If you're going to challenge a central dogma, you've got to be prepared to defend your stance. Which is exactly what Richard Marsh from Northeastern University, Boston, does in this issue of The Journal of Experimental Biology. So what is the dogma that Marsh and his team have challenged?That the energetic cost of the swing phase in walking and running is negligible. Perceived wisdom held that the leg muscles supporting a walker's body weight while in contact with the ground accounted for the energetic cost of walking, but Marsh and his team challenged this in 2004 with a novel technique looking at blood flow to muscles. This approach suggested that muscles involved in swinging the leg account for 25% of the energetic cost. Having come to this unexpected conclusion, Marsh had to test further. He needed to somehow isolate the cost of swinging the leg from the cost of supporting the body. He decided to measure the metabolic cost and blood flow in running guinea fowl when carrying a weight on their backs, and weights near their feet, to see which muscles worked most during walking and running.
First the team designed a backpack that allowed the birds to carry lead weights on their backs without interfering with their breathing. They also designed lead bands for the birds' lower legs, before setting the animals running on a treadmill. David Ellerby, Havalee Henry and Marsh then measured the animals' metabolic rates while running freely, running in their backpacks,and running with the lower leg weights at speeds ranging from 0.5-2 m s-1. The team also filmed the running birds to see whether the loads hampered their running gaits and to calculate the mechanical energy required to swing the extra weight at the ends of their legs().
Analysing the metabolic readings from the running guinea fowl, the team realised that the birds' metabolic rate only increased by 17% when bearing the 333 g load on their back. Marsh explains that it had been believed that the increase in metabolic rate was directly proportional to the extra load. But the 333 g weight was 23% of the bird's mass; guinea fowl were running more economically than expected.
Teaming up with Jonas Rubenson, the scientists analysed the extra mechanical work required to move the bird's weighted legs, expecting that the majority of the extra work would be done while swinging the weighted legs. But they soon realised that only 60% of the increased work was required to swing the leg weights. 40% of the increased work was unexpectedly performed while the foot was in contact with the ground. Scrutinising the bird's running technique, the team realised that the bird began to accelerate the extra weight forward while the foot was still in contact with the ground, increasing the mechanical energy of the stance phase more than expected.
Curious to know which leg muscles contributed most as the birds laboured with their leg and back loads, Marsh and Ellerby returned to the blood flow monitoring technique to investigate which leg muscles came into action when the birds ran with, and without, their weights(). Injecting the birds with coloured microscopic spheres that became lodged in tiny capillaries, the team were able to monitor which muscles received increased blood flow as they worked harder by recording the quantity of beads trapped in muscles. Injecting the birds with different coloured beads (depending on whether the birds were running freely, running with the backpack, or running with the ankle weights) the team could clearly see which muscles had the highest blood flow and metabolic demands during each running test. The team noticed that 12 muscles were involved in supporting the bird's weight when carrying the 333 g backpacks. However, three of those leg muscles accounted for 70% of this metabolic increase. Which probably explains why the backpacked birds are unable to run much faster than 1.5 m s-1; the three supporting muscles were already working close to their peak, and couldn't support the birds at faster speeds.
The team also noticed that the same three major stance muscles functioned as extensor muscles across several joints when supporting the extra weight. Marsh suspects that this could account for the birds' remarkably economic gait, as the muscle provides support and propulsion without wasting energy at other joints. Looking at the blood flow in the leg muscles of the birds running with ankle weights, the team found that muscles involved in swinging the leg increased their blood flow by 58% while the muscles active in the stance phase of a stride increased their blood flow by 42%, agreeing well with the team's earlier mechanical measurements. It seems that the energetic cost of running is much more complex than had been originally thought.
