Warm-blooded mammals don't realise how easy life is. Before any cold-blooded creature can get going, they either have to sit in the sun or shiver to generate heat. Nicole George, from the University of Washington, USA, explains that Manduca sexta moths have to warm their muscles to about 32°C before take off, and regularly run their flight muscles at a sizzling 40°C. But when George's thesis advisor, Tom Daniel, and Michael Tu inserted a thermocouple in the insect's main flight muscle (the dorsolongitudinal muscle) during flight, they were amazed to see that the temperature in the muscle was not uniform. There was a gradient running from the warmest tissue on the ventral side to the coolest on the dorsal. But how would this temperature gradient affect the muscle's function? Knowing that temperature can dramatically affect the power output of a muscle, George and Daniel decided to find out how the temperature gradient affects the muscle (p. 471).

‘We used the work-loop method to replicate in vivo muscle contraction’, says George. Leaving the insect's thorax intact and attaching a motor to the muscle to simulate its natural 25 Hz contraction cycle, George electrically stimulated the muscle and measured the force that it exerted over the course of each contraction. By plotting the force generated by the muscle against muscle length – as it varied over a contraction cycle – and calculating the area under the curve, George could calculate the amount of power generated by the muscle.

Admitting that the measurements were fiddly, George says, ‘It took three repeats to do this. The setup changed dramatically from a very homemade setup to a second round using bought equipment and then we found out that extra muscles were being stimulated so I had to do another round where I removed the extra muscles.’ However, after perfecting her technique with the help of Simon Sponberg, George was able to measure the power produced by the muscle at temperatures ranging from 25°C up to 40°C.

At the highest temperatures, the muscle produced high power output in the region of 100 W kg–1. However, as the temperature decreased, so too did the power output, until at 30°C, the power output became negative. ‘The muscle's negative power output doesn't make sense, it doesn't help the moth to fly, it doesn't achieve lift so it really suggested that the cooler regions that produced zero or negative power output are functioning differently’, says George. She adds, ‘Negative power output is reflective of muscles that act as a break, so it may be a damping element that stabilises the oscillation of the thorax.’

George also repeated the experiments stimulating just the dorsal and ventral sections of the muscle. She found that the power output again switched from positive values at higher temperatures to negative at the lower temperatures, and suggests a possible alternative function for the cooler dorsal portion of the muscle. ‘Our theory suggests that since the cool muscle is contracting a lot slower, then myosin cross-bridges will remain deformed and bound to the thin filament, which will mean they can store energy in their deformation and they can release that in the next part of the cycle.’

So the Manduca dorsolongitudinal muscle could function as a two-stroke engine. The team suggests that the warm ventral portion of the muscle pulls the wing down during the first half of the contraction cycle to power flight directly, while the cooler dorsal segment of the muscle releases stored energy during the relaxation half of the cycle to help raise the wings ready for the start of the next wing beat.

N. T.
T. L.
Temperature gradients drive mechanical energy gradients in the flight muscle of Manduca sexta
J. Exp. Biol.