A bio-robotic platform for integrating internal and external mechanics during muscle-powered swimming

To explore the interplay between muscle function and propulsor shape in swimming animals, we built a robotic foot to mimic the morphology and hind limb kinematics of Xenopus laevis frogs. Four foot shapes ranging from low aspect ratio (AR = 0.74) to high (AR = 5) were compared to test whether low-AR feet produce higher propulsive drag force resulting in faster swimming. Using feedback loops, two complementary control modes were used to rotate the foot: force was transmitted to the foot either from (1) a living plantaris longus (PL) muscle stimulated in vitro or (2) an in silico mathematical model of the PL. To mimic forward swimming, foot translation was calculated in real time from fluid force measured at the foot. Therefore, bio-robot swimming emerged from muscle-fluid interactions via the feedback loop. Among in vitro-robotic trials, muscle impulse ranged from 0.12 ± 0.002 to 0.18 ± 0.007 N s and swimming velocities from 0.41 ± 0.01 to 0.43 ± 0.00 m s(-1), similar to in vivo values from prior studies. Trends in in silico-robotic data mirrored in vitro-robotic observations. Increasing AR caused a small (∼10%) increase in peak bio-robot swimming velocity. In contrast, muscle force-velocity effects were strongly dependent on foot shape. Between low- and high-AR feet, muscle impulse increased ∼50%, while peak shortening velocity decreased ∼50% resulting in a ∼20% increase in net work. However, muscle-propulsion efficiency (body center of mass work/muscle work) remained independent of AR. Thus, we demonstrate how our experimental technique is useful for quantifying the complex interplay among limb morphology, muscle mechanics and hydrodynamics.