Flight thermogenesis and energy conservation in hovering hummingbirds

As the smallest homeotherms, hummingbirds suffer from low thermal inertia and high heat loss. Flapping flight is energetically expensive, and convective cooling due to wing and air movements could further exacerbate energy drain. Energy conservation during flight is thus profoundly important for hummingbirds. The present study demonstrates that heat produced by flight activity can contribute to thermoregulatory requirements in hovering hummingbirds. The rate of oxygen consumption, as an indicator of metabolic cost, was measured during hover-feeding and compared with that during perch-feeding. In hover-feeding, oxygen consumption increased only moderately between 35 and 5 degreesC in contrast to the sharp increase during perch-feeding over the same temperature range. This result suggests that heat produced by contraction of the flight muscles substituted for regulatory thermogenesis to accommodate for heat loss during exposure to low temperature. With declining air temperatures, the mechanical power requirements of hovering decreased slightly, but metabolic costs increased moderately. As a result, the mechanical efficiency of the muscle in converting metabolic power to mechanical power was reduced. Changes in wingbeat kinematics also accompanied the reduction in muscle efficiency. Wingbeat frequency increased but stroke amplitude decreased when hovering in the cold, suggesting thermoregulatory roles for the flight muscles. Hovering hummingbirds modulated their wingbeat frequency within a narrow range, reflecting the physical constraints of tuning to a natural resonant frequency with an elastic restoring force. We hypothesize that, by forcing the resonant system of the wings and thorax to oscillate at different frequencies, muscle contraction in the cold generates more heat at the expense of mechanical efficiency. This mechanism of modulating the efficiency of muscle contraction and heat production allows flying hummingbirds to achieve energy conservation at low air temperatures.