Running over rough terrain: guinea fowl maintain dynamic stability despite a large unexpected change in substrate height

Author:

Daley Monica A.1,Usherwood James R.1,Felix Gladys1,Biewener Andrew A.1

Affiliation:

1. Concord Field Station, MCZ, Harvard University, Old Causeway Road,Bedford, MA 01730, USA

Abstract

SUMMARY In the natural world, animals must routinely negotiate varied and unpredictable terrain. Yet, we know little about the locomotor strategies used by animals to accomplish this while maintaining dynamic stability. In this paper, we perturb the running of guinea fowl with an unexpected drop in substrate height (ΔH). The drop is camouflaged to remove any visual cue about the upcoming change in terrain that would allow an anticipatory response. To maintain stability upon a sudden drop in substrate height and prevent a fall, the bird must compensate by dissipating energy or converting it to another form. The aim of this paper is to investigate the control strategies used by birds in this task. In particular, we assess the extent to which guinea fowl maintain body weight support and conservative spring-like body dynamics in the perturbed step. This will yield insight into how animals integrate mechanics and control to maintain dynamic stability in the face of real-world perturbations. Our results show that, despite altered body dynamics and a great deal of variability in the response, guinea fowl are quite successful in maintaining dynamic stability, as they stumbled only once(without falling) in the 19 unexpected perturbations. In contrast, when the birds could see the upcoming drop in terrain, they stumbled in 4 of 20 trials(20%, falling twice), and came to a complete stop in an additional 6 cases(30%). The bird's response to the unexpected perturbation fell into three general categories: (1) conversion of vertical energy(EV=EP+EKv) to horizontal kinetic energy (EKh), (2) absorption of EV through negative muscular work(-ΔEcom), or (3) converting EPto vertical kinetic energy (EKv), effectively continuing the ballistic path of the animal's center of mass (COM) from the prior aerial phase. However, the mechanics that distinguish these categories actually occur along a continuum with varying degrees of body weight support and actuation by the limb, related to the magnitude and direction of the ground reaction force(GRF) impulse, respectively. In most cases, the muscles of the limb either produced or absorbed energy during the response, as indicated by net changes in COM energy (Ecom). The limb likely begins stance in a more retracted, extended position due to the 26 ms delay in ground contact relative to that anticipated by the bird. This could explain the diminished decelerating force during the first half of stance and the exchange between EP and EK during stance as the body vaults over the limb. The varying degree of weight support and energy absorption in the perturbed step suggests that variation in the initial limb configuration leads to different intrinsic dynamics and reflex action. Future investigation into the limb and muscle mechanics underlying these responses could yield further insight into the control mechanisms that allow such robust dynamic stability of running in the face of large, unexpected perturbations.

Publisher

The Company of Biologists

Subject

Insect Science,Molecular Biology,Animal Science and Zoology,Aquatic Science,Physiology,Ecology, Evolution, Behavior and Systematics

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