OXYGEN consumption(1) and muscle power output(2) of hovering hummingbirds are among the highest recorded for vertebrates. Maximum performance of hummingbirds thus approaches the upper limits of vertebrate aerobic locomotion(3). Because air density is a major determinant of aerodynamic power requirements(4), hovering flight performances(5) can be manipulated non-invasively using normoxic gas mixtures of variable density(6). Here we show that limits to the locomotor capacity of hovering ruby-throated hummingbirds are unequivocally indicated by aerodynamic failure at low densities less than half that of sea-level air. Hummingbirds demonstrate considerable power reserves, with muscle mass-specific power (assuming perfect elastic energy storage) averaging from 98 W kg(-1) in normal air to a maximum value of 133 W kg(-1) before aerodynamic failure, in contrast to such variable power expenditure, however, muscle efficiency remains approximately constant at 10%. Modulation of power output is attained primarily through variation in wing-stroke amplitude, with aerodynamic failure occurring near 180 degrees.