Posture, gait and the ecological relevance of locomotor costs and energy-saving mechanisms in tetrapods
Introduction
In recent decades the study of terrestrial locomotion has seen a welcome and varied array of perspectives from muscle to organismal levels. Studies of terrestrial locomotion can be divided roughly into three groups: functional studies, looking at limb movements and musculoskeletal function (e.g., Fischer et al., 2002; Roberts, 2002); energetic studies, relating oxygen consumption to the work, power and cost of movement (e.g., Cavagna et al., 1977; Donelan et al., 2002); and mechanical studies, using data on locomotor forces to examine movements of the center of mass (COM) of the whole body (or its components) as well as energy-saving mechanisms (e.g., Griffin et al., 2004a; Biewener, 2005). Each of these approaches has its body of work and general concepts, with a modest amount of overlap, but there are few examples of full integration (e.g., Minetti et al., 1999; Rubenson et al., 2004). In this paper, we review and attempt to integrate some of the emerging conceptual patterns from functional, energetic and mechanical approaches to the study of locomotion. We offer new interpretations and insights on the costs of locomotion and actual cost savings in terrestrial vertebrates when effects of limb posture (sprawling or crouched limbs versus erect limbs), gait and the ecological relevance of locomotor costs are considered.
A conceptual framework for understanding the relationship between animal function and the cost of locomotion is presented in Fig. 1. Legged animals are literally crawling all over this planet but they share three common goals regarding locomotion: food resource acquisition, predator avoidance and participation in social interactions critical for survival and reproduction. Although the importance of locomotion in animal fitness philosophically overlies all studies of locomotion, it is generally only mentioned in passing, if at all, in most of our atomized studies of locomotion. Animals move through a decision-making process (Fig. 1) linking the ecological relevance of locomotion (why they are moving) to the kind of locomotor behavior needed (how they will need to move) in order to instruct the body how to move. Issues of speed, substrate and stability inherently influence how animals need to move and how much it will cost, yet we have only begun to understand how these needs affect locomotor output and metabolic costs (Dickinson et al., 2000). Organismal function and metabolic cost of locomotion have seen considerable study independently but little effort has been made to link aspects of locomotor output to factors influencing metabolic costs. Ultimately, we want to know how metabolic economy relates to the ecological relevance of locomotion.
Section snippets
Understanding the metabolic cost of locomotion
Body movements are produced via a locomotor output axis (Fig. 1): the nervous system controls motor output of the musculoskeletal system and coordinates footfalls (gaits) that deliver forces to the substrate in order to move the COM. The energetic cost of locomotion is directly related to overall muscular effort, yet the level of muscular activity itself is modulated by limb design, gait and several energy-saving mechanisms.
Muscle mass and mechanical advantage
Given that the cost of locomotion is primarily driven by the metabolic cost of muscle activation, we first consider how postural effects on relative limb muscle size and joint mechanical advantage influence metabolic and mechanical energy costs (Figs. 3b, c). Here, again, the broad-scale approach appears to mask clear differences between the posture groups. For example, leg muscle mass (relative to body mass) scales linearly and nearly isometrically with body size in shrew-to-buffalo
Contributions of dynamic energy-saving mechanisms
Why is the metabolic cost of locomotion so much lower in erect animals? While decreasing muscle mass accompanied by increasing EMA partially explains this lower cost, another part of the answer may also be related to the actual capacity of dynamic energy-saving mechanisms (pendular and spring savings; Fig. 1) to effectively contribute to reducing muscular effort and thus metabolic cost.
Gait effects on locomotor costs
Animals appear to fine-tune limb dynamics within gaits to move at certain preferred speeds at which metabolic cost is minimal (Hoyt and Taylor, 1981). More radical changes in limb dynamics are made between gaits. Gait transitions occur as changes in neuromotor output affecting inter-limb and intra-limb coordination (Fig. 1, locomotor output axis), yielding shifts in how the COM moves and thereby influencing fluctuations of kinetic, gravitational potential and elastic strain energies (Cavagna et
The relative costs of gaits versus the ecological relevance of locomotion
Legged animals have in common three main motivations for moving: acquiring food resources, avoiding predation and social interaction (Fig. 1). Although these critical selective factors drive the evolution of locomotion, very little understanding exists on how much animals move, how often they move fast or slow, what gaits they use in these behaviors or how locomotor behavior differs across the postural array of animals discussed in this study. In order to begin to consider the relevance of
Conclusions and future directions
That small and large animals face different challenges is not new, and many studies have noted size-dependent differences in many aspects of locomotion. The reevaluation of anatomical and locomotor energetic data presented here further highlights that size does matter but primarily because of correlated changes in posture. Several clear patterns emerge from our reanalysis.
There are nonlinear patterns of change in metabolic cost, limb muscle mass, EMA and stride characteristics with body size in
Acknowledgments
Parts of this analysis were presented in the “Integrating Approaches to the Study of Terrestrial Locomotion” Symposium at the 7th International Congress of Vertebrate Morphology. We are grateful for the input from the Ohio University Evolutionary Biomechanics Group and three anonymous reviewers. Discussions with John Bertram and John Hermanson helped forge some of our thinking about horses. Special thanks go to Lee Boyd for digging up more details on horse locomotor time budgets. Support of the
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