Circadian rhythms of body temperature and locomotor activity in the antelope ground squirrel, Ammospermophilus leucurus.

We studied circadian rhythms of body temperature and locomotor activity in antelope ground squirrels (Ammospermophilus leucurus) under laboratory conditions of a 12L:12D light-dark cycle and in constant darkness. Antelope ground squirrels are diurnally active and, exceptionally among ground squirrels and other closely related members of the squirrel family in general, they do not hibernate. Daily oscillations in body temperature consisted of a rise in temperature during the daytime activity phase of the circadian cycle and a decrease in temperature during the nighttime rest phase. The body temperature rhythms were robust (71% of maximal strength) with a daily range of oscillation of 4.6°C, a daytime mean of 38.7°C, and a nighttime mean of 34.1°C (24-h overall mean 36.4°C). The body temperature rhythm persisted in continuous darkness with a free-running period of 24.2h. This pattern is similar to that of hibernating species of ground squirrels but with a wave form more similar to that of non-hibernating rodents. Daily oscillations in body temperature were correlated with individual bouts of activity, but daytime temperatures were higher than nighttime temperatures even when comparing short episodes of nocturnal activity that were as intense as diurnal activity. This suggests that although muscular thermogenesis associated with locomotor activity can modify the level of body temperature, the circadian rhythm of body temperature is not simply a consequence of the circadian rhythm of activity.

Seasonal patterns of body temperature in response to experimental photoperiod variation in a non-hibernating ground squirrel.

Unlike numerous other members of the holarctic Tribe Marmotini of the squirrel family (Sciuridae) that typically exhibit spontaneous bouts of torpor that progress into an annual season of hibernation, members of the genus Ammospermophilus (antelope ground squirrels) do not enter torpor, and they remain active throughout the year in nature. We have experimentally evaluated seasonal patterns of variation in the circadian rhythm of body temperature in captive A. leucurus over a two-and-a-half-year period by exposing groups to either a constant daily photoperiod of 12 h light or a seasonally changing photoperiod that cycled between a summer maximum of 16 h per day and a winter minimum of 8 h; ambient air temperature was maintained at 26 °C. All squirrels showed continuous, year-round diurnal locomotor activity, and the group exposed to seasonally changing photoperiod adjusted onset and end of activity to changes in duration of the photoperiod. Animals in both groups showed a marked circadian rhythm of core body temperature with a typical daytime level of about 38 °C and nighttime level of about 35 °C for most of each year, but the group exposed to naturally changing daylength surprisingly reduced the level of its circadian oscillation by about 2 °C at the winter seasonal extreme of shortest daily illumination to a daytime level about 36 °C and a nocturnal level of about 33 °C. Despite this modest experimentally induced reduction in the level of the circadian rhythm of body temperature, we conclude that A. leucurus shows an overall stable annual pattern of circadian rhythmicity of its core body temperature that is consistent with a lack of any other evidence that the species engages in torpor or hibernation.

Genetic and phenotypic variation across a hybrid zone between ecologically divergent tree squirrels (Tamiasciurus).

A hybrid zone along an environmental gradient should contain a clinal pattern of genetic and phenotypic variation. This occurs because divergent selection in the two parental habitats is typically strong enough to overcome the homogenizing effects of gene flow across the environmental transition. We studied hybridization between two parapatric tree squirrels (Tamiasciurus spp.) across a forest gradient over which the two species vary in coloration, cranial morphology and body size. We sampled 397 individuals at 29 locations across a 600-km transect to seek genetic evidence for hybridization; upon confirming hybridization, we examined levels of genetic admixture in relation to maintenance of phenotypic divergence despite potentially homogenizing gene flow. Applying population assignment analyses to microsatellite data, we found that Tamiasciurus douglasii and T. hudsonicus form two distinct genetic clusters but also hybridize, mostly within transitional forest habitat. Overall, based on this nuclear analysis, 48% of the specimens were characterized as T. douglasii, 9% as hybrids and 43% as T. hudsonicus. Hybrids appeared to be reproductively viable, as evidenced by the presence of later-generation hybrid genotypes. Observed clines in ecologically important phenotypic traits-fur coloration and cranial morphology-were sharper than the cline of putatively neutral mtDNA, which suggests that divergent selection may maintain phenotypic distinctiveness. The relatively recent divergence of these two species (probably late Pleistocene), apparent lack of prezygotic isolating mechanisms and geographic coincidence of cline centres for both genetic and phenotypic variation suggest that environmental factors play a large role in maintaining the distinctiveness of these two species across the hybrid zone.

Nuclear and mitochondrial DNA reveal contrasting evolutionary processes in populations of deer mice (Peromyscus maniculatus).

We investigated a major geographic break in mitochondrial DNA (mtDNA) haplotypes in deer mice, Peromyscus maniculatus, by analysing spatial variation in a 491-bp fragment of the mtDNA control region from 455 samples distributed across a north-south transect of 2000 km in Western North America. To determine whether the mtDNA break was reflected in the nuclear genome, we then compared spatial variation in 13 nuclear microsatellites of 95 individuals surrounding the mtDNA break. Using a canonical correlation analysis we found that nuclear genomic variation was not correlated with mtDNA differentiation. The contrasting patterns of variation in mtDNA and nuclear DNA are consistent with a hypothesis of historic genetic drift that occurred in isolated refugia combined with recent gene flow between the formerly isolated refugial populations. A Mantel test of genetic vs. geographic distance revealed that recent gene flow between deer mouse populations has been high. We conclude that past vicariant events associated with Pleistocene climate changes together with recent gene flow have created the observed intra-specific cytonuclear discordance in Western North America.

Saltbush leaves: excision of hypersaline tissue by a kangaroo rat.

Dipodomys microps climbs into shrubs and harvests leaves of the halophyte Atriplex confertifolia throughout the year. The epidermal vesicles of these leaves are high in electrolyte concentration, but the specialized photosynthetic parenchyma which is arranged concentrically about the vascular bundles is low in electrolytes and high in starch. The lower incisors of D. microps are broad, flattened anteriorly, and chisel-shaped (unlike those of other kangaroo rats, which are rounded and awl-shaped) and are used to shave off the hypersaline, peripheral tissue of the leaves so that the inner tissue can be eaten. This atypical feeding behavior should minimize the reliance of D. microps on the unpredictable seed crops of desert annuals, and also favor its coexistence with other species of Dipodomys, which are primarily granivorous.

Exploring determinants of behavioral chronotype in a diurnal-rodent model of human physiology.

Numerous studies conducted with human participants have shown that differences in chronotype, defined as individual patterns of early or late beginning of daily activity, have implications for many biobehavioral processes, such as cognitive performance, mood, impulsivity, academic achievement of college students, and mental health. However, the determinants of individual variation in chronotype have not been investigated. Basic research on circadian rhythms has provided a basis for investigating the causes of chronotype variation, but experimental tests of pertinent hypotheses are difficult to conduct with human subjects. This limitation can be overcome by use of animal models. This study was conducted with a rodent species, the antelope ground squirrel (Ammospermophilus leucurus), that, like humans, is active during the daytime, exhibits a spread of chronotypes, and has a similar average free-running circadian period. We found chronotype to be a stable trait within individuals based on strong consistency of separate determinations made six months apart (correlation r = 0.91). We also found a moderate correlation of chronotype with the duration of the active phase (r = -0.51) and with free running period (r = 0.34), but weak correlation with rhythm robustness (r = 0.16), and no correlation with photic responsiveness or with masking responses. The best multiple regression model, incorporating the duration of the active phase, free-running period, and rhythm robustness, explained 38% of the variance in chronotype. Although 62% of the variance in chronotype remained unaccounted for, the results are encouraging because they document the possibility of using a diurnal rodent as a model for the investigation of the determinants of chronotype variation in humans.

Diurnally active rodents for laboratory research.

Although inbred domesticated strains of rats and mice serve as traditional mammalian animal models in biomedical research, the nocturnal habits of these rodents make them inappropriate for research that requires a model with human-like diurnal activity rhythms. We conducted a literature review and recorded locomotor activity data from four rodent species that are generally considered to be diurnally active, the Mongolian gerbil ( Meriones unguiculatus), the degu ( Octodon degus), the African (Nile) grass rat ( Arvicanthis niloticus), and the antelope ground squirrel ( Ammospermophilus leucurus). Our data collected under 12-hour light/dark cycles confirmed and expanded the existing literature in showing that the activity rhythms of antelope ground squirrels and African grass rats are stronger and more concentrated in the light phase of the light/dark cycle than the activity rhythms of Mongolian gerbils and degus, making the former two species preferable and more reliable as models of consistent diurnal activity in the laboratory. Among the two more strongly diurnal species, antelope ground squirrels are more exclusively diurnal and have more robust activity rhythms than African grass rats. Although animals of these two species are not currently available from commercial suppliers, African grass rats are indigenous to a wide area across the north of Africa and thus available to researchers in the eastern hemisphere, whereas antelope ground squirrels can be found throughout much of western North America's desert country and, therefore, are more easily accessible to North American researchers.

NPY and galanin in a hibernator: hypothalamic gene expression and effects on feeding.

Neuropeptides such as neuropeptide Y (NPY) and galanin may play a role in regulating the pronounced seasonal changes in food intake shown by golden-mantled ground squirrels (Spermophilus saturatus). We used in situ hybridization histochemistry to localize the expression of NPY and galanin mRNA in the hypothalamus of normally feeding animals. NPY mRNA was abundantly expressed in the arcuate nucleus, while galanin mRNA was concentrated in both the arcuate nucleus and the dorsomedial nuclei. When NPY (0.1, 0.5, 2, and 8 micrograms) or galanin (0.1, 0.5, 2, and 8 micrograms) were injected into the third cerebral ventricle, food intake was significantly and dose-dependently increased over the subsequent 30 min. NPY stimulated significant increases in food intake for up to 2 h whereas galanin's effect did not extend beyond 30 min. Our results suggest that hibernating and nonhibernating rodents share common neural substrates for the regulation of food intake. Seasonal modulation of these neural pathways may contribute to annual cycles of food intake in hibernating mammals.

Adaptations for leaf eating in the great basin kangaroo rat, Dipodomys microps.

Dipodomys microps forages in saltbush (Atriplex confertifolia), gathering the leaves into its external check pouches and returning them to the burrow to be cached or eaten. The leaves are available throughout the year and contain 50-80% water. D. microps can survive on these leaves in the laboratory without other food or water, but it is unusual among kangaroo rats in that it quickly succumbs when placed on a diet of air-dried seeds without water or succulent plant material. Its mean urine concentration on the seed diet was 2827 mOsm/l, which is lower than any previously reported for the genus. On the other hand, D. merriami, which occurs with D. microps and is well known as a seed specialist, cannot survive on the saltbush leaves, although it is capable of living on a seed diet without water or green vegetation. D. microps is behaviorally and morphologically specialized for exploiting the unusual leaves of A. confertifolia. The leaves are higher in electrolyte content than the leaves of most plants; but the electrolytes, which are most highly concentrated on the leaf surfaces, apparently serve in the maintenance of water balance in the leaves. D. microps does not usually consume saltbush leaves in toto, but rather uses its unique, chisel-shaped lower incisors to shave off the outer tissue from both sides of the leaf, and then consumes the inner tissue. Sodium concentration with respect to water in the eaten tissue was only 3% that of the discarded shavings, and the specialized photosynthetic parenchyma which is eaten is high in starch content.The highly divergent dietary habits of D. microps should serve to minimize competition with its granivorous congeners. Some of the present limits to the geographic distribution of D. microps are a reflection of its reliance on the leaves of perennial shrubs throughout the year; but where its does occur, D. microps should be independent of the unpredictable availability of ephemeral annuals.

The periodicity of daily activity and its seasonal changes in free-ranging and captive kangaroo rats.

Populations ofDipodomys microps andD. merriami in eastern California (37°11'N. Lat.) are active on the surface throughout the night and during the whole year. These two species, and the males and females within each species, show no significant differences in times of beginning or end of activity. Beginning and end of nightly activity generally fall within the brighter part of the twilights, even though the total time spent on the surface by individuals is at times only an hour or two, or even less, per night. Near the summer solstice in southern Saskatchewan, Canada (50°45'N. Lat.), when sunset and sunrise were 7 h 43 min apart, the time from onset to end of activity in a population ofD. ordii (the northernmost of all kangaroo rats) was only 6 h; these animals were also only on the surface at intervals during the night.During the course of the year, the light intensity at which the first individualD. microps andD. merriami became active on the surface varied between 200 and 2,000 lux, and the light intensity at which the last individual was active in the morning varied between 50 and 20,000 lux. There was no apparent influence of the moonlight cycle upon the onset and end of activity; in fact the light levels at beginning and end of activity are about 2 to 4 orders of magnitude brighter than that at full moon. The onset of activity is fairly synchronous within the population in that most individuals surface within about a fhalf hour of each other; furthermore, two-thirds of the individuals appearing in the first 32 min of activity had already appeared within the first 12 min. There appears to be a similar, synchronous, but less well marked end of activity in the morning.There were systematic seasonal changes in the time relative to sunset and sunrise respectively, and in the corresponding light intensities, at which the animals began and ended activity. The phase relationship between the onset of activity and sunset (ψ onset) showed tow maxima and two minima per year, but the phase relationship between the end of activity and sunrise (ψ end) showed only one maximum and one minimum per year. On the other hand, the annual range of change in the evening phaseψ onset (28 min) was half the annual range of change in the morning phaeψ end (57 min). Such a conspicuous difference in frequency and amplitude ofψ onset andψ end has not previously been reported for any species, nor has it been predicted by models of circadian rhythms and phase relationships. The resemblance of the course of annual change inψ onset to annual change in length of twilight and the resemblance of annual change inψ end to change in length of night are discussed. These differences may underline a circadian system based on two separate, but normally coupled components, which could be separately synchronized by dusk and dawn respectively.The daily running-wheel activity of 10 individually housedD. merriami under natural skylight in Los Angeles (34°05'N. Lat.) began and ended at light intensities two to three orders of magnitude lower than corresponding values for surface activity in the field. The onset and end of activity for the captive population did not show the synchronous peaks typical of the field populations; nor did the nightly activity patterns of individuals show peaks at the beginning and end of the night. The social isolation of the captive kangaroo rats is suggested as a factor contributing to differences between activity parameters in captivity and field.Proximate and ultimate factors shaping the periodicity of activity in kangaroo rats are discussed. It is hypothesized that social interactions involving some form of territoriality may give rise to a population peak in onset of activity in some solitary mammals such as kangaroo rats. A set of criteria is presented for comparing vertebrate species with regard to the periodicity and synchronization of both daily and seasonal functions.

Life with fur and without: experimental field energetics and survival of naked meadow voles.

Hair is considered to be a basic mammalian feature that provides protection and insulation, promoting energy conservation and survival. To quantify the functional significance of mammalian pelage, we tested the short-term experimental effects of fur removal in a natural population of the California vole, Microtus californicus, in winter. The daily energy expenditure (DEE) of seven voles was directly measured in the field using stable isotopes, first with the animals in their natural condition and then again after experimental removal of pelage by shaving. The initial mean±SD DEE of 96.0±23.1 kJ/day increased by only about 10%, to 106.3±21.4 kJ/day, following shaving. The voles showed a body mass loss of 5%, about half of which was due to fur removal. Comparing slightly larger samples of all animals whose local survival could be documented, we found 100% survival over the 5 initial days of the experimental manipulation in 16 control animals and nine shaved animals; over the following 3 weeks the survival of shaved mice did not differ significantly from that of controls. We were surprised that the average increase in energy expenditure of voles without fur was so modest, though the range of individual values was great, and likewise we were surprised that shaved voles survived as well as they did. M. californicus survives naturally in winter under conditions of social aggregation that include huddling together of individuals in nests; this situation probably provided our experimentally shaved voles an opportunity to minimize the energetic disadvantages of pelage loss. They may also have employed a variety of compensatory physiological and behavioral responses, including reduction in activity time and food intake, and perhaps a related small decline in body mass. Our limited sample sizes made it difficult to detect subtle differences that may have been biologically significant in the system we studied. Nonetheless, we can reaffirm that fur has an insulative value that promotes energy economy and survival. However, we also conclude that mammalian physiology and behavior are sufficiently complex and flexible that a variety of responses can be deployed to promote survival under unusual circumstances such as those of our experimental test.

Effects of seed distribution and competitors on seed harvesting efficiency in heteromyid rodents.

The foraging strategies of four naturally co-existing heteromyid rodent species were investigated: Dipodomys deserti (≈100 g), D. merriami (≈38 g), Microdipodops pallidus (≈13 g), and Perognathus longimembris (≈7 g). In 208 over-night laboratory foraging trials animals were provided with millet seed distributed in clumped and scattered patterns. Net removal of seeds from the foraging arena and amounts of seeds in cheek pouches and in caches were determined. When alone in an areana none of these species specialized extensively on either clumped or scattered seeds, although each tended to take more clumped than scattered seeds. When placed together with other individuals, animals once again tended to cache more clumped than scattered seeds in all but one paired combination of species: P. longimembris cached more scattered than clumped seeds when opposed by D. deserti. This suggests that the smaller species obtained a less preferred distribution of seeds in the face of competition. The two smaller species showed a great reduction in general foraging success in the presence of either of the two larger species. In general, a species cached less seeds when faced by larger opponent species.

Reingestion of feces in rodents and its daily rhythmicity.

The ingestion of feces is widespread among rodent species and is an extensively employed component of the repertoire of feeding behaviors in some species. Coprophagy is thus a significant consideration in the nutrition and dietary ecology of many rodents. As certain fecal pellets pass from the anus, they are taken up directly into the mouth, chewed, and swallowed. The nocturnally active herbivorous kangaroo rat Dipodomys microps ingests about 1/4 of the feces it produces daily and the daily pattern of reingestion shows a consistent rhythm. For about 8 h of the daytime, during the non-foraging, resting phase of the day, D. microps reingests all fecal pellets produced; during the remainder of the day it leaves all feces produced. The reingested feces contain more nitrogen and water, and less inorganic ions than the non-reingested feces. The extent of reingestion varies among rodent species in relation to diet, and coprophagy is more important in the more herbivorous species. The granivorous kangaroo rat D. merriami ingests feces rarely. The herbivorous vole Microtus californicus ingests about 1/4 of its feces, as does D. microps. However, in contrast to D. microps, M. californicus shows a series of rhythmic, short-term (one to several hour duration) alternations between reingestion and non-reingestion during the course of the day and night. This pattern correlates with the pattern of foraging in M. californicus, which extends over both night and day.

Annual cycle of energy and time expenditure in a golden-mantled ground squirrel population.

We have analyzed seasonal shifts of energy and time allocation in a population of golden-mantled ground squirrels (Spermophilus saturatus) by directly measuring total daily energy expenditure (DEE) with an isotopic technique ("doubly labeled water"=dlw), and by estimating components of total DEE through an integration of field behavioral observations with laboratory-measured rates of energy expenditure (oxygen consumption) associated with major behavioral and physiological states. Hibernation laster about 7 1/2 months, and the 4 1/2-month activity season consisted of mating, a 28-d gestation of 3-5 young, 5 1/2 weeks of postnatal growth building to a peak in lactation just before the young emerged above ground, an additional 2-3-week period of maternal care before dispersal, and finally restoration of body mass preceding hibernation. Although the hibernation season comprised nearly two-thirds of the year, it involved only 13-17% of annual energy expenditure, leaving about 85% of energy expenditure for the active season. Ground squirrels were actually present on the surface for only about 11% of the year's time, and the foraging time required to obtain the total annual energy supply amounted to only about 2% of the year's time. The squirrels fed mainly on herbs in the early season and hypogeous fungi later; both were used extensively during peak lactation when female energy expenditure and demand were maximal. Average daily foraging time increased steadily throughout the season to a maximum of 28% of aboveground time as availability of greens diminished and fungus predominated in the diet; time availability did not limit foraging since the animals sat on average for 65% of the daily surface time of about 7 h. Timing of reproduction is apparently optimized such that peak reproductive energy demands are matched with maximal food availability and moderate thermal conditions that minimize energy demand. Despite the greater body mass of males, the greatest total DEE (measured by dlw) of any squirrels at any time of year was that of females during peak lactation. For production of young and lactation through above-ground emergence of an average litter of 2.7, females required a total energy increase of 24% above annual nonreproductive metabolism. Yearling females all bred and performed similarly to older females, yet some costs were greater because the yearlings began and ended hibernation at smaller mass, compensated by giving birth later, and finally showed a greater absolute increase in body mass over the active season than older females. Annual metabolic energy expenditure of breeding males was about 18% greater than that of females, due to greater male body mass. Yet the annual energy intake requirement for both sexes was essentially identical (about 42MJ) due to the greater reproductive export by females in the form of newborn and milk. During the mating season males showed wide-ranging exploratory behavior and social interactions, including aggression, that involved considerable locomotory energy expenditures. Although we did not directly account for the energetics of these specific reproductive behaviors, they are critical to male reproductive success and on a daily basis they probably involved much greater energy expenditure than sperm production. Some yearling males avoided these costs by foregoing testicular development, yet they allocated four times as much energy to growth as older males, thereby increasing somatic condition for the future.

Daily rhythms of food intake and feces reingestion in the degu, an herbivorous Chilean rodent: optimizing digestion through coprophagy.

Animals must match their foraging and digestion to seasonal changes in availability and quality of food. When these parameters decline, the animal's performance limits for extracting energy and nutrients may be challenged. In the laboratory, we investigated daily patterns of food processing on a low-quality (high-fiber) diet of alfalfa in an herbivorous, day-active rodent, the degu (Octodon degus), which inhabits semiarid central Chile. We manipulated timing of food availability, from continuous availability down to as little as 5 h/d. Degus maintained weight while digesting only 53% of dry-matter consumption. With food continuously available in a metabolic cage, the animals ate more food and deposited about twice as much feces in the day as at night. Continuous 24-h behavioral observation revealed that degus were actually defecating at the same rate both night and day but then ingesting most of the feces they produced at night. Further experimental treatments challenged animals with limited periods of food availability that matched natural foraging patterns. With either 11 h of daytime food availability or only 5 h (in morning and afternoon periods of 2.5 h each), degus consumed as much food as those with 24-h food availability. Continuous 24-h behavioral observations revealed in the 11-h group that nearly all feces produced at night were reingested and nearly none were reingested in the day, whereas the 5-h group resorted to further coprophagy during the 6-h midday interval with no food. Despite these differences in timing of food intake and coprophagy in response to the three experimental treatments, the degus were defecating at the same rate both night and day, which indicated a constant rate of output from the colon. This suggests a range of adjustments of digestive physiology to the timing of gut function by balancing coprophagy with ingestion of food. Overall, 38% of 24-h feces production was reingested, and 87% of this coprophagy occurred at night. The ingestion of feces during parts of the day when food is unavailable provides for continued intake into the digestive tract and appears to represent an increase in overall efficiency of gut use.

Diversification and gene flow in nascent lineages of island and mainland North American tree squirrels (Tamiasciurus).

Pleistocene climate cycles and glaciations had profound impacts on taxon diversification in the Boreal Forest Biome. Using population genetic analyses with multilocus data, we examined diversification, isolation, and hybridization in two sibling species of tree squirrels (Tamiasciurus douglasii and Tamiasciurus hudsonicus) with special attention to the geographically and genetically enigmatic population of T. hudsonicus on Vancouver Island, Canada. The two species differentiated only about 500,000 years ago, in the Late Pleistocene. The island population is phylogenetically nested within T. hudsonicus according to our nuclear analysis but within T. douglasii according to mitochondrial DNA. This conflict is more likely due to historical hybridization than to incomplete lineage sorting, and it appears that bidirectional gene flow occurred between the island population and both species on the mainland. This interpretation of our genetic analyses is consistent with our bioclimatic modeling, which demonstrates that both species were able to occupy this region throughout the Late Pleistocene. The divergence of the island population 40,000 years ago suggests that tree squirrels persisted in a refugium on Vancouver Island at the last glacial maximum, 20,000 years ago. Our observations demonstrate how Pleistocene climate change and habitat shifts have created incipient divergence in the presence of gene flow. Sequence data have been archived in GenBank­accession numbers: KF882736­KF885216.

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.

Seasonal glucocorticoid responses to capture in wild free-living mammals.

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

Photoperiod affects daily torpor and tissue fatty acid composition in deer mice.

Photoperiod and dietary lipids both influence thermal physiology and the pattern of torpor of heterothermic mammals. The aim of the present study was to test the hypothesis that photoperiod-induced physiological changes are linked to differences in tissue fatty acid composition of deer mice, Peromyscus maniculatus ( approximately 18-g body mass). Deer mice were acclimated for >8 weeks to one of three photoperiods (LD, light/dark): LD 8:16 (short photoperiod), LD 12:12 (equinox photoperiod), and LD 16:8 (long photoperiod). Deer mice under short and equinox photoperiods showed a greater occurrence of torpor than those under long photoperiods (71, 70, and 14%, respectively). The duration of torpor bouts was longest in deer mice under short photoperiod (9.3 +/- 2.6 h), intermediate under equinox photoperiod (5.1 +/- 0.3 h), and shortest under long photoperiod (3.7 +/- 0.6 h). Physiological differences in torpor use were associated with significant alterations of fatty acid composition in approximately 50% of the major fatty acids from leg muscle total lipids, whereas white adipose tissue fatty acid composition showed fewer changes. Our results provide the first evidence that physiological changes due to photoperiod exposure do result in changes in lipid composition in the muscle tissue of deer mice and suggest that these may play a role in survival of low body temperature and metabolic rate during torpor, thus, enhancing favourable energy balance over the course of the winter.

Polyunsaturated lipid diet lengthens torpor and reduces body temperature in a hibernator.

Membrane lipids of vertebrate animals that tolerate cold are high in polyunsaturated fatty acids. Because the lipid composition of cellular membranes in mammals can be experimentally altered by diet, we investigated whether a diet rich in polyunsaturated fatty acids would lengthen bouts of torpor and reduce the minimum body temperature in hibernating chipmunks (Eutamias amoenus) compared with a diet rich in saturated fatty acids. Animals on the highly unsaturated diet showed significantly longer bouts of torpor, lower minimum body temperatures, and lower metabolic rates than those on a saturated diet. Animals on a control diet were intermediate. These dietary adjustments apparently influence the control of body temperature by the central nervous system, which results in a modification of the pattern of torpor. The observations also suggest a role of nutritional ecology in hibernation.