As grasshoppers increase in size during ontogeny, they have mass specifically greater whole body tracheal and tidal volumes and ventilation than predicted by an isometric relationship with body mass and body volume. However, the morphological and physiological bases to this respiratory hypermetry are unknown. In this study, we use synchrotron imaging to demonstrate that tracheal hypermetry in developing grasshoppers (Schistocerca americana) is due to increases in air sacs and tracheae and occurs in all three body segments, providing evidence against the hypothesis that hypermetry is due to gaining flight ability. We also assessed the scaling of air sac structure and function by assessing volume changes of focal abdominal air sacs. Ventilatory frequencies increased in larger animals during hypoxia (5% O(2)) but did not scale in normoxia. For grasshoppers in normoxia, inflated and deflated air sac volumes and ventilation scaled hypermetrically. During hypoxia (5% O(2)), many grasshoppers compressed air sacs nearly completely regardless of body size, and air sac volumes scaled isometrically. Together, these results demonstrate that whole body tracheal hypermetry and enhanced ventilation in larger/older grasshoppers are primarily due to proportionally larger air sacs and higher ventilation frequencies in larger animals during hypoxia. Prior studies showed reduced whole body tracheal volumes and tidal volume in late-stage grasshoppers, suggesting that tissue growth compresses air sacs. In contrast, we found that inflated volumes, percent volume changes, and ventilation were identical in abdominal air sacs of late-stage fifth instar and early-stage animals, suggesting that decreasing volume of the tracheal system later in the instar occurs in other body regions that have harder exoskeleton.