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.

Fig. 1

Model of forelimb mechanics during quadrupedal suspension in various elbow joint angles from (A) flexed to (D) extended. The elbow is subject to an extensor torque induced by body weight and resisted by counteracting muscle forces times moment arms (M_n). M₂ and M₁ are maximized at the specific elbow joint angle shown in (B) and (C), where the lines E-Lsc and E-Rt are perpendicular to Fl₂ and Fl₁, respectively. E, centre of elbow joint rotation; Fl₁ and Fl₂, flexor muscle groups along the brachium and antebrachium, respectively; M₁ and M₂, moment arms of Fl₁ and Fl₂, respectively; Lsc, lateral supracondylar crest; Rt, radial tuberosity; S and W, shoulder and wrist joints, respectively.

Fig. 2

Radiographs of (A,B) Choloepus (UMUT unnumbered) and (C,D) Nycticebus (NSM M 35960) forelimbs in (A,C) flexed and (B,D) extended elbow joint angles. The cranial margin of the humerus is assumed to be nearly parallel to the shaft of the humerus (br-shft), and the line connecting the olecranon (Ol) and the wrist joint (W) is assumed to be nearly parallel to the shaft of the antebrachium (ab-shft). ab, antebrachium; hm, humerus; sc, scapula; S and W, shoulder and wrist joints, respectively.

Fig. 3

Measurements of distances E-Ol, E-Rt and E-Lsc used to calculate the maximum possible moment arms of elbow joint extensors and flexors, respectively, along the brachium and antebrachium. (A) Non-scansorial upright quadruped example (Canis; Type A). (B) Non-upright suspended quadruped example (Choloepus; Type F). See Materials and methods and Fig. 5 for the categories of locomotor ability. E, centre of elbow joint rotation; Lsc, lateral supracondylar crest; Ol, olecranon; Rt, radial tuberosity; trc, trochlea; trn, trochlear notch.

Fig. 4

Elbow joint flexors of (A–C) Choloepus (UMUT unnumbered), (D) Pteropus (UMUT unnumbered), (E) Cynocephalus (ZRC 4.9464) and (F,G) Nycticebus (KPM 3684), in lateral (A,F) and medial views (B–E,G). Pectoral muscles are reflected or removed in C, E and G. A flexor muscle along the brachium (Fl₁) is represented as a line connecting the inter-turbecular groove (itg) and the radial shaft (Rt). A flexor muscle along the antebrachium (Fl₂) is represented as a line connecting the mid-portion of the lateral supracondylar crest (Lsc) and the wrist joint (W). bib, M. biceps brachii; brd, M. brachioradialis; cb, M. coracobrachialis; clb, M. cleidobrachialis; ecr, M. extensor carpi radialis; ld, M. latissimus dorsi; p, M. pectoralis; pa, part of M. pectoralis which inserts onto the antebrachium; st, sternum; E, S, and W, elbow, shoulder, and wrist joints, respectively. Note that our Fl₁ and Fl₂ groups best represent the paths of M. biceps brachii and M. extensor carpi radialis, respectively, but nonetheless are reasonable approximations of the paths, and thus moment arms, of the two major groups of elbow flexor muscles.

Fig. 5

Locomotor abilities of mammals categorized into six types (see Materials and methods).

Fig. 6

Muscle mass ratios of elbow joint extensors (Ex) and flexors along the brachium (Fl₁) and antebrachium (Fl₂). The length of each bar represents the relative mass of each muscle, when the total mass of the extensors and flexors of an individual is 100% (see bottom bar for abstract example). No data were obtainable for taxa in types D and E. Asterisks indicate juvenile specimens. (1) M. triceps brachii (1a, long head; 1b, lateral head; 1c, medial head; 1d, accessory head; 1e, intermediate head); (2) M. dorsiepitrochlearis; (3) M. anconeus; (4) M. epitrochleoanconeus; (5) M. flexor carpi ulnaris. A, M. biceps brachii (A₁, short head; A₂, long head); B, M. brachialis; C, M. brachioradialis (C₁, short head; C₂, long head); D, M. extensor carpi radialis; E, M. cleidobrachialis; F, M. ectoantebrachialis; G, M. supinator; H, M. pronator teres; I, M. flexor carpi radii; J, M. flexor digiti profundus; K, M. flexor digiti sublimis. See institution abbreviations in Tables 1 and 2.

Fig. 7

(A–D) Observed elbow joint angles, including the changes of the joint angle during stance phase (Stnc) and the angle in static postures (Stat), estimated elbow joint angles where the moment arms of the flexors along the brachium (Fl₁) and the antebrachium (Fl₂) are maximized, and the ranges of elbow joint motion (ROM), are compared for our study taxa of four suspended quadrupeds: (A) Choloepus, (B) Pteropus, (C) Cynocephalus (no Stnc data recorded) and (D) Nycticebus. Solid and dotted lines of the transitions in Stnc indicate, respectively, the portions of the stance phase where the humerus is more abducted (first half) or adducted (second half). The horizontal bar in each section of Stat, Fl₁ and Fl₂ is a mean value of the measurements.

Fig. 8

Estimated elbow joint angles (maximizing flexor moment arms) for the Fl₁ and Fl₂ muscles of selected specimens. ROM was measured after the flight membrane was removed in Pteropus specimens: (A) Choloepus hoffmanni (UMUT unnumbered), (B) Pteropus dasymallus (NSM PO 127), (C) Cynocephalus variegatus (ZRC 4.8112) and (D) Nycticebus coucang (KPM 3674). The antebrachia of Choloepus and Nycticebus specimens are held in semi-supinated position. E, centre of elbow joint rotation; Lsc, lateral supracondylar crest; Rt, radial tuberosity; S and W, shoulder and wrist joints, respectively.

Fig. 9

Comparison between maximum possible moment arms of the elbow joint extensor (Ex: vertical axis) and flexor (Fl₁ or Fl₂, whichever is larger: horizontal axis) muscles. See Figs 3 and 5 and main text for the details of the measurements and the locomotor ability categories. Animals plotted on the upper left possess relatively large extensor moment arms (e.g. upright quadrupeds), and the one on lower right possesses relatively large flexor moment arms (e.g. suspended quadrupeds).

Fig. 10

Elbow joint extensor/flexor ratios for (A) maximum possible moment arm and (B) total muscle masses. Extensor (Ex) and flexor (Fl) ratios are plotted along the vertical axis, and quartiles for each type of locomotor ability are shown in box plots.