Hovering flight, elegantly employed by hummingbirds, is the most energetically expensive form of exercise known among vertebrate animals. Despite the great energetic costs incurred by hummingbirds as they hover to feed on floral nectar, these animals are capable of astounding rates of positive net energy intake and weight gain. Progress towards understanding of the ways in which hummingbirds balance the large energetic demands of hovering flight with the drive to replenish and build fat stores requires a better accounting of the effects of variation in environmental parameters on the cost of hovering, as well as identification of behavioral and physiological mechanisms that serve to economize the use of ingested fuels. I obtained respirometric data on hovering hummingbirds under field conditions at a variety of elevations and determined that the metabolic cost of hovering is significantly greater at low temperature and at higher altitude. Further, effects of these two parameters are additive such that the cost of hovering increases with decreasing temperature as much at high elevation as at low elevation. By combining respirometry with estimates of mechanical power output, I found that hovering hummingbirds consume less oxygen when oxidizing carbohydrates than when oxidizing fat. This study provides the first direct evidence of the quantitative difference between carbohydrate and fat oxidation in ATP yield per oxygen atom consumed in whole animals. The requirement for less oxygen suggests that burning carbohydrates is advantageous to hummingbirds when hovering at high elevation. By combining respirometry with stable isotope tracking of expired carbon dioxide, I show several North American hummingbird species are capable of the rapid utilization of ingested sugar to fuel hovering metabolism when nectar resources are available. Sugar turnover is rapid and hummingbirds are able to support virtually all of their metabolism during hovering with recently ingested sugar. This strict reliance on metabolism of recently ingested sugars enables hovering hummingbirds to avoid the inefficiency of depleting fat stores, then necessitating their later resynthesis, during foraging. Together, these studies integrate tissue level biochemistry and whole animal physiology and behavior, and highlight the relevance of such integration to a better understanding of hummingbird ecology.