Scaling of the ankle extensor muscle‐tendon units and the biomechanical implications for bipedal hopping locomotion in the post‐pouch kangarooMacropus fuliginosus

Abstract

Bipedal hopping is used by macropods, including rat-kangaroos, wallabies and kangaroos (superfamily Macropodoidea). Interspecific scaling of the ankle extensor muscle-tendon units in the lower hindlimbs of these hopping bipeds shows that peak tendon stress increases disproportionately with body size. Consequently, large kangaroos store and recover more strain energy in their tendons, making hopping more efficient, but their tendons are at greater risk of rupture. This is the first intraspecific scaling analysis on the functional morphology of the ankle extensor muscle-tendon units (gastrocnemius, plantaris and flexor digitorum longus) in one of the largest extant species of hopping mammal, the western grey kangaroo Macropus fuliginosus (5.8-70.5 kg post-pouch body mass). The effective mechanical advantage of the ankle extensors does not vary with post-pouch body mass, scaling with an exponent not significantly different from 0.0. Therefore, larger kangaroos balance rotational moments around the ankle by generating muscle forces proportional to weight-related gravitational forces. Maximum force is dependent upon the physiological cross-sectional area of the muscle, which we found scales geometrically with a mean exponent of only 0.67, rather than 1.0. Therefore, larger kangaroos are limited in their capacity to oppose large external forces around the ankle, potentially compromising fast or accelerative hopping. The strain energy return capacity of the ankle extensor tendons increases with a mean exponent of ~1.0, which is much shallower than the exponent derived from interspecific analyses of hopping mammals (~1.4-1.9). Tendon safety factor (ratio of rupture stress to estimated peak hopping stress) is lowest in the gastrocnemius (< 2), and it decreases with body mass with an exponent of -0.15, extrapolating to a predicted rupture at 160 kg. Extinct giant kangaroos weighing 250 kg could therefore not have engaged in fast hopping using 'scaled-up' lower hindlimb morphology of extant western grey kangaroos.

Limb bone scaling in hopping macropods and quadrupedal artiodactyls

“…The largest extant artiodactyls are an order of magnitude more massive than the largest extant macropods while the smallest of both clades included in this study are ~1-2 kg. It would be unwise to extrapolate macropod scaling trends beyond the current series, because bipedal hopping was likely not a feature of the extinct giant kangaroos and may not be physiologically possible beyond ~160 kg [7][8][9][10]. Janis et al (2014) suggested that large, extant kangaroos are functionally specialised for hopping in contrast to their larger extinct kin that did not hop, somewhat similar to the medium-sized, gracile and hyper-athletic cheetah (Acinonyx jubatus, M = 35-70 kg) compared to bigger and more robust felids such as lion (Panthera leo, M = 120-250 kg) [9].…”

“…In extinct sthenurine macropods, the thoracic limb displays features of a browsing adaptation with elongated manus, reduced lateral digits, slender radius, ulna and humerus, and a 'human-like' scapula, which may have enabled these animals to forage browse above their heads [8]. Hopping is likely not possible at body mass over ~160 kg, at which the distal tendons' safety factor (ratio of actual to ultimate stress) drops below 1, meaning that extinct 'giant kangaroos' would have used slower gaits [7][8][9][10].…”

“…Tammar wallabies (Macropus eugenii) spend up to twice as much time per day in pentapedal walking than in bipedal hopping (6% vs 3-5%), and both gaits are eclipsed in the locomotor time budget by bipedal standing (50-70%), quadrupedal crouching (15-30%), and bipedal rearing (3-12%) [3,5,6]. During hopping, the forelimbs are held away from ground contact for the entire stride cycle and thus are relatively unloaded [2], while hindlimb tissues experience near-ultimate stresses from ground reaction forces and muscle-tendon action, especially in larger Macropodiformes [7]. The tail's role in pentapedal locomotion during slow-speed locomotion might enable reduced forelimb mass, potentially assisting more efficient bipedal hopping [4].…”

“…In extinct sthenurine macropods, the thoracic limb displays features of a browsing adaptation with elongated manus, reduced lateral digits, slender radius, ulna and humerus, and a 'human-like' scapula, which may have enabled these animals to forage browse above their heads [8]. Hopping is likely not possible at body mass over ~160 kg, at which the distal tendons' safety factor (ratio of actual to ultimate stress) drops below 1, meaning that extinct 'giant kangaroos' would have used slower gaits [7][8][9][10].In contrast to macropods, artiodactyl mammals (even-toed ungulates in the eutherian lineage; deer, sheep, camels and kin) have limited manual dexterity, and quadrupedal gaits in which the loads are spread evenly among fore-and hindlimbs during both slow and fast gaits, reflected in similarity of forelimb and hindlimb bones' cross-sectional properties [11]. Artiodactyls and macropods spend a large proportion of their time grazing or resting as they are foregut fermenter herbivores [12] and may be considered ecological equivalents [13].…”

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

“…There appear to be size limits on the use of hopping locomotion. Hopping mammals do not alter their locomotor posture with increasing body size; larger hoppers maintain the same crouched limb posture as smaller ones, which results in increasing tendon strain in the hind legs of larger kangaroos (McGowan et al 2008;Snelling et al 2017). The optimal size for hopping has been estimated at around 50 kg (which is around the average body weight of large extant kangaroos) (Bennett and Taylor 1995).…”