Carolyn M. Bauer

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.

Habitat type influences endocrine stress response in the degu (Octodon degus)

While many studies have examined whether the stress response differs between habitats, few studies have examined this within a single population. This study tested whether habitat differences, both within-populations and between-populations, relate to differences in the endocrine stress response in wild, free-living degus (Octodon degus). Baseline cortisol (CORT), stress-induced CORT, and negative feedback efficacy were measured in male and female degus from two sites and three habitats within one site during the mating/early gestation period. Higher quality cover and lower ectoparasite loads were associated with lower baseline CORT concentrations. In contrast, higher stress-induced CORT but stronger negative feedback efficacy were associated with areas containing higher quality forage. Stress-induced CORT and body mass were positively correlated in female but not male degus across all habitats. Female degus had significantly higher stress-induced CORT levels compared to males. Baseline CORT was not correlated with temperature at time of capture and only weakly correlated with rainfall. Results suggest that degus in habitats with good cover quality, low ectoparasite loads, and increased food availability have decreased endocrine stress responses.

Seasonal variation in the degu (Octodon degus) endocrine stress response

Many wild animals show seasonal variation in circulating levels of stress hormones. Seasonal changes in the stress response may help animals better cope with the different challenges faced during each life history stage. We determined the seasonal stress profile of wild, free-living degus in Chile. Female degus were sampled during non-breeding (January), mating/early gestation (July), late gestation (August), and lactation (1st litter-September, 2nd litter-January). Male degus were sampled during the first three time-points. We measured baseline cortisol (CORT), stress-induced CORT, and negative feedback efficacy using a dexamethasone suppression test. While we found that neither males nor females showed seasonal variation in baseline CORT or negative feedback levels, we did find significant seasonal variation in stress-induced CORT levels of both sexes. Male stress-induced CORT was lowest during mating while female stress-induced CORT was highest during late gestation and lactation. Overall, females had higher stress-induced CORT compared to males. Our data suggest that stress-induced levels of CORT are highest during periods with increased chance of stressor exposure or times of positive energy balance. Consequently, CORT responses to stress appear to be regulated according to different life history needs.

Testing the role of patch openness as a causal mechanism for apparent area sensitivity in a grassland specialist

Area sensitivity, species being disproportionately present on larger habitat patches, has been identified in many taxa. We propose that some apparently area-sensitive species are actually responding to how open a habitat patch is, rather than to patch size. We tested this hypothesis for Bobolinks (Dolichonyx oryzivorus) by comparing density and occupancy to a novel openness index, patch area, and edge effects. Bobolink density and occupancy showed significant relationships with openness, but logistic models based on an openness occupancy threshold had greater explanatory power. Thresholds remained approximately consistent from June through August, and shifted to be more open in September. Variance partitioning supported the openness index as unique and relevant. We found no relationships between measures of body condition (body mass, body size, circulating corticosterone levels) and either openness or area. Our findings have implications for studies of area sensitivity, especially with regards to inconsistencies reported within species: specifically, (1) whether or not a study finds a species to be area sensitive may depend on whether small, open sites were sampled, and (2) area regressions were sensitive to observed densities at the largest sites, suggesting that variation in these fields could lead to inconsistent area sensitivity responses. Responses to openness may be a consequence of habitat selection mediated by predator effects. Finally, openness measures may have applications for predicting effects of habitat management or development, such as adding wind turbines, in open habitat.

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

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

A test of reactive scope: Reducing reactive scope causes delayed wound healing.

Reactive scope predicts that all animals have an adaptive ability to respond to stressors in their environment, termed reactive homeostasis, and that only when an animals response to stressful stimuli exceeds a certain threshold (homeostatic overload) will stress have pathological effects. While this framework has successfully helped interpret effects of stressors on wildlife, no study has designed an experiment to directly test this framework. This study was designed to expose house sparrows (Passer domesticus) to treatments that would result in varying ranges of reactive homeostasis during chronic stress, which based on the reactive scope model should cause birds with the lowest reactive homeostasis range to exhibit signs of pathology during a subsequent challenge. To modulate the reactive homeostasis range, we altered allostatic load of birds by exposing them to chronic stress while either elevating, blocking, or not manipulating corticosterone. After concluding chronic stress treatments, birds were exposed to the subsequent challenge of a superficial wound. Individuals treated with corticosterone during chronic stress (high allostatic load) experienced the most pathology, including both weight loss and slower wound healing. Unmanipulated birds (medium allostatic load) also experienced weight loss but had normal healing rates, while birds with blocked corticosterone (low allostatic load) had minimal weight loss and normal healing rates. Our results indicate that increased allostatic load reduces the reactive homeostasis range, thereby causing individuals to cross the homeostatic overload threshold sooner, and thus support the reactive scope framework.

Maternal stress and plural breeding with communal care affect development of the endocrine stress response in a wild rodent.

Maternal stress can significantly affect offspring fitness. In laboratory rodents, chronically stressed mothers provide poor maternal care, resulting in pups with hyperactive stress responses. These hyperactive stress responses are characterized by high glucocorticoid levels in response to stressors plus poor negative feedback, which can ultimately lead to decreased fitness. In degus (Octodon degus) and other plural breeding rodents that exhibit communal care, however, maternal care from multiple females may buffer the negative impact on pups born to less parental mothers. We used wild, free-living degus to test this hypothesis. After parturition, we manipulated maternal stress by implanting cortisol pellets in 0%, 50-75%, or 100% of adult females within each social group. We then sampled pups for baseline and stress-induced cortisol, negative feedback efficacy, and adrenal sensitivity. From groups where all mothers were implanted with cortisol, pups had lower baseline cortisol levels and male pups additionally had weaker negative feedback compared to 0% or 50-75% implanted groups. Contrary to expectations, stress-induced cortisol did not differ between treatment groups. These data suggest that maternal stress impacts some aspects of the pup stress response, potentially through decreased maternal care, but that presence of unstressed mothers may mitigate some of these effects. Therefore, one benefit of plural breeding with communal care may be to buffer post-natal stress.

Livetrapping is not Biased by the Endocrine Stress Response: A Preliminary Study in the Degu (Octodon degus)

While livetrapping is a vital field research tool, it is not a completely unbiased method of sampling. Biased trapping arises during field endocrinological studies whenever hormone levels or response influence the probability of capture of a subject. We repeatedly captured wild, free-living adult degus (Octodon degus) from the same location over 12 days to determine whether individuals with a certain endocrine stress profile were more likely to be captured repeatedly than others. We measured baseline cortisol (CORT), stress-induced CORT, and negative feedback efficacy via a dexamethasone suppression test in adult male and lactating and nonlactating female degus upon initial capture. We successfully recaptured approximately half of the degus. None of the 3 indices of the stress response at initial capture predicted whether a degu would be recaptured. However, baseline CORT levels at 1st capture had a weak, negative relationship with the number of days between 1st and 2nd capture. Because most animals interpret capture and restraint as an acute stressor, we also analyzed the effect of recapture on the endocrine stress response. Baseline and stress-induced CORT concentrations were measured upon each subsequent recapture for up to 5 total captures. Upon subsequent recaptures, neither stress-induced CORT nor baseline CORT changed significantly. Additionally, individual stress-induced and baseline CORT titers were repeatable within our sample population. These findings suggest that livetrapping does not select for animals with certain endocrine stress profiles, and that degus fail to habituate to repeated capture and restraint stress.

Postnatal Development of the Degu (Octodon degus) Endocrine Stress Response Is Affected by Maternal Care.

Maternal stress and care significantly affect offsprings future behavior and physiology. Studies in laboratory rats have shown that maternal stress decreases maternal care and that low rates of certain maternal behaviors cause offspring to develop hyperreactive stress responses. Plurally breeding rodents that practice communal care, such as degus (Octodon degus), may be able to buffer some of these effects since offspring receive care from multiple females. Directly after parturition, 0% (Control group), 50% (Mixed group), or 100% (CORT group) per cage of pair-housed female degus were implanted with 21-day release cortisol pellets. The amount of maternal care provided by females was determined from video recordings during the next 3 weeks. Females with cortisol implants did not alter rates of maternal care. However, females recently introduced to captivity had low rates of pup contact and pup retrievals compared to females of captive origin. When pups reached 4 weeks of age, we determined their baseline and stress-induced cortisol levels, in addition to assessing their negative feedback efficacy and adrenal sensitivity. Pups from mothers recently introduced to captivity had weak negative feedback. Within captive pups, those from CORT mothers weighed less compared to pups from either Control or Mixed mothers. Captive CORT pups also had weak adrenal sensitivity compared to captive Control pups. These findings demonstrate that maternal care and glucocorticoid elevation impact certain components of the degu pup stress response, but that plural breeding with communal care may buffer some of these effects.

Seasonally sympatric but allochronic: differential expression of hypothalamic genes in a songbird during gonadal development

Allochrony, the mismatch of reproductive schedules, is one mechanism that can mediate sympatric speciation and diversification. In songbirds, the transition into breeding condition and gonadal growth is regulated by the hypothalamic–pituitary–gonadal (HPG) axis at multiple levels. We investigated whether the difference in reproductive timing between two seasonally sympatric subspecies of dark-eyed juncos (Junco hyemalis) was related to gene expression along the HPG axis. During the sympatric pre-breeding stage, we measured hypothalamic and testicular mRNA expression of candidate genes via qPCR in captive male juncos. For hypothalamic mRNA, we found our earlier breeding subspecies had increased expression of gonadotropin-releasing hormone (GnRH) and decreased expression of androgen receptor, oestrogen receptor alpha and mineralocorticoid receptor (MR). Subspecies did not differ in expression of hypothalamic gonadotropin-inhibitory hormone (GnIH) and glucocorticoid receptor (GR). While our earlier breeding subspecies had higher mRNA expression of testicular GR, subspecies did not differ in testicular luteinizing hormone receptor, follicle-stimulating hormone receptor or MR mRNA expression levels. Our findings indicate increased GnRH production and decreased hypothalamic sensitivity to sex steroid negative feedback as factors promoting differences in the timing of gonadal recrudescence between recently diverged populations. Differential gene expression along the HPG axis may facilitate species diversification under seasonal sympatry.