Free-living Arctic Ground Squirrels Research Articles

Survival estimates of free-living arctic ground squirrels (Urocitellus parryii): effects of sex and biologging

Hibernation is associated with long lifespan: on average, hibernating mammals live 15% longer than nonhibernators of equivalent mass. We investigated how survival varies with sex, season, and the deployment of biologgers in arctic ground squirrels (Urocitellus parryii (Richardson, 1825)), a widely distributed northern hibernator. The duration of hibernation in arctic ground squirrels differs markedly by sex: females hibernate 30% longer each year than males, a behavioural trait that could positively affect female survival. Additionally, males engage in aggressive territorial and food cache defense in spring and fall, which may decrease survival in this sex. From 13 years of mark–recapture data, we estimated apparent survival of arctic ground squirrels in Arctic Alaska (USA) using Cormack–Jolly–Seber models in program MARK. We found that females had higher annual survival ([Formula: see text] (95% confidence interval (CI): 0.469, 0.913)) than males ([Formula: see text] (95% CI: 0.416, 0.670)), with a maximum observed lifespan (10 years) that exceeded that of males (6 years). We also show that biologger use and implantation did not significantly impact survival. Quantifying basic arctic ground squirrel demographics from this well-studied population illustrates how sex-specific hibernation parameters may influence lifespan differences in male and female arctic ground squirrels and provides support for the safety of biologging devices.

Plasticity and repeatability of activity patterns in free-living Arctic ground squirrels

Social interactions can shape daily activity patterns, and this is an area of growing research interest. The propensity for individuals to be active at certain times of day may structure interactions with competitors and potential mates, influencing fitness outcomes. Aspects of daily activity such as timing of activity onset and offset exhibit within-individual repeatability, which raises the possibility that they may be subject to natural and sexual selection. This study used a biologging approach in free-living Arctic ground squirrels, Urocitellus parryii , to test the hypothesis that interactions between the sexes shape temporal patterns of daily activity. We predicted that males would become active earlier than females during the mating period, consistent with sexual selection on activity timing. We also examined repeatability in activity timing and how repeatability estimates are affected by sampling methodology. We deployed collar-mounted light loggers on ground squirrels and used timing of light transitions to determine daily onset and offset of above-ground activity. We observed 87 animals over 3 years, collecting over 7500 observations of daily activity. We found that daily activity timing had moderate (onset) to low (offset) adjusted repeatability. The difference in daily activity timing between the sexes varied seasonally: males remained active later than females during mating, while females initiated activity earlier and extended activity later during lactation. Adjusted repeatability estimates were sensitive to sampling methodology: they varied seasonally and declined with increased behavioural sampling. These results suggest that offset, not onset, may be shaped by sexual selection and that life history differences shape sex-dependent activity patterns in ground squirrels. We propose that activity onset may be under more strict circadian control than offset. This study suggests that researchers must consider seasonality and sampling design when estimating behavioural repeatability. Biologging could transform studies of individual variation by enabling high-frequency sampling of free-living animals. • Arctic ground squirrels showed evidence of circadian chronotypes. • Activity onset and offset differed by sex, especially during mating and lactation. • Activity onset reflected life-history energetics rather than sexual selection. • Repeatability estimates were affected by sampling frequency and design.

Glucocorticoids and activity in free-living arctic ground squirrels: Interrelationships between weather, body condition, and reproduction

The dynamic relationship between glucocorticoids and behavior are not well understood in wild mammals. We investigated how weather, body condition, and reproduction interact to affect cortisol levels and activity patterns in a free-living population of arctic ground squirrels (Urocitellus parryii). As a proxy for foraging and escape behaviors, collar-mounted accelerometers and light loggers were used to measure above-ground activity levels and the amount of time squirrels spent below the surface, respectively. Fecal cortisol metabolites (FCMs) were quantified to assess glucocorticoid secretion in squirrels. Male and female squirrels differed in above-ground activity levels and time spent below-ground across the active season, with males being most active during mating and females most active during lactation. We also found that female, but not male, squirrels exhibited seasonal variation in FCM levels, with concentrations highest during mid-lactation and lowest after the lactation period. In female squirrels, the seasonal relationships between breeding stage, activity, and FCM levels were also consistent with changes in maternal investment and the preparative role that glucocorticoids are hypothesized to play in energy mobilization. Body condition was not associated with FCM levels in squirrels. As predicted, deteriorating weather also influenced FCM levels and activity patterns in squirrels. FCM concentrations were affected by an interaction between temperature and wind speed when seasonal temperatures were lowest. In addition, above-ground activity, but not time spent below-ground, positively correlated with FCM levels. These results suggest that, although ground squirrels avoid inclement weather by remaining below-ground, activation of the stress axis may stimulate foraging activity.

Environmental heterogeneity affects seasonal variation in thyroid hormone physiology of free-living arctic ground squirrels (Urocitellus parryii)

Thyroid hormones (TH) are key regulators of metabolism that could play an important role in altering physiology and energy allocation across life-history stages. Here, we examine seasonal TH dynamics from 345 plasma samples collected from 134 free-living arctic ground squirrels (Urocitellus parryii (Richardson, 1825)) across three consecutive years (2014–2016). We also examine whether unbound levels of triiodothyronine (free T3) in plasma are correlated with total T3levels and total thyroxine (T4) levels, and whether fecal T3metabolite levels correlate with plasma TH levels. We found significant differences in plasma TH levels across stages of the annual cycle, but these differences were highly inconsistent across years. However, within a given time period, pregnant females had lower free T3levels compared with lactating females. We also found that although free T3was correlated with both total T3and total T4in plasma, fecal T3was not positively correlated with plasma TH levels. Given the lack of consistent differences across life-history stages, we suggest environmental heterogeneity may be the primary driver of TH dynamics, masking any potential endogenous seasonal rhythms in TH secretion. We urge caution in the use of fecal T3metabolites as a proxy for circulating levels and encourage further research to understand the observed discrepancy.

Coping with differences in snow cover: the impact on the condition, physiology and fitness of an arctic hibernator.

The Earth's climate is changing at an unprecedented rate and, as ecologists, we are challenged with the difficult task of predicting how individuals and populations will respond to climate-induced changes to local and global ecosystems. Although we are beginning to understand some of the responses to changing seasonality, the physiological mechanisms that may drive these responses remain unknown. Using long-term data comparing two nearby populations (<20 km apart) of free-living arctic ground squirrels in northern Alaska, we have previously shown that the timing of spring snowmelt greatly influences their phenology of hibernation and reproduction in a population and site-specific manner. Here, we integrate these site-specific phenologies with body condition, stress physiology, reproductive success and juvenile recruitment to understand phenotypic selection in the two populations. We found that at the site with relatively late spring snowmelt and early autumn snow cover: (i) adult females were larger and in better body condition but had significantly higher stress hormone levels; (ii) females had similar numbers of comparably sized offspring, but offspring had higher stress hormone levels; and (iii) offspring density was lower just prior to hibernation. Thus, adult females at the two sites appear to use different coping strategies that allow them to maintain reproductive fitness; however, marked shortening of the active season because of later snowmelt in spring and earlier snow cover in autumn may compromise juvenile recruitment. We discuss the significance of these findings within the broader context of changing animal-environment relationships.

Seasonal loss and resumption of circadian rhythms in hibernating arctic ground squirrels.

Circadian clocks are near universal among organisms and play a key role in coordinating physiological and metabolic functions to anticipate or coincide with predictable daily changes in the physical and social environment. However, whether circadian rhythms persist and are functionally important during hibernation in all mammals is currently unclear. We examined whether circadian rhythms of body temperature (T b) persist during multi-day, steady-state torpor and investigated the association between timing of animal emergence, exposure to light, and resumption of activity and T b rhythms in free-living and captive male arctic ground squirrels. High-resolution (0.02 °C) temperature loggers revealed that circadian rhythms of T b were not present during deep torpor in free-living arctic ground squirrels. Significant circadian rhythms of T b resumed, however, following the resumption of euthermia, but prior to emergence, though rhythms became much more robust coincident with aboveground emergence. Additionally, squirrels maintained in captivity under conditions of constant darkness spontaneously developed significant circadian rhythms of T b and activity soon after ending torpor. Exposing animals to a 5-s pulse of light within a week when they ended torpor increased the strength of rhythms. Our results are consistent with the hypothesis that circadian clock function is inhibited during hibernation in arctic ground squirrels, and we postulate that exposure to external stimuli, such as light in free-living animals, and meals or acute disturbance for captive squirrels, may enhance T b rhythmicity by synchronizing loosely coupled circadian oscillators within the suprachiasmatic nucleus.

Metabolic Rate and Prehibernation Fattening in Free-Living Arctic Ground Squirrels

Hibernating mammals become sequestered and cease foraging during prolonged seasonal periods of reduced or unpredictable food availability and instead rely on cached food and/or endogenous reserves of fat and protein accumulated during the previous active season. The gain in weight is due to increased food consumption, but it also has been hypothesized that hibernators maximize rates of fattening by decreasing costs of maintenance before weight gain, reflected in reduced resting metabolic rate (RMR). We recorded repeated measures of total body, lean, and fat mass in individual adult male and female arctic ground squirrels across their active season and found that squirrels increased body mass by 42% (males) and 62% (females). This gain was achieved through a 17% increase in lean mass and a 7-8-fold increase in fat mass; however, mass gain was not linear and patterns differed between sexes. Contrary to our hypothesis, decreases in RMR were not associated with rapid mass gain. We found RMR of males increased (whole-animal RMR or lean-mass-specific RMR) or remained constant (mass-specific RMR) for most of the active season and decreased only after the majority of mass had been gained. In females, although RMR (whole-animal, mass-specific, and lean-mass RMR) generally decreased across the active season, the greatest decrease occurred late in the active season after the majority of mass had been gained. In conclusion, arctic ground squirrels do not trade off metabolism to facilitate rates of weight gain before hibernation, but they do use energy sparing strategies before hibernation that help maintain peak mass.

Hibernation and Circadian Rhythms of Body Temperature in Free-Living Arctic Ground Squirrels

In mammals, the circadian master clock generates daily rhythms of body temperature (T(b)) that act to entrain rhythms in peripheral circadian oscillators. The persistence and function of circadian rhythms during mammalian hibernation is contentious, and the factors that contribute to the reestablishment of rhythms after hibernation are unclear. We collected regular measures of core T(b) (every 34 min) and ambient light conditions (every 30 s) before, during, and following hibernation in free-living male arctic ground squirrels. Free-running circadian T(b) rhythms at euthermic levels of T(b) persisted for up to 10 d in constant darkness after animals became sequestered in their hibernacula in fall. During steady state torpor, T(b) was constant and arrhythmic for up to 13 d (within the 0.19°C resolution of loggers). In spring, males ended heterothermy but remained in their burrows at euthermic levels of T(b) for 22-26 d; patterns of T(b) were arrhythmic for the first 10 d of euthermia. One of four squirrels exhibited a significant free-running T(b) rhythm (τ = 22.1 h) before emergence; this squirrel had been briefly exposed to low-amplitude light before emergence. In all animals, diurnal T(b) rhythms were immediately reestablished coincident with emergence to the surface and the resumption of surface activity. Our results support the hypothesis that clock function is inhibited during hibernation and reactivated by exposure to light, although resumption of extended surface activity does not appear to be necessary to reinitiate T(b) cycles.

Thermoregulatory changes anticipate hibernation onset by 45 days: data from free-living arctic ground squirrels

Hibernation is a strategy of reducing energy expenditure, body temperature (T(b)) and activity used by endotherms to escape unpredictable or seasonally reduced food availability. Despite extensive research on thermoregulatory adjustments during hibernation, less is known about transitions in thermoregulatory state, particularly under natural conditions. Laboratory studies on hibernating ground squirrels have demonstrated that thermoregulatory adjustments may occur over short intervals when animals undergo several brief, preliminary torpor bouts prior to entering multiday torpor. These short torpor bouts have been suggested to reflect a resetting of hypothalamic regions that control T(b) or to precondition animals before they undergo deep, multiday torpor. Here, we examined continuous records of T(b) in 240 arctic ground squirrels (Urocitellus parryii) prior to hibernation in the wild and in captivity. In free-living squirrels, T(b) began to decline 45 days prior to hibernation, and average T(b) had decreased 4.28 °C at the onset of torpor. Further, we found that 75 % of free-living squirrels and 35 % of captive squirrels entered bouts of multiday torpor with a single T(b) decline and without previously showing short preliminary bouts. This study provides evidence that adjustments in the thermoregulatory component of hibernation begin far earlier than previously demonstrated. The gradual reduction in T(b) is likely a component of the suite of metabolic and behavioral adjustments, controlled by an endogenous, circannual rhythm, that vary seasonally in hibernating ground squirrels.

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.

Data logging of body temperatures provides precise information on phenology of reproductive events in a free-living arctic hibernator

Precise measures of phenology are critical to understanding how animals organize their annual cycles and how individuals and populations respond to climate-induced changes in physical and ecological stressors. We show that patterns of core body temperature (T (b)) can be used to precisely determine the timing of key seasonal events including hibernation, mating and parturition, and immergence and emergence from the hibernacula in free-living arctic ground squirrels (Urocitellus parryii). Using temperature loggers that recorded T (b) every 20min for up to 18months, we monitored core T (b) from three females that subsequently gave birth in captivity and from 66 female and 57 male ground squirrels free-living in the northern foothills of the Brooks Range Alaska. In addition, dates of emergence from hibernation were visually confirmed for four free-living male squirrels. Average T (b) in captive females decreased by 0.5-1.0°C during gestation and abruptly increased by 1-1.5°C on the day of parturition. In free-living females, similar shifts in T (b) were observed in 78% (n=9) of yearlings and 94% (n=31) of adults; females without the shift are assumed not to have given birth. Three of four ground squirrels for which dates of emergence from hibernation were visually confirmed did not exhibit obvious diurnal rhythms in T (b) until they first emerged onto the surface when T (b) patterns became diurnal. In free-living males undergoing reproductive maturation, this pre-emergence euthermic interval averaged 20.4days (n=56). T (b)-loggers represent a cost-effective and logistically feasible method to precisely investigate the phenology of reproduction and hibernation in ground squirrels.

BODY TEMPERATURE AND ACTIVITY PATTERNS IN FREE-LIVING ARCTIC GROUND SQUIRRELS

We investigated influences of the thermal environment on patterns of body temperature (Tb), activity, and use of burrows during the active season in a population of free-living arctic ground squirrels (Spermophilus parryii). Arctic ground squirrels normally exhibited a daily 58C range in Tb, and had higher Tb when above ground than when in burrows (P , 0.0001). This difference decreased as standard operative temperature (Tes; an index of environmental heat load) increased. Ground squirrels entered burrows more frequently on warmer compared to average or cooler days and when Tb exceeded 398C. On cool days with heavy precipitation, ground squirrels remained almost exclusively below ground, and peaks in Tb were associated with brief aboveground forays. Time on the surface was maximal (about 80% between 0500 and 2200 h) at Tes ¼ 17‐338C and decreased proportionately with decreasing Tes from 178 Ct o� 28C. Forty-six percent of variation in timing of presence above ground could be explained by a series of thermal and nonthermal variables related to environmental heat transfer. This suggests that diurnal activity patterns in this arctic environment with 24-h daylight result from a strategy that minimizes thermoregulatory costs.

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.

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.

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.

Annual Cycle of Body Composition and Hibernation in Free-Living Arctic Ground Squirrels

We monitored a natural population of arctic ground squirrels ( Spermophilus parryii kennicottii ) on the North Slope of Alaska for seasonal changes in body mass and composition and dates of immergence into and emergence from hibernation. Yearlings and adult females were at the lowest body mass of their active season at emergence in spring. Their mean body mass did not increase for 1 month after emergence and peaked in July (adult females) and August (yearlings). Body mass of adult males was near the highest of the active season when they emerged from hibernation and decreased by 21% over the subsequent 10-day mating season. Juveniles gained body mass during their active season, except for significant losses associated with dispersal. During hibernation, females lost >30% of their body mass, but adult males emerged in spring without significant decreases in body mass, fat, or lean. Yearling and nonreproductive males were significantly lower in fat but not lean mass at emergence than immergence, and females were significantly lower in fat and lean mass. Arctic ground squirrels entered hibernation over a >1 -month interval beginning in early August; females entered before males, and adults of each sex immerged before juveniles. Reproductive males emerged before females, and fatter females emerged significantly earlier than leaner females. Vaginal estrus was maximal at 3 days post-emergence. Nonreproductive males emerged last from hibernation. Mean ± SE days in hibernation was 240.1 ± 12.1 for adult females (69% of the year), 235.8 ± 10.3 for juvenile females, 230.3 ± 4.2 for nonreproductive males, 220.3 ± 12.5 for adult males, and 214.7 ± 6.5 for juvenile males. Timing of immergence into and emergence from hibernation for arctic ground squirrels did not differ significantly from sciurid populations in temperate latitudes.