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.     

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.     

Cape ground squirrels as ecosystem engineers: modifying habitat for plants,small mammals and beetles in Namib Desert grasslands

Burrowing and foraging of semi‐fossorial rodents can affect species distribution and composition. Ground squirrels dig large burrow systems for refuge from predators and temperature extremes. Burrowing and foraging around burrows by squirrels may affect habitat and resource distributions for other organisms. We examined the impact of Cape ground squirrels (Xerus inauris) on vegetation, small mammals and beetles during winter and summer in grasslands on the edge of the Namib Desert. At each burrow system and paired control site without burrows, we estimated plant cover and height using quadrats (N = 8 paired sites), small mammal abundance and species richness using mark‐recapture techniques (N = 8 paired sites) and beetle abundance and species richness using pitfall traps (N = 6 paired sites, winter only). Squirrel burrowing and foraging activities resulted in lower plant cover and height, higher small mammal abundance and lower beetle abundance and species richness. Squirrels also reduced more plant cover in winter compared to summer, but had no effect on small mammal species richness. Furthermore, plant cover and height were higher in summer, whereas small mammal abundance and species richness were higher in winter. Our results suggest that Cape ground squirrels are important ecosystem engineers that influence plant and animal communities in the Namib Desert grasslands.     

Body temperature and behaviour of golden hamsters (Mesocricetus auratus) and ground squirrels (Spermophilus tridecemlineatus) in a thermal gradient

Golden hamsters and thirteen-lined ground squirrels were maintained individually in a thermal gradient (14°C to 33°C) for several weeks under a 14L: 10D light-dark cycle. Animals of both species showed robust daily rhythms of body temperature and locomotor activity with acrophases consistent with the habits of the species (diurnal acrophases in the diurnal squirrels and nocturnal acrophases in the nocturnal hamsters). Hamsters showed a robust daily rhythm of temperature selection 180° out of phase with the rhythms of body temperature and locomotor activity. Squirrels did not show a daily rhythm of temperature selection. These results raise the hypothesis that a daily rhythm of temperature selection is exhibited by nocturnal but not by diurnal endotherms.     

Eavesdropping of an African ground squirrel on the heterospecific alarm calls of a noisy ground-nesting bird

Animals gather information about their environment from a variety of sources to enable adaptive decision-making behaviour. Eavesdropping on heterospecific alarm calls enhances predator avoidance, reduces time spent vigilant and allows for more time on daily activities such as foraging. If the information is relevant and reliable, individuals that respond to heterospecific signals may benefit from a wider range of information at a low marginal cost. The Cape ground squirrel (Xerus inauris) and crowned lapwing (Vanellus chilensis) are ground-dwelling species that are taxonomically distant but share similar predators, habitat and anti-predatory behaviours. We used playback experiments of the alarm calls produced by conspecifics and lapwings to investigate the vigilance responses of adult female Cape ground squirrels. Squirrels responded with greater vigilance to both squirrel and lapwing alarm calls, and no changes of vigilance levels were observed in response to a control sound. However, contrary to our predictions, changes in vigilance and time to relax did not differ between conspecific versus heterospecific playbacks. The results from our study suggest that squirrels perceive lapwing alarm calls as relevant and reliable information and that responding to it could increase their survival.     

The Social Organization of the Cape Ground Squirrel (Xerus inauris; Rodentia: Sciuridae)

The Cape ground squirrel (Xerus inauris) of southern Africa is a tropical species that does not hibernate. Field observations using scan and all-occurrence sampling revealed that this species was highly social. Female Cape ground squirrels formed social units of related females and their subadult young, as is typical for other ground squirrels. Female social groups were usually composed of 2–3 adult females and 2–3 subadults of either sex. Members of these female social groups shared sleeping burrows and feeding ranges. Female social groups did not cooperatively defend their feeding ranges from adjacent groups in other burrow clusters. Interactions within female social groups were highly amicable, and no dominance hierarchy was evident. Males in this species also lived in groups. These all-male bands of up to 19 individuals lived almost independently from female groups. The entire male band shared one home range, although ephemeral sub-bands were formed daily. The composition and size of these sub-bands changed daily. Interactions among males, which were largely amicable, included allogrooming and sleeping together. Analysis of interactions within the band indicated a stable, linear, dominance hierarchy among males. Dispersal in this species appeared to be male biased as is typical of other ground-dwelling squirrels, with males dispersing at reproductive maturity. Males joining male bands were thus dispersers and were not likely to be closely related. Sociality in the Cape ground squirrel may be summarized as highly social female kin clusters and associated social non-kin bands of males.     

Antipredator behaviour and predator recognition in Belding's ground squirrels

This study evaluates whether Belding's ground squirrels (Spermophilus beldingi) recognize predators under natural conditions. I observed these squirrels for 300 h during two consecutive summers, during which I described 1029 aerial and terrestrial interactions, including 299 interactions with animals known to prey on squirrels. Squirrels responded differentially to predators and non-predators, to predators that hunt differently, and to contextually different interactions with the same predator. Responses shown in encounters with predators included Trill and Chirp vocalizing, upright Posting, crouching, running to burrow entrances, entering burrows, Approaching or chasing predators, and doubling-back on pursuing predators. Ground squirrels appear to adjust their antipredator behaviour depending on the amount and kind of danger they face during an encounter.     

Direct vs. Indirect Benefits of Caching by Gray Squirrels (Sciurus carolinensis)

Individuals of many species cache food to gain direct benefits from consuming their own caches, but individuals of a few species also gain indirect benefits by sharing caches with kin. We investigated whether gray squirrels cache primarily to gain direct benefits or if they also gain indirect benefits by sharing caches with kin. If squirrels share caches with kin, then genetically related squirrels should live near one another and cache near one another to facilitate cache sharing. In contrast, if squirrels cache primarily for direct benefits, then they should clump their caches near the center of their ranges to facilitate cache defense. This study was conducted with 140 squirrels in a 10 ha forest. DNA was extracted from blood samples taken from squirrels, and genetic similarity scores from randomly amplified polymorphic DNA (RAPD) loci were used to measure relatedness. Squirrels were given piles of pecans for caching at six sites and observed from a blind. We recorded the direction squirrels took nuts from piles and at one site determined the location of caches. For male–female comparisons, related squirrels lived significantly closer to one another than unrelated squirrels, but this was not the case for female–female and male–male comparisons. The genetic similarity of neighboring squirrels did not influence the location of caches or the direction that squirrels took nuts from piles. Squirrels clumped their own caches and moved nuts toward their own home range centers. These results suggest that gray squirrels cache primarily to gain direct benefits rather than indirect benefits.     

A test of non‐kin social foraging in the southern flying squirrel (Glaucomys volans)

It can be challenging to understand the evolution of sociality, particularly the occurrence of co‐operation by non‐kin. Southern flying squirrels (Glaucomys volans) are an interesting example of non‐kin co‐operation because of the mutual benefits obtained by social thermoregulation during winter. Because group survival confers benefits to the entire group, flying squirrels may also follow an aggregation economy, whereby co‐operative foraging during winter is advantageous. However, the extent of such social foraging in flying squirrels is unknown. We tested for social foraging of southern flying squirrels, and also for relatedness among foraging groups. To determine the structure of foraging groups, we set up and remotely monitored feeding stations and nest cavities. All squirrels at the study site were tagged with passive integrated transponder (PIT) tags and nests and feeding stations were monitored with automated PIT‐tag recorders for a 24‐month period. Squirrels were found most often foraging alone. Squirrels that were recorded foraging together comprised unrelated individuals that were also found to share nest cavities. Squirrels were also recorded travelling farther distances between nest cavity and feeding station in the winter season than in the summer season, suggesting that, during winter, squirrels trade‐off proximity to food caches for membership in a nest group. Our data suggest that squirrels forage and cache alone in their summer home range and make solitary returns to this summer range to collect their cache during the winter months, despite exhibiting social winter nesting. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 1126–1135.     

Use of space by the African Striped Ground Squirrel Xerus erythropus

Five Striped Ground Squirrels Xerus erythropus were radio-tracked at Katumani, Kenya, for periods of up to 10 days. The results were used to explore their short-term use of space. Definitions of the terms 'home range' and 'core', and some aspects of the methodology of home-range analysis are discussed. In an area of low-productivity bushland, subject to intermittent drought, where their food supply was patchy and unpredictable, the squirrels travelled about 1.5 km per day, and occupied rather large home ranges averaging 12.4 ha. Levels of aggression between conspecifics was low, home ranges were not defended, and there was considerable range overlap. Nights were spent in burrows which were commonly shared with conspecifics. On most days a single relatively long exploratory excursion was made outside the home range, extending the average area of the total range to some 40 ha. Despite the presence of major environmental features which might have been expected to affect the squirrels' foraging behaviour, such as cultivated fields, home range use was very symmetrical, suggesting that essential resources (food, shade, burrows) were widely dispersed throughout the range. Squirrels foraged alone, harvesting small, scattered, high-quality food items, mainly vegetable. Activity was interrupted from time to time to retire to the shade to lose heat, and a midday rest was taken. Only part of the home range was used each day. A variable degree of central concentration of activity could be observed. The squirrels' use of space enabled them to exploit available food resources opportunistically and efficiently, and made them difficult to control effectively.     

The relative roles of the parasol-like tail and burrow shuttling in thermoregulation of free-ranging Cape ground squirrels,Xerus inauris

As small arid-zone mammals, Cape ground squirrels (Xerus inauris) are unusual in being diurnally active. It is postulated that they remain active during the day by using their parasol-like tails to shade their bodies whilst foraging. However, no studies have continuously measured body temperature to determine the effect of using the tail as a parasol, relative to other thermoregulatory behaviours, such as burrow retreat. We caught four free-ranging Cape ground squirrels (673 ± 36 g) and surgically implanted miniature temperature-sensitive data loggers into their abdomens, to record body temperature every 5 min to an accuracy of 0.04 °C, before they were released back into their home range and observed for two weeks. Mean daily peak black globe temperature was 41 °C, and daily peak body temperature reached 40 °C. Ground squirrels raised their tails significantly more often at globe temperatures above 30 °C, but raising the tail did not decrease body temperature, nor prevent body temperature rising. Ground squirrels retreated to burrows, at 18 °C, significantly more often at high body temperatures and body temperature dropped 1–2 °C before re-emergence. We believe that the tail was raised to provide thermal comfort during high solar radiation exposure, and that burrow retreat was employed to dissipate a heat load and remain active diurnally.     

Daily rhythms of oxygen consumption, body temperature, activity and melatonin in the Norwegian lemming Lemmus lemmus under northern summer photoperiod

Rodents inhabiting high latitudes, close to the Arctic Circle or above it, are exposed to near 24 h daylight during the summer season. An example to such rodent species is the Norwegian lemming Lemmus lemmus, which is distributed in northern Fennoscandia. We measured daily rhythms of heat production (VO₂), body temperature (T_b), motor activity and melatonin secretion (measured from its metabolite 6-sulfatoximelatonin 6-SMT) in individuals exposed to natural day light, Oulu Finland, in August 1997 and at a controlled ambient temperature of 22 °C. Our results show a daily rhythm of VO₂ with an acrophase at 04:00 h and minimal values measured at 16:00 h, with a significant difference (p<0.001) between mean day and night values. 6-SMT also shows a daily rhythm with maximal secretion during the dark phase 24:00 and 06:00 h in which total 6-SMT values were 2.92±1.1 and 3.87±1.2 ng, respectively. The lowest values were recorded at 12:00 h; 0.86±0.63 ng. These results suggest that lemmings show a VO₂ and melatonin daily rhythms, which seem to correlate with each other and it appears that melatonin secretion increases heat production.     

The effects of season and dietary salt content on body temperature daily rhythms of common spiny mice from different micro-habitats

We compared body temperature (T(b)) daily rhythms in two populations of common spiny mice, Acomys cahirinus, during summer and winter months in relation to increasing dietary salt content. Mice were collected from the North and South facing slopes (NFS and SFS) of the same valley, that are exhibiting mesic and xeric habitats, respectively. During the summer, whilst mice were offered a water source containing 0.9% NaCl, SFS individuals had T(b) peak values at 24:00, whereas NFS individuals had peak values at 18:00. When the salinity of the water source was increased, from 0.9 to 2.5% and then 3.5%, the difference between maximal and minimal T(b) of both populations increased. In addition, with increased salinity, the T(b) daily peak of SFS mice shifted to 18:00. During the winter, the mean daily T(b) values of both populations of mice were lower than during the summer. At 0.9% salinity, the NFS mice exhibited a daily T(b) variation with a peak at the beginning of the night. However, we did not detect any significant variation in daily T(b) in the SFS mice. At 2.5% salinity, the difference between the mean daily T(b) of mice from the two slopes increased. In winter we were unable to increase the salinity to 3.5% as the animals began to lose weight rapidly. We suggest that common spiny mice that inhabit these two micro-habitats are forming two discrete populations that respond differently to the environmental pressures prevailing in each habitat, by evolving different physiological capacities.     

Thirteen-lined ground squirrel (Sciuridae: Spermophilus tridecemlineatus) antipredator vigilance decreases as vigilance cost increases

Vigilance is a commonly studied antipredator phenomenon. However, little research has been conducted on the effects of visual obstruction coupled with a manipulation of the cost of performing vigilance behaviours. We tested the hypothesis that antipredator vigilance decreases as the cost of performing antipredator vigilance increases in free-ranging thirteen-lined ground squirrels. We presented adult ground squirrels with peanut butter within six rectangular Plexiglas boxes (opaque on all sides; clear on top) ranging in length from 15.2 to 91.4 cm. Squirrels repeatedly entered and withdrew from the boxes, to scan visually the surrounding area. As box length increased and, therefore, the cost of the vigilance behaviour increased, the ground squirrels increased their mean time within the box per entry and decreased their alertness per unit of trial time. Squirrels took longer to traverse the longer boxes, but their travel time into the boxes was significantly slower than their travel time out of the boxes. We interpreted this difference in travel time to indicate a behavioural conflict that occurred only when the squirrels entered the box (food versus vigilance) and did not exist once the squirrels had begun to exit from the box. The hypothesis that a decrease in ground squirrel antipredator vigilance would benefit the squirrels by decreasing their time exposed to predators (i.e. decreased trial duration, which was determined by the squirrels' behaviour), was not supported. Copyright 1999 The Association for the Study of Animal Behaviour.     

Intra- and inter-individual variability in the circadian rhythm of body temperature of rats,squirrels, dogs,and horses

In order to explore the often neglected issue of the relationship between intra- and inter-subject variability of circadian rhythms, we evaluated the variability in four parameters of the circadian rhythm of body temperature under controlled laboratory conditions. To avoid the bias of potential selection of an idiosyncratic species, we conducted the study on four different species: the laboratory rat, the thirteen-lined ground squirrel, the domestic dog, and the horse. In rats and squirrels, three of the four parameters of the body temperature rhythm (mean level, amplitude, and regularity of waveform) showed greater inter-subject variability than intra-subject variability. The two variabilities were not different from each other in dogs and horses. Intra- and inter-subject variabilities of acrophase (time of peak) were not significantly different in any of the species, and their magnitudes were similar in all species, which suggests that acrophase is a very dependable parameter in the analysis of circadian rhythms, even though its overall variability is not particularly low.     

Rattlesnake Rattles and Burrowing Owl Hisses: A Case of Acoustic Batesian Mimicry

Burrowing owls nest and roost in ground squirrel burrows, a refuge frequently used by rattlesnakes. When cornered, burrowing owls produce a vocal hiss that has been suggested to mimic a rattlesnake's rattle. To test this hypothesis, we conducted an experiment using two populations of Douglas ground squirrels that differ in their evolutionary histories with rattlesnakes. Both squirrel populations were sympatric with burrowing owls. Squirrels from a population subjected to natural selection by rattlesnakes treated the owl hiss as cautiously as they did the rattle, and responded with greater caution to the rattle and hiss than to two control sounds. Squirrels from a rattlesnake-free area, however, were less systematic in differentiating among the rattle, the hiss, and the control treatments. Such variation between ground-squirrel populations provides evidence that the burrowing owl's defensive hiss currently functions as an acoustic Batesian mimic of a rattlesnake's rattle.     

Chronotype predicts positive affect rhythms measured by ecological momentary assessment

Evening chronotype, a correlate of delayed circadian rhythms, is associated with depression. Altered positive affect (PA) rhythms may mediate the association between evening chronotype and depression severity. Consequently, a better understanding of the relationship between chronotype and PA may aid in understanding the etiology of depression. Recent studies have found that individuals with evening chronotype show delayed and blunted PA rhythms, although these studies are relatively limited in sample size, representativeness and number of daily affect measures. Further, published studies have not included how sleep timing changes on workday and non-workdays, or social jet lag (SJL) may contribute to the chronotype-PA rhythm link. Healthy non-depressed adults (n?=?408) completed self-report affect and chronotype questionnaires. Subsequently, positive and negative affects were measured hourly while awake for at least two workdays and one non-workday by ecological momentary assessment (EMA). Sleep variables were collected via actigraphy and compared across chronotype groups. A cosinor variant of multilevel modeling was used to model individual and chronotype group rhythms and to calculate two variables: (1) amplitude of PA, or the absolute amount of daily variation from peak to trough during one period of the rhythm and (2) acrophase, or the time at which the peak amplitude of affect rhythms occurred. On workdays, individuals with evening chronotype had significantly lower PA amplitudes and later workday acrophase times than their morning type counterparts. In contrast to predictions, SJL was not found to be a mediator in the relationship between chronotype and PA rhythms. The association of chronotype and PA rhythms in healthy adults may suggest the importance of daily measurement of PA in depressed individuals and would be consistent with the hypothesis that evening chronotype may create vulnerability to depression via delayed and blunted PA rhythms.     

Temporal and temperature effects on the maximum rate of rewarming from hibernation

During hibernation animals oscillate from near ambient (T(a)) to euthermic body temperatures (T(b)). As animals arouse, the rate of rewarming (RRW) might be expected to simply increase as a function of time. We monitored the T(b) of golden-mantled ground squirrels (Spermophilus lateralis) housed at 4, 8, 12, and 16 degrees C during natural arousals. The maximum RRW, the time required to reach a maximum RRW, and the relative time index all demonstrated negative relationships with T(a). The T(b) corresponding to maximal RRW demonstrated a positive relationship with T(a). Squirrels reached maximal RRW when they had generated 30 to 40% of the heat required to reach a euthermic T(b). These data suggest that arousal is more constrained than expected and that both time and temperature influence the RRW.     

Morning release into artificial burrows with retention caps facilitates success of European ground squirrel (<Emphasis Type="Italic">Spermophilus citellus</Emphasis>) translocations

Relocating ground squirrels within their natural distribution range is a popular tool in wildlife management in Central–Eastern Europe. Nevertheless, wildlife management lacks both a carefully developed and tested translocation guide and methods. We evaluated conditions of release method (time of release and retention of animals) that affect short-term settlement of translocated ground squirrels in the central region of Hungary. In a field experiment, we translocated 117 individuals from an international airport to a protected site in 2000. We found that release time should precede the animals' natural, daily activity peak. The use of retention caps combined with artificial burrows instead of complex acclimation cages works successfully to prevent animals from dispersing from the release site.     

Scaling the daily oscillations of breathing frequency and skin temperature in mammals

Among mammals, the peak-trough difference (PTD) of the circadian pattern of body temperature (T(b)) drops very little with the increase in body mass (W), despite the large increase in heat capacitance and thermal inertia. We asked whether this might be contributed by systematic differences in the circadian pattern of breathing frequency (f) and skin temperature (Tskin), which are parts of the control mechanisms of heat loss. Measurements had been conducted on animals of eight species, chosen to cover a four-fold range in W, while resting and awake. The oscillation of f preceded that of T(b) in 7 of the 8 species, and its acrophase did not correlate with W. The daily mean and PTD of f scaled with W in a similar manner (respectively, W(-)(23) and W(-)(0.29)), the PTD averaging about 20% of the daily mean. The circadian oscillations of Tskin, measured in specimens of five species at three locations (abdomen, ear and thigh), were in phase with T(b). Neither the PTD nor the acrophase of Tskin changed systematically with W. The differences between T(b) and Tskin (means, peaks and troughs) decreased significantly with W; on average, the T(b)-Tskin difference scaled to W(-)(0.19). In conclusion, the relative amplitudes and the acrophase of Tskin and f did not show systematic inter-species differences. The progressive increase of Tskin with W could be a factor in maintaining the PTD of T(b) within a narrow range among mammals of very different size.