Oxygen consumption rates in hovering hummingbirds reflect substrate-dependent differences in P/O ratios: carbohydrate as a `premium fuel'

Abstract

SUMMARY The stoichiometric relationship of ATP production to oxygen consumption,i.e. the P/O ratio, varies depending on the nature of the metabolic substrate used. The latest estimates reveal a P/O ratio approximately 15% higher when glucose is oxidized compared with fatty acid oxidation. Because the energy required to produce aerodynamic lift for hovering is independent of the metabolic fuel oxidized, we hypothesized that the rate of oxygen consumption, V̇O2, should decline as the respiratory quotient, RQ(V̇CO2/V̇O2),increases from 0.71 to 1.0 as hummingbirds transition from a fasted to a fed state. Here, we show that hovering V̇O2 values in rufous (Selasphorus rufus) and Anna's hummingbirds (Calypte anna) are significantly greater when fats are metabolized (RQ=0.71) than when carbohydrates are used (RQ=1.0). Because hummingbirds gained mass during our experiments, making mass a confounding variable, we estimated V̇O2 per unit mechanical power output. Expressed in this way, the difference in V̇O2 when hummingbirds display an RQ=0.71 (fasted) and an RQ=1.0 (fed) is between 16 and 18%, depending on whether zero or perfect elastic energy storage is assumed. These values closely match theoretical expectations, indicating that a combination of mechanical power estimates and `indirect calorimetry', i.e. the measurement of rates of gas exchange, enables precise estimates of ATP turnover and metabolic flux rates in vivo. The requirement for less oxygen when oxidizing carbohydrate suggests that carbohydrate oxidation may facilitate hovering flight in hummingbirds at high altitude.