Limb bone scaling in hopping macropods and quadrupedal artiodactyls.

Michael Doube,Sandra J Shefelbine,Melissa Y Chua,Kalyani Lodhia,John R Hutchinson,Michał M Kłosowski,Alessandro A Felder

doi:10.1098/rsos.180152

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 (suborder Macropodiformes; kangaroos and kin) and quadrupedal galloping (order Artiodactyla; goats, deer and kin). Forelimb and hindlimb bones were collected from 20 artiodactyl and 15 macropod species (body mass M 1.05–1536 kg) and scanned in computed tomography or X-ray microtomography. Second moment of area (Imax) and bone length (l) were measured. Scaling relations (y = axb) were calculated for l versus M for each bone and for Imax versus M and Imax versus l for every 5% of length. Imax versus M scaling relationships were broadly similar between clades despite the macropod forelimb being nearly unloaded, and the hindlimb highly loaded, during bipedal hopping. Imax versus l and l versus M scaling were related to locomotor and behavioural specializations. 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.

Highlights

Bone adaptation is modulated by the timing, direction, rate and magnitude of mechanical loads
Radius and ulna lengths scale with positive allometry (b in macropods, but with isometry (b not significantly different from 1) in artiodactyls
Scaling of the forelimb and hindlimb segments is similar within clades, except the stylopod, in which the Imax versus length scaling displays positive allometry in the artiodactyl and macropod femur and artiodactyl humerus, but negative allometry in the macropod humerus, meaning that in macropods the humerus becomes more gracile with increasing length while the femur becomes more robust

Summary

Introduction

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 (suborder Macropodiformes; kangaroos and kin) and quadrupedal galloping (order Artiodactyla; goats, deer and kin). During daily rest and activity in development, growth and adulthood, bones experience a range of mechanical loading conditions that relate to each behaviour’s physical intensity Kangaroos, wallabies and their macropodiform kin are famed for their hopping hindlimb gait which they use for bursts of efficient high-speed locomotion [1,2,3]. If the more frequently used, slower gaits’ loading environment drives bone shape, we should expect to see similar scaling between macropods’ fore- and hindlimbs, and between equivalent bones in macropods and artiodactyls, because the low-speed pentapedal gait and quadrupedal walking, respectively, dominate these clades’ locomotor repertoires

Methods

Results

Conclusion