Increased non-linear locomotion alters diaphyseal bone shape

Abstract

SUMMARY Comparative studies of vertebrate morphology that link habitual locomotor activities to bone structural properties are often limited by confounding factors such as genetic variability between groups. Experimental assessment of bone's adaptive response to altered activity patterns typically involves superimposing exercise onto a normal locomotor repertoire, making a distinction between qualitative changes to locomotor repertoires and quantitative increases in activity level difficult. Here, we directly tested the hypothesis that an increase in turning activity, without the application of exercise per se, will alter femoral cross-sectional shape. Thirty day-old female BALB/cByJ mice (n=10 per group) were single-housed for 8 weeks in custom-designed cages that either accentuated linear or turning locomotion or allowed subjects to freely roam standard cages. Consistent with a lack of difference in physical activity levels between groups, there were no significant differences in body mass, femoral length, midshaft cortical area,and individual measures of mediolateral (ML) and anteroposterior (AP) bending rigidity. However, the ratio of ML to AP diaphyseal rigidity, an indicator of cross-sectional shape, was significantly greater (P<0.05) in turning subjects than in linear or control subjects. Considering that across all groups mice were genetically identical and had equivalent levels of bone quantity and physical activity, differences in femoral shape were attributed to qualitative differences in locomotor patterns (i.e. specific locomotor modes). These data indicate that increased turning can alter distribution of bone mass in the femoral diaphysis, and that turning should be considered in efforts to understand form–function relationships in vertebrates.

Does skeletal anatomy reflect adaptation to locomotor patterns? cortical and trabecular architecture in human and nonhuman anthropoids

“…The hind limb dominance of most anthropoids undoubtedly influences the distribution of cortical bone robusticity and trabecular bone architectural properties. The ability to control for this variability when analyzing cortical and trabecular bone structure would provide a more nuanced understanding of the influence that locomotor patterning has on skeletal and fossil morphology (Carlson and Judex, 2007;Carlson et al, 2008a). VOI, the area from which trabecular measurements are taken, can be extracted from multiple areas within a given anatomical region (e.g., the femoral head).…”

“…The analysis of both sub-articular trabeculae and diaphyseal cortical bone is a relatively new approach (see Carlson and Judex, 2007;Carlson et al, 2008a;Lazenby et al, 2008) that allows for direct comparisons of morphological variation in two types of osseous tissue, within the same skeletal element. The integrated consideration of diaphyseal and trabecular bone properties is a perspective that attempts to move away from the reductionism that often occurs with trabecular bone analyses in the comparative literature.…”

“…Experimental studies have demonstrated that both diaphyseal cortical bone and sub-articular trabecular bone can respond physiologically to in vivo mechanical loading (cf. Pontzer et al, 2006;Carlson and Judex, 2007). It has also been suggested that these tissues may contain an osteological signal reflective of adaptation to locomotor behavior (Ruff and Runestad, 1992;Rafferty and Ruff, 1994).…”

Locomotor variation and bending regimes of capuchin limb bones

“…To capture the loads associated with locomotion in a natural habitat, our efforts should clearly be focused on trying to expand the range of activities solicited in a laboratory experimental environment. Nonlinear locomotion is a particularly important activity that has been widely neglected in vertebrate locomotor studies (but see Burr et al, 1996;Walter, 2003;Demes et al, 2006;Carlson and Judex, 2007;Jindrich et al, 2007;Moreno et al, 2008). The advice by Dickinson et al (2000) to ''leave the straight and narrow'' in laboratory studies of locomotion is still highly relevant.…”

Comparisons of Limb Structural Properties in Free-ranging Chimpanzees from Kibale, Gombe, Mahale, and Taï Communities

“…When comparing limb loading during terrestrial quadrupedal locomotion and select modes of a primate arboreal locomotor repertoire (i.e., vertical climbing, brachiation), the latter are characterized by relatively greater variation in load orientations (Demes et al, 2001;Swartz et al, 1989). When using additional, but indirect measures to infer limb loading, e.g., substrate reaction forces, kinematics, and second moments of area, during even more locomotor behaviors, variability in loading regimes seems even greater than currently appreciated (Carlson and Judex, 2007;Demes et al, 2006; Demes and Carlson, in review). In addition to activity-induced deformations, other non-mechanical factors, e.g., genetics, hormones, and age affect bone modeling/remodeling process, which potentially could 4 affect cross-sectional geometric properties independent of activity patterns (Devlin and Lieberman, 2007;Martin et al, 1998;Robling et al, 2007;Turner et al, 2000;Wergedal et al, 2005;Xiong et al, 2006).…”