Physiological constraints in the aerobic performance of hummingbirds.

Hovering flight has been described as the most energetically expensive form of locomotion. Among the vertebrates, hummingbirds weighing only 1.5-20 g are the elite practitioners of this aerial art. Their flight muscles are, therefore, the most oxygen demanding locomotor muscles per unit tissue mass of all vertebrates. Tissue level functional and structural adaptations for oxygen transport are compared between hummingbirds and mammals in this paper. Hummingbirds present extreme structural adaptations in their flight muscles. Mitochondrial densities greater than 30% are observed in their pectoral muscles, and the surface area of the inner membrane of their mitochondria is twice that of mammals. This doubling of their mitochondrial oxidative capacity is accompanied by a proportional increase in the specific activity (per g tissue) of the mitochondrial manganese superoxide dismutase (SOD-Mn) in their flight muscles, thus indicating that oxygen toxicity is not a constraint in the aerobic performance of hummingbirds during hovering flight. Finally, the liver appears to play a major role in providing the necessary substrates for their high aerobic performance, and also in eliminating the oxygen free radicals formed during oxidative phosphorylation.