Baseline corticosterone is associated with parental care in virgin Japanese quail (Coturnix japonica).

Glucocorticoids (GCs) are thought to impact reproductive success, and ultimately fitness. In this study we focus specifically on the relationship between GCs and parental care. Captive bred Japanese quail (Coturnix japonica) do not show spontaneous parental care behavior, however this behavior can be induced through a sensitization procedure. We investigated how the GC status of Japanese quail relates to parental care in animals of both sexes exposed or not to a chick sensitization treatment. To assess GC status, we obtained baseline plasma and feather cort samples, and used the HPA-axis function test to assess stress responsiveness by examining the response to a standardized stressor as well as negative feedback efficacy through dexamethasone injection. Next, birds were either exposed to chicks overnight in a small enclosure (sensitization treatment) or were enclosed but not exposed to chicks (control). The following morning, adult behaviors were filmed in the presence of a fresh set of chicks for 20 min. A final serum GC sample was obtained to assess if exposure to novel chicks was perceived as stressful. In control animals, baseline GCs were associated with increased total parental care duration and decreased latency to first parental care event. Interestingly, the opposite relationship was found in the sensitization group. Finally, exposure to novel chicks was not associated with an increase in corticosterone in either group. Overall it appears that baseline GCs are correlated with parental care in captive bred Japanese quail, and that the relationship changes direction depending on whether or not sensitization has occurred.

Exploring relationships between cardiovascular activity and parental care behavior in nesting smallmouth bass: A field study using heart rate biologgers.

Research in a variety of vertebrate taxa has found that cardiac function is a major limiting factor in the ability of animals to cope with physiological challenges, and thus is suggested to play an important role in mediating fitness-related behaviors in the wild. Yet, there remains a paucity of empirical assessments of the relationships between physiological performance and biological fitness in wild animals, partially due to challenges in measuring these metrics remotely. Using male smallmouth bass (Micropterus dolomieu) as a model, we tested for relationships between cardiac performance (measured using heart rate biologgers) and fitness-related behaviors (assessed using videography and snorkeler observations) in the wild during the parental care period. Our results showed that heart rates were not significantly related to any measured parental care behaviors (e.g., nest tending) except for individual aggression level. After accounting for the effect of water temperature on heart rate, we found within-individual heart rate differed between days and also differed between nights. There was, however, evidence of diel variation in heart rate, where heart rate was higher during the day than at night. Although fitness is thought to be dependent on physiological capacity for exercise in wild animals, inter-individual variation in heart rate alone does not appear to relate to parental care behavior in smallmouth bass at the temporal scales examined here (i.e., hours to days). Further studies are required to confirm relationships between physiological performance and parental care behavior to elucidate the apparently complex relationships between physiology, behavior, and fitness in wild animals.

The role of glucocorticoids in the vertebrate response to weather.

Changes in the environment related to inclement weather can threaten survival and reproductive success both through direct adverse exposure and indirectly by decreasing food availability. Glucocorticoids, released during activation of the hypothalamic-pituitary-adrenal axis as part of the stress response, are an important candidate for linking vertebrate coping mechanisms to weather. This review attempts to determine if there is a consensus response of glucocorticoids to exposure to weather-related stimuli, including food availability, precipitation, temperature and barometric pressure. The included studies cover field and laboratory studies for all vertebrate taxa, and are separated into four exposure periods, e.g., hours, days, weeks and months. Each reported result was assigned a score based on the glucocorticoid response, e.g., increased, no change, or decreased. Short-term exposure to weather-related stimuli, of up to 24 h, is generally associated with increased glucocorticoids (79% of studies), suggesting that these stimuli are perceived as stressors by most animals. In contrast, the pattern for exposures longer than 24 h shows more variation, even though a majority of studies still report an increase (64%). Lack of glucocorticoid increases appeared to result from instances where: (1) prolonged exposure was a predictable part of the life history of an animal; (2) environmental context was important for the ultimate effect of a stimulus (e.g., precipitation limited food availability in one environment, but increased food in another); (3) prolonged exposure induced chronic stress; and (4) long-term responses appeared to reflect adaptations to seasonal shifts, instead of to short-term weather. However, there is a strong bias towards studies in domesticated laboratory species and wild animals held in captivity, indicating a need for field studies, especially in reptiles and amphibians. In conclusion, the accumulated literature supports the hypothesis that glucocorticoids can serve as the physiological mechanism promoting fitness during inclement weather.

Artificial rain and cold wind act as stressors to captive molting and non-molting European starlings (Sturnus vulgaris).

Free-roaming animals continually cope with changes in their environment. One of the most unpredictable environmental phenomena is weather. Being able to respond to weather appropriately is crucial as it can be a threat to survival. The stress response, consisting of increases in heart rate and release of glucocorticoids, is an important mechanism by which animals cope with stressors. This study examined behavioral, heart rate, and corticosterone responses of captive European starlings (Sturnus vulgaris) to two aspects of weather mimicked under controlled conditions, a subtle (3 °C) decrease in temperature and a short, mild bout of rain. Both decreased temperature and exposure to rain elicited increases in heart rate and corticosterone in non-molting starlings. Molt is an important life history stage in birds that affects feather cover and may require a different response to weather-related stressors. We repeated the experiment in molting starlings and found increases in heart rate in response to rain and cold wind. However, the hypothalamic-pituitary-adrenal (HPA)-axis was suppressed during molt, as molting starlings did not increase corticosterone release in response to either stimulus. These data suggest these stimuli induce increased allostatic load in starlings, and that animals may adjust their response depending on the life-history stage.

Hypothalamus-pituitary-adrenal axis activity and the subsequent response to chronic stress differ depending upon life history stage.

The hypothalamus-pituitary-adrenal (HPA) axis is modulated seasonally in many species, and chronic stress can alter HPA functioning. However, it is not known how these two factors interact - are there particular life history stages when animals are more or less vulnerable to chronic stress? We captured wild house sparrows (Passer domesticus) in Massachusetts during six different life history stages: early and late winter, pre-laying, breeding, late breeding, and molt. At each time point, we tested HPA function by measuring baseline and stress-induced corticosterone (CORT), negative feedback in response to an injection of dexamethasone, and maximum adrenal response through an injection of adrenocorticotropic hormone. We then brought birds into captivity as a model for chronic stress, and repeated the four tests 5 days later. At capture, all HPA variables varied seasonally. Birds showed increased negative feedback during breeding and late winter compared to pre-laying. Furthermore, birds during the late breeding period had down-regulated their HPA axis, perhaps in preparation for molt. After 5 days of captivity, house sparrows lost ∼11% of initial body mass, although birds lost more weight during molt and early winter. Overall, captive sparrows showed elevated baseline CORT and increased negative feedback, although negative feedback did not show a significant increase during any individual life history stage. During most of the year, adrenal sensitivity was unaffected by captivity. However, during late breeding and molt, adrenal sensitivity increased during captivity. Taken together, these data provide further support that HPA function naturally varies throughout the year, with the interesting consequence that molting birds may potentially be more vulnerable to a chronic stressor such as captivity.

Pharmacological characterization of intracellular glucocorticoid receptors in nine tissues from house sparrow (Passer domesticus).

Glucocorticoid hormones play a key role in the stress response, but plasma concentrations vary based on physiological, environmental, or social parameters. However, hormone titers alone do not determine organismal response. To enhance our understanding of glucocorticoid actions we can examine 'downstream' factors in the organismal stress response, measuring glucocorticoid receptors across target tissues. Here, we characterized intracellular binding sites for CORT (corticosterone, the avian glucocorticoid) in house sparrow (Passer domesticus) brain, liver, skeletal muscle, spleen, fat, testes, ovary, kidney and skin. We used radioligand binding assays to identify total capacity, relative density and affinity for CORT of intracellular receptors in each tissue. Most evidence supported two binding sites similar to mammalian low-affinity glucocorticoid receptor (GR) and a high-affinity mineralocorticoid receptor (MR) for brain, liver, kidney and testes, and only a GR-like receptor for muscle, spleen, fat, ovary and skin. However, kidney data were somewhat more complicated, possibly hinting at a mineralocorticoid function for CORT and/or GR in birds. In all tissues, GR and MR affinities were close to published house sparrow values (K(d)~6 nM for GR, and ~0.2 nM for MR). Taken together, these data show that CORT receptor distribution appears to be as widespread in birds as it is in mammals, and suggest that independent regulation of peripheral receptors in different target tissues may play a role in CORT's diverse physiological effects.

Behavioral and physiological responses of wild-caught European starlings (Sturnus vulgaris) to a minor, rapid change in ambient temperature.

Free-ranging animals continuously adjust to changes in their environment. The stress response, typified by increases in heart rate and glucocorticoids, is an important physiological response regulating these changes. This study investigated heart rate, corticosterone and behavioral responses of European starlings (Sturnus vulgaris) to a rapid 30min decrease in temperature using an air-conditioning unit. Ten wild-caught birds were divided into pairs and exposed to four different trials. Three trials were controls: undisturbed birds; exposing birds to only the noise of the air-conditioning unit; and exposing the birds to 20°C airflow. For the experimental trial birds were exposed to 12°C air, leading to a rapid but modest 3°C drop in ambient temperature inside the birdcages. Heart rate and behavior were recorded before and during trials, while blood samples were collected before and after each trial for corticosterone measurements. Cooling, but none of the control conditions, induced an increase in heart rate and corticosterone. Additionally, cooling led to an increase in perch hopping and feather ruffling. We conclude that minor changes in temperature can elicit a stress response in European starlings, which suggests that this may be an important mechanism by which animals cope with minor rapid environmental changes.

Neurotranscriptomic changes associated with chick-directed parental care in adult non-reproductive Japanese quail.

For many species, parental care critically affects offspring survival. But what drives animals to display parental behaviours towards young? In mammals, pregnancy-induced physiological transformations seem key in preparing the neural circuits that lead towards attraction (and reduced-aggression) to young. Beyond mammalian maternal behaviour, knowledge of the neural mechanisms that underlie young-directed parental care is severely lacking. We took advantage of a domesticated bird species, the Japanese quail, for which parental behaviour towards chicks can be induced in virgin non-reproductive adults through a sensitization procedure, a process that is not effective in all animals. We used the variation in parental responses to study neural transcriptomic changes associated with the sensitization procedure itself and with the outcome of the procedure (i.e., presence of parental behaviours). We found differences in gene expression in the hypothalamus and bed nucleus of the stria terminalis, but not the nucleus taeniae. Two genes identified are of particular interest. One is neurotensin, previously only demonstrated to be causally associated with maternal care in mammals. The other one is urocortin 3, causally demonstrated to affect young-directed neglect and aggression in mammals. Because our studies were conducted in animals that were reproductively quiescent, our results reflect core neural changes that may be associated with avian young-directed care independently of extensive hormonal stimulation. Our work opens new avenues of research into understanding the neural basis of parental care in non-placental species.

Chronic stress reverses enhanced neophobia following an acute stressor in European starlings.

Neophobia is an animal's avoidance of novelty. Animals tend to respond to novel objects by increasing their latency to approach the objects, and they eventually habituate after repeated exposure by attenuating this increased approach latency. Interestingly, the physiological stress response does not appear to have a causal link to neophobia, although acute stress can prevent animals from habituating to novel objects, possibly through a permissive effect. Chronic stress can induce an anxiety-like state in animals, while often disrupting the ability to respond to acute stress. We thus hypothesized that chronic stress may increase neophobia and tested this by inducing chronic stress in wild-caught European starlings (Sturnus vulgaris). Four distinct anthropogenic stressors were administered daily for 30 min each in a randomized order for 21 days. We then evaluated whether exposure to chronic stress altered the latency to approach a novel object placed on or near a food dish presented after overnight fasting. Chronically stressed birds and nonstressed controls exhibited similar initial neophobic responses to novel objects and showed similar habituation in response to repeated exposure. However, when birds were exposed to 15 min of restraint before repeated exposure to the same object, habituation was eliminated in control birds (i.e., they continued to respond with neophobia), whereas chronically stressed birds continued to show habituation as measured by attenuated approach latencies. These results demonstrate that an acute stress response (restraint) has a different impact on neophobia depending upon whether the bird is or is not concurrently exposed to chronic stress.

Prior restraint stress inhibits habituation to novel objects in the European starlings (Sturnus vulgaris).

Animals often avoid novel objects, a behavior known as neophobia. We examined behavioral responses of captive European starlings to novel objects placed at their food dishes. Exposure occurred concurrently to food reintroduction following overnight fasting. Behavior was analyzed for 10 min via video recording. We expected an increase in avoidance behavior compared with trials in which food was reintroduced without a novel object. Seven of 10 novel objects increased latency to approach the dish. In contrast to our expectations, neither prior restraint nor exogenous corticosterone changed the neophobic response to novel objects. While exposure to a novel object increased approach latency, there was no additional effect of restraining animals in a cloth bag for 15 min before food reintroduction. Furthermore, the subcutaneous injection of corticosterone did not affect approach latency by itself, nor did it affect the response to a novel object. Finally, we expected repeated exposure to the same object to extinguishing the neophobic response, and that restraint stress would prevent habituation. Our results show that European starlings habituate rapidly to exposure to a novel object, as approach latency returned to baseline within three repeated exposures to the same object. When the repeated presentation of the object was combined with prior restraint, however, the latency to approach never returned to baseline. These results reveal that neophobia in starlings is object-specific and that, while neither acute stress nor corticosterone directly affects the behavioral response to a novel object, acute stress appears to have a permissive effect on neophobia by inhibiting habituation.

Hypoxia augments apnea-induced increase in hemoglobin concentration and hematocrit.

Increased hemoglobin concentration (Hb) and hematocrit (Hct), attributable to spleen contraction, raise blood gas storage capacity during apnea, but the mechanisms that trigger this response have not been clarified. We focused on the role of hypoxia in triggering these Hb and Hct elevations. After horizontal rest for 20 min, 10 volunteers performed 3 maximal apneas spaced by 2 min, each preceded by a deep inspiration of air. The series was repeated using the same apneic durations but after 1 min of 100% oxygen (O(2)) breathing and O(2) inspiration prior to each apnea. Mean apneic durations were 150, 171, and 214 s for apneas 1, 2, and 3, respectively. Relative to pre-apnea values, the mean post-apneic arterial O(2) saturation nadir was 84.7% after the air trial and 98% after the O(2) trial. A more pronounced elevation of both Hb and Hct occurred during the air trial: after apnea 1 with air, mean Hb had increased by 1.5% (P < 0.01), but no clear increase was found after the first apnea with O(2). After the third apnea with air Hb had increased by 3.0% (P < 0.01), and with O(2) by 2.0% (P < 0.01). After the first apnea with air Hct had increased by 1.9% (P < 0.01) and after 3 apneas by 3.0% (P < 0.01), but Hct did not change significantly in the O(2) trial. In both trials, Hb and Hct were at pre-apneic levels 10 min after apneas. Diving bradycardia during apnea was the same in both trials. We conclude that hypoxia contributes to spleen contraction during apnea, likely through chemosensor-related sympathetic output. There are, however other factors involved that trigger spleen contraction even in the absence of hypoxia.

Chronic repeated exposure to weather-related stimuli elicits few symptoms of chronic stress in captive molting and non-molting European starlings (Sturnus vulgaris).

Repeated exposure to acute stressors causes dramatic changes in an animal's stress physiology and the cumulative effects are often called chronic stress. Recently we showed that short-term exposure to weather-related stimuli, such as temperature change, artificial precipitation, and food restriction, cause acute responses in captive European starlings (Sturnus vulgaris). Here, we examined the effect of repeated exposure to weather-related stressors on heart rate and corticosterone (CORT) of captive non-molting and molting European starlings. Four times every day for 3 weeks, birds were exposed to either 30 min of a subtle (3°C) decrease in temperature, a short bout of simulated rain, or 2 hr of food removal. The order and time of presentation were randomly assigned on each day. We found no differences in heart rate or heart rate variability. Furthermore, there were no changes in baseline CORT levels, CORT negative feedback efficacy, or maximal adrenal capacity. Mass increased across the experimental period only in molting birds. CORT responses to restraint were decreased in both groups following treatment, suggesting the birds had downregulated their responses to acute stress. Molting birds showed evidence of suppression of the HPA axis compared with non-molting birds, which is consistent with previous research. Overall, our data show that repeated exposure to weather-related stressors does not elicit most of the symptoms normally associated with chronic stress.

Oxygen-conserving effect of the diving response in the immersed human.

INTRODUCTION: The human cardiovascular diving response has been shown to have an oxygen-conserving effect during simulated breath-hold diving by apnoea with face immersion. However, it is not known if facial immersion enhances the response to the same extent as that in the diver with the body immersed and if this leads to oxygen conservation. METHODS: Seventeen subjects each completed a total of 12 apnoeas of fixed, near-maximal duration. Four series of three apnoeas were conducted: dry body with apnoea (DA), dry body with face-immersion apnoea (DFIA), immersed body with apnoea (IA), and immersed body with face-immersion apnoea (IFIA). Air and water temperatures were 23 degrees Celcius. Heart rate, skin blood flow, arterial blood pressure, arterial haemoglobin saturation, lung volume and end-tidal fractions of carbon dioxide and oxygen were recorded non-invasively. RESULTS: Face immersion led to a greater reduction in heart rate during apnoea, regardless of body immersion (DA-DFIA 9.3%, 95% confidence interval (CI) 3.54, 0.1; IF-IFIA 7.9%, 95% CI 4.8, 0.2). Both DFIA and DA resulted in skin vasoconstriction, which was more pronounced during DFIA (16%, 95% CI 8.4, 0.3). During body immersion, skin vasoconstriction was reduced considerably, and neither IA nor IFIA reduced blood flow further. Mean arterial pressure increased more in the immersed condition than on dry land. Arterial saturation remained higher after DFIA (0.4%, 95% CI 0.2, 0.01) and IFIA (0.4%, 95% CI 0.4, 0.01) series, suggesting an oxygen-conserving effect of the more powerful diving response associated with face immersion. CONCLUSION: We conclude that the oxygen-conserving effect of the diving response in the immersed diver is the same as that observed in the dry, horizontal, simulated diving model.

Increased erythropoietin concentration after repeated apneas in humans.

Hypoxia-induced increases in red blood cell production have been found in both altitude-adapted populations and acclimatized lowlanders. This process is mediated by erythropoietin (EPO) released mainly by the hypoxic kidney. We have previously observed high hemoglobin concentrations in elite breath-hold divers and our aim was to investigate whether apnea-induced hypoxia could increase EPO concentration. Ten healthy volunteers performed 15 maximal duration apneas, divided into three series of five apneas, each series separated by 10 min of rest. Apneas within series were separated by 2 min and preceded by 1 min of hyperventilation to increase apnea duration and arterial oxygen desaturation. When EPO concentration after serial apneas was compared to baseline values, an average maximum increase of 24% was found (P < 0.01). No changes in EPO concentration were observed during a control day without apnea, eliminating possible effects of a diurnal rhythm or blood loss. We therefore conclude that serial apneas increase circulating EPO concentration in humans.

Increase of hemoglobin concentration after maximal apneas in divers, skiers, and untrained humans.

Human splenic contraction occurs both during apnea and maximal exercise, increasing the circulating erythrocyte volume. We investigated the hematological responses to 3 maximal apneas performed by elite apneic divers, elite cross-country skiers, and untrained subjects. Post-apnea hemoglobin concentration had increased in all groups, but especially in divers. The increases disappeared within 10 min of recovery. Apneic duration across apneas also increased the most in divers. Responses in divers could be more pronounced as a result of apnea training.