C. Loren Buck

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.

Central nervous system regulation of mammalian hibernation: implications for metabolic suppression and ischemia tolerance

Torpor during hibernation defines the nadir of mammalian metabolism where whole animal rates of metabolism are decreased to as low as 2% of basal metabolic rate. This capacity to decrease profoundly the metabolic demand of organs and tissues has the potential to translate into novel therapies for the treatment of ischemia associated with stroke, cardiac arrest or trauma where delivery of oxygen and nutrients fails to meet demand. If metabolic demand could be arrested in a regulated way, cell and tissue injury could be attenuated. Metabolic suppression achieved during hibernation is regulated, in part, by the central nervous system through indirect and possibly direct means. In this study, we review recent evidence for mechanisms of central nervous system control of torpor in hibernating rodents including evidence of a permissive, hibernation protein complex, a role for A1 adenosine receptors, mu opiate receptors, glutamate and thyrotropin‐releasing hormone. Central sites for regulation of torpor include the hippocampus, hypothalamus and nuclei of the autonomic nervous system. In addition, we discuss evidence that hibernation phenotypes can be translated to non‐hibernating species by H2S and 3‐iodothyronamine with the caveat that the hypothermia, bradycardia, and metabolic suppression induced by these compounds may or may not be identical to mechanisms employed in true hibernation.

Effects of nutritional restriction on nitrogen and carbon stable isotopes in growing seabirds

When using stable isotopes as dietary tracers it is essential to consider effects of nutritional state on isotopic fractionation. While starvation is known to induce enrichment of 15N in body tissues, effects of moderate food restriction on isotope signatures have rarely been tested. We conducted two experiments to investigate effects of a 50–55% reduction in food intake on δ15N and δ13C values in blood cells and whole blood of tufted puffin chicks, a species that exhibits a variety of adaptive responses to nutritional deficits. We found that blood from puffin chicks fed ad libitum became enriched in 15N and 13C compared to food-restricted chicks. Our results show that 15N enrichment is not always associated with food deprivation and argue effects of growth on diet–tissue fractionation of nitrogen stable isotopes (Δ15N) need to be considered in stable isotope studies. The decrease in δ13C of whole blood and blood cells in restricted birds is likely due to incorporation of carbon from 13C-depleted lipids into proteins. Effects of nutritional restriction on δ15N and δ13C values were relatively small in both experiments (δ15N: 0.77 and 0.41‰, δ13C: 0.20 and 0.25‰) compared to effects of ecological processes, indicating physiological effects do not preclude the use of carbon and nitrogen stable isotopes in studies of seabird ecology. Nevertheless, our results demonstrate that physiological processes affect nitrogen and carbon stable isotopes in growing birds and we caution isotope ecologists to consider these effects to avoid drawing spurious conclusions.

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

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

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.

Energetics of arousal episodes in hibernating arctic ground squirrels

Arctic ground squirrels overwintering in northern Alaska experience average soil temperature of −10°C. To examine energetic costs of arousing from hibernation under arctic compared to temperate conditions, captive ground squirrels were maintained in ambient temperatures (Ta) of 2, −5 and −12°C. Rates of oxygen consumption and carbon dioxide production were used to estimate metabolic rate and fuel use during the three phases of arousal episodes: rewarming, euthermia, and recooling. Respiratory quotient comparisons suggest exclusive use of lipid during rewarming and mixed fuel use during euthermia. Animals rewarming from torpor at Ta −12°C took longer, consumed more oxygen, and attained higher peak rates of oxygen consumption when compared to 2°C. Ta had no significant effect on cost or duration of the euthermic phase. Animals recooled faster at −12°C than at 2°C, but total oxygen consumption was not different. Ta had no significant effect on the total cost of arousal episodes when all three phases are included. Arousal episodes account for 86% of estimated costs of a complete hibernation cycle including torpor when at 2°C and only 23% at −12°C. Thus, due to the higher costs of steady-state metabolism during torpor, proportional metabolic costs of arousal episodes at Ta characteristic of the Arctic are diminished compared to relative costs of arousals in more temperate conditions.

Androgen in free-living arctic ground squirrels: seasonal changes and influence of staged male-male aggressive encounters

We tested the responsiveness of plasma androgen in free-living male arctic ground squirrels (Spermophilus parryii) to challenges from conspecific males by staging aggressive encounters between males and then comparing androgen concentrations in manipulated and unmanipulated animals. The effect of staged encounters on androgen depended on time of year. In spring, androgen levels significantly increased after staged encounters, except during the peak of mating activity when levels were maximal in all reproductive males. In late summer, staged encounters had no significant effect on androgen levels. In spring but not summer, androgen was positively correlated to the relative intensity of encounters. These results suggest that circulating levels of androgen in male arctic ground squirrels result from a combination of seasonal and social factors. Responsiveness of androgen to encounters during spring but not late summer support the challenge hypothesis for this polygynous mammal.

Corticosterone levels of tufted puffins vary with breeding stage, body condition index, and reproductive performance

Corticosterone (CORT) levels in free-living animals are seasonally modulated and vary with environmental conditions. Although most studies measure total CORT concentrations, levels of corticosteroid binding globulin (CBG) may also be modulated, thus altering the concentration of CORT available for diffusion into tissues (free CORT). We investigated the seasonal dynamics of CBG, total CORT, and free CORT in breeding tufted puffins (Fratercula cirrhata) during 2 years characterized by high rates of nestling growth and survival. We then compared concentrations of total CORT in this population to levels in chick-rearing puffins at another colony during 2 years with low productivity. At the high productivity colony, levels of CBG, total baseline CORT, free baseline CORT, and total maximum CORT were all higher prior to egg-laying than during late incubation and late chick-rearing. Levels of CBG were positively correlated with body condition index (BCI) and free baseline CORT was negatively correlated with BCI. Total baseline levels of CORT during chick-rearing were two to four times higher at the colony with low rates of nestling growth and survival. Our results demonstrate the need for long-term datasets to disentangle seasonal trends in CORT levels from trends driven by changes in environmental conditions. Given the negative effects associated with chronic elevation of CORT, our results indicate the cost of reproduction may be higher during years characterized by low productivity.

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

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

USING FATTY ACIDS AS DIETARY TRACERS IN SEABIRD TROPHIC ECOLOGY: THEORY, APPLICATION AND LIMITATIONS

Analysis of fatty acids (FAs) is an increasingly utilized tool in studies of trophic ecology in marine ecosystems. This powerful technique has proved useful in delineating spatial and temporal variability in diets, identifying the consumption of key species, and providing quantitative estimates of diet composition. Although consumer FA signatures are undeniably influenced by diet, they can also be affected by other factors including life-history stage, diet quality, and physiological state. Here, we review how FAs are assimilated, deposited, and metabolized in birds, and the implications of these processes on the various tissues commonly sampled for FA analyses. We then examine the assumptions underlying FA signature analysis when used in studies of seabird trophic ecology and propose a direction for future laboratory experiments that are needed to refine the approach. The correct interpretation of FA data relies on accounting for factors that alter predator FA metabolism and controlling for variability in the lipid content and FA composition of prey. Efforts should also be made to incorporate uncertainty associated with predator metabolism into models designed for quantitative diet estimation.