Insects Change Locomotion Modes to Traverse 3-D Obstacles with Varied Potential Energy Barriers

Our recent work showed that legged locomotion in complex 3-D terrain can be understood as a locomotor-terrain interaction system that explores a potential energy landscape, where kinetic energy fluctuations from intermittent body/leg-terrain interactions help the system explore the landscape to form locomotor transition pathways. Here, we study cockroaches traversing grass-like obstacles to understand how the relative size of potential energy barriers and kinetic energy fluctuations affect system behavior. We created a terrain with grass-like beams whose torsional stiffness is precisely controlled and systematically varied to change potential energy barriers of the terrain, relative to the animal’s kinetic energy fluctuations. We discovered that, as potential energy barriers increased with beam stiffness, the animal switched its dominant traversal mode from running over with high beam deflection (95 ± 5 %), to a low beam deflection, body roll maneuver (90 ± 6 %), with traversal time increasing from 1.1 ± 1.1 s to 2.7 ± 1.4 s (P < 0.001, ANOVA). Our locomotion energy landscape model revealed that as potential energy barriers increase, it takes longer for the system to find low barrier transition pathways; potential energy barriers that are too low do not affect system behavior.