As hummingbirds flit from flower to flower slurping up sugary nectar, more than 90% of the oxygen they breathe in is gobbled up by the mitochondria burning fuel to power their flight muscles. If a cell uses one `unit' of oxygen to burn glucose, it will get 15% more ATP than if it used fat as fuel instead. However, researchers haven't yet made the connection between oxygen consumption and ATP production to fuel use in whole animals. As Ken Welch explains, `hummingbirds are a unique model organism to investigate, since fasted birds make a rapid and predictable switch from fatty acid to carbohydrate metabolism after they begin feeding'. As they switch from burning fat to glucose, the birds' ratio of carbon dioxide production to oxygen consumption changes, so Welch and his mentor Raul Suarez predicted that as the birds switch between fuels, their rate of oxygen consumption would also go down (p. 2146).
The team fasted Anna's and rufous hummingbirds overnight to make sure that they were burning fat as the experiment started. Once released into the test enclosure, the birds eagerly fed from the tip of a syringe that dispensed sweet nectar within a respirometry mask. As they feasted on the nectar, air drawn through the mask passed into gas analysers which measured an increase in the birds' carbon dioxide production relative to their oxygen use. This told the team that the birds changed from burning fats to carbohydrate. `The switch was very rapid, about 20 to 30 minutes', says Welch. During this time, the team calculated that the rate of oxygen consumption went down, showing that the birds needed less oxygen to make ATP after switching to sugar.
However, the team hadn't yet taken into account the fact that the sugary load caused the birds to gain weight, which in turn affected how much oxygen the muscles needed to produce enough power to keep the birds aloft. In between visits to the feeder, the hummingbirds sat on a perch which rested on a set of scales, allowing the team to measure their weight gain. Armed with their data,the team enlisted the help of hummingbird flight expert Doug Altshuler, who helped them to calculate how much oxygen the birds needed to produce a set amount of power during hovering flight. They used models which took into account the birds' changing mass, the forces generated by the wings during hovering and storage of energy by the birds' wings.
When they assumed that the wings stored energy between wing beats, they calculated that the rate of oxygen consumption went down by 16% as the birds switched from burning fat to glucose. If no energy is stored by the wings, the rate went down by 18%. These results were `delightfully surprising', says Welch, since they were very close to theoretical estimates made by other researchers of different oxygen consumption rates when burning sugar or fat. This means that the hummingbirds need less oxygen to extract energy from carbohydrate, making it a more efficient fuel, and probably facilitating hovering at high altitudes where oxygen is scarce. Their quick fuel switch also shows that the hummingbirds are `carbohydrate maximisers', says Welch; if carbohydrate is available, they will always use it over their precious fat reserves which will see them through leaner times.