Musculoskeletal modeling of an ostrich (Struthio camelus) pelvic limb: Influence of limb orientation on muscular capacity during locomotion
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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.
Cite this as
2014. Musculoskeletal modeling of an ostrich (Struthio camelus) pelvic limb: Influence of limb orientation on muscular capacity during locomotion. PeerJ PrePrints 2:e513v1 https://doi.org/10.7287/peerj.preprints.513v1note This preprint is not peer-reviewed. You may wish to reference the subsequent peer-reviewed version of this article.
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This is a submission to PeerJ for review.
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Supplemental Information
Movie S1
Musculoskeletal model of the right and left pelvic limbs of an ostrich, visualized statically to show 3D anatomy represented in the model; posed at mid-stance of running (right limb) and corresponding swing phase (left limb).
Supplementary Figures S1-S4
Hip muscle moment arms in long-axis rotation (LAR) or ab/adduction plotted against hip LAR or ab/adduction angles (cf. Figures 12-15 plotted against hip flexion/extension angles), for key proximal thigh muscles. See caption for Figure 9.
Additional Information
Competing Interests
John R Hutchinson is an Academic Editor for PeerJ.
Author Contributions
John R Hutchinson conceived and designed the experiments, performed the experiments, analyzed the data, wrote the paper, prepared figures and/or tables, reviewed drafts of the paper.
Jeffery W Rankin conceived and designed the experiments, performed the experiments, analyzed the data, wrote the paper, prepared figures and/or tables, reviewed drafts of the paper.
Jonas Rubenson conceived and designed the experiments, performed the experiments, wrote the paper, reviewed drafts of the paper.
Kate H Rosenbluth conceived and designed the experiments, performed the experiments, analyzed the data, reviewed drafts of the paper.
Robert A Siston conceived and designed the experiments, performed the experiments, contributed reagents/materials/analysis tools, reviewed drafts of the paper.
Scott L Delp conceived and designed the experiments, contributed reagents/materials/analysis tools, reviewed drafts of the paper.
Funding
This work was completed as part of a postdoctoral fellowship from the National Science Foundation awarded to J.R.H. in 2001, and subsequent funding from the BBSRC, grant number BB/I02204X/1, as well as the Leverhulme Trust (grant number RPG-2013-108). Additional support was provided by the Biomechanical Engineering Division at Stanford University, and from The Royal Veterinary College, Department of Comparative Biomedical Sciences. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
