Fluoromicrometry reveals minimal influence of tendon elasticity during snake locomotion.

Abstract

Multiarticular muscle systems are widespread across vertebrates, including in their necks, digits, tails and trunks. In secondarily limbless tetrapods, the multiarticular trunk muscles power nearly all behaviors. Using snakes as a study system, we previously used anatomical measurements and mathematical modeling to derive an equation relating multiarticular trunk muscle shortening to postural change. However, some snake trunk muscles have long, thin tendinous connections, raising the possibility of elastic energy storage, which could lead to a decoupling of muscle length change from joint angle change. The next step, therefore, is to determine whether in vivo muscle shortening produces the postural changes predicted by mathematical modeling. A departure from predictions would implicate elastic energy storage. To test the relationship between muscle strain and posture in vivo, we implanted radio-opaque metal beads in three muscles of interest in four corn snakes (Pantherophis guttatus), then recorded X-ray videos to directly measure muscle shortening and vertebral column curvature during locomotion. Our in vivo results produced evidence that elastic energy storage does not play a substantial role in corn snake lateral undulation or tunnel concertina locomotion. The ability to predict muscle shortening directly from observed posture will facilitate future work. Moreover, the generality of our equation, which uses anatomical values that can be measured in many types of animals, means that our framework for understanding multiarticular muscle function can be applied in numerous study systems to provide a stronger mechanistic understanding of organismal function.