Arctic Ground Squirrel Populations Research Articles

Landscape drivers of site occupancy by remnant populations of arctic ground squirrels (Urocitellus parryii)

Landscape drivers of site occupancy by remnant populations of arctic ground squirrels (Urocitellus parryii)

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.

Autumn conditions as a driver of spring phenology in a free-living arctic mammal

Several studies have shown that birds and mammals are breeding earlier in response to earlier spring conditions. Delay in the onset of winter should also affect reproductive timing and may allow for breeding later instead of earlier in spring, if extended autumns lengthen the season that food is available to offspring. Using 4 years of fine-scale environmental and phenological data of annual timing of hibernation and reproduction in two free-living populations of arctic ground squirrels in Northern Alaska, we show that the onset of winter snow-cover may influence females’ spring phenology via its interaction with the timing of hibernation of young-of-the-year (YoY). At the Atigun site, snowmelt occurs 26 days earlier and snow-cover occurs 14 days later than at the Toolik site. Previously, we found that Atigun females emerged and bred earlier than those at Toolik; however, here we show that this shift is not equivalent in magnitude to the earlier timing of spring conditions. At Atigun, females emerged and bred 13 days prior to snowmelt, while those at Toolik emerged and bred 34 days prior to snowmelt. We also found, importantly, that YoY entered hibernation after a set amount of time from birth regardless of site or environmental conditions. This resulted in Atigun YoY entering hibernation 24 (females) and 12 (males) days before snow-cover, but those at Toolik entering hibernation 0 (females) days before and 9 (males) days after snow-cover.This may allow females at Atigun to breed later (relative to snowmelt) in spring but select for early emergence and breeding of females at Toolik to allow sufficient time for offspring growth and preparation for hibernation. These results indicate that autumn conditions may influence subsequent spring phenology and changes in spring conditions may be only one factor influencing phenological shifts associated with climate change. We suggest that in areas with harsh spring conditions, such as the Arctic, animals may not shift their phenology to match earlier, but still unfavorable spring conditions, but may delay their timing of spring breeding if climate change also delays the onset of snow-cover, allowing sufficient timing for offspring growth and preparation prior to winter.

Mountain‐top and valley‐bottom experiences: the stress axis as an integrator of environmental variability in arctic ground squirrel populations

AbstractEnvironmental variation in mountainous regions can impose major differences in demography and physiology on animal populations that occupy a large elevation range. This variation can be both predictable and unpredictable. In the south‐western Yukon, arctic ground squirrel (AGS) populations occur all the way from the forested valley bottoms to the alpine meadows and, in so doing, experience a wide range of predation risk, forage quality and exposure to weather variables. To assess how AGS integrate these factors and respond to them, we measured fecal glucocorticoid metabolites (FCM) as an index of the stress axis on four sites at different elevations. We first validated the enzyme immunoassay with a hormonal challenge protocol and a simulated predator stressor. AGS show a strong diurnal pattern in FCM levels, with peaks at mid‐day and a marked increase in response to adrenocorticotropic hormone and the simulated predator and a decline in response to dexamethasone. The lag time between the challenge and its reflection in the feces was 4–12 h. Using this method in our field studies, we found that FCM levels decreased as the active season progressed; however, specific patterns differed among sites. We hypothesized that the early season peak in FCM levels followed by the general decline was due to brief, intense early season breeding, followed by the necessity of AGS to increase mass in preparation for hibernation. Although we found no clear, single explanation for the different FCM patterns among sites, we hypothesized that differences in seasonal climate and adverse weather may be major factors affecting FCM levels. The environment was markedly different between years, with 2008 being colder and wetter than 2009 and this was associated with AGS in 2008 having much higher FCM levels in general than 2009. We found that population density and visibility may also contribute. In conclusion, AGS live in a mosaic of habitats and each population is faced with a variety of environmental stressors; how they cope and respond to these stressors may not depend on a single factor but the complete aggregate of these stressors.

Evidence for source - sink dynamics in a regional population of arctic ground squirrels (Urocitellus parryii plesius)

Context Variable demographic rates can manifest themselves between habitat types in the form of source–sink dynamics where populations in sink habitats would not exist without the addition of migrants from source habitats. Aims Arctic ground squirrels (Urocitellus parryii pleisus (Osgood, 1900)) occupy a large geographic area in northern Canada and live in a variety of habitat types, including boreal forest, low-elevation meadows and alpine meadows, providing an opportunity to investigate the possible existence of source–sink dynamics. Methods We hypothesised that arctic ground squirrels in the south-western Yukon exhibit demographic characteristics indicative of source–sink dynamics. Boreal forest habitat could be a sink in spite of previous high squirrel densities, whereas meadows could be a source. We investigated this by mark–recapture live-trapping and radio-telemetry. Key Results In the boreal forest in the Kluane region, we found reduced recruitment, reduced population growth rates (λ), and reduced survivorship for radio-collared individuals that moved from low-elevation meadows into the boreal forest. There was no evidence from radio-collared juveniles of dispersal from high-density ground squirrel populations in alpine meadows down into boreal forest. Conclusions Boreal forest is a sink habitat for arctic ground squirrels. Source–sink dynamics observed between low-elevation meadow and boreal forest habitats appear to result from increased predation pressure in the boreal forest. The result has been a near extirpation of boreal forest arctic ground squirrels in the Kluane region since 1998. Implications Because the source areas of low-elevation meadows occupy only 7–9% of the lowland habitat, recolonisation of boreal forest sites has been very slow. Whereas alpine populations remain high in 2011, boreal forest populations remain near zero. Alpine populations do not appear to be a source for the boreal forest.

Phenological variation in annual timing of hibernation and breeding in nearby populations of Arctic ground squirrels

Ecologists need an empirical understanding of physiological and behavioural adjustments that animals can make in response to seasonal and long-term variations in environmental conditions. Because many species experience trade-offs between timing and duration of one seasonal event versus another and because interacting species may also shift phenologies at different rates, it is possible that, in aggregate, phenological shifts could result in mismatches that disrupt ecological communities. We investigated the timing of seasonal events over 14 years in two Arctic ground squirrel populations living 20 km apart in Northern Alaska. At Atigun River, snow melt occurred 27 days earlier and snow cover began 17 days later than at Toolik Lake. This spatial differential was reflected in significant variation in the timing of most seasonal events in ground squirrels living at the two sites. Although reproductive males ended seasonal torpor on the same date at both sites, Atigun males emerged from hibernation 9 days earlier and entered hibernation 5 days later than Toolik males. Atigun females emerged and bred 13 days earlier and entered hibernation 9 days earlier than those at Toolik. We propose that this variation in phenology over a small spatial scale is likely generated by plasticity of physiological mechanisms that may also provide individuals the ability to respond to variation in environmental conditions over time.

Early Wisconsinan (MIS 4) Arctic ground squirrel middens and a squirrel-eye-view of the mammoth-steppe

Fossil arctic ground squirrel ( Spermophilus parryii) middens were recovered from ice-rich loess sediments in association with Sheep Creek-Klondike and Dominion Creek tephras (ca 80 ka) exposed in west-central Yukon. These middens provide plant and insect macrofossil evidence for a steppe-tundra ecosystem during the Early Wisconsinan (MIS 4) glacial interval. Midden plant and insect macrofossil data are compared with those previously published for Late Wisconsinan middens dating to ∼25–29 14C ka BP (MIS 3/2) from the region. Although multivariate statistical comparisons suggest differences between the relative abundances of plant macrofossils, the co-occurrence of steppe-tundra plants and insects (e.g., Elymus trachycaulus, Kobresia myosuroides, Artemisia frigida, Phlox hoodii, Connatichela artemisiae) provides evidence for successive reestablishment of the zonal steppe-tundra habitats during cold stages of the Late Pleistocene. Arctic ground squirrels were well adapted to the cold, arid climates, steppe-tundra vegetation and well-drained loessal soils that characterize cold stages of Late Pleistocene Beringia. These glacial conditions enabled arctic ground squirrel populations to expand their range to the interior regions of Alaska and Yukon, including the Klondike, where they are absent today. Arctic ground squirrels have endured numerous Quaternary climate oscillations by retracting populations to disjunct “interglacial refugia” during warm interglacial periods (e.g., south-facing steppe slopes, well-drained arctic and alpine tundra areas) and expanding their distribution across the mammoth-steppe biome during cold, arid glacial intervals.

EVOLUTIONARY HISTORY OF THE ARCTIC GROUND SQUIRREL (SPERMOPHILUS PARRYII) IN NEARCTIC BERINGIA

Pleistocene glaciations had significant effects on the distribution and evolution of arctic species. We focus on these effects in Nearctic Beringia, a high-latitude ice-free refugium in northwest Canada and Alaska, by examining variation in mitochondrial cytochrome b (Cytb) sequences to elucidate phylogeographic relationships and identify times of evolutionary divergence in arctic ground squirrels (Spermophilus parryii). This arctic-adapted species provides an excellent model to examine the biogeographic history of the Nearctic due to its extensive subspecific variation and long evolutionary history in the region. Four geographically distinct clades are identified within this species and provide a framework for exploring patterns of biotic diversification and evolution within the region. Phylogeographic analysis and divergence estimates are consistent with a glacial vicariance hypothesis. Estimates of genetic and population divergence suggest that differentiation within Nearctic S. parryii occurred as early as the Kansan glaciation. Timing of these divergence events clusters around the onset of the Kansan, Illinoian, and Wisconsin glaciations, supporting glacial vicariance, and suggests that S. parryii survived multiple glacial periods in Nearctic Beringia. Across the Arctic, Beringia has been identified as an important regional refugium for a number of species. Within Nearctic Beringia, genetic differentiation across populations of arctic ground squirrels further reflects the effect of glacial patterns on a finer scale. The arctic ground squirrel has had a long evolutionary history in the Nearctic, with strong phylogeographic structure and stable clades persisting through multiple glacial cycles.

Dispersal in Adult Arctic Ground Squirrels: Why Do Males Do What They Do?

... The primary goal of my research on ground squirrels is to determine why adult males disperse. I use this system to understand the ecology of mating behaviour and the evolutionary implications of different mating strategies. Two hypotheses I am investigating are (1) that adult males disperse to avoid mating with their daughters, who breed very close to where they were born, and (2) that adult males disperse to increase their access to females for mating. I also quantify survival and reproductive costs and benefits associated with dispersal for adult males in order to identify potential explanations for the different mating strategies used by individuals within a population. To address these objectives, I study a population of arctic ground squirrels in the ruby ranges, located along the eastern shore of Kluane Lake, Yukon Territory. ... I live-trap, ear-tag, and radio-collar adult male ground squirrels and follow them throughout the summers to determine dispersal distances and rates and adult male survival. To measure male reproductive success, I monitor the female population for signs of pregnancy and, after locating the pregnant females' natal nests, monitor them for the presence of juveniles. As the juveniles emerge, I trap them to determine litter sizes and take tissue samples. I am now analyzing the DNA of these tissue samples to determine which males sired which litters. ... My data analysis is not yet complete, but preliminary results challenge many of the assumptions previously held about dispersal of adult arctic ground squirrels and male mating strategies in general. ... The high survival rate among dispersers contradicts the common assumption that dispersing animals are at high risk of death. Interesting results are also emerging from the comparison of population dynamics of ground squirrels at the alpine and lower-elevation sites. The majority of mortality in the boreal forest population occurs because of predation during the active season, but overwinter mortality appears to contribute most to yearly death in the alpine population. Contrary to most species that inhabit a range of elevations, arctic ground squirrels at the higher-elevation site have significantly higher birth rates than those at the lower-elevation site. In addition, there is a trend toward larger litters and survival of more young to weaning age at the higher elevation. Usually, we expect high-elevation sites to have extreme conditions with lower food availability, resulting in reduced reproductive performance. Arctic ground squirrels at high elevation may experience reproductive success because they have evolved in open tundra areas and rely on sight for predator detection. Trees at low elevations obscure visibility, and this may be the reason why squirrels in the boreal forest are physiologically stressed. ... These results suggest that many factors predicted by global climate change, such as shifts in tree line and predator distribution, as well as changes in the winter climate that affect overwinter survival, have the potential to interact and affect ground squirrel population size. ...

Territoriality and male reproductive success in arctic ground squirrels

Although territorial defense is a common form of reproductive competition among male vertebrates, the exact reproductive consequences of this behavior are often poorly understood. To explore relationships between territoriality and reproductive success in a nongroup-living mammal, we quantified patterns of space use, mating success, and fertilization success for males in a free-living population of arctic ground squirrels (Spermophilus parryii plesius). Because litters of this species are sired almost exclusively by a female’s first mate, we predicted that territory ownership would be associated with first access to estrous females. During the 2-week period when mating occurred, each male in the study population attempted to defend a distinct portion of the habitat, although the success of this defense varied among individuals. Twenty-six of 28 females monitored mated with the male on whose territory they resided. However, the majority of females observed throughout estrus (65%; n 20) also mated with at least one other male, indicating that territory ownership was not associated with exclusive access to females. In contrast, territory ownership was significantly associated with first access to estrous females; 20 (71.4%) of 28 females mated first with the male on whose territory they resided. In this regard, the behavior of S. parryii plesius parallels that of socially monogamous birds in which territorial defense by males functions to deter extrapair copulations by females. Although territorial defense represents an important component of male reproductive success in arctic ground squirrels, other aspects of male behavior (e.g., the ability to dominate agonistic interactions on the day of a female’s estrus) are also critical. We suggest that future studies of vertebrate mating systems will benefit by viewing such defense as only one of multiple axes along which conspecific males compete for access to females.

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.

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.

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.

Population Limitation in Arctic Ground Squirrels: Effects of Food and Predation

1. We examined the relative importance of food and predators in limiting Arctic ground squirrel (Spermophilus parryii plesius Richardson) populations in the boreal forest of the southwestern Yukon during the peak and early decline of a snowshoe hare cycle (Lepus americanus Erxleben). 2. Squirrels were live-trapped from 1990 to 1992 on two control grids and three experimental treatments (food addition, mammalian and avian predator exclosure, and food addition plus mammalian predator exclosure). Adult squirrels were radiocollared on all areas in 1992. 3. Food addition increased densities 3-8 times, generally increased reproductive traits (increased proportion of females lactating, doubled recruited litter sizes, resulted in earlier emergence of juveniles), increased immigration rates (but only in 1992), resulted in heavier females though not males at emergence in spring, and resulted in more rapid growth rates of juvenile males, but not of juvenile females. It had no effect on active season or overwinter survival rates. 4. Exclusion of predators had virtually no effect on any demographic variable measured, except for population densities in 1991 when they were approximately double those of the control populations. 5. Food addition plus exclusion of mammalian predators resulted in demographic changes that were comparable to those of food addition alone. 6. Thus, it appeared that food, not predators, limited ground squirrel populations at this stage of the hare cycle. However, independent of experimental treatment, active season survival of adult squirrels declined markedly from 1990 (high hare numbers) to 1992 (low hare numbers). Most of the radiocollared squirrels disappearing in 1992 were killed by predators and this was coincident with high densities of predators. In the predator exclosures, all predation mortalities resulted from avian predators which we could not exclude. 7. We conclude that both food and predators interact to limit Arctic ground squirrel populations during the peak and early decline of the hare cycle.

Paternal behaviour and killing of young in Arctic ground squirrels

During the summers of 1977, 1978 and 1979, I investigated killing of infants and young juveniles (for simplicity referred to herein as infanticide) and paternal behaviour in a population of Arctic ground squirrels, Spermophilus parryii, near Haines Junction, Yukon Territory. Males defended territories primarily during the period when young ground squirrels were mot susceptible to being killed. Killing was most likely after removal of males that had been resident during the mating period. Immigrant males, which were unlikely to have sired the young in their new area of residence, tended to kill young, and it appeared that infanticide was a consequence of a male's establishing residence in a new area. An analysis of the time budget of males and females suggested that males acted as lookouts during lactation, when females were spending the most time feeding. I suggest that males behave paternally through defending territories because they increase the likelihood of survival of young that they may have sired; I also discuss the various tactics that both males and females might be expected to adopt given the existence of infanticide in the population.