Uncoupling Basal and Summit Metabolic Rates in White-Throated Sparrows: Digestive Demand Drives Maintenance Costs, but Changes in Muscle Mass Are Not Needed to Improve Thermogenic Capacity

Abstract

Avian basal metabolic rate (BMR) and summit metabolic rate (M) vary in parallel during cold acclimation and acclimatization, which implies a functional link between these variables. However, evidence suggests that these parameters may reflect different physiological systems acting independently. We tested this hypothesis in white-throated sparrows (Zonotrichia albicollis) acclimated to two temperatures (-8° and 28°C) and two diets (0% and 30% cellulose). We expected to find an uncoupling of M and BMR where M, a measure of maximal shivering heat production, would reflect muscle and heart mass variation and would respond only to temperature, while BMR would reflect changes in digestive and excretory organs in response to daily food intake, responding to both temperature and diet. We found that the gizzard, liver, kidneys, and intestines responded to treatments through a positive relationship with food intake. BMR was 15% higher in cold-acclimated birds and, as expected, varied with food intake and the mass of digestive and excretory organs. In contrast, although M was 19% higher in cold-acclimated birds, only heart mass responded to temperature (+18% in the cold). Pectoral muscles did not change in mass with temperature but were 8.2% lighter on the cellulose diet. Nevertheless, M varied positively with the mass of heart and skeletal muscles but only in cold-acclimated birds. Our results therefore suggest that an upregulation of muscle metabolic intensity is required for cold acclimation. This study increases support for the hypothesis that BMR and M reflect different physiological systems responding in parallel to constraints associated with cold environments.

The effects of dietary linoleic acid and hydrophilic antioxidants on basal, peak, and sustained metabolism in flight‐trained European starlings

“…As with a number of previous studies (Barceló, Love, & Vézina, ; McKechnie & Swanson, ; Swanson, Thomas, Liknes, & Cooper, ), we found no correlation between BMR and PMR or between either and any of our measures of sustained metabolism in the wind tunnel. This discontinuity suggests that basal, sustained, and peak metabolism are regulated differently from one another, albeit with a shared, underlying link to diet.…”

Ecological and evolutionary consequences of metabolic rate plasticity in response to environmental change

“…For example, although there is often a correlation between an individual's BMR and its M-sum [8], Barceló et al [12] were able to demonstrate through environmental manipulations that BMR and M-sum are under independent control: while cold exposure led to an increase in both the BMR and the M-sum of white-throated sparrows (Zonotrichia albicollis), a diet shift only altered their BMR and had no effect on their M-sum. Exploration of the body composition of these birds showed that in both experimental manipulations, the increase in BMR was related to increases in the relative size of digestive and excretory organs, whereas the increase in M-sum after cold exposure was presumed to be owing to changes in the metabolic intensity of the muscles (because there was no increase in their size) [12], a response that is thought to be, at least in part, driven by changes in gene expression of several key metabolic pathways [67]. BMR was also found to change faster than either M-sum or MMR in birds exposed to an abrupt shift in ambient temperature, possibly because of differences in the relative rates at which organs can change their size versus their metabolic intensity [68].…”

“…The scale of this variation is at first sight puzzling because metabolic rates have fitness consequences [6] but is likely owing to the optimal metabolic rate being context-dependent [2,7]. It should be noted that while the different forms of metabolic rates are often found to be correlated, especially when comparing among species [8,9], minimal and maximal metabolic rates are best treated as independent traits because they are under different selection pressures that may vary in parallel but can be uncoupled [10][11][12].…”

The performing animal: causes and consequences of body remodeling and metabolic adjustments in red knots facing contrasting thermal environments

“…3, 9, 30, 31, 66, 88, 89 but see Ref. 42), only a few experimental studies have presented data supporting it (3,9,83,89). In fact, the energy consumption per unit mass of tissue, called metabolic intensity and reflected in the activity of key aerobic enzymes, may also change in parallel, independently, or in an opposite direction to that observed in whole organ mass, thus bringing increased variation to the analyses (50,79,81,88,89).…”

“…34,35, and 66 for reviews). These changes are generally interpreted as resulting from internal organ remodeling (26,34,45,66,68) where elevated food consumption in the cold leads to enlargement of digestive organs (38), in turn influencing BMR (3,24,45,47,83,88,89 but see Ref. 42), and increases in the size of the heart and muscles such as the pectoralis are thought to elevate M sum , thus improving cold endurance (43,68,69,76,85).…”