Measurements of basal metabolic rate (BMR), body water, fat, and lean dry mass of different organs were obtained in 22 bird species, ranging from 10.8 to 1,253 g body mass. Residuals of BMR (after subtracting BMR allometrically predicted from body mass) were positively correlated with residuals of lean dry heart and kidney mass. Measurements of both BMR and the daily energy expenditure of parent birds (DEEpar) during the period of nestling care as assessed by labeled-water turnover were collected from the literature for 26 altricial bird species. The allometric relationships with body mass in this data set were: log BMR (W) = -1.385 + 0.684 log mass (g) [fraction of variance (r2) = 0.973] and log DEEpar (W) = -0.797 + 0.659 log mass (g) (r2 = 0.967). Residuals of log BMR and log DEEpar were positively correlated with each other. The parallel regressions and correlation of residuals lead to reduced variance in the ratio of BMR/DEEpar (mean 0.301; SD 0.086). We suggest that natural selection has led to an adjustment of the size of organs (such as heart and kidney) involved in sustaining energy metabolism at the DEE maximized during parental care and that size-independent variation in BMR reflects the relative size of this highly metabolically active machinery. These relationships of BMR lead to new interpretations of the decline in mass-specific BMR with increasing body size and decreasing latitude and of the difference in mass-specific BMR between birds and mammals.