are then used to interpret a literature concerning differences in the stress response among individuals of different ranks among a variety of social animal species. In a broad manner, social dominance in a stable hierarchy, with its attendant psychological rewards, is associated with a more adaptive stress response, as measured by a number of physiological endpoints. However, considerable subtleties in this relationship exist, transcending the mere issue of rank. Instead, rank and its physiological correlates are sensitive to the society in which the rank occurs, the individual's experience of both that rank and that society, and personality factors that color the perception of external events. Finally, these primate studies are used to interpret data in the health psychology field concerning individual differences and coping mechanisms in humans.
As in most social groups, agonistic interactions of various intensities are common in a goose flock. This may cause social stress, modulating heart rate (HR), which may serve as a measure of energetic investment and also of individual emotional involvement. We investigated HR responses to social encounters in 24 free-living greylag geese in an intact social environment. We recorded 1602 social interactions of various intensities in which the focal individual either attacked another member of the flock or was attacked itself. We analysed five HR parameters (mean HR, maximum HR, HR increase, duration until maximum, time until the baseline value was reached again). Generally, HR scaled positively with increasing intensity of agonistic interactions as well as with increasing duration. Individuals showed higher HRs when attacking than when being attacked. In addition, focal individuals responded with a greater HR increase when confronted with an opponent winning a higher percentage of interactions than itself. Repeated agonistic interactions against a specific opponent were related to greater HR responses than single events and focal individuals responded more strongly to male opponents than to females. Our results indicate a differential HR response depending on the intensity and duration of an interaction as well as the identity of the opponent. This differential physiological investment may reflect differences in emotional involvement depending on the social context of a particular agonistic interaction.
In the pied flycatcher there exists an anomaly in the relationship between cortical histology and plasma levels of corticosterone during the breeding period. In an attempt to study this anomaly, binding capacity and binding affinity of plasma corticosterone-binding proteins (CBP) were studied in free-living pied flycatchers during the early and late parts of the breeding period. Binding capacity of CBP showed a significant decrease with the progress of the breeding season in both males and females. During the early parts of the breeding season binding capacity was significantly higher in males than in females. No difference between sexes was observed during the nestling period. In males there also was a seasonal decrease in the binding affinity of CBP. The results show that there is a good relationship between periods with high plasma levels of corticosterone and its binding capacity in the blood. A second study showed that an experimentally increased plasma level of corticosterone during the nestling period drastically reduced reproductive succes. Parents given silastic implants containing corticosterone fed their nestlings less frequently and produced significantly fewer fledglings than did controls. Unlike the control birds, the body weight of the corticosterone-implanted birds did not decrease during the nestling period. Birds given corticosterone implants in which one small hole had been punched, in order to facilitate diffusion of corticosterone, all abandoned their territories and, consequently, these parents produced no fledglings. Thus, the results show that an elevation of plasma levels of corticosterone in adult pied flycatchers during the nestling period affects parental as well as territorial behavior.
Sexual selection theory predicts that signals reflecting the relative quality of individuals should be used in mate choice. Females could base their choice of copulation partners on male secondary sexual traits that honestly signal male age, as predicted by the age-based indicator mechanism. Studies have shown that female blue tits prefer older males and that aspects of dawn song reflect male quality, but it remains unknown whether dawn song characteristics correlate with male age. We compared dawn song characteristics of second-year (SY) and older (ASY) male blue tits (cross-sectional analysis), and tested for age-related changes within individuals (longitudinal analysis) and differential overwinter survival of SY males. We further investigated the relation between dawn song and paternity gain and loss. We found that ASY male blue tits began to sing earlier relative to sunrise than did SY males. This difference in the onset of dawn singing was due to age-related changes in individual performance rather than differential survival of individuals with varying expression of the trait. Males that began to sing earlier at dawn had more mating partners, and were more likely to gain extrapair paternity. Our findings suggest that the onset of dawn song can provide a simple mechanism for females to assess the relative quality of their mate and of neighbouring males. We propose that females use the onset of singing as a cue for their choice of extrapair partners.
The concept of personality implies individual differences in behavior and physiology that show some degree of repeatability/consistency over time and across contexts. Most studies of animal personality, particularly studies of individuals' variation in physiological mechanisms, have been conducted on selected individuals in controlled conditions. We attempted to detect consistent behaviors as well as physiological patterns in greylag ganders (Anser anser) from a free-roaming flock living in semi-natural conditions. We tested 10 individuals repeatedly, in a handling trial, resembling tests for characterization of “temperaments” in captive animals. We recorded the behavior of the same 10 individuals during four situations in the socially intact flock: (1) a “low density feeding condition”, (2) a “high density feeding condition”, (3) a “low density post-feeding situation” and (4) while the geese rested. We collected fecal samples for determination of excreted immuno-reactive corticosterone (BM) and testosterone metabolites (TM) after handling trials, as well as the “low density feeding” and the “high density feeding” conditions. BM levels were very highly consistent over the repeats of handling trials, and the “low density feeding condition” and tended to be consistent over the first two repeats of the “high density feeding condition”. Also, BM responses tended to be consistent across contexts. Despite seasonal variation, there tended to be inter-test consistency of TM, which pointed to some individual differences in TM as well. Aggressiveness turned out to be a highly repeatable trait, which was consistent across social situations, and tended to correlate with an individual's resistance during handling trials. Also, “proximity to the female partner” and “sociability” – the average number of neighboring geese in a close distance while resting – were consistent. We conclude that aggressiveness, “affiliative tendencies” and levels of excreted corticosterone and testosterone metabolites may be crucial factors of personality in geese.
A group of 10 territorial male song sparrows, Melospiza melodia, were given subcutaneous implants of corticosterone in Silastic tubing. A second group of 10 territorial males were given empty implants as controls. After 18–24 hr all males were then subjected to a simulated territorial intrusion (STI) by placing a caged male song sparrow in the center of the subject's territory, and playing tape recorded songs through a speaker placed alongside. Significantly fewer males with corticosterone implants responded to STI than to controls, and the latency to respond was longer. Of the 3 experimental males that did respond to STI, all had a lower frequency of songs and did not approach the simulated intruder as closely as controls. Many males were captured 2–7 days after implantation and blood samples collected for measurement of circulating hormone levels. As expected, plasma levels of corticosterone were high in the group given corticosterone implants. However, plasma levels of luteinizing hormone (LH) were not affected by treatment with corticosterone, and although circulating levels of testostrone were depressed slightly compared with controls, they were within the normal range for territorial and breeding males. There were no differences in body mass despite greatly increased fat depots in males treated with corticosterone. These data suggest that high levels of corticosterone, similar to those measured during stressful episodes both in the laboratory and field, may suppress territorial behavior independently of the adenohypophysial-gonad axis. Since plasma levels of LH and testosterone are not depressed markedly, thus maintaining the gonads in a near functional state, renesting can begin as soon as environmental conditions ameliorate. Such mechanisms could potentially increase the probability of raising viable young after unpredictable, severe weather resulted in failure of the previous breeding attempt.
It has been half a century since Selye’s first paper on stress and the General Adaptation Syndrome. As is apparent from this volume, stress physiology is now a rigorous and credible biomedical discipline. It is not clear, however, if those would have been the first attributes to come to mind at the mention of the subject during its earlier days. Much of this credibility has emerged with the uncovering of precise mechanisms to explain the relationships between environmental or emotional perterbations and physiological processes. Certainly, sensitive physicians long before Selye recognized that a patient’s emotional state could influence disease outcome. Few, one suspects, imagined that emotion and disease would be shown to be linked by precise biochemical events.
Previous work has shown that physiological amounts of cortisol added to rat thymus cells in vitro begin to inhibit glucose transport (as measured by the accumulation of glucose 6-phosphate during a 5-min glucose pulse)
by 15 to 20 min; the effect of cortisol is blocked by actinomycin D present from 0 to 5 min, suggesting a rapid stimulation
by cortisol of RNA synthesis. It is now shown that during the period from 15 to 30 min, but not prior to 15 min, the hormone
effect is blocked by cycloheximide or puromycin. The coincidence in time of sensitivity to these inhibitors of protein synthesis
with the development of inhibition of glucose transport, together with our earlier results, has led us to postulate that the
hormone effect is expressed through induction of a protein that rapidly inhibits glucose transport.
The preceding RNA-synthetic step possibly represents synthesis of mRNA for this protein. The previously demonstrated temperature-sensitive
step is shown to lie between the RNA- and protein-synthetic steps. It perhaps corresponds to transfer of mRNA from nucleus
to cytoplasm.
Decay rates of the hypothetical cortisol-induced RNA and protein have been measured following removal of hormone from specific
binding sites or addition of inhibitors of RNA or protein synthesis. The protein appears to have a life span of not more than
2 hours at 37°, while the RNA has a life span of less than 40 min.
When male rough-skinned newts (Taricha granulosa) are exposed to presumptive stressors, the incidence of courtship decreases and plasma corticosterone concentration increases. When sexually active males are injected intraperitoneally with corticosterone (1, 5, 10, 15, 20, or 25 micrograms), the incidence of courtship decreases rapidly and in proportion to the dose of corticosterone. Intracerebroventricular infusion of synthetic corticotropin-releasing factor (CRF) elevates plasma corticosterone levels and suppresses courtship. When male newts receive an injection of metyrapone, a drug that interferes with corticosterone synthesis, the inhibitory effects of stress or CRF infusion on courtship are reduced. These results support the hypothesis that, in this amphibian, elevated levels of corticosterone associated with exposure to stressful stimuli inhibit sexual behaviors.
The hypothesis proposed in this review is that normal diurnal rhythms in the hypothalamic-pituitary-adrenal (HPA) axis are highly regulated by activity in medial hypothalamic nuclei to effect an interaction between corticosteroids and insulin such that optimal metabolism results in response to changes in the fed or fasted state of the animal. There are marked diurnal rhythms in function of the HPA axis under both basal and stress conditions. The HPA axis controls corticosteroid output from the adrenal and, in turn, forward elements of this axis are inhibited by feedback from circulating plasma corticosteroid levels. Basal activity in the HPA axis of mammals fed ad lib peaks about 2 h before the peak of the diurnal feeding rhythm, and is controlled by input from the suprachiasmatic nuclei. The rhythm in stress responsiveness is lowest at the time of the basal peak and highest at the time of the basal trough in the HPA axis activity. There are also diurnal rhythms in corticosteroid feedback sensitivity of basal and stress-induced ACTH secretion which peak at the time of the basal trough. These rhythms are all overridden when feeding, and thus insulin secretion, is disrupted. Corticosteroids interact with insulin on food intake and body composition, and corticosteroids also increase insulin secretion. Corticosteroids stimulate feeding at low doses but inhibit it at high doses; however, it is the high levels of insulin, induced by high levels of corticosteroids, that may inhibit feeding. The effects of corticosteroids on liver, fat, and muscle cell metabolism, with emphasis on their interactions with insulin, are briefly reviewed. Corticosteroids both synergize with and antagonize the effects of insulin. The effects of stress hormones, and their interactions with insulin on lipid and protein metabolism, followed by some of the metabolic effects of injury stress, with or without nutritional support, are evaluated. In the presence of elevated insulin stimulated by glucocorticoids and nutrition, stress causes less severe catabolic effects. In the central nervous system, regulation of function in the HPA axis is clearly affected by the activity of medial hypothalamic nuclei that also alter feeding, metabolism, and obesity in rats. Lesions of the arcuate (ARC) and ventromedial (VMN) paraventricular (PVN) nuclei result in obesity and hyperactivity in the HPA axis. Moreover, adrenalectomy inhibits or prevents development of the lesion-induced obesity. There are interactions among these nuclei; one mode of communication is via inputs of neuropeptide Y (NPY) cells in the ARC to the VMN, dorsomedial nuclei, and PVN.(ABSTRACT TRUNCATED AT 400 WORDS)
We have previously studied the relationship between social subordinance (by approach-avoidance criteria) and physiology among male olive baboons (Papio anubis) living freely in a national park in Africa. In stable hierarchies, subordinate individuals have elevated basal glucocorticoid concentrations and a blunted glucocorticoid response to stress, as well as a prompt suppression of testosterone concentrations during stress. These facets have been interpreted as reflecting the chronic stress of social subordinance. In the present report, we find that these endocrine features do not mark all subordinate individuals. Instead, endocrine profiles differed among subordinate males as a function of particular stylistic traits of social behavior.
I investigated the effects of high plasma levels of corticosterone in male pied flycatchers, Ficedula hypoleuca, during the period of territorial establishment and the nestling period. In a second experiment males were exposed to a territorial intruder, a great spotted woodpecker model and a weasel model during the nest-building and nestling periods and their behavioural and hormonal reactions studied. Males were also exposed to handling stress (hormonal study) during these periods. During the period of territorial establishment, corticosterone-treated males, as well as control males, abandoned the territory in which they were captured; however, males in both groups very soon established new territories. During the nestling period, corticosterone-treated males, but not control males, abandoned their nests. During the nest-building period, intact males frequently attacked the territorial intruder but corticosterone-treated males never did; the woodpecker was only rarely attacked by intact males, and the weasel never. During the nestling period, the weasel was not attacked and territorial intruders only rarely; but woodpeckers were frequently attacked. With the progress of the breeding season, male flycatchers significantly reduced their sensitivity, in terms of the adrenocortical response, to all stressors tested. During the nest-building period, corticosterone levels were significantly higher in males exposed to handling, a weasel and a territorial intruder than in unmanipulated males; corticosterone levels in males exposed to a woodpecker did not differ from those in unmanipulated males; and testosterone levels were significantly elevated in males exposed to a woodpecker and to an intruder, but were reduced in males exposed to a weasel. Handling did not affect the testosterone level. During the nestling period, all groups showed low testosterone levels, and only exposure to a weasel and to handling increased corticosterone levels significantly. The results indicate that environmentally induced changes in testosterone and corticosterone secretion can be affected independently from one another, and that there are ecological bases for the differentiated hormonal responses to stress. Copyright 1998 The Association for the Study of Animal Behaviour. Copyright 1998 The Association for the Study of Animal Behaviour.
Recent evidence supports the hypothesis that corticosteroids influence behavioral changes associated with stressful events. Most investigations into this relationship focus on the long-term behavioral effects of corticosterone. Because many behavioral responses to environmental perturbations occur within minutes, we determined what rapid effects corticosterone may have on behavior. With this goal in mind, we devised and evaluated a method of corticosterone delivery which allowed us to examine immediate effects of corticosterone on behavior in a noninvasive manner. White-crowned sparrows (Zonotrichia leucophrys gambelii) were allowed access to mealworms (Tenebrio molitor) injected with corticosterone. Once ingested, the corticosterone moves across the digestive epithelium into the circulation. This method was evaluated using two vehicles: dimethyl sulfoxide and peanut oil. We tested the efficiency and consistency of corticosterone transfer into the circulation for both vehicles. Dimethyl sulfoxide gave a more efficient transfer of corticosterone. Injecting mealworms with corticosterone (carried in dimethyl sulfoxide) and feeding those worms to white-crowned sparrows increased circulating corticosterone to a discrete, repeatable level which peaked within 7 min and was cleared within 60 min. Using this method, we demonstrated that intermediate levels of corticosterone caused an increase in perch hopping in white-crowned sparrows within 15 min of hormone administration. An increase in perch hopping indicated elevated locomotor activity that is consistent with behavioral responses to natural perturbations. High levels of corticosterone did not induce this behavioral change. In light of the rapid effect of corticosterone on behavior, we propose that corticosterone was acting through a nongenomic mechanism.
We examined the effect of corticosterone on plasma levels of reproductive hormones (testosterone, dihydrotestosterone, and luteinizing hormone) and territorial defense behavior in male tree sparrows, Spizella arborea. Birds receiving Silastic implants filled with corticosterone (B) had significantly higher plasma levels of B than control birds, which received empty implants, and exhibited pectoral muscle wastage and a decrease in body mass. We evaluated the hormonal and agonistic responses of the two implanted groups of birds using a simulated territorial intrusion (STI) 2 to 4 days after they were implanted. Corticosterone-treated and control birds did not differ in their circulating levels of reproductive hormones or in their behavioral responses to STI (latency to respond to intrusion, number of songs, and closest approach to a decoy and tape recording). Unlike previous studies of north temperate passerines, high physiological levels of exogenous B had no effect either on circulating levels of reproductive hormones or on territorial behaviors associated with breeding. Nonetheless, untreated tree sparrows do mount a robust adrenocortical response, having a two- to fourfold increase in plasma B levels during a 1-h period of capture. Thus, adrenocortical responsiveness is maintained in these birds, but elevated levels of glucocorticoids do not suppress reproductive hormones or associated behaviors. We believe that this hormonal and behavioral refractoriness to glucocorticoids-or uncoupling of the stress response from the reproductive axis-may be advantageous for species having extreme temporal constraints on their breeding schedules.
The magnitude of the adrenocortical response to stress can be modulated by a variety of environmental and physiological factors, such as daylength and body condition. To determine the consequences of this modulation for the organism, one also needs to investigate behavioral sensitivity to glucocorticoids. We examined the behavioral response of Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii) to elevated glucocorticoids. Using a behavioral assay in which a rapid and transient dose of corticosterone (CORT: the avian glucocorticoid) rapidly increases perch hopping, we first investigated the photoperiodic regulation of this behavioral response. Intermediate levels of CORT ( approximately 24 ng/ml), which increased activity in sparrows exposed to a long-day (breeding) photoperiod, had no behavioral effect in sparrows exposed to a short-day (winter) photoperiod. Hence, the neural mechanisms which regulate the behavioral response to CORT appear to be less sensitive under a winter photoperiod. Using the same behavioral assay, we also measured a dose-response curve for CORT's effects on activity in sparrows exposed to the long-day photoperiod. Intermediate levels (24 and 40 ng/ml) increased activity to threefold background levels, whereas high physiological levels (65 and 97 ng/ml) had no effect. Given that the behavioral response does not increase linearly with CORT, we can no longer assume that modulation of the adrenocortical response to stress will result in linear changes in behavior.
The corticosterone response to the sight of a natural predator was investigated in free-living and captive great tits (Parus major). Free-living great tits responded to the sight of a stuffed, slowly moving Tengmalm's owl, a major predator of great tits, with warning calls and a change in behaviour around a feeder. Great tits returned to the feeder within a few minutes and began to approach the owl, and there was no increase in plasma corticosterone levels in birds sampled 30-50 min after they first saw the owl. Captive great tits in an aviary were exposed for 30 min to a stuffed Tengmalm's owl, to a stuffed brambling, and to a cardboard box. All three stimulus objects were slowly rotated during the exposure period. Great tits exposed to the owl changed their behaviour immediately, and spent most of the time when the owl was visible flying around the aviary and hanging from the roof, with very few visits to a feeder. Great tits exposed to the brambling and to the moving box also changed their behaviour and made fewer visits to the feeder. The great tits responded to the sight of the owl with a marked increase in plasma corticosterone levels, whereas there was no change in corticosterone levels (mean levels < 11 ng/ml) in birds exposed to the brambling or to the moving box. Mean corticosterone levels were high (37.1 +/- 4.9 ng/ml) 0.5 h after exposure to the owl, remained high (38.9 +/- 6.0 ng/ml) 1 h after exposure, and had returned to basal (5.3 plus minus 1.3 ng/ml) 3 h after exposure to the owl. This is the first demonstration for any bird of a complete corticosterone response to a predator. The sight of a predator initiated a corticosterone response in great tits that could not move more than 3 m away, whereas free-living great tits that could choose how far to fly away from the predator either did not initiate a corticosterone response, or had a small corticosterone response in which corticosterone levels were not significantly different from basal 30-50 min later. The results indicate that the initiation of a corticosterone response in birds depends on whether or not a bird perceives that a stimulus is a threat. Furthermore, they illustrate the importance of not making generalised conclusions based on laboratory experiments.
Social interactions can profoundly affect the hypothalamic-pituitary-adrenal (HPA) axis. Although most research on social modulation of glucocorticoid concentrations has focused on the consequences of exposure to stressful social stimuli, there is a growing body of literature which suggests that social support in humans and affiliative behaviors in some animals can provide a buffer against stress and have a positive impact on measures of health and well-being. This review will compare HPA axis activity among individuals for whom social relationships are maintained through aggressive displays, such as dominance hierarchies, vs. individuals engaging in high levels of prosocial behavior. We also will examine oxytocin, a neuropeptide that is well known for promoting social behavior, as the physiological link between positive social interactions and suppression of the HPA axis. Despite many examples of social interaction modulating the HPA axis and improving health outcomes, there is relatively little known regarding the underlying mechanisms through which social behavior can provide a buffer against stress-related disease.
An increasing body of evidence suggests that glucocorticoids--besides their well-known genomic effects--can affect neuronal function via mechanisms that do not involve the genome. Data obtained mainly in amphibians and birds suggest that such mechanisms play a role in the control of behavior. Acute glucocorticoid treatments increase aggressive behavior in rats, but the mechanism of action has not been investigated to date. To clarify the issue, we have assessed the aggressiveness of male rats after treating them with the corticosterone synthesis inhibitor metyrapone, corticosterone, and the protein synthesis inhibitor cycloheximide. Metyrapone applied intraperitoneally (i.p.) decreased the aggressiveness of residents faced with smaller opponents. Corticosterone administered i.p. 20 or 2 min before a 5-min encounter abolished these changes irrespective of the delay of behavioral testing. Thus, the effects of glucocorticoids on aggressive behavior occurred in less than 7 min (the delay and duration of testing taken together), and lasted more than 25 min. Corticosterone applied centrally (infused into the right lateral ventricle) also stimulated aggressive behavior rapidly, which shows that the effect was centrally mediated. The protein synthesis inhibitor cycloheximide did not affect the aggression-promoting effects of corticosterone when the hormone was injected 2 min before the aggressive encounter. Surprisingly, however, the effects were completely abolished when the hormone was injected 20 min before the encounter. These data suggest that glucocorticoids rapidly increase aggressive behavior via non-genomic mechanisms. In later phases of the aggressive encounter, aggressive behavior appears to be stimulated by genomic mechanisms.
In many species, seasonal activities such as reproduction or migration need to be fine-tuned with weather conditions. Air pressure and temperature changes are the best parameters for such conditions. Adapting to climatic changes invariably involves physiological and behavioral reactions associated with the adrenals. In the present study, we investigated the effects of ambient temperature and air pressure on excreted immuno-reactive metabolites of corticosterone (BM) and androgens (AM). Focal individuals were 14 paired male greylag geese (Anser anser) from a semi-tame, unrestrained flock. BM and AM were measured in individual fecal samples over 25 days in November and December. Two different ACTH-validated assays were used for the assessment of BM: the first one cross-reacting with 11beta,21-diol-20-one structures ("old assay") and the second one with 5beta,3alpha,11beta-diol structures ("new assay"). With the "new assay," BM correlated negatively with the minimum ambient temperature of the night before, which may reflect corticosterone involvement in thermoregulation. BM also correlated positively with the minimum air pressure of the previous afternoon, which supports the value of air pressure for predicting weather conditions. Together, these reactions suggest a role of the adrenals in responding behaviorally and physiologically to changes in weather. Preliminary analysis indicated a higher sensitivity to the excreted glucocorticosteroid metabolites in the "new assay." As expected for outside the mating season, no relationships were found between excreted AM and the weather parameters considered. The gradual changes in BM excretion in parallel with weather conditions may be part of the fine-tuning of physiology and behavior by environmental clues.
Living organisms have regular patterns and routines that involve obtaining food and carrying out life history stages such as breeding, migrating, molting, and hibernating. The acquisition, utilization, and storage of energy reserves (and other resources) are critical to lifetime reproductive success. There are also responses to predictable changes, e.g., seasonal, and unpredictable challenges, i.e., storms and natural disasters. Social organization in many populations provides advantages through cooperation in providing basic necessities and beneficial social support. But there are disadvantages owing to conflict in social hierarchies and competition for resources. Here we discuss the concept of allostasis, maintaining stability through change, as a fundamental process through which organisms actively adjust to both predictable and unpredictable events. Allostatic load refers to the cumulative cost to the body of allostasis, with allostatic overload being a state in which serious pathophysiology can occur. Using the balance between energy input and expenditure as the basis for applying the concept of allostasis, we propose two types of allostatic overload. Type 1 allostatic overload occurs when energy demand exceeds supply, resulting in activation of the emergency life history stage. This serves to direct the animal away from normal life history stages into a survival mode that decreases allostatic load and regains positive energy balance. The normal life cycle can be resumed when the perturbation passes. Type 2 allostatic overload begins when there is sufficient or even excess energy consumption accompanied by social conflict and other types of social dysfunction. The latter is the case in human society and certain situations affecting animals in captivity. In all cases, secretion of glucocorticosteroids and activity of other mediators of allostasis such as the autonomic nervous system, CNS neurotransmitters, and inflammatory cytokines wax and wane with allostatic load. If allostatic load is chronically high, then pathologies develop. Type 2 allostatic overload does not trigger an escape response, and can only be counteracted through learning and changes in the social structure.
Measuring hormone metabolites from excreta is a powerful method to study hormone-behavior relationships. Currently, fecal corticosterone metabolite concentrations are used to estimate individual short-term stress responses. From the free-roaming, semitame flock of greylag geese (Anser anser), as many fecal samples as possible were collected over 3 h following a challenge (social density stress) or in a control situation. This time span corresponds to the gut passage time of geese. It was asked how many samples were necessary to determine differences in excreted corticosterone immunoreactive metabolites (CORTs) between control and social density stress and which parameters (means, maxima, range) reliably showed this difference. A large variation of CORT was found between consecutive samples. Still, means, maxima, and ranges of the samples in a fecal series consistently showed the response to a stressor both within and between individuals. Three samples sufficed if the maximum value of CORT was used, whereas four or more samples were necessary to work with the mean. It was concluded that by increasing the number of fecal samples collected, the course of CORT could be measured more precisely and an individual's acute stress response inferred more reliably.
During the past 20 years, measuring steroid hormone metabolites in fecal samples has become a widely appreciated technique, because it has proved to be a powerful, noninvasive tool that provides important information about an animal's endocrine status (adrenocortical activity and reproductive status). However, although sampling is relatively easy to perform and free of feedback, a careful consideration of various factors is necessary to achieve proper results that lead to sound conclusions. This article aims to provide guidelines for an adequate application of these techniques. It is meant as a checklist that addresses the main topics of concern, such as sample collection and storage, time delay extraction procedures, assay selection and validation, biological relevance, and some confounding factors. These issues are discussed briefly here and in more detail in other recent articles.
Corticosterone is an important hormone of the stress response that regulates physiological processes and modifies animal behavior. While it positively acts on locomotor activity, it may negatively affect reproduction and social activity. This suggests that corticosterone may promote behaviors that increase survival at the cost of reproduction. In this study, we experimentally investigate the link between corticosterone levels and survival in adult common lizards (Lacerta vivipara) by comparing corticosterone-treated with placebo-treated lizards. We experimentally show that corticosterone enhances energy expenditure, daily activity, food intake, and it modifies the behavioral time budget. Enhanced appetite of corticosterone-treated individuals compensated for increased energy expenditure and corticosterone-treated males showed increased survival. This suggests that corticosterone may promote behaviors that reduce stress and it shows that corticosterone per se does not reduce but directly or indirectly increases longer-term survival. This suggests that the production of corticosterone as a response to a stressor may be an adaptive mechanism that even controls survival.
Socially aggressive interaction is stressful, and as such, glucocorticoids are typically secreted during aggressive interaction in a variety of vertebrates, which may both potentiate and inhibit aggression. The behavioral relationship between corticosterone and/or cortisol in non-mammalian (as well as mammalian) vertebrates is dependent on timing, magnitude, context, and coordination of physiological and behavioral responses. Chronically elevated plasma glucocorticoids reliably inhibit aggressive behavior, consistent with an evolutionarily adaptive behavioral strategy among subordinate and submissive individuals. Acute elevation of plasma glucocorticoids may either promote an actively aggressive response via action in specialized local regions of the brain such as the anterior hypothalamus, or is permissive to escalated aggression and/or activity. Although the permissive effect of glucocorticoids on aggression does not suggest an active role for the hormone, the corticosteroids may be necessary for full expression of aggressive behavior, as in the lizard Anolis carolinensis. These effects suggest that short-term stress may generally be best counteracted by an actively aggressive response, at least for socially dominant proactive individuals. An acute and active response may be evolutionarily maladaptive under chronic, uncontrollable and unpredictable circumstances. It appears that subordinate reactive individuals often produce compulsorily chronic responses that inhibit aggression and promote submissive behavior.
Exogenous corticosterone alters behavior in House Sparrows (Passer domesticus)
- Jl Brubaker
- J Schulkin
- Romero
Brubaker JL, Schulkin J, Romero LM. Exogenous corticosterone alters behavior in House Sparrows (Passer domesticus). Abstract. Society for Integrative and Comparative Biology; 2009.