Non-passerine birds and mammals of similar body weight have a roughly comparable metabolic rate, but the life span and the metabolic potential, i.e. the total amount of energy consumed per unit of body mass during life, is several times higher in the birds. The objective of this study was to explore the possible basis of this characteristic in the context of the predictions of the free radical hypothesis of aging. Accordingly, pigeon and rat, which have a similar body weight, were compared by examining the mitochondrial rates of O2.- and H2O2 generation and activities of superoxide dismutase, catalase and glutathione peroxidase and concentration of glutathione in the brain, heart and kidney. Compared with the rat, the rate of mitochondrial O2.- generation in the pigeon ranged between 50 and 67%, and H2O2 production between 31 and 77%. Activity of superoxide dismutase was uniformly higher and catalase activity consistently lower in the tissues of the pigeon compared with the rat. Glutathione peroxidase activity and glutathione concentration were higher in the pigeon in two out of the three organs studied, and comparable in the third organ. The magnitude of the differences between the two species was greater in the rates of O2.- and H2O2 generation than in anti-oxidant defenses. Results indicate that the relatively greater longevity and metabolic potential of the pigeon may be related to significantly lower rates of O2.- and H2O2 generation and higher overall level of anti-oxidant defenses.