Contrasting stress response of male arctic ground squirrels and red squirrels

A hormonal-challenge protocol was used to compare the stress response of males of Arctic ground squirrels and red squirrels during the breeding season (May). These squirrels live in the same boreal forest of the Yukon, but have very different life histories and utilize the forest in markedly different ways. Red squirrels had levels of total cortisol, maximum corticosteroid-binding capacity, and free cortisol that were 5, 7, and 2 times, respectively, those of Arctic ground squirrels. Red squirrels were resistant to suppression by an artificial glucocorticoid, dexamethasone (DEX); Arctic ground squirrels were not. Cortisol levels in red squirrels responded slowly but continuously to the ACTH injection; Arctic ground squirrels responded rapidly and then stabilized. Testosterone levels in red squirrels were extremely sensitive to the challenge, being suppressed by both DEX and ACTH; levels in Arctic ground squirrels were resistant to the challenge, being modestly suppressed by DEX and stimulated by ACTH. Energy mobilization, as measured by glucose and free fatty acid responses, was not affected. Red squirrels had four times the levels of white blood cells and higher proportions of lymphocytes and lower proportions of eosinophils than Arctic ground squirrels, indicating that the latter were in worse condition immunologically. Our evidence suggests that the functions associated with the hypothalamic-pituitary-adrenal axis are compromised in breeding male Arctic ground squirrels, but not in red squirrels. We propose that in male red squirrels this axis has evolved in the context of a stable social system based on long-lived animals with individual territories which are needed to deal with unpredictable winter food supplies. In contrast, Arctic ground squirrels escape the rigors of winter by hibernation and this hormonal axis has evolved in short-lived males in the context of intense intra-sexual competition in a social system based on female kin groups and regular male dispersal to avoid inbreeding. J. Exp. Zool. 286:390-404, 2000.     

A validation of extraction methods for noninvasive sampling of glucocorticoids in free-living ground squirrels

Fecal hormone assays provide a powerful tool for noninvasive monitoring of endocrine status in wild animals. In this study we validated a protocol for extracting and measuring glucocorticoids in free-living and captive Belding's ground squirrels (Spermophilus beldingi). We first compared two commonly used extraction protocols to determine which performed better with commercially available antibodies. We next verified the preferred extraction method by correlating circulating and fecal glucocorticoid measures from a group of individuals over time. For this comparison, we used both a cortisol and a corticosterone antibody to determine which had greater affinity to the fecal metabolites. Cortisol was the primary circulating glucocorticoid, but both hormones were present in well above detectable concentrations in the blood, which does not occur in other sciurids. In addition, the cortisol antibody showed greater binding with the fecal extracts than did the corticosterone antibody. Finally, we used adrenocorticotropic hormone and dexamethasone challenges to demonstrate that changes in adrenal functioning are reflected in changing fecal corticoid levels. These results suggest that our extraction protocol provides a fast, reliable assay of stress hormones in free-living ground squirrels without the confounding influence of short-term rises in glucocorticoid concentrations caused by handling and restraint stress and that it can facilitate ecological and evolutionary studies of stress in wild species.     

Pituitary luteinizing hormone responses to single doses of exogenous GnRH in female social Cape ground squirrels exhibiting low reproductive skew

The Cape ground squirrel Xerus inauris is unusual among social mammals as it exhibits a low reproductive skew, being a facultative plural breeder with not all females breeding within a group. We investigated pituitary function to assess whether there was reproductive inhibition at the level of the pituitary and potentially the hypothalamus in breeding and non-breeding female Cape ground squirrels. We did so during the summer and winter periods by measuring luteinizing hormone (LH) responses to single doses of 2 g exogenous gonadotropin-releasing hormone (GnRH) and physiological saline administered to 42 females from 11 colonies. Basal LH concentrations of females increased in response to the GnRH challenge. Basal plasma LH concentrations were greater during winter, when most oestrus events are observed. However, we found no differences in plasma LH concentrations between breeding and non-breeding females. We showed that the anterior pituitary of non-breeding female ground squirrels is no less sensitive to exogenously administered GnRH than that of breeding females. We therefore concluded that the pituitary is no more active in breeding than non-breeding females. The lack of differentiation in response to GnRH suggests that either non-breeding females have ovaries that are less sensitive to LH or that they refrain from sexual activity with males through an alternative mechanism of self-restraint.     

Seasonal glucocorticoid responses to capture in wild free-living mammals

We determined baseline and capture-induced glucocorticoid concentrations during two different seasons in three species of wild free-living rodents: brown lemmings (Lemmus trimucronatus), golden-mantled ground squirrels (Spermophilus saturatus), and yellow-pine chipmunks (Tamias amoenus). Initial blood samples were obtained within 3 min of capture, so that initial glucocorticoid levels reflect baseline titers of undisturbed animals. Animals were held for an additional 30 min, when a second blood sample was taken to measure stress-induced glucocorticoid titers. The primary glucocorticoid differed in each species. Lemmings secreted extremely large amounts of corticosterone (as high as 8,000 ng/ml). These high concentrations were accompanied by high corticosterone-binding globulin capacity and resistance to negative feedback. Squirrels and chipmunks secreted a mixture of cortisol and corticosterone (10-400 ng/ml). In males of all three species and female squirrels and chipmunks, glucocorticoid levels were significantly elevated 30 min after capture. Baseline and 30-min glucocorticoid levels differed seasonally in each species. Levels were higher during summer (with no snow cover) than in spring (with approximately 60% snow cover) in female lemmings, higher during breeding than before hibernation in squirrels, and higher postreproductively than during breeding in chipmunks. Together, these data indicate that glucocorticoid responses to stress in these free-living species are similar to those in laboratory species, but the magnitude of the response appears to depend on life-history features specific to each species.     

Seasonal and Acute Changes in Adrenocortical Responsiveness in an Arctic-Breeding Bird

The Lapland longspur,Calcarius lapponicus,times its breeding season so that chicks hatch coincident with the brief period of food abundance in the high arctic. This synchronization requires that all reproductive activities occur in over a much shorter period than at lower latitudes. Because of the known influence of stress hormones on delaying breeding in temperate-zone birds and the detrimental effects of such delays in the arctic, we expected the performance of the hypothalamic–pituitary–adrenal (HPA) axis of arctic-breeding birds to show less sensitivity to environmental stress than their mid-latitude counterparts. We found that adrenocortical responsiveness to the standardized stress of capture and handling, measured by taking five serial blood samples for corticosterone during the course of a 1-hr period, was similar to many temperate passerines and was also similar both between male and female longspurs and between the migratory and reproductive phases. However, the profile of plasma corticosterone during capture stress was significantly damped in longspurs sampled as they began their postnuptial molt. In addition, we had the opportunity to examine endocrine responses to a natural environmental stress in 1989 during a 3-day snowstorm which concealed available food resources. During this storm longspurs formed progressively larger flocks each day, with females abandoning incubation duties by the third day. Birds captured during the storm showed highly significant increases in both the rate of plasma corticosterone increase during capture and the peak postcapture level compared with birds sampled before the storm. This increased adrenal potential suggests increased activity of the HPA axis in response to severe conditions and is reminiscent of the response to fasting. Although the storm occurred during incubation, and reproductive hormone levels had begun to decline, we measured significant reductions in luteinizing hormone in both males and a subset of females captured during the storm.     

Androgen in free-living arctic ground squirrels: seasonal changes and influence of staged male-male aggressive encounters

We tested the responsiveness of plasma androgen in free-living male arctic ground squirrels (Spermophilus parryii) to challenges from conspecific males by staging aggressive encounters between males and then comparing androgen concentrations in manipulated and unmanipulated animals. The effect of staged encounters on androgen depended on time of year. In spring, androgen levels significantly increased after staged encounters, except during the peak of mating activity when levels were maximal in all reproductive males. In late summer, staged encounters had no significant effect on androgen levels. In spring but not summer, androgen was positively correlated to the relative intensity of encounters. These results suggest that circulating levels of androgen in male arctic ground squirrels result from a combination of seasonal and social factors. Responsiveness of androgen to encounters during spring but not late summer support the challenge hypothesis for this polygynous mammal.     

Fat ablation and food restriction influence reproductive development and hibernation in ground squirrels

The role of white adipose tissue in development of the reproductive apparatus of male golden-mantled ground squirrels was assessed by surgical removal of fat (lipectomy) immediately prior to onset of hibernation or by manipulation of fat levels through food restriction for 5 wk preceding hibernation. Animals then were maintained without food at 6 degrees C, and they hibernated from November 1983 until April 1984. At that time, blood plasma was assayed for hormone levels, and body mass, body composition, and masses of the testes and seminal vesicle-prostate complex were determined. At autopsy, testes and sexual accessory organs were heavier in Control squirrels than in Food-Restricted or Lipectomized (LIPX) animals. Paired-testes mass was positively correlated with body mass. Testosterone, luteinizing hormone (LH), and follicle-stimulating hormone (FSH) levels were uniformly low in animals sampled during torpor, but were elevated in 2 animals that had regained the euthermic state. The Food-Restricted animals spent more time in torpor than did the other two groups, and the percentage of decrease in body mass over the hibernation season was less for Food-Restricted than for LIPX or Control animals. Adequate lipid stores may be essential for the normal development of the reproductive apparatus of male ground squirrels. In the field, animals with insufficient fat stores may forego reproduction and thereby conserve energy for survival.     

Daily body temperature rhythms persist under the midnight sun but are absent during hibernation in free-living arctic ground squirrels

In indigenous arctic reindeer and ptarmigan, circadian rhythms are not expressed during the constant light of summer or constant dark of winter, and it has been hypothesized that a seasonal absence of circadian rhythms is common to all vertebrate residents of polar regions. Here, we show that, while free-living arctic ground squirrels do not express circadian rhythms during the heterothermic and pre-emergent euthermic intervals of hibernation, they display entrained daily rhythms of body temperature (T(b)) throughout their active season, which includes six weeks of constant sun. In winter, ground squirrels are arrhythmic and regulate core body temperatures to within ±0.2°C for up to 18 days during steady-state torpor. In spring, after the use of torpor ends, male but not female ground squirrels, resume euthermic levels of T(b) in their dark burrows but remain arrhythmic for up to 27 days. However, once activity on the surface begins, both sexes exhibit robust 24 h cycles of body temperature. We suggest that persistence of nycthemeral rhythms through the polar summer enables ground squirrels to minimize thermoregulatory costs. However, the environmental cues (zeitgebers) used to entrain rhythms during the constant light of the arctic summer in these semi-fossorial rodents are unknown.     

Temporal Dynamics of the Cecal Gut Microbiota of Juvenile Arctic Ground Squirrels: a Strong Litter Effect across the First Active Season

Arctic ground squirrels (Urocitellus parryii) are active for a scant 3 to 5 months of the year. During the active season, adult squirrels compete for mates, reproduce, and fatten in preparation for hibernation, while juvenile squirrels, weaned in early July, must grow and acquire sufficient fat to survive their first hibernation season. During hibernation, the gut microbial community is altered in diversity, abundance, and activity. To date, no studies have examined the gut microbiota of hibernators across the truncated active season. We characterized trends in diversity (454 pyrosequencing), density (flow cytometry), viability (flow cytometry), and metabolism (short-chain fatty acid analysis) of the gut microbial community of juvenile arctic ground squirrels across their first active season at weaning and at 4, 6, 8, and 10 weeks postweaning. At 8 weeks postweaning, the mean bacterial density was significantly higher than that at weaning, and the mean percentage of live bacteria was significantly higher than that at either weaning or 4 weeks postweaning. No significant differences in microbial diversity, total short-chain fatty acid concentrations, or molar proportions of individual short-chain fatty acids were observed among sample periods. The level of variability in gut microbial diversity among squirrels was high across the active season but was most similar among littermates, except at weaning, indicating strong maternal or genetic influences across development. Our results indicate that genetic or maternal influences exert profound effects on the gut microbial community of juvenile arctic ground squirrels. We did not find a correlation between host adiposity and gut microbial diversity during prehibernation fattening, likely due to a high level of variability among squirrels.     

Arctic ground squirrels Urocitellus parryii as drivers and indicators of change in northern ecosystems

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Effects of capture stress on free-ranging, reproductively active male Weddell seals

Physiological stress responses to capture may be an indicator of welfare challenges induced by animal handling. Simultaneously, blood chemistry changes induced by stress responses may confound experimental design by interacting with the biological parameters being measured. Cortisol elevation is a common indicator of stress responses in mammals and reproductive condition can profoundly influence endocrine response. We measured changes in blood cortisol and testosterone induced by handling reproductively active male Weddell seals (Leptonychotes weddellii) early and late in the breeding season. Weddell seals have the highest resting cortisol levels of all mammals yet showed a clear, prolonged elevation in cortisol in response to capture. Responses were similar when first caught and when caught a second time, later in the breeding season. Baseline testosterone levels declined over the breeding season but were not altered by capture. Administering a light dose of diazepam significantly ameliorated the cortisol response of handled animals without affecting testosterone levels. This may be an effective way of reducing acute capture stress responses. Male breeding success in years males were handled was no different to the years they were not, despite the acute capture response, suggesting no long-term impact of handling on male reproductive output.     

Effects of Season and Host Physiological State on the Diversity,Density, and Activity of the Arctic Ground Squirrel Cecal Microbiota

We examined the seasonal changes of the cecal microbiota of captive arctic ground squirrels (Urocitellus parryii) by measuring microbial diversity and composition, total bacterial density and viability, and short-chain fatty acid concentrations at four sample periods (summer, torpor, interbout arousal, and posthibernation). Abundance of Firmicutes was lower, whereas abundances of Bacteroidetes, Verrucomicrobia, and Proteobacteria were higher during torpor and interbout arousal than in summer. Bacterial densities and percentages of live bacteria were significantly higher in summer than during torpor and interbout arousal. Likewise, total short-chain fatty acid concentrations were significantly greater during summer than during torpor and interbout arousal. Concentrations of individual short-chain fatty acids varied across sample periods, with butyrate concentrations higher and acetate concentrations lower during summer than at all other sample periods. Characteristics of the gut community posthibernation were more similar to those during torpor and interbout arousal than to those during summer. However, higher abundances of the genera Bacteroides and Akkermansia occurred during posthibernation than during interbout arousal and torpor. Collectively, our results clearly demonstrate that seasonal changes in physiology associated with hibernation and activity affect the gut microbial community in the arctic ground squirrel. Importantly, similarities between the gut microbiota of arctic ground squirrels and thirteen-lined ground squirrels suggest the potential for a core microbiota during hibernation.     

The implications of stress on male mating behavior and success in a sexually dimorphic polygynous mammal, the grey seal

Studies on primates and other taxa have shown that the physiological response of an individual to stress reflects their social status. We combined behavioral observations with measures of stress to test the hypothesis that stress is an important physiological determinant of mating behavior and success in the male grey seal. Known-age males (N=19) were studied during the breeding seasons of 2004 and 2005 at Sable Island, Canada. The stressor was a capture and restraint period of 35 min and serial samples of cortisol and testosterone were taken as measures of stress. The mean baseline concentrations of cortisol and testosterone were 9.7+/-0.5 ug/dl and 6.2+/-0.6 ng/mL, respectively. The baseline cortisol concentration was negatively correlated with the duration of time a male spent at a site (r=-0.507, P=0.027), which was a strong correlate of mating success (r=0.659, P=0.002). All males experienced an increase in the concentration of cortisol during the restraint period (79.1+/-8.4%; CV=46.1%). The percentage rise in cortisol during restraint was correlated with the mean duration of time spent at a site (r=0.544, P=0.016) and thus success. The concentration of testosterone also increased during the restraint period (32.8+/-9.7%). This might be an adaptive response to maintaining the ability to reproduce while under stress. Our study indicates that stress is an important determinant of success in male grey seals. More successful males might exhibit an adaptive response to stress by maintaining low concentrations of cortisol during breeding.     

Eimeria species (Apicomplexa: Eimeriidae) from arctic ground squirrels (Spermophilus parryii) and red squirrels (Tamiasciurus hudsonicus) in Alaska and in Siberia, Russia

Fecal samples from arctic ground squirrels (Spermophilus parryii) collected in Alaska (n = 90) and Russia (n = 46) and from red squirrels (Tamiasciurus hudsonicus) in Alaska (n = 35) were examined for the presence of Eimeria spp. (Apicomplexa: Eimeriidae). Four species were recovered from arctic ground squirrels, including Eimeria callospermophili (prevalence = 18%), Eimeria cynomysis (23.5%), Eimeria lateralis (19%), and Eimeria morainensis (77%). A single species, Eimeria tamiasciuri (91%), was recovered from red squirrels. Eimerians recovered from arctic ground squirrels represent new host records, and the single species from red squirrels is a new geographic record. Alaskan arctic ground squirrel prevalence was higher for E. callospermophili (Alaska = 22% vs. Russia = 9%), E. cynomysis (34% vs. 2%), and E. lateralis (27% vs. 4%), but not E. morainensis (78% vs. 76%).     

Ecological factors affecting the adrenocortical response to stress in chestnut-collared and McCown's longspurs (Calcarius ornatus, Calcarius mccownii)

Secretion of the steroid hormone corticosterone (CORT) in response to perturbations results in behavior patterns that can maximize survival. Three commonly cited hypotheses suggest that during breeding, there are advantages associated with suppressed (CORT) secretion in (1) the sex that is most important for parental care, (2) individuals in good body condition, and (3) species with a short breeding season and limited renesting opportunities. We addressed these hypotheses in two midlatitude breeders, chestnut-collared and McCown's longspurs, by assessing CORT secretion over a 1-h period of handling. These species have congeners that are exclusively arctic breeders, and this provides a unique opportunity to assess adrenocortical responsiveness both within a phylogenetic framework and across environmental variables. In both species, males and females showed similar CORT secretion patterns in response to handling, and body condition was unrelated to CORT secretion. Additionally, although these midlatitude breeders have more opportunities to attempt a renest than their arctic congeners, their hormonal response to stress was similar to that reported for their arctic congeners. We suggest that an attenuated stress response may relate to the severity of the breeding environment and a low likelihood of successful renesting, since these variables are common to both arctic and grassland habitats.     

Glucose but not protein or fat load amplifies the cortisol response to psychosocial stress

We previously reported that glucose intake amplifies cortisol response to psychosocial stress and smoking in healthy young men, while low blood glucose levels prevented the stress-induced activation of the hypothalamus pituitary adrenal (HPA) axis. However, it remains unknown whether this modulation is specific for glucose load or a more common effect of energy availability. To elucidate this question, 37 healthy men, who fasted for at least 8 h before the experiment, were randomly assigned to four experimental groups, who received glucose (n = 8), protein (n = 10), fat (n = 10), and water (n = 9), one h before their exposure to the Trier Social Stress Test (TSST). Blood glucose levels were measured at baseline and following stress, while salivary cortisol was assessed repeatedly measured before after the TSST. The results show that both absolute cortisol levels and net cortisol increase were greater in the glucose group in comparison to the other groups (F(3,33) = 3.00, P < 0.05 and F(3,33) = 3.08, P < 0.05, respectively. No group differences were observed with respect to perceived stress and mood. Furthermore, the cortisol response was positively correlated with blood glucose changes (r = 0.49, P < 0.002). In conclusion, the results suggest a central mechanism responsible for regulation of energy balance and HPA axis activation, rather than peripheral mechanisms. We thus recommend controlling for blood glucose levels when studying HPA axis responsiveness.     

Epizootic cutaneous papillomatosis, cortisol and male ornamentation during and after breeding in the roach Rutilus rutilus

The prevalence of epidermal papillomatosis in roach is known to peak during the spawning period and to be higher in males than in females. The high occurrence of papillomatosis in polluted waters suggests that stress may contribute to the outbreak of the disease. However, little is known about breeding-induced stress in fish and its relationship with diseases. In this study, plasma cortisol concentration, hematocrit and the relative size of the spleen were determined in healthy and diseased male and female roach Rutilus rutilus during and shortly after spawning in a wild population. In addition, the sexual ornamentation (breeding tubercles on the lateral sides and on the frontal) of male roach during spawning was examined. Plasma cortisol concentration was higher during than after the spawning period, and higher in males than in females during spawning, indicating a spawning-induced stress and higher spawning stress among males. There was no correlation between cortisol concentration and the intensity of papillomatosis (number of scales under papilloma tumors) among the diseased fish. However, the significant interaction sex x disease status revealed by ANCOVA suggested that diseased males could be more prone to increased cortisol levels than diseased females or healthy males. Hematocrit values (ratio of the volume of red blood cells to total volume of blood) but not condition factor were lowered in papilloma-diseased fish after spawning. The relative size of the spleen was greater in males than in females. The number of frontal breeding tubercles correlated negatively with the intensity of papillomatosis. Experimental studies are needed to investigate the association of papillomatosis with stress and cortisol.     

Ovine corticotropin-releasing hormone stimulation test in patients with chronic renal failure: pharmacokinetic properties, and plasma adrenocorticotropic hormone and serum cortisol responses

The data on the status of the hypothalamic-pituitary-adrenal (HPA) axis in haemodialysis (HD) patients are conflicting. Moreover, a state reminiscent of Cushing's syndrome has been reported in this group of patients. Corticotropin-releasing hormone (CRH), that is produced by the hypothalamus and modulates the secretion of adrenocorticotropic hormone (ACTH), has been shown to be useful as a provocative test of the HPA axis. We investigated the effect of exogenous ovine CRH (oCRH) on plasma levels of ACTH and cortisol in 13 chronic HD patients. The plasma concentrations of immunoreactive CRH following oCRH administration were similar in patients and controls. In all patients, oCRH given intravenously as bolus injection caused a further increase in the already elevated levels of cortisol. The mean basal plasma levels of ACTH were within the normal range. There was, however, a blunted ACTH response to oCRH. We conclude that the HPA axis in chronic HD patients retains the ability to respond to exogenous oCRH. The patterns of the ACTH and cortisol response to this peptide resemble those observed in chronic stress (depression, anorexia nervosa). Besides, the kinetics of disappearance of oCRH indicate that the kidney may not be the major organ that metabolizes oCRH.     

The awakening cortisol response and blood glucose levels

The hypothalamic-pituitary-adrenal axis is characterized by a marked circadian cycle with heightened activity in the morning. This is synchronized to awakening such that free cortisol increases two to three fold in the first thirty to forty five minutes following awakening -- the awakening cortisol response. It has been suggested that this activity, by mobilizing energy reserves prepares the body for the metabolic demands of the day. Similar arguments are applied to the cortisol response to psychological challenge. Paradoxically the cortisol response to a psychosocial stressor is abrogated in fasted individuals with low blood glucose. Also cortisol response to a psychosocial stressor is positively correlated to blood glucose levels after glucose load. We examined if the same relationship applies to the awakening cortisol response. There was no correlation between the cortisol response and awakening blood glucose levels. Moreover a group with mean blood glucose at the bottom of the euglycemic range, identified by split at the median for glucose level upon awakening, showed no deficit in cortisol response. Hence the physiology of the awakening response differs to that of a psychological stress response. These data challenge the view that an oxidisable substrate for energy metabolism is permissive for cortisol responses. In addition the present findings do not support a predominantly gluconeogenic role for morning cortisol activation.     

Integrated Inflammatory Stress (ITIS) Model

During the last decade, there has been an increasing interest in the coupling between the acute inflammatory response and the Hypothalamic–Pituitary–Adrenal (HPA) axis. The inflammatory response is activated acutely by pathogen- or damage-related molecular patterns, whereas the HPA axis maintains a long-term level of the stress hormone cortisol which is also anti-inflammatory. A new integrated model of the interaction between these two subsystems of the inflammatory system is proposed and coined the integrated inflammatory stress (ITIS) model. The coupling mechanisms describing the interactions between the subsystems in the ITIS model are formulated based on biological reasoning and its ability to describe clinical data. The ITIS model is calibrated and validated by simulating various scenarios related to endotoxin (LPS) exposure. The model is capable of reproducing human data of tumor necrosis factor alpha, adrenocorticotropic hormone (ACTH) and cortisol and suggests that repeated LPS injections lead to a deficient response. The ITIS model predicts that the most extensive response to an LPS injection in ACTH and cortisol concentrations is observed in the early hours of the day. A constant activation results in elevated levels of the variables in the model while a prolonged change of the oscillations in ACTH and cortisol concentrations is the most pronounced result of different LPS doses predicted by the model.