Musculoskeletal modelling of an ostrich (Struthio camelus) pelvic limb: influence of limb orientation on muscular capacity during locomotion

Abstract

We developed a three-dimensional, biomechanical computer model of the 36 major pelvic limb muscle groups in an ostrich (Struthio camelus) to investigate muscle function in this, the largest of extant birds and model organism for many studies of locomotor mechanics, body size, anatomy and evolution. Combined with experimental data, we use this model to test two main hypotheses. We first query whether ostriches use limb orientations (joint angles) that optimize the moment-generating capacities of their muscles during walking or running. Next, we test whether ostriches use limb orientations at mid-stance that keep their extensor muscles near maximal, and flexor muscles near minimal, moment arms. Our two hypotheses relate to the control priorities that a large bipedal animal might evolve under biomechanical constraints to achieve more effective static weight support. We find that ostriches do not use limb orientations to optimize the moment-generating capacities or moment arms of their muscles. We infer that dynamic properties of muscles or tendons might be better candidates for locomotor optimization. Regardless, general principles explaining why species choose particular joint orientations during locomotion are lacking, raising the question of whether such general principles exist or if clades evolve different patterns (e.g., weighting of muscle force–length or force–velocity properties in selecting postures). This leaves theoretical studies of muscle moment arms estimated for extinct animals at an impasse until studies of extant taxa answer these questions. Finally, we compare our model’s results against those of two prior studies of ostrich limb muscle moment arms, finding general agreement for many muscles. Some flexor and extensor muscles exhibit self-stabilization patterns (posture-dependent switches between flexor/extensor action) that ostriches may use to coordinate their locomotion. However, some conspicuous areas of disagreement in our results illustrate some cautionary principles. Importantly, tendon-travel empirical measurements of muscle moment arms must be carefully designed to preserve 3D muscle geometry lest their accuracy suffer relative to that of anatomically realistic models. The dearth of accurate experimental measurements of 3D moment arms of muscles in birds leaves uncertainty regarding the relative accuracy of different modelling or experimental datasets such as in ostriches. Our model, however, provides a comprehensive set of 3D estimates of muscle actions in ostriches for the first time, emphasizing that avian limb mechanics are highly three-dimensional and complex, and how no muscles act purely in the sagittal plane. A comparative synthesis of experiments and models such as ours could provide powerful synthesis into how anatomy, mechanics and control interact during locomotion and how these interactions evolve. Such a framework could remove obstacles impeding the analysis of muscle function in extinct taxa.

Gearing effects of the patella (knee extensor muscle sesamoid) of the helmeted guineafowl during terrestrial locomotion

“…A modified ex vivo experiment, recording tendon tensions from the patellar complex of an instrumented Numida cadaver(s) subjected to dynamic extensor forces estimated from in vivo data, would perhaps represent the best of both methods, or at least a useful test of the methods and data presented here. However, estimation of the individual muscle forces needed for such an experiment requires a musculoskeletal simulation based on complete skeletal kinematics, limb endpoint forces, segment inertial properties and detailed muscle–tendon unit properties (see Hutchinson et al ., 2015 for an equivalent model of an ostrich). As such, it is beyond the scope of this project, but is a promising line of enquiry for future work.…”

Comparison of human gastrocnemius forces predicted by Hill-type muscle models and estimated from ultrasound images

“…For example, Hill-type models have been used, together with reconstructions of musculoskeletal geometry, to analyse the moment-generating capacities of animals during terrestrial locomotion (O'Neill et al, 2013;Hutchinson et al, 2015) and to estimate the locomotor capabilities of extinct species based on fossil records (Hutchinson and Garcia, 2002). Muscle models have also been used in simulations of human locomotion to infer the functions of individual muscles during walking and running (Hamner et al, 2010) and to uncover important insights into the biomechanical factors that contribute to gait abnormalities (e.g.…”

Guineafowl with a twist: asymmetric limb control in steady bipedal locomotion

“…Based on their stance phase activity pattern, muscles such as the iliotrochantericus caudalis and medius appear to be ideally situated to induce internal hip LAR (Gatesy, 1994(Gatesy, , 1999b). Yet, Hutchinson et al (2015) found that several of the most significant hip extensors have large internal rotation (called medial rotation in their paper) moment arms at relevant joint angles as well. Determining how these muscles (and active antagonists) interact with inertial loads and passive forces to modulate LAR during stance will require a more sophisticated, fully 3D approach.…”