Long-axis rotation: a missing degree of freedom in avian bipedal locomotion

Ground-dwelling birds are typically characterized as erect bipeds having hind limbs that operate parasagittally. Consequently, most previous research has emphasized flexion/extension angles and moments as calculated from a lateral perspective. Three-dimensional (3D) motion analyses have documented non-planar limb movements, but the skeletal kinematics underlying changes in foot orientation and transverse position remain unclear. In particular, long-axis rotation of the proximal limb segments is extremely difficult to measure with topical markers. Here, we present six degree of freedom skeletal kinematic data from maneuvering guineafowl acquired by marker-based XROMM (X-ray Reconstruction of Moving Morphology). Translations and rotations of the hips, knees, ankles and pelvis were derived from animated bone models using explicit joint coordinate systems. We distinguished sidesteps, sidestep yaws, crossover yaws, sidestep turns and crossover turns, but birds often performed a sequence of blended partial maneuvers. Long-axis rotation of the femur (up to 38 deg) modulated the foot's transverse position. Long-axis rotation of the tibiotarsus (up to 65 deg) also affected medio-lateral positioning, but primarily served to either re-orient a swing phase foot or yaw the body about a stance phase foot. Tarsometatarsal long-axis rotation was minimal, as was hip, knee and ankle abduction/adduction. Despite having superficially hinge-like joints, birds coordinate substantial long-axis rotations of the hips and knees to execute complex 3D maneuvers while striking a diversity of non-planar poses.