The sugar oxidation cascade: convergent metabolic strategies in hovering vertebrate nectarivores

The smallest flying vertebrate pollinators, including hummingbirds and nectar bats, exist at an energetic extreme. Nectarivores must balance the need for high rates of metabolic power output to sustain comparatively high costs of thermoregulation and the intense energetic demands of forward and hovering flight with the constraint against building and carrying large, heavy energy stores. Work over the past half century has quantified metabolic rate and daily energy requirements for these animals and revealed that hummingbirds and nectar bats achieve energy homeostasis through exceptional physiological flexibility. They can rapidly and completely switch from fueling costly flight with lipid oxidation, when fasted, to oxidizing nectar sugar, ingested minutes prior, at rates that completely support hovering while foraging. This physiological capacity for rapid flux and oxidation of dietary sugar to completely fuel intense exercise, termed the 'sugar oxidation cascade', stands in stark contrast to models of fuel use in running mammals. Remarkably, the capacity for rapid absorption and oxidation of fructose is as elevated in hummingbirds and nectar bats as is their capacity to use glucose. Here, we review insights into convergently and divergently evolved features of the sugar oxidation cascade among hummingbirds and nectar bats, as revealed by advances in comparative genomic, molecular and biochemical techniques. We then review available evidence and hypothesize that additional groups of nectar and fruit-eating bats and birds exhibit similar fuel use patterns during exercise, and we call on researchers to develop techniques to assess fuel use during forward flight in these non-hovering taxa.