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A locust in flight. Photo credit: Edward Snelling.

Most insects have pretty sluggish metabolisms until they jump into the air; but when they take off, these animals are virtually on fire. Boosting their metabolic rates by as much as 100 times, fliers have to ensure that they can keep the furnace that powers flight well supplied with oxygen. Roger Seymour from the University of Adelaide, Australia, explains that insect bodies are plumbed with air capillaries – trachea – that supply oxygen directly to every tissue and this system is matched to the tissues that they supply: the tracheal system of the locust flight muscles is 6 times larger than that of the leg muscles, in line with the flight muscle's high energy consumption. However, the flight muscle contains 20 times more mitochondria – which consume oxygen during ATP production – than the leg muscles; could the muscle consume even more oxygen and if so could the tracheal system meet the demand? Seymour and graduate student Edward Snelling wondered how well the flight muscle's oxygen delivery system was matched to its oxygen demands.

Reasoning that the insects would be very sensitive to the amount of oxygen in the air at low concentrations if their oxygen delivery system and oxygen consumption were matched, Seymour realised that he could measure the locusts’ sensitivity by creating a variety of different atmospheres –oxygen mixed in different ratios with either nitrogen, light helium or heavy sulphur hexafluoride – and recording the insects’ oxygen consumption while they flew in the gases. If the insects’ performance dropped off below a specific oxygen concentration, then their respiratory system and muscle would be well matched.

Seymour assigned the task of designing the atmospheres to Honours student Rebecca Duncker and worked with her and Edward Snelling to figure out how to attach insects to a tether during flight via a tiny magnet glued to the insect’s back. However, he recalls that the locusts weren't always happy to fly in the unfamiliar atmospheres. ‘The difference in resistance of their wings… apparently stopped them from flapping’, he says.

Finally, Duncker plotted the metabolic rate of the insects against the fraction of oxygen in the air and realised that the metabolic rate of the insects plummeted below ∼21% oxygen: the oxygen delivery system was perfectly matched to the flight muscle. ‘The flight motor of locust seems to be either on or off, and it has only one gear. No excess oxygen supply is required’, says Seymour, who is keen to find out whether species that carry cargo can turn up oxygen delivery to power flight in a way that unburdened locusts cannot.

Having developed the novel atmospheres, the trio realised that altering the main gas component would also change how fast oxygen diffuses into the tissue and this could allow them to test whether oxygen was delivered to the flight muscle by diffusion through the trachea or by the contraction of the flight muscles pumping air through. Duncker scoured the literature to find out how to combine oxygen, helium and sulphur hexafluoride to create one atmosphere that had a normal density where oxygen diffused fast and a second where oxygen diffused at the normal rate but the atmosphere was relatively dense in order to find out whether increasing the diffusion rate of oxygen in the flight muscle trachea permitted the insects to increase their metabolic rate. However, when she compared the metabolic rates of the locusts flying in the two atmospheres, they were essentially identical, confirming that oxygen is pumped into the flight muscle by the muscle's own contraction.

• © 2017. Published by The Company of Biologists Ltd