The material composition of vertebrate connective tissue is highly conserved across taxa. Existing data suggest that the compressive and tensile strength of limb bones are very similar despite marked variation in limb posture and locomotor patterns. However, the material properties of limb bone tissue from suspensory taxa have not been formally evaluated. Sloths are nearly obligatory in their use of below-branch suspensory locomotion and posture, thus placing their limb bones and associated soft tissue structures under routine tensile loading. It is possible that sloth limb bones are modified for enhanced tensile strength, perhaps at the expense of compressive strength. Fore- and hindlimb bones of two-toed (Choloepus hoffmanni) and three-toed (Bradypus variegatus) sloths were tested in compression and bending to evaluate this hypothesis. Strength and elastic (Young's) modulus were similarly lower in sloth limb bones during both compression and bending, as compared to pronograde taxa. Ratios of peak bending strength to compressive strength additionally were elevated (sloths: 1.4–1.7; upright taxa: 0.6–1.2) for sloth limb bones. Overall, the material properties measured from the limb bones of tree sloths support our hypothesis of predicted function in a tensile limb system. Future studies should aim to directly test bones in tension to confirm indications of elevated axial tensile strength. Nevertheless, the results herein expand understanding of functional adaptation in mammalian tissue for a range of locomotor/postural behaviors that were previously unexplored.

Modern tree sloths are one of few mammalian taxa for which quadrupedal suspension is obligatory. Sloth limb musculature is specialized for slow velocity, large force contractions that stabilize their body below branches and conserves energy during locomotion. However, it is unknown if two and three-toed sloths converge in their use of limb biomechanics and whether these patterns are comparable to how primates perform arboreal suspensory locomotion. This study addresses this need by collecting limb loading data in three-toed sloths (Bradypus variegatus; N=5) during suspensory walking. Sloths performed locomotor trials at their preferred speed on an instrumented beam apparatus with a force platform as the central supporting segment. Peak forces and impulses of the forelimb and hindlimb were recorded and analyzed in three dimensions. The hindlimbs of B. variegatus apply large braking forces greater in magnitude than peak forces generated by the forelimbs in propulsion, a pattern consistent with that observed in two-toed sloths. However, B. variegatus exhibits hindlimb-biased bodyweight support in vertical peak forces and impulse, with appreciable laterally-directed forces in each limb pair, both of which vary from limb loading distributions in two-toed sloths. Moreover, bodyweight distribution between limb pairs is opposite to that employed by primates during quadrupedal suspension. Thus, there appear to be multiple strategies for achieving suspensory locomotion in arboreal mammals. These differences may be attributable to anatomical variation or phylogenetic position, but as of yet an explanation remains unknown. Future EMG analyses are expected to provide insight into how specific hindlimb muscle groups contribute to braking forces and stabilizing the center of mass of sloths during suspension.

Tendons must be able to withstand the tensile forces generated by muscles to provide support while avoiding failure. The properties of tendons in mammal limbs must therefore be appropriate to accommodate a range of locomotor habits and posture. Tendon collagen composition provides resistance to loading that contributes to tissue strength which could, however, be modified to not exclusively confer large strength and stiffness for elastic energy storage/recovery. For example, sloths are nearly obligate suspenders and cannot run, and due to their combined low metabolic rate, body temperature, and rate of digestion, they have an extreme need to conserve energy. It is possible that sloths have a tendon ‘suspensory apparatus’ functionally analogous to that in upright ungulates, thus allowing for largely passive support of their body weight below-branch, while concurrently minimizing muscle contractile energy expenditure. The digital flexor tendons from the fore- and hindlimbs of two-toed (Choloepus hoffmanni) and three-toed (Bradypus variegatus) sloths were loaded in tension until failure to test this hypothesis. Overall, tensile strength and elastic (Young’s) modulus of sloth tendons were low, and these material properties were remarkably similar to those of equine suspensory ‘ligaments’. The results also help explain previous findings in sloths showing relatively low levels of muscle activation in the digital flexors during postural suspension and suspensory walking.

Tree sloths evolved below‐branch locomotion making them one of few mammalian taxa beyond primates for which suspension is nearly obligatory. Suspension requires strong limb flexor muscles that provide both propulsion and braking/support, and available locomotor kinetics data indicate that these roles differ between fore‐ and hindlimb pairs. Muscle structure in the pelvic limb is hypothesized to be a key anatomical correlate of function in braking/support during suspensory walking and propulsion and/or support during vertical climbing. This expectation was tested by quantifying architecture properties in the hindlimb limb musculature of brown‐throated three‐toed sloths (Bradypus variegatus: N = 7) to distinguish the roles of the flexor/extensor functional muscle groups at each joint. Measurements of muscle moment arm (rm), mass, belly length, fascicle length, pennation angle, and physiological cross‐sectional area (PCSA) were taken from n = 45 muscles. Overall, most muscles studied show properties for contractile excursion and fast joint rotational velocity. However, the flexor musculature is more massive (p = 0.048) and has larger PCSA (p = 0.003) than the extensors, especially at the knee joint and digits where well‐developed and strong flexors are capable of applying large joint torque. Moreover, selected hip flexors/extensors and knee flexors have modified long rm that can amplify applied joint torque in muscles with otherwise long, parallel fascicles, and one muscle (m. iliopsoas) was capable of moderately high power in B. variegatus. The architectural properties observed in the hip flexors and extensors match well with roles in suspensory braking and vertical propulsion, respectively, whereas strong knee flexors and digital flexors appear to be the main muscles providing suspensory support in the pelvic limb. With aid in support by the forelimbs and the use of adaptive slow locomotion and slow muscle fiber recruitment patterns, structure–function in the tensile limb systems of sloths appears to collectively represent an additional mechanism for energy conservation.