Gwendolyn C. Bachman

Repeatability of Maximal Aerobic Performance in Belding’s Ground Squirrels, Spermophilus beldingi

Summary 1. The repeatability of a trait is a critical factor in determining how that trait is affected by natural selection. We examined the repeatability of a key physiological trait, maximum oxygen consumption ( O 2max ), in a wild population of Belding’s Ground Squirrels, Spermophilus beldingi. O 2max is an integrated measure of organismal metabolic performance. It can be intuitively related to fitness because it sets an upper limit to sustainable power output during ecolog ically important activites such as locomotion and thermoregulatory heat production. 2. We used respirometry to determine O 2max during exercise and thermogenesis. Exercise O 2max was elicited in an enclosed running wheel. Thermogenic O 2max was obtained with acute cold exposure in a helium-oxygen gas mixture. 3. Repeatability of both exercise and thermogenic O 2max was high over 2 h intervals but declined over longer test periods (6-18 days and 1-2 years). In general, repeatability was higher for exercise O 2max than for thermogenic O 2max . 4. We found no repeatability for animals tested initially as juveniles and then 1 or 2 years later as adults; evidently there is sufficient plasticity in O 2max to decouple aerobic performance between these life stages. A small number of adults tested in successive years showed significant repeatability of exercise O 2max but no repeatability of thermogenic O 2max .

The heat increment of feeding in house wren chicks: magnitude, duration, and substitution for thermostatic costs

The heat increment of feeding (HIF), a transient postprandial increase in metabolic rate, is the energy cost of processing a meal. We measured HIF in house wren chicks (Troglodytes aedon) ranging in mass from 1.6 to 10.3 g. This mass range (age 2–10 days) spanned a transition from blind, naked, ectothermic chicks through alert, endothermic birds with nearly complete feathering. We fed chicks crickets (2.7–10% of chick body mass) and determined HIF from continuous measurements of oxygen consumption rate (O2) before and after meals. At warm ambient temperatures (Ta) of 33–36 °C, the magnitude of HIF (in ml O2 or joules) was linearly related to meal mass and was not affected by chick mass. HIF accounted for 6.3% of ingested energy, which is within the range of results for other carnivorous vertebrates. The duration of HIF was inversely related to chick mass; 10-g chicks processed a standard meal approximately twice as fast as 2-g chicks. HIF duration increased with increasing meal mass. The peak O2 during HIF, expressed as the factorial increase above resting metabolism, was independent of body mass and meal mass. In large, endothermic chicks ( > 8 g), HIF substituted for thermoregulatory heat production at low Ta.

Regulatory changes contribute to the adaptive enhancement of thermogenic capacity in high-altitude deer mice

In response to hypoxic stress, many animals compensate for a reduced cellular O2 supply by suppressing total metabolism, thereby reducing O2 demand. For small endotherms that are native to high-altitude environments, this is not always a viable strategy, as the capacity for sustained aerobic thermogenesis is critical for survival during periods of prolonged cold stress. For example, survivorship studies of deer mice (Peromyscus maniculatus) have demonstrated that thermogenic capacity is under strong directional selection at high altitude. Here, we integrate measures of whole-organism thermogenic performance with measures of metabolic enzyme activities and genomic transcriptional profiles to examine the mechanistic underpinnings of adaptive variation in this complex trait in deer mice that are native to different elevations. We demonstrate that highland deer mice have an enhanced thermogenic capacity under hypoxia compared with lowland conspecifics and a closely related lowland species, Peromyscus leucopus. Our findings suggest that the enhanced thermogenic performance of highland deer mice is largely attributable to an increased capacity to oxidize lipids as a primary metabolic fuel source. This enhanced capacity for aerobic thermogenesis is associated with elevated activities of muscle metabolic enzymes that influence flux through fatty-acid oxidation and oxidative phosphorylation pathways in high-altitude deer mice and by concomitant changes in the expression of genes in these same pathways. Contrary to predictions derived from studies of humans at high altitude, our results suggest that selection to sustain prolonged thermogenesis under hypoxia promotes a shift in metabolic fuel use in favor of lipids over carbohydrates.

Aerobic Performance in Belding's Ground Squirrels (Spermophilus beldingi): Variance, Ontogeny, and the Aerobic Capacity Model of Endothermy

Metabolic rate is one of the most intensively studied aspects of organismal physiology, but much of the large body of data on metabolism concerns adult animals while largely ignoring juvenile stages, and focuses on mean values of traits while neglecting to consider the significance of intraspecific variation. To study the importance of ontogenic change and individual differences in aerobic performance in a typical small mammal, we measured minimal resting oxygen consumption (V̇o2mr) and maximal oxygen consumption (V̇o2max) during exercise and thermogenesis in juvenile and adult Beldings ground squirrels (Spermophilus beldingi). Across a 5.5-fold body mass range, the relationship between mass and V̇o2 was best described with two-phased regressions with inflections at 212-281 g, instead of the simple linear relationship reported for other species. The reason for inflections is unclear, but they are possibly related to growth costs since they approximately correspond to body mass at the end of the rapid growth period in the juvenile year. We also found higher than expected intraspecific mass exponents for both V̇o2mr and V̇o2max; this may also be related to rapid growth of juveniles. The aerobic scope (V̇o2max/V̇o2mr) increased from about 5.4 in newly independent juveniles to about 7.5 in adults. Interindividual variance was lowest for exercise V̇o2max and highest for V̇o2mr. Residual analysis revealed that V̇o2mr was significantly correlated with exercise V̇o2max (i. e., individuals with above-average V̇o2mr for their mass tended to have high V̇o2max, and vice versa). However, there was no correlation between V̇o2mr and thermogenic V̇o2max. These results provide limited support for the aerobic capacity model for the evolution of endothermy.

Energetic Costs of Begging Behaviour

Energy expenditure during begging by nestling birds is of interest because of its potential role in the social dynamic between provisioning parents and their young. In this chapter we discuss methods of measuring the energy cost of begging and argue that continuous-flow respirometry is the method of choice. Evaluating the impact of begging on nestling energetics and fitness requires an estimate of nestling energy budgets. To date, studies show that the energy cost of begging comprises a very small fraction of the nestling’s total energy budget. With existing estimates of the time budget and energy cost of begging, we calculate that even large increases in begging activity are likely to have little negative impact on nestling fitness. We suggest that additional work on begging energetics should broaden the range of behaviours and social groupings that are examined in order to explore the limits to begging activity in nestling birds.

Food supplements modulate changes in leucocyte numbers in breeding male ground squirrels.

SUMMARY Immunosuppression may be an important cost of reproduction in breeding males. It can result from elevated levels of testosterone or stress hormones and may serve to lower the energetic cost of maintaining immune function at a time of high demand. This suggests that greater access to energy resources could reduce immunosuppression as a cost of reproduction, minimizing the trade-off between energetic investment in current reproductive effort and survival. I examined the impact of food availability on immune function by provisioning male Beldings ground squirrels in the field from the time they emerged from hibernation to the start of breeding. Temporal changes in immune status, measured by leucocyte counts, differed between provisioned males and un-provisioned controls. Provisioning advanced the increase in lymphocytes and neutrophils from after breeding to before. At the start of breeding, the leucocyte count was three times greater in provisioned males than in controls and was still nearly twice as great at the end of breeding. Control males increased all leucocyte numbers after breeding. This experiment demonstrates that variation in food intake can lead to individual variation in the extent of immunosuppression during breeding and therefore that reduced immune function may not be an obligatory cost of reproduction.

Contributions of phenotypic plasticity to differences in thermogenic performance between highland and lowland deer mice

SUMMARY Small mammals face especially severe thermoregulatory challenges at high altitude because the reduced O2 availability constrains the capacity for aerobic thermogenesis. Adaptive enhancement of thermogenic performance under hypoxic conditions may be achieved via physiological adjustments that occur within the lifetime of individuals (phenotypic plasticity) and/or genetically based changes that occur across generations, but their relative contributions to performance differences between highland and lowland natives are unclear. Here, we examined potentially evolved differences in thermogenic performance between populations of deer mice (Peromyscus maniculatus) that are native to different altitudes. The purpose of the study was to assess the contribution of phenotypic plasticity to population differences in thermogenic performance under hypoxia. We used a common-garden deacclimation experiment to demonstrate that highland deer mice have enhanced thermogenic capacities under hypoxia, and that performance differences between highland and lowland mice persist when individuals are born and reared under common-garden conditions, suggesting that differences in thermogenic capacity have a genetic basis. Conversely, population differences in thermogenic endurance appear to be entirely attributable to physiological plasticity during adulthood. These combined results reveal distinct sources of phenotypic plasticity for different aspects of thermogenic performance, and suggest that thermogenic capacity and endurance may have different mechanistic underpinnings.

Food Restriction Effects on the Body Composition of Free-Living Ground Squirrels, Spermophilus beldingi

I conducted a field experiment to examine the use of body fat as an energy reserve by juvenile female Beldings ground squirrels, Spermophilus beldingi, prior to hibernation. Squirrels were divided into two groups: the squirrels in one group had their foraging times restricted by being placed in a cage for part of each day for four consecutive days (deprived group), and the squirrels in the other group foraged ad lib. (ad lib. group). The deprived group foraged in its normal habitat morning and evening but had access only to water and lettuce while captive. Total body electrical conductivity (TOBEC), an in vivo method of estimating fat-free mass, was used to follow changes in body composition. The deprived group lost mass, while the ad lib. group gained mass. Total body electrical conductivity measurements indicated that the deprived group lost fat-free mass and not fat, whereas mass gained by the ad lib. group was mostly fat. This is consistent with an emphasis on fat anabolism prior to hibernation. I also show that the TOBEC method is affected by variation in stomach contents, and I evaluate conditions under which an intraspecific calibration equation is needed