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First published online June 11, 2007
Journal of Experimental Biology 210, 2146-2153 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.005389
Oxygen consumption rates in hovering hummingbirds reflect substrate-dependent differences in P/O ratios: carbohydrate as a `premium fuel'
1 Department of Ecology, Evolution and Marine Biology, University of
California, Santa Barbara, CA 93106-9610, USA
2 Department of Biology, University of California, Riverside, CA 92521,
USA
* Author for correspondence (e-mail: k_welch{at}lifesci.ucsb.edu)
Accepted 10 April 2007
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,
O2, should
decline as the respiratory quotient, RQ
(
CO2/
O2),
increases from 0.71 to 1.0 as hummingbirds transition from a fasted to a fed
state. Here, we show that hovering
O2 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
O2 per unit
mechanical power output. Expressed in this way, the difference in
O2 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.
Key words: P/O ratio, carbohydrate, fatty acid, hummingbird, oxygen consumption
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