The mechanical power required from a bird's flight muscles was recalculated at regular intervals (default 6 min), and the energy consumed in the interval was accounted for by reducing fuel reserves, which also reduced the all-up mass and the body cross-sectional area. Part of the energy requirement was met by consuming flight muscle tissue, according to one of three alternative "muscle burn criteria". These were (1) specific work held constant, (2) power density held constant and (3) muscle mass held constant, i.e. no muscle consumed. Holding the specific work constant produced results in the best agreement with the results of other studies. This criterion was therefore selected to compare simulated flights of three very different species whose flight and migrations have been extensively studied, (1) Thrush Nightingale (Luscinia luscinia), (2) Knot (Calidris canutus) and (3) Whooper Swan (Cygnus cygnus). The ratio of protein to fat consumed ranged from 0.19 to 0.36, depending mainly on the starting value assumed for the muscle fraction. Specific work and starting power density were much higher for the Whooper Swan than for the two smaller species, suggesting that the latter have power to spare for climbing to high cruising altitudes, whereas the swan has not. If all three species were able to reach high cruising altitudes, the result would be a large reduction in journey time, which in turn would result in a small increase in range, due to a saving of energy required for basal metabolism. On current assumptions, the proportion of the fuel energy spent on basal metabolism would be eight times higher in the Thrush Nightingale than in the Whooper Swan, consequently the gain in range due to flying high would be greater in the smaller bird. In order to run the simulation, assumptions have been made at the primary physical level, to calculate the mechanical power required, and also at the secondary physiological level, to convert this into fuel consumption. The physical assumptions mostly take the form of variables whose existence is not in doubt, but whose values are poorly known, whereas in the case of some of the most important physiological variables, even the principles are unknown. Attention is drawn to a number of problems in need of attention, including (1) the mass and energy requirements of respiratory and circulatory organs required to sustain aerobically a given level of mechanical power; (2) the capabilities of bird lungs at high altitudes; (3) the possibility that heart muscle and lung tissue may be consumed in flight; (4) the two "biological constants", isometric force per myosin fibril and inverse power density of mitochondria; (5) the energy density of different fuels, and the conversion efficiency of the flight muscles; and (6) the manner in which basal metabolism combines with other demands for power in an exercising animal. Copyright 1998 Academic Press Limited