Limb bone scaling in hopping macropods and quadrupedal artiodactyls

Abstract

Bone adaptation is modulated by the timing, direction, rate, and magnitude of mechanical loads. To investigate whether frequent slow, or infrequent fast, gaits could dominate bone adaptation to load, we compared scaling of the limb bones from two mammalian herbivore clades that use radically different high-speed gaits, bipedal hopping and quadrupedal galloping. Forelimb and hindlimb bones were collected from 20 artiodactyl and 15 diprotodont species (body mass M 1.05 -1536 kg) and scanned in clinical computed tomography or X-ray microtomography. Second moment of area (I max ) and bone length (l) were measured. Scaling relations (y = ax b ) were calculated for l vs M for each bone and for I max vs M and I max vs l for every 5% of length. I max vs M scaling relationships were broadly similar between clades despite the diprotodont forelimb being nearly unloaded, and the hindlimb highly loaded, during bipedal hopping. I max vs l and l vs M scaling were related to locomotor and behavioural specialisations. Low-intensity loads may be sufficient to maintain bone mass across a wide range of species. Occasional high-intensity gaits might not break through the load sensitivity saturation engendered by frequent low-intensity gaits. IntroductionDuring daily rest and activity, bones experience a range of mechanical loading conditions that relate to each behaviour's physical intensity. Bones respond anabolically, that is, by increasing bone tissue formation and decreasing bone resorption, when they experience a small number of novel high strain and high strain rate events with a rest period between bouts of loading [1,2]. Repetitive loading has a saturation or habituation effect, in which tissue is no longer responsive to mechanical loads after a few tens of cycles [2]. Large numbers of loading cycles without sufficient rest are associated with fatigue or 'stress' fractures, typically seen in new military recruits [3] and racing animals such as greyhounds [4] and horses [5,6]. The distributions of occasional maximal loads and habitual moderate loads vary within the skeleton and depend on locomotor activity, which should appear as a morphological signal in clades that adopt very different characteristic gaits [7].

The evolution of femoral cross‐sectional properties in sciuromorph rodents: Influence of body mass and locomotor ecology

“…Hence, interpretations in this regard have to be taken with care. Contrary to our findings, positive allometry of SMA to body mass was found in artiodactyls and diprotodonts in this area (Doube et al, ). Perhaps, this can be linked to the lack of a distinct third trochanter (at least in artiodactyls), giving more weight to the morphological adjustment to bending than to tension forces.…”

“…It is surprising that in the proximal epiphyseal region, which is mostly affected by compressive forces (femoral head) or tensile forces (greater trochanter as a muscle attachment site), not only the CSA but also the SMA variables displayed positive allometry, the latter expected to be rather important for regions experiencing bending (i.e., diaphysis). Similarly, Doube et al () also found positive allometry for SMA (we assume SMA cc as it was not specified) in artiodactyls and diprotodonts in this region. However, by demonstrating positive allometry when regressing CSA on SMA at epiphyses in felids, Doube et al () showed that compression forces are considerably higher than bending forces in the epiphyseal regions.…”

“…Here, we aimed to gain insight into the evolution of adaptations of the cross‐sectional properties (CSP) of the sciuromorph femur. For this purpose, we quantified them in 5% increments along the length of the bone following the approach of Doube et al (, ) and Kilbourne and Hutchinson (). The three CSP analyzed here are proxies of different uni‐ or multidimensional forces the bones experience (Ruff & Runestad, ; Schaffler, Burr, Jungers, & Ruff, ).…”

“…Furthermore, different substrate textures (e.g., branches vs. dirt) appear to also impact the properties of bones (Polk et al, 2000). Morphological correlates to these differing functional demands, which are posed during the locomotion in a specific habitat, therefore often have been identified in several tetrapod lineages (Botton-Divet, Cornette, Fabre, Herrel, & Houssaye, 2016;Burr et al, 1989;Doube et al, 2018;Kilbourne, 2017;Kilbourne & Hutchinson, 2019;Kimura, 1991Kimura, , 1995Polk et al, 2000;Polly, 2007).…”

“…Here, we aimed to gain insight into the evolution of adaptations of the cross-sectional properties (CSP) of the sciuromorph femur. For this purpose, we quantified them in 5% increments along the length of the bone following the approach of Doube et al (2009Doube et al ( , 2018 and Kilbourne and Hutchinson (2019).…”