Environmentally induced mechanical feedback in locomotion: Frog performance as a model

Abstract

A c c e p t e d m a n u s c r i p t 2 AbstractAt first glance, the strategy for generating propulsive impulses for both jumping and swimming in frogs is quite similar. Both modes rely on powerful extension of the hind limbs.However, in Rana esculenta (the semi-aquatic green frog), propulsive impulses for jumping were found to be much larger than those generated during swimming (Nauwelaerts and Aerts, 2003). The hypothesis that differences in propulsive impulse between swimming and jumping are largely caused by specific environmental constraints rather than being due to changes in motor control is tested in the present study. To assess this question, the actuator of a simple mathematical model, mimicking a frog with symmetrically kicking hind limbs, is first tuned to perform frog-like jumps. Next, the same actuator activation is applied to drive the model in an 'aquatic environment'. Despite the entirely identical activation, the resulting in silico propulsive swimming impulse was less than half that produced during jumping, just as observed in vivo. Although duration of limb extension is similar for both locomotor modes (both in vivo and in silico), this conspicuous difference in model behaviour is entirely explained by the actuator working at different positions along its force-velocity curve. These findings suggest that the same environmentally induced effects are also involved in real swimming and jumping as well, thus explaining the apparent difference in performance level.

Kinematic control of extreme jump angles in the red leg running frog (Kassina maculata)

“…Hence, we propose that although traditional 2D models of vertical jumps have been used as a template for all jumps (e.g. Alexander, 1995;Galantis and Woledge, 2003;Aerts and Nauwelaerts, 2009), they may not be appropriate for the entire range of jumping. Future investigation would be required to determine whether vertical jumping and horizontal jumping represent two distinct behaviours.…”

“…Small vertebrates such as frogs and lizards tune their performance by shifting their take-off velocity and angle (Marsh, 1994;Toro et al, 2004). While this 2D view has expanded our understanding of the musculoskeletal system (Galantis and Woledge, 2003;Roberts and Marsh, 2003;Aerts, 1998;Aerts and Nauwelaerts, 2009), it does not fully explain the control of performance. As a jumping frog traces a simple path along the vertical plane, how do the elaborate 3D leg rotations (Nauwelaerts and Aerts, 2003;Astley and Roberts, 2014) act to carry the body upward and forward?…”

“…Recent evidence suggests that variations between swimming versus jumping kinematics are not strongly dependent on muscle activation patterns. Rather, kinematic differences largely emerge from differences in the fluid versus solid substrates (Nauwelaerts and Aerts, 2003;Aerts and Nauwelaerts, 2009), despite similar muscle firing patterns (Emerson and De Jongh, 1980;Kamel et al, 1996;Gillis and Biewener, 2000;d'Avella and Bizzi, 2005). In contrast, limb motions within terrestrial modes of locomotion (walking, climbing, jumping, etc.…”

Built for rowing: frog muscle is tuned to limb morphology to power swimming

“…Based upon recent models [19,20], we assumed that muscle F-V properties dominate muscle function in frog swimming. For a rigid, flat, fin rotating at 908 angle-of-incidence, we expressed hydrodynamic thrust in terms of inertia, muscle contractile properties, gearing and fin size.…”

Muscle function and hydrodynamics limit power and speed in swimming frogs

“…On the basis of geometry, we apply three scaling rules: mass (for example, muscle mass) aM 1 , length (for example, limb length) aM 1/3 and area (for example, webbed foot area) aM 2/3 . Simple models have often served to reveal general principals in complex systems [27][28][29] . We follow these examples and have modelled the movement of X. laevis as a simple muscle lever system, powered by the plantaris muscle, with a rigid flat fin rotating around about the ankle joint (Fig.…”