Abstract
Metabolism fuels fundamental biological processes and commonly scales with body mass with an exponent, b , between 2/3 and 1. We, here, explore how differences in physical activity can reveal contrasting interspecific metabolic scaling between major groups of arthropods. The Metabolic‐level Boundaries Hypothesis predicts that increased behavioural activity increases b . We test this hypothesis by comparing b during flight, non‐flight locomotion, and rest in winged and wingless insects, and spiders. We find that interspecific b values increase with activity only with flight in winged insects which co‐occurs with a substantial flight‐related rise in metabolic level. Spiders show a shallower interspecific metabolic scaling relative to insects, potentially reflecting slower life‐history strategies with increasing body size. Consequently, large resting or walking insects consume 6–15 times more oxygen than do spiders of corresponding size and activity level. These fundamental differences offer new insights into the evolutionary dynamics of arthropod energetics.