Using lactation in mice as a model, we sought to determine whether ceilings on sustained energy expenditure reside in the capacities of energy-acquiring and input organs (such as the intestine) or of energy-expending and output organs (such as the mammary glands). To distinguish between these possibilities experimentally, we surgically varied the teat number of lactating mother mice while simultaneously varying their litter size. The energy burden on each teat (i.e. the pup/teat ratio) could thus be varied independently of the energy burden (i.e. litter size) on the mother herself or on her intestine. At each teat number, pup mass proved to be maximal at intermediate litter sizes. At a given pup/teat ratio, mothers with five teats weaned pups no larger than the pups of normal (10-teat) mothers, even though the total energy burden on the former mothers was only half as large. Mothers with only two teats could not wean any pups. Litter size controlled maternal food intake, which in turn controlled intestinal mass and nutrient uptake capacity. Disproportionately high food intake for the smallest litters appears to reflect capital start-up costs of lactation. Pup mass is evidently limited by inadequate suckling stimulation of mammary glands.