Arctic Ground Squirrels Research Articles

Reproduction at All Costs: The Adaptive Stress Response of Male Arctic Ground Squirrels

We tested the hypothesis that adult male arctic ground squirrels (Spermophilus parryii plesius) exhibit an adaptive stress response during the mating period that may compromise their survival, whereas males at other times (nonreproductive adult males and juvenile males) have a normal functional stress response. We assessed the physiological responsiveness of the stress axis, of energy mobilization, and of the immune response by subjecting adult breeding males, adult nonbreeding males, and juvenile males to a hormonal challenge and an immunocompetence challenge. At the onset of the breeding season in spring, only 25–30% of the population were males, and of those present during the mating period, half disappeared soon thereafter, and 82% were not replaced by immigrants. Adult breeding males had the highest levels of free cortisol, the lowest maximum corticosteroid-binding capacity, slight dexamethasone resistance, the lowest hematocrit, the lowest number of white blood cells, the highest number of eosinophils, and the poorest ability to respond to the foreign antigen challenge in comparison with the other two male classes. All of these characteristics were indicative of chronic stress in breeding males that may directly compromise their survival. Juvenile males in mid-August also showed many, but not all of these characteristics, indicative of a prolonged period of stress, presumably associated with the period of dispersal. Testosterone levels remained high irrespective of age or breeding condition, decreased when dexamethasone was injected, and increased when ACTH was injected. These latter results are unique in mammals. High testosterone levels and their augmentation with stressors may play a key role in maintenance of aggressive behavior. We conclude that breeding male arctic ground squirrels exhibit an adaptive stress response in which they trade off survival for reproduction. We hypothesize that similar stress responses may have evolved in other species with comparable life histories.

REPRODUCTION AT ALL COSTS: THE ADAPTIVE STRESS RESPONSE OF MALE ARCTIC GROUND SQUIRRELS

We tested the hypothesis that adult male arctic ground squirrels ( Spermo- philus parryii plesius) exhibit an adaptive stress response during the mating period that may compromise their survival, whereas males at other times (nonreproductive adult males and juvenile males) have a normal functional stress response. We assessed the physiological responsiveness of the stress axis, of energy mobilization, and of the immune response by subjecting adult breeding males, adult nonbreeding males, and juvenile males to a hormonal challenge and an immunocompetence challenge. At the onset of the breeding season in spring, only 25-30% of the population were males, and of those present during the mating period, half disappeared soon thereafter, and 82% were not replaced by immigrants. Adult breeding males had the highest levels of free cortisol, the lowest maximum corticosteroid- binding capacity, slight dexamethasone resistance, the lowest hematocrit, the lowest number of white blood cells, the highest number of eosinophils, and the poorest ability to respond to the foreign antigen challenge in comparison with the other two male classes. All of these characteristics were indicative of chronic stress in breeding males that may directly com- promise their survival. Juvenile males in mid-August also showed many, but not all of these characteristics, indicative of a prolonged period of stress, presumably associated with the period of dispersal. Testosterone levels remained high irrespective of age or breeding condition, decreased when dexamethasone was injected, and increased when ACTH was injected. These latter results are unique in mammals. High testosterone levels and their augmentation with stressors may play a key role in maintenance of aggressive behavior. We conclude that breeding male arctic ground squirrels exhibit an adaptive stress response in which they trade off survival for reproduction. We hypothesize that similar stress re- sponses may have evolved in other species with comparable life histories.

Hibernation, a Model of Neuroprotection

Hibernation, a natural model of tolerance to cerebral ischemia, represents a state of pronounced fluctuation in cerebral blood flow where no brain damage occurs. Numerous neuroprotective aspects may contribute in concert to such tolerance. The purpose of this study was to determine whether hibernating brain tissue is tolerant to penetrating brain injury modeled by insertion of microdialysis probes. Guide cannulae were surgically implanted in striatum of Arctic ground squirrels before any of the animals began to hibernate. Microdialysis probes were then inserted in some animals after they entered hibernation and in others while they remained euthermic. The brain tissue from hibernating and euthermic animals was examined 3 days after implantation of microdialysis probes. Tissue response, indicated by examination of hematoxylin and eosin-stained tissue sections and immunocytochemical identification of activated microglia, astrocytes, and hemeoxygenase-1 immunoreactivity, was dramatically attenuated around probe tracks in hibernating animals compared to euthermic controls. No difference in tissue response around guide cannulae was observed between groups. Further study of the mechanisms underlying neuroprotective aspects of hibernation may lead to novel therapeutic strategies for stroke and traumatic brain injury.

The influence of herbivores and neighboring plants on risk of browsing: a case study using arctic lupine (Lupinus arcticus) and arctic ground squirrels (Spermophilus parryii plesius)

We examined how herbivore distribution and density, neighboring plant density and species composition, and individual plant morphology all influence the risk that individual arctic lupines (Lupinus arcticus) will be browsed by arctic ground squirrels (Spermophilus parryii plesius). Risk of being browsed was significantly influenced by the number of resident ground squirrels but not by overall squirrel density at a site. As the leaf density of neighboring conspecifics increased, risk of browsing to an individual lupine decreased except when palatable neighbors were also present. The presence of other palatable species increased the risk of browsing. Risk was highest when both lupine and other palatable neighbors were present. The presence of unpalatable neighbors reduced the risk of browsing of individual lupines. We discuss these results in the context of three hypotheses: (1) attractant decoy, (2) resource concentration, and (3) repellent plant. No single hypothesis accounts for our observations, but an interaction between herbivores, neighbors, and individual lupine morphology determined risk of browsing.

Why are Arctic ground squirrels more stressed in the boreal forest than in alpine meadows?

Arctic ground squirrels (Spermophilus parryii plesius Richardson) in the southeastern Yukon live in both boreal forest and alpine tundra habitats. We live-trapped young male and female squirrels in both habitat types and subjected them to a standardized hormonal-challenge protocol to assess the responsiveness of their hypothalamic-pituitary-adrenal axis. Alpine squirrels had levels of free cortisol at the baseline (initial) bleed following their removal from traps that were 3 times higher in males and 5 times higher in females compared with boreal forest squirrels. Females, but not males, from the boreal forest were dexamethasone resistant, while neither sex from the alpine habitat was resistant. Free cortisol in alpine squirrels also responded more dramatically after the injection of adrenocorticotropic hormone. Corticosteroid-binding globulin levels were significantly lower in forest than alpine squirrels and these levels were not markedly affected by the challenge protocol. Glucose levels were significantly higher in boreal than alpine squirrels and the pattern differed between the two sites in response to the protocol. Hematocrits were significantly higher in alpine squirrels. Collectively, this evidence suggests that Arctic ground squirrels were more chronically stressed in the boreal forest than in the alpine meadows. The most likely explanation for our results is higher predation risk in the forest compared with alpine meadows, as forage availability and population density were not significantly different between the two habitats.

Seasonal changes in glucocorticoid and testosterone concentrations in free-living arctic ground squirrels from the boreal forest of the Yukon

We examined how glucocorticoid and testosterone concentrations changed from spring to summer by livetrapping free-living populations of arctic ground squirrels (Spermophilus parryii). The primary glucocorticoid was found to be cortisol, with corticosterone below measurable concentrations in most individuals. Livetrapping elicited a strong stress response in both sexes: breeding males and females trapped in spring had free cortisol concentrations 4 and 34 times, respectively, those of base-line animals. The maximum corticosteroid-binding capacity (MCBC) was unaffected by trapping and was about 3 times higher in breeding females than in breeding males. Over the active season, MCBC values were lowest in all male classes (juveniles, nonreproductive adults, and reproductive adults), being less than half those in all female classes; pregnant females had values approximately twice those of juvenile females. However, free cortisol concentrations were similar in all female classes and in juvenile males and about half those in adult males. Livetrapping increased testosterone concentrations in males over those found in samples from base-line males, and testosterone concentrations did not affect MCBC values. Testosterone concentrations in livetrapped animals differed significantly among male classes, with nonreproductive males maintaining concentrations 64% of those in breeding males and 10 times those in juveniles.

Seasonal changes in glucocorticoid and testosterone concentrations in free-living arctic ground squirrels from the boreal forest of the Yukon

We examined how glucocorticoid and testosterone concentrations changed from spring to summer by livetrapping free-living populations of arctic ground squirrels (Spermophilus parryii). The primary glucocorticoid was found to be cortisol, with corticosterone below measurable concentrations in most individuals. Livetrapping elicited a strong stress response in both sexes: breeding males and females trapped in spring had free cortisol concentrations 4 and 34 times, respectively, those of base-line animals. The maximum corticosteroid-binding capacity (MCBC) was unaffected by trapping and was about 3 times higher in breeding females than in breeding males. Over the active season, MCBC values were lowest in all male classes (juveniles, nonreproductive adults, and reproductive adults), being less than half those in all female classes; pregnant females had values approximately twice those of juvenile females. However, free cortisol concentrations were similar in all female classes and in juvenile males and about half those in adult males. Livetrapping increased testosterone concentrations in males over those found in samples from base-line males, and testosterone concentrations did not affect MCBC values. Testosterone concentrations in livetrapped animals differed significantly among male classes, with nonreproductive males maintaining concentrations 64% of those in breeding males and 10 times those in juveniles.

Concurrent density dependence and independence in populations of arctic ground squirrels.

No population increases without limit. The processes that prevent this can operate in either a density-dependent way (acting with increasing severity to increase mortality rates or decrease reproductive rates as density increases), a density-independent way, or in both ways simultaneously. However, ecologists disagree for two main reasons about the relative roles and influences that density-dependent and density-independent processes have in determining population size. First, empirical studies showing both processes operating simultaneously are rare. Second, time-series analyses of long-term census data sometimes overestimate dependence. By using a density-perturbation experiment on arctic ground squirrels, we show concurrent density-dependent and density-independent declines in weaning rates, followed by density-dependent declines in overwinter survival during hibernation. These two processes result in strong, density-dependent convergence of experimentally increased populations to those of control populations that had been at low, stable levels.

MRNA stability and polysome loss in hibernating Arctic ground squirrels (Spermophilus parryii).

All small mammalian hibernators periodically rewarm from torpor to high, euthermic body temperatures for brief intervals throughout the hibernating season. The functional significance of these arousal episodes is unknown, but one suggestion is that rewarming may be related to replacement of gene products lost during torpor due to degradation of mRNA. To assess the stability of mRNA as a function of the hibernation state, we examined the poly(A) tail lengths of liver mRNA from arctic ground squirrels sacrificed during four hibernation states (early and late during a torpor bout and early and late following arousal from torpor) and from active ground squirrels sacrificed in the summer. Poly(A) tail lengths were not altered during torpor, suggesting either that mRNA is stabilized or that transcription continues during torpor. In mRNA isolated from torpid ground squirrels, we observed a pattern of 12 poly(A) residues at greater densities approximately every 27 nucleotides along the poly(A) tail, which is a pattern consistent with binding of poly(A)-binding protein. The intensity of this pattern was significantly reduced following arousal from torpor and undetectable in mRNA obtained from summer ground squirrels. Analyses of polysome profiles revealed a significant reduction in polyribosomes in torpid animals, indicating that translation is depressed during torpor.

Experimental manipulation of predation and food supply of arctic ground squirrels in the boreal forest

We examined whether arctic ground squirrel (Spermophilus parryii plesius) populations in northern boreal forest in the Yukon Territory, Canada, were limited by food, predators, or a combination of both, during the decline and low phases of a snowshoe hare cycle. From 1990 to 1995, populations were monitored in large-scale (1 km2) experimental manipulations. Squirrels were studied on eight 9-ha grids: four unmanipulated control grids, two food-supplemented grids, a predator-exclosure grid, and a predator-exclosure + food-supplemented grid. Population density was measured on all grids by livetrapping and active-season survival was measured using radiotelemetry. Population densities were lowest in 1992 and 1993 (2 years after the snowshoe hare population decline). Rates of population change were negative from 1991 to 1993, when predation pressure was most intense after the snowshoe hare decline, and positive from 1993 to 1995, when hares and predators were at low densities. Predation accounted for 125 of 130 mortalities (96%) of radio-collared squirrels. Adult survival was significantly lower in 1992 and 1993 than in 1994 and 1995, and was a strong predictor of annual rates of population change in arctic ground squirrels. Treatments were ranked as follows in their effect on adult survival: predator exclosure + food-supplemented > food-supplemented > predator exclosure > controls. Juvenile survival was lowest in 1992, and food addition and predator removal separately increased juvenile survival. On average, predator exclusion increased population densities twofold, food supplementation increased densities fourfold, and food supplementation and predator removal together increased densities 10-fold. We conclude that food and predation interact to limit arctic ground squirrel populations in the boreal forest during the decline and low phases of the snowshoe hare cycle. The snowshoe hare cycle may indirectly create a lagged secondary fluctuation in arctic ground squirrel populations through shared cyclic predators.

Effects of ambient temperature on metabolic rate, respiratory quotient, and torpor in an arctic hibernator

Arctic ground squirrels (Spermophilus parryii) overwinter in hibernaculum conditions that are substantially below freezing. During torpor, captive arctic ground squirrels displayed ambient temperature (T(a))-dependent patterns of core body temperature (T(b)), metabolic rate (TMR), and metabolic fuel use, as determined by respiratory quotient (RQ). At T(a) 0 to -16 degrees C, T(b) remained relatively constant, and TMR rose proportionally with the expanding gradient between T(b) and T(a), increasing >15-fold from a minimum of 0.0115 +/- 0.0012 ml O(2). g(-1). h(-1). At T(a) 0-20 degrees C, T(b) increased with T(a); however, TMR did not change significantly from T(b) 0 to 12 degrees C, indicating temperature-independent inhibition of metabolic rate. The overall change in TMR from T(b) 4 to 20 degrees equates to a Q(10) of 2.4, but within this range of T(b), Q(10) changed from 1.0 to 14.1. During steady-state torpor at T(a) 4 and 8 degrees C, RQ averaged 0.70 +/- 0.013, indicating exclusive lipid catabolism. At T(a) -16 and 20 degrees C, RQ increased significantly to >0.85, consistent with recruitment of nonlipid fuels. RQ was negatively correlated with maximum torpor bout length. For T(a) values <0 degrees C, this relationship supports the hypothesis that availability of nonlipid metabolic fuels limits torpor duration in hibernating mammals; for T(a) values >0 degrees C, hypotheses linked to body temperature are supported. Because anterior body temperatures differ from core, overall, the duration torpor can be extended in hibernating mammals may be dependent on brain temperature.

Production of tumor necrosis factor in cells of hibernating ground squirrels Citellus Undulatus during annual cycle

TNF production has been studied in peritoneal macrophages and splenic T cells of Arctic Yakutian ground squirrel ( Citellus Undulatus Pallas) in hibernating and awake animals in winter and in prehibernating autumn as well as in active euthermic spring-summer animals. A high level of TNF production in macrophages of ground squirrel is observed over the active period and during arousals in winter. There are no significant season variations in TNF production in splenic T lymphocytes of ground squirrels. This suggests the major role of activated macrophages in the arousals of hibernating animals. T lymphocyte proliferation in ground squirrels in the active period is higher than in winter, and the most significant seasonal variations are found in T cell mitogenic response, which increases in spring-summer period. Evidence is presented that functional activity of macrophages of squirrel in autumn has much in common with that in winter rather than in spring-summer period.

The interactive effects of food and predators on reproduction and overwinter survival of arctic ground squirrels

Summary 1. We examined the effects of food and predators on population limitation in the arctic ground squirrel (Spermophilus parryii plesius Richardson) in the boreal forest of the south‐western Yukon. We focused on ground squirrel reproduction and overwinter survival. 2. Squirrel populations were monitored by live‐trapping and radio‐telemetry from 1993 to the spring of 1996 on four control and four experimental areas (one predator exclosure treatment, two food addition treatments, and one predator exclosure plus food addition treatment). 3. Predator exclusion increased body condition, percentage lactating, percentage weaning litters, litter size, and doubled population density relative to controls, but had no effect on juvenile growth rate, overwinter survival, or juvenile emergence date. 4. Food addition advanced juvenile emergence date and increased adult body condition, percentage lactating, percentage weaning litters, litter size, population density relative to controls (4–7 fold), but had no effect on juvenile growth rate or overwinter survival. 5. Predator exclusion combined with food addition increased adult body condition, percentage lactating, percentage weaning litters, and population density relative to controls (19‐fold). 6. We conclude that arctic ground squirrels in the boreal forest are limited by an interaction between food and predation, acting primarily through changes in reproduction, and that their impact on density was multiplicative.

Contrasting stress response of male Arctic ground squirrels and red squirrels

Contrasting stress response of male Arctic ground squirrels and red squirrels

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.

Experimental manipulation of predation and food supply of arctic ground squirrels in the boreal forest

We examined whether arctic ground squirrel (Spermophilus parryii plesius) populations in northern boreal forest in the Yukon Territory, Canada, were limited by food, predators, or a combination of both, during the decline and low phases of a snowshoe hare cycle. From 1990 to 1995, populations were monitored in large-scale (1 km2) experimental manipulations. Squirrels were studied on eight 9-ha grids: four unmanipulated control grids, two food-supplemented grids, a predator-exclosure grid, and a predator-exclosure + food-supplemented grid. Population density was measured on all grids by livetrapping and active-season survival was measured using radiotelemetry. Population densities were lowest in 1992 and 1993 (2 years after the snowshoe hare population decline). Rates of population change were negative from 1991 to 1993, when predation pressure was most intense after the snowshoe hare decline, and positive from 1993 to 1995, when hares and predators were at low densities. Predation accounted for 125 of 130...

MRNA Stability and Polysome Loss in Hibernating Arctic Ground Squirrels (Spermophilus parryii)

mRNA Stability and Polysome Loss in Hibernating Arctic Ground Squirrels (Spermophilus parryii)

Indices of Population Size for Burrowing Mammals

There are few quick, precise indices for predicting population size of semifossorial mammals. We assessed the utility of powder-tracking and infrared thermal imaging to predict population size in the Aretic ground squirrel Spermophilus parryii) in the boreal forest of southwestern Yukon. Density estimated from livetrapping was strongly and linearly correlated with both indices (r = 0.81 for powder-tracking; r = 0.91 for infrared imaging). The slope of the relationship between density and the infrared index (0.10) deviated from a slope of 1, The slope of the relationship between density and the powder-tracking index (0.82) did not deviate from a slope of 1, but our power to detect departures from this slope using this index was low (0.10., We recommend infrared imaging and powder-tracking for monitoring population sizes of semifossorial mammals.

Temperatures of Hibernacula and Changes in Body Composition of Arctic Ground Squirrels over Winter

Soil temperatures near hibernacula of free-living arctic ground squirrels (Spermophilus parryii) were recorded over 3 winters (October–April 1993–1996) at Toolik Lake, Alaska. Means and minima of soil temperature at 20 burrows averaged −8.9 and −18.8°C, respectively. Soil temperatures were <−3°C for, on average, >5 months, which represented the duration of winter that hibernating arctic ground squirrels were actively thermogenic. Individual burrows did not differ significantly in mean soil temperature over 3 years, but significant differences in mean and minimum soil temperatures were observed among burrows. Sites of burrows with shrubby vegetation accumulated more snow and had significantly higher soil temperatures over winter than windswept sites in non-shrubby vegetation. Female ground squirrels hibernated in burrows that had significantly higher mean and minimum soil temperatures than burrows of males, and adults hibernated in burrows with significantly higher soil temperatures than burrows of juveniles. Although ground squirrels occupying colder burrows were predicted to lose more body mass during hibernation than those in warmer burrows, changes in body, fat, and lean masses over winter were not correlated with soil temperature for any sex or age. Relationships between change in body composition of hibernating arctic ground squirrels and temperatures of their hibernacula may be confounded by use of food caches, differing thermal conductance of nests, or differences in individual's energetics of hibernating not related to the gradient between body and soil temperatures.

Ascorbate and glutathione regulation in hibernating ground squirrels

Ground squirrels withstand up to 90% reductions in cerebral blood flow during hibernation as well as rapid reperfusion upon periodic arousals from torpor. Metabolic suppression likely plays a primary adaptive role which allows hibernating species to tolerate such phenomena. However, several other aspects of hibernation physiology are also consistent with tolerance to dramatic fluctuations in cerebral blood flow, suggesting that multiple neuroprotective adaptations may work in concert during hibernation. The purpose of the present work was to study the dynamics of the low molecular weight antioxidants, ascorbate and glutathione (GSH), during hibernation. Alterations in concentrations of ascorbate during hibernation and arousal in two species of hibernating ground squirrels suggest that it could play a protective role during hibernation or arousal. Samples were collected during the hibernation season from arctic ground squirrels (AGS; Spermophilus parryii) and 13-lined ground squirrels (TLS; S. tridecemlineatus) during prolonged torpor and in squirrels that did not hibernate or had not been hibernating for several weeks. We determined antioxidant levels in plasma, cerebrospinal fluid (CSF), and in frontal cortex, hippocampus and cerebellum using high-performance liquid chromatography (HPLC). Plasma ascorbate concentrations increased dramatically (3–4-fold) in both species during hibernation and rapidly returned to prehibernation levels upon arousal. By contrast, plasma GSH concentrations fell slightly or remained stable during hibernation. Ascorbate levels in the CSF doubled in hibernating AGS (not determined in TLS), while brain ascorbate content fell slightly (10–15%) in both species. Substantial increases in plasma and CSF ascorbate concentrations suggest that this antioxidant could play a protective role during hibernation and reperfusion upon arousal from hibernation.