Biomechanical consequences of scaling.

To function over a lifetime of use, materials and structures must be designed to have sufficient factors of safety to avoid failure. Vertebrates are generally built from materials having similar properties. Safety factors are most commonly calculated based on the ratio of a structure's failure stress to its peak operating stress. However, yield stress is a more likely limit, and work of fracture relative to energy absorption is likely the most relevant measure of a structure's safety factor, particularly under impact loading conditions characteristic of locomotion. Yet, it is also the most difficult to obtain. For repeated loading, fatigue damage and eventual failure may be critical to the design of biological structures and will result in lower safety factors. Although area:volume scaling predicts that stresses will increase with size, interspecific comparisons of mammals and birds show that skeletal allometry is modest, with most groups scaling (l proportional, variant d0.89) closer to geometric similarity (isometry: l proportional, variant d1.0) than to elastic similarity (l proportional, variant d0.67) or stress similarity (l proportional, variant d0.5). To maintain similar peak bone and muscle stresses, terrestrial mammals change posture when running, with larger mammals becoming more erect. More erect limbs increases their limb muscle mechanical advantage (EMA) or ratio of ground impulse to muscle impulse (r/R= integral G/integral Fm). The increase in limb EMA with body weight (proportional, variant W0.25) allows larger mammals to match changes in bone and muscle area (proportional, variant W0.72-0.80) to changes in muscle force generating requirements (proportional, variantW0.75), keeping bone and muscle stresses fairly constant across a size range 0.04-300 kg. Above this size, extremely large mammals exhibit more pronounced skeletal allometry and reduced locomotor ability. Patterns of ontogenetic scaling during skeletal growth need not follow broader interspecific scaling patterns. Instead, negative allometric growth (becoming more slender) is often observed and may relate to maturation of the skeleton's properties or the need for younger animals to move at faster speeds compared with adults. In contrast to bone and muscle stress patterns, selection for uniform safety factors in tendons does not appear to occur. In addition to providing elastic energy savings, tendons transmit force for control of motion of more distal limb segments. Their role in elastic savings requires that some tendons operate at high stresses (and strains), which compromises their safety factor. Other 'low stress' tendons have larger safety factors, indicating that their primary design is for stiffness to reduce the amount of stretch that their muscles must overcome when contracting to control movement.