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Flying insects achieve the highest mass-specific aerobic metabolic rates of all animals. However, few studies attempt to maximise the metabolic cost of flight and so many estimates could be sub-maximal, especially where insects have been tethered. To address this issue, oxygen consumption was measured during tethered flight in adult locusts Locusta migratoria, some of which had a weight attached to each wing (totalling 30-45% of body mass). Mass-specific metabolic rate increased from 28 +/- 2 mu mol O-2 g(-1) h(-1) at rest to 896 +/- 101 mu mol O-2 g(-1) h(-1) during flight in weighted locusts, and to 1032 +/- 69 mu mol O-2 g(-1) h(-1) in unweighted locusts. Maximum metabolic rate of locusts during tethered flight ((M) over dot(MO2); mu mol O-2 h(-1)) increased with body mass (M-b; g) according to the allometric equation (M) over dot(MO2)=994M(b)(0.75 +/- 0.19), whereas published metabolic rates of moths and orchid bees during hovering free flight ((M) over dot(HO2)) are approximately 2.8-fold higher, (M) over dot(HO2)=2767 M-b(0.72 +/- 0.08). The modest flight metabolic rate of locusts is unlikely to be an artefact of individuals failing to exert themselves, because mean maximum lift was not significantly different from that required to support body mass (95 +/- 8%), mean wingbeat frequency was 23.7 +/- 0.6 Hz, and mean stroke amplitude was 105 +/- 5 deg in the forewing and 96 +/- 5 deg in the hindwing - all of which are close to free-flight values. Instead, the low cost of flight could reflect the relatively small size and relatively modest anatomical power density of the locust flight motor, which is a likely evolutionary trade-off between flight muscle maintenance costs and aerial performance.