The substrate as a skeleton: ground reaction forces from a soft-bodied legged animal

The measurement of forces generated during locomotion is essential for the development of accurate mechanical models of animal movements. However, animals that lack a stiff skeleton tend to dissipate locomotor forces in large tissue deformation and most have complex or poorly defined substrate contacts. Under these conditions, measuring propulsive and supportive forces is very difficult. One group that is an exception to this problem is lepidopteran larvae which, despite lacking a rigid skeleton, have well-developed limbs (the prolegs) that can be used for climbing in complex branched structures and on a variety of surfaces. Caterpillars therefore are excellent for examining the relationship between soft body deformation and substrate reaction forces during locomotion. In this study, we devised a method to measure the ground reaction forces (GRFs) at multiple contact points during crawling by the tobacco hornworm (Manduca sexta). Most abdominal prolegs bear similar body weight during their stance phase. Interestingly, forward reaction forces did not come from pushing off the substrate. Instead, most positive reaction forces came from anterior abdominal prolegs loaded in tension while posterior legs produced drag in most instances. The counteracting GRFs effectively stretch the animal axially during the second stage of a crawl cycle. These findings help in understanding how a terrestrial soft-bodied animal can interact with its substrate to control deformation without hydraulic actuation. The results also provide insights into the behavioral and mechanistic constraints leading to the evolution of diverse proleg arrangements in different species of caterpillar.