Mitochondrial metabolism in blood more reliably predicts whole-animal energy needs compared to other tissues.

Understanding energy metabolism in free-ranging animals is crucial for ecological studies. In birds, red blood cells (RBCs) offer a minimally invasive method to estimate metabolic rate (MR). In this study with European starlings Sturnus vulgaris, we examined how RBC oxygen consumption relates to oxygen use in key tissues (brain, liver, heart, and pectoral muscle) and versus the whole organism measured at basal levels. The pectoral muscle accounted for 34%-42% of organismal MR, while the heart and liver, despite their high mass-specific metabolic rate, each contributed 2.5%-3.0% to organismal MR. Despite its low contribution to organismal MR (0.03%-0.04%), RBC MR best predicted organismal MR (r = 0.70). Oxygen consumption of the brain and pectoralis was also associated with whole-organism MR, unlike that of heart and liver. Overall, our findings demonstrate that the metabolism of a systemic tissue like blood is a superior proxy for organismal energy metabolism than that of other tissues.

Age-related changes of physiological performance and survivorship of bank voles selected for high aerobic capacity.

Variation in lifespans is an intriguing phenomenon, but how metabolic rate influence this variation remains unclear. High aerobic capacity can result in health benefits, but also in increased oxidative damage and accelerated ageing. We tested these contradictory predictions using bank voles (Myodes=Clethrionomys glareolus) from lines selected for high swim-induced aerobic metabolism (A), which had about 50% higher maximum metabolic rate and a higher basal and routine metabolic rates, than those from unselected control lines (C). We measured sprint speed (VSmax), forced-running maximum metabolic rate (VO2run), maximum long-distance running speed (VLmax), running speed at VO2run (VVO2), and respiratory quotient at VO2run (RQ) at three age classes (I: 3-5, II: 12-14, III: 17-19months), and analysed survivorship. We asked if ageing, understood as the age-related decline of the performance traits, differs between the A and C lines. At age class I, voles from A lines had 19% higher VO2run, and 12% higher VLmax, but tended to have 19% lower VSmax, than those from C lines. RQ was nearly 1.0 for both A and C lines. The pattern of age-related changes differed between the lines mainly between age classes I and II, but not in older animals. VSmax increased by 27% in A lines and by 10% in C lines between age class I and II, but between classes II and III, it increased by 16% in both selection directions. VO2run decreased by 7% between age class I and II in A lines only, but in C lines it remained constant across all age classes. VLmax decreased by 8% and VVO2 by 12% between age classes II and III, but similarly in both selection directions. Mortality was higher in A than in C lines only between the age of 1 and 4months. The only trait for which the changes in old animals differed between the lines was RQ. In A lines, RQ increased between age classes II and III, whereas in C lines such an increase occurred between age classes I and II. Thus, we did not find obvious effects of selection on the pattern of ageing. However, the physiological performance and mortality of bank voles remained surprisingly robust to ageing, at least until the age of 17-19months, similar to the maximum lifespan under natural conditions. Therefore, it is possible that the selection could affect the pattern of ageing in even older individuals when symptoms of senility might be more profound.

A dopamine and noradrenaline reuptake inhibitor (bupropion) does not alter exercise performance of bank voles.

Physical performance is determined both by biophysical and physiological limitations and behavioral characteristic, specifically motivation. We applied an experimental evolution approach combined with pharmacological manipulation to test the hypothesis that evolution of increased aerobic exercise performance can be triggered by evolution of motivation to undertake physical activity. We used a unique model system: bank voles from A lines, selected for high swim-induced aerobic metabolism (VO2swim), which achieved a 61% higher mass-adjusted VO2swim than those from unselected C lines. Because the voles could float on the water surface with only a minimum activity, the maximum rate of metabolism achieved in that test depended not only on their aerobic capacity, but also on motivation to undertake intensive activity. Therefore, we hypothesized that signaling of neurotransmitters putatively involved in regulating physical activity (dopamine and noradrenaline) had changed in response to selection. We measured VO2swim after intraperitoneal injections of saline or the norepinephrine and dopamine reuptake inhibitor bupropion (20 mg/kg or 30 mg/kg). Additionally, we measured forced-exercise VO2 (VO2max). In C lines, VO2swim (mass-adjusted mean ± standard error (SE): 4.0 ± 0.1 mLO2/min) was lower than VO2max (5.0 ± 0.1 mLO2/min), but in A lines VO2swim (6.0 ± 0.1 mLO2/min) was as high as VO2max (6.0 ± 0.1 mLO2/min). Thus, the selection effectively changed both the physiological-physical performance limit and mechanisms responsible for the willingness to undertake vigorous locomotor activity. Surprisingly, the drug had no effect on the achieved level of VO2swim. Thus, the results did not allow firm conclusions concerning involvement of these neurotransmitters in evolution of increased aerobic exercise performance in the experimental evolution model system.

Hindlimb muscle fibre size and glycogen stores in bank voles with increased aerobic exercise metabolism.

To test hypotheses concerning physiological factors limiting the rate of aerobic exercise metabolism, we used a unique experimental evolution model: lines of bank voles selected for high swim-induced aerobic metabolism (A) and unselected, control lines (C). We investigated putative adaptations that result in the increased performance of the hindlimb muscle (gastrocnemius joined with plantaris). The body mass-adjusted muscle mass was higher in A-lines (0.093 g) than in C-lines (0.083 g; P=0.01). However, selection did not affect mean muscle fibre cross-sectional area (P=0.34) or glycogen content assessed with a histochemical periodic acid-Schiff reaction (PAS; P=0.82). The results suggest that the increased aerobic performance is achieved by an increase of total muscle mass, without major qualitative changes in the muscle fibre architecture. However, such a conclusion should be treated with caution, because other modifications, such as increased density of capillaries or mitochondria, could occur.