Topsy-turvy locomotion: biomechanical specializations of the elbow in suspended quadrupeds reflect inverted gravitational constraints

Abstract

Some tetrapods hang upside down from tree branches when moving horizontally. The ability to walk in quadrupedal suspension has been acquired independently in at least 14 mammalian lineages. During the stance (supportive) phase of quadrupedal suspension, the elbow joint flexor muscles (not the extensors as in upright vertebrates moving overground) are expected to contract to maintain the flexed limb posture. Therefore muscular control in inverted, suspended quadrupeds may require changes of muscle control, and even morphologies, to conditions opposite to those in upright animals. However, the relationships between musculoskeletal morphologies and elbow joint postures during the stance phase in suspended quadrupeds have not been investigated. Our analysis comparing postures and skeletal morphologies in Choloepus (Pilosa), Pteropus (Chiroptera), Nycticebus (Primates) and Cynocephalus (Dermoptera) revealed that the elbow joints of these animals were kept at flexed angles of 70-100°during the stance phase of quadrupedal suspension. At these joint angles the moment arms of the elbow joint flexors were roughly maximized, optimizing that component of antigravity support. Our additional measurements from various mammalian species show that suspended quadrupeds have relatively small extensor ⁄ flexor ratios in both muscle masses and maximum moment arms. Thus, in contrast to the pattern in normal terrestrial quadrupeds, suspended quadrupeds emphasize flexor over extensor muscles for body support. This condition has evolved independently multiple times, attendant with a loss or reduction of the ability to move in normal upright postures.

Gait kinetics of above- and below-branch quadrupedal locomotion in lemurid primates

“…Although the quantification of kinematic patterns during belowbranch quadrupedal locomotion is beyond the scope of this study, other studies that have quantified patterns of kinematic movement during below-branch quadrupedal locomotion (Fujiwara et al, 2011;Ishida et al, 1990;Turnquist, 1975) and brachiation (Bertram, 2004;Michilsens et al, 2011) provide compelling evidence for a potential mechanism that may explain the higher f V,peak in the forelimbs. Consistent across all kinematic studies of below-branch quadrupedal locomotion (Fujiwara et al, 2011;Ishida et al, 1990;Turnquist, 1975), and some studies on brachiation (Bertram, 2004;Michilsens et al, 2011) is a tendency for animals to actively flex the forelimbs during the support phase. Data for hindlimbs during inverted quadrupedalism in sloths show that the hindlimbs maintain more extended positions throughout the stride.…”

“…This ability seems especially important in a complex arboreal milieu occupied by many mammalian species (Blanchard and Crompton, 2011;Fleagle, 2013). In the trees, some animals have the ability to switch between above-and below-branch movement, and primates seem particularly adept at this behavior compared with other mammals (Table S1; but see Fujiwara et al, 2011). The idea that primates have a well-developed capacity for adjusting aspects of gait in order to effectively adjust to particular environmental circumstances is not new (Nyakatura et al, 2008;Schmitt, 1999;Vilensky and Larson, 1989), and this mechanical flexibility (Iriarte-Diaz et al, 2012;Wainwright et al, 2008) mechanisms that may have allowed for the great amount of locomotor diversity within the primate order (Schmitt, 2010;Vilensky and Larson, 1989).…”

“…One remarkable form of locomotor mode switching is the ability of an animal to drop below an arboreal support and adopt suspensory locomotion -any form of forward progression in which the body's center of mass (COM) lies below the point of contact (Stern and Oxnard, 1973). Suspensory locomotion has evolved in at least eight clades of extant mammals (Fujiwara et al, 2011), but primates are particularly adept at this form of locomotion (Table S1) and have an exceptional ability to quickly and seamlessly move between aboveand below-branch locomotion when compared with other arboreal mammals. Currently, little information exists on how primates are so readily able to adopt suspensory locomotion.…”

“…sloths, bats, kinkajous), few studies (Fujiwara et al, 2011;Ishida et al, 1990;Jouffroy and Petter, 1990;Jouffroy and Stern, 1990;Mendel, 1981;Nyakatura, 2012;Parsons and Taylor, 1977;Turnquist, 1975) have specifically focused on the mechanics of below-branch quadrupedal locomotion in mammals, and of those only one has measured substrate reaction forces (Ishida et al, 1990). Ishida et al (1990) collected multiaxial force data from freely moving slow lorises (Nycticebus coucang) on an upright and inverted instrumented runway.…”

Functional Morphology and Comparative Anatomy of Appendicular Musculature in CubanAnolisLizards with Different Locomotor Habits

“…The length of each muscle moment arm was measured as a second trait. The length was defined as the distance from the center of rotation in each joint to the point of the muscle insertion, which theoretically represents the maximum moment arm Fujiwara et al, 2011). Given the trade-off between torque and excursion, muscles with longer moment arms exert larger torque and muscles with shorter moment arms produce grater excursion.…”