We examined the oxygen consumption rates and activity levels of respiratory enzymes involved in the aerobic (citrate synthase [CS]) and anaerobic (octopine dehydrogenase [ODH]) metabolism of gonatid squids (Gonatus onyx and Gonatus pyrus) as a function of body size. The energy expenditure rates of gonatids (ranging from 2.51 to 8.79 micromol O(2) g(-1) h(-1) at 5 degrees C) are among the highest in Animalia when mass and temperature are taken into account. They reflect the low efficiency of jet propulsion and the animals' active life strategy as diel vertical migrants in the pelagic environment. Both metabolic rate and aerobic muscle potential (CS activity) were size independent across a size range of four orders of magnitude, which may be a result of their unusual body geometric allometry, extensive cutaneous respiration, and decreased energy-saving opportunities at larger sizes. Anaerobic metabolic potential (ODH activity) revealed a shift from positive scaling in juveniles to negative scaling among larger sizes. Juveniles are found in shallow water, where they are more susceptible to visually cued predators and require quicker size-specific escape responses and higher burst swimming capacities. Conversely, adults have reduced requirements for predator/prey interactions in the light-limited deep sea. Anaerobic metabolic scaling reflects an adaptive response to the changing physical and ecological demands across a depth gradient during this species's ontogenetic vertical migration.