Diversity of Limb-Bone Safety Factors for Locomotion in Terrestrial Vertebrates: Evolution and Mixed Chains

Abstract

During locomotion over land, vertebrates' limb bones are exposed to loads. Like most biological structures, limb bones have a capacity to withstand greater loads than they usually experience, termed a safety factor (SF). How diverse are limb-bone SFs, and what factors correlate with such variation? We have examined these questions from two perspectives. First, we evaluated locomotor SF for the femur in diverse lineages, including salamanders, frogs, turtles, lizards, crocodilians, and marsupials (opossums). Comparisons with values for hind-limb elements in running birds and eutherian mammals indicate phylogenetic diversity in limb-bone SF. A high SF (∼7) is primitive for tetrapods, but low magnitudes of load and elevated strength of bones contribute to different degrees across lineages; moreover, birds and eutherians appear to have evolved lower SFs independently. Second, we tested the hypothesis that SFs would be similar across limb bones within a taxon by comparing data from the humerus and femur of alligators. Both in bending and in torsion, we found a higher SF for the humerus than for the femur. Such a "mixed chain" of different SFs across elements has been predicted if bones have differing variabilities in load, different costs to maintain, or high SF values in general. Although variability in load is similar for the humerus and femur, a high SF may be less costly for the humerus because it is smaller than the femur. The high SFs of alligators also might facilitate differences in SF among their limb bones. Beyond these specific findings, however, a more general implication of our results is that evaluations of the diversity of limb-bone SFs can provide important perspective to direct future research. In particular, more complete understanding of variation in SF could provide insight into factors that promoted the evolutionary radiation of terrestrial locomotor function in vertebrates.

Pelvic girdle mobility of cryptodire and pleurodire turtles during walking and swimming

“…LAR, long-axis rotation; var., variance. Sheffield et al, 2011;Blob et al, 2014). In this context, our data on pelvic and femoral movement in turtles are noteworthy in two regards.…”

Comparative limb bone loading in the humerus and femur of the tiger salamander Ambystoma tigrinum: testing the ‘mixed-chain’ hypothesis for skeletal safety factors

“…Comparisons between bones of the forelimb and hindlimb are also appropriate to consider in the context of 'mixed-chains' because, although the girdles and vertebrae intervene between these limbs, both limbs function to support the body in quadrupeds, and a break in any leg would impair locomotion. However, data for such comparisons are more limited, with a single study finding higher SFs in the humerus versus the femur of alligators (Blob et al, 2014). With respect to proposed factors contributing to 'mixed-chains' (Alexander, 1997;Diamond, 2002), the higher humeral SFs of alligators were attributed to the generally high SFs in the limbs of reptiles and the smaller size of the humerus that might make high SFs less costly than for the femur (Blob et al, 2014).…”

“…SFs for bones commonly allow protection against loads ranging from 2 to 10 times greater than ordinary, with variation across taxa and among the limb bones within a species (Alexander, 1981;Biewener, 1993;Blob et al, 2014;Currey, 2002;Diamond, 2002;. Several factors contribute to interspecific variation in SFs (Blob and Biewener, 1999;Blob et al, 2014), but explanations for intraspecific variation are less intuitive.…”

“…Several factors contribute to interspecific variation in SFs (Blob and Biewener, 1999;Blob et al, 2014), but explanations for intraspecific variation are less intuitive. For a single structure, the SF is expected to be sufficiently high to prevent it from being compromised by applied loads, but low enough to minimize the energetic costs to produce such a structure (Alexander, 1997).…”

“…However, data for such comparisons are more limited, with a single study finding higher SFs in the humerus versus the femur of alligators (Blob et al, 2014). With respect to proposed factors contributing to 'mixed-chains' (Alexander, 1997;Diamond, 2002), the higher humeral SFs of alligators were attributed to the generally high SFs in the limbs of reptiles and the smaller size of the humerus that might make high SFs less costly than for the femur (Blob et al, 2014). However, with such patterns evaluated for only a single species, their generality is unclear.…”