Extensive phosphate-water oxygen exchange occurs when ATP is hydrolyzed in an [18O]water medium by length oscillated and Ca2+-activated, chemically skinned fibers from the flight muscle of the giant waterbug Lethocerus indicus. For fibers which are length oscillated under conditions not optimal for ATPase activity or oscillatory work, the pattern of exchange shows two pathways for hydrolysis. One pathway has low exchange, because steps controlling Pi release are rapid; the other pathway has high exchange and slow Pi release. Steps controlling Pi release appear rate-limiting for changes in the high-exchange ATPase activity that occur on varying the frequency and amplitude of oscillation. On length oscillation under conditions of optimal ATPase activity or work, only the high-exchange pathway is present. Cross-bridges following the high-exchange pathway are therefore responsible for oscillatory work, the physiological function of the muscle, and behave uniformly with respect to oxygen exchange. The single pathway and the magnitude of the ATPase activity are both similar to results with isometric strained fibers (Lund, J., Webb, M. R., and White, D. C. S. (1987) J. Biol. Chem. 262, 8584-8590). A qualitative model is suggested for oscillatory work by cross-bridges, arising from the common periodicity of the thick and thin filaments in insect flight muscle.