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 (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.

Proximal Humerus Morphology Indicates Divergent Patterns of Locomotion in Extinct Giant Kangaroos

“…We note that preliminary trackway data from the Pliocene of central Australia (Camens and Worthy 2019) also supports this hypothesis of bipedal striding in sthenurines. Protemnodon has a proximal humeral morphology resembling that of scansorial or terrestrial carnivorans, supporting the hypothesis of a predominantly quadrupedal or pentapedal mode of locomotion at all speeds (Kear et al 2008;Den Boer 2018).…”

“…7) also indicates a relatively larger greater tuberosity, but a smaller lesser tuberosity, than most extant macropodoids. Thus Protemnodon evinces aspects of the proximal humerus that may be indicative of more extensive weight-bearing on the forelimbs than in extant macropodids, perhaps suggestive of a greater degree of quadrupedal activity, as suggested by Den Boer (2018).…”

“…8c). This might be indicative of an enlarged area of insertion for the supraspinatus, although the supraspinous fossa on the scapula is of a similar size to that of extant macropodids (see Den Boer 2018). The position of Protemnodon anak in the ternary plot ( Fig.…”

“…Protemnodon species also had skeletons that appear robust in comparison with large species of Macropus (Janis et al 2014). The skeleton of Protemnodon does not appear well adapted for hopping, with short metatarsals in comparison to other large kangaroos, and it has been suggested that at least some species were quadrupedal at all gaits (Kear et al 2008;Den Boer 2018). Den Boer (2018) considered the limb proportions of Protemnodon anak, but did not specifically consider the capacity for weight-bearing on the forelimbs; if this animal was indeed primarily quadrupedal, then one would predict that it would have morphology evidencing better capacity for this behavior than extant kangaroos.…”

“…The familiar locomotor mode of kangaroos is hopping: that is, bipedal locomotion using the hind limbs in tandem, unaided by the forelimbs. But, at the slower speeds that make up the majority of the daily locomotor repertoire of kangaroos, some sort of forelimb-supported gait is employed, and this locomotion dominates the pattern of daily movement (see Doube et al 2018). In the Pleistocene there was a diversity of kangaroo species much larger than the extant ones, the so-called "giant kangaroos."…”