Limb bone morphology, bone strength, and cursoriality in lagomorphs

Abstract

The primary aim of this study is to broadly evaluate the relationship between cursoriality (i.e. anatomical and physiological specialization for running) and limb bone morphology in lagomorphs. Relative to most previous studies of cursoriality, our focus on a size-restricted, taxonomically narrow group of mammals permits us to evaluate the degree to which 'cursorial specialization' affects locomotor anatomy independently of broader allometric and phylogenetic trends that might obscure such a relationship. We collected linear morphometrics and lCT data on 737 limb bones covering three lagomorph species that differ in degree of cursoriality: pikas (Ochotona princeps, non-cursorial), jackrabbits (Lepus californicus, highly cursorial), and rabbits (Sylvilagus bachmani, level of cursoriality intermediate between pikas and jackrabbits). We evaluated two hypotheses: cursoriality should be associated with (i) lower limb joint mechanical advantage (i.e. high 'displacement advantage', permitting more cursorial species to cycle their limbs more quickly) and (ii) longer, more gracile limb bones, particularly at the distal segments (as a means of decreasing rotational inertia). As predicted, highly cursorial jackrabbits are typically marked by the lowest mechanical advantage and the longest distal segments, non-cursorial pikas display the highest mechanical advantage and the shortest distal segments, and rabbits generally display intermediate values for these variables. Variation in long bone robusticity followed a proximodistal gradient. Whereas proximal limb bone robusticity declined with cursoriality, distal limb bone robusticity generally remained constant across the three species. The association between long, structurally gracile limb bones and decreased maximal bending strength suggests that the more cursorial lagomorphs compromise proximal limb bone integrity to improve locomotor economy. In contrast, the integrity of distal limb bones is maintained with increasing cursoriality, suggesting that the safety factor takes priority over locomotor economy in those regions of the postcranial skeleton that experience higher loading during locomotion. Overall, these findings support the hypothesis that cursoriality is associated with a common suite of morphological adaptations across a range of body sizes and radiations.

Fluctuating and directional asymmetry in the long bones of captive cotton‐top tamarins (Saguinus oedipus)

“…A new finding in this study, however, is that asymmetry in external articular dimensions increases distally; and both the FA and DA show this pattern. Safety factors of bone (a ratio of fracture stress to peak functional stress, that is, how "over engineered" a bone is (Biewener, 1983)) have been documented to decrease distally along limbs (Alexander, 1981;Young et al, 2014), and patterns of bone functional adaptation likewise differ between the proximal and distal cortices of limb bones (Lieberman et al, 2003). Whether these biomechanical aspects of limb bones correspond with the proximodistal pattern in asymmetry cannot be made, however the link among them is compelling; it is possible that the distal portions of bone are more sensitive to their mechanical environment than proximal portions, and therefore lead to more asymmetry (Lieberman et al, 2003).…”

Changes in shape and cross‐sectional geometry in the tibia of mice selectively bred for increases in relative bone length

“…; Ruff, , ; Young et al. , ). Then, one‐way anova s were used to determine whether intensive selection for increases in bone length caused changes in the mean cross‐sectional properties (CSA, Z p ) and scaled bending strength (IR) of the Longshanks and Control tibiae.…”

“…improved running economy) and reduced bone safety factors (Young et al. ). Intra‐specifically, a study by Kemp et al.…”

“…Second, the cross‐sectional geometry of the tibia mid‐shaft is examined to determine whether there has been a change in the bone's inferred strength in relation to increased bone length, as observed in lagomorphs (Young et al. ) and certain dog breeds (Kemp et al. ).…”

Scaling of the appendicular skeleton of the giraffe (Giraffa camelopardalis)

“…Previous authors proposed the giraffe metapodials to be the seat of limb propulsion and elongation (Thompson, ; Colbert, ; McMahon, ). In proficient runners, it has been shown that the elongated distal elements are more energy efficient and increase stride length (Carrier, ; Christiansen, ; Lammers and German, ; Young et al, ). Our data show, however, that the metapodials of giraffes do not elongate more than other limb bones over their lifetime.…”