Abstract
Metabolic rate is a key ecological variable that quantifies the energy expenditure needed to fuel almost all biological processes in an organism. Metabolic rates are typically measured at the whole-organism level (woMR) with protocols that can elicit stress responses due to handling and confinement, potentially biasing resulting data. Improved, non-stressful methodology would be especially valuable for measures of field metabolic rate, which quantifies the energy expenditure of free-living individuals. Recently, techniques to measure cellular metabolic rate (cMR) in mitochondria of blood cells have become available, suggesting that blood-based cMR can be a proxy of organismal aerobic performance. Aerobic metabolism actually takes place in the mitochondria. Quantifying cMR from blood samples offers several advantages such as direct estimates of metabolism and minimized disturbance of individuals. To our knowledge, the hypothesis that blood-based cMR correlates with woMR has not yet been directly tested. We measured cMR in red blood cells of captive great tits (Parus major), first during their morning activity period and second after subjecting them to a 2.5 h day-time respirometry protocol to quantify woMR. We predicted cMR to decrease as individuals transitioned from an active to a resting state. In the two blood samples we also assessed circulating corticosterone concentrations to determine the perceived disturbance of individuals. From respirometry traces we extracted initial and final woMR measures to test for a predicted positive correlation with cMR measures, while accounting for corticosterone concentrations. Indeed, cMR declined from the first to the second measurement. Furthermore, woMR and cMR were positively related in individuals that had relatively low corticosterone concentrations and displayed little locomotor activity throughout respirometry. By contrast, woMR and cMR covaried negatively in birds that increased corticosterone concentrations and activity levels substantially. Our results show that red blood cell cMR represents a proxy for woMR when birds do not display signs of stress, i.e., either before increases in hormonal or behavioral parameters have occurred or after they have abated. This method represents a valuable tool for obtaining metabolic data repeatedly and in free-living individuals. Our findings also highlight the importance of accounting for individual stress responses when measuring metabolic rate at any level.
Highlights
Aerobic metabolism is a cornerstone of physiological research because of its fundamental function in fueling most biological processes in aerobic organisms
Corticosterone concentrations were expected to be associated with both woMR and cellular metabolic rate (cMR) but were instead only related to woMR, further justifying their inclusion in our main model to analyze the relationship between woMR and cMR
Our second prediction was generally confirmed in that we detected a positive association between woMR and cMR in individuals that showed low final plasma corticosterone concentrations and displayed little activity during respirometry (Figure 3, orange regression line), i.e., in birds that either did not display pronounced hormonal and behavioral responses over the course of respirometry, or more likely, managed to terminate their endocrine stress response and return to low concentrations by the end of the procedure
Summary
Aerobic metabolism is a cornerstone of physiological research because of its fundamental function in fueling most biological processes in aerobic organisms. Metabolic rate is typically measured as the amount of oxygen (O2) that an aerobic organism consumes per unit of time, representing an indirect measure of energy expenditure. Oxygen consumption is typically measured in intact organisms through indirect calorimetry, a technique better known as respirometry (Lighton, 2008). To address ecologically relevant questions we need to quantify metabolic rates in free-living individuals as they go about their natural daily activities, i.e., measure “field” or “active” metabolic rates (Butler et al, 2004; Mitchell et al, 2015; Hicks et al, 2020). Available field methods like the doubly-labeled water technique are often impractical (requiring repeated captures of individuals on subsequent days) or errorprone (Butler et al, 2004; Speakman and Hambly, 2016), emphasizing that we urgently need a more direct and less intrusive methodology
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