Myology of the pelvic limb of the brown-throated three-toed sloth (Bradypus variegatus)

Abstract

Tree sloths rely on their limb flexors for bodyweight support and joint stability during suspensory locomotion and posture. This study aims to describe the myology of three-toed sloths and identify limb muscle traits that indicate modification for suspensorial habit. The pelvic limbs of the brown-throated three-toed sloth (Bradypus variegatus) were dissected, muscle belly mass was recorded, and the structural arrangements of the muscles were documented and compared with the available myological accounts for sloths. Overall, the limb musculature is simplified by containing muscles with generally long and parallel fascicles. A number of specific and informative muscle traits are additionally observed in the pelvic limb of B. variegatus: well-developed hip flexors and hip extensors each displaying several fused bellies; massive knee flexors; two heads of the m. adductor longus and m. gracilis; robust digital flexors and flexor tendons; m. tibialis cranialis muscle complex originating from the tibia and fibula and containing a modified m. extensor digitorum I longus; appreciable muscle mass devoted to ankle flexion and hindfoot supination; only m. extensor digitorum brevis acts to extend the digits. Collectively, the findings for tree sloths emphasize muscle mass and organization for suspensory support namely by the hip flexors, knee flexors, and limb adductors, for which the latter two groups may stabilize suspensory postures by exerting appreciable medially-directed force on the substrate. Specializations in the distal limb are also apparent for sustained purchase of the substrate by forceful digital flexion coupled with strong ankle flexion and supination of the hind feet, which is permitted by the reorganization of several digital extensors. Moreover, the reduction or loss of other digital flexor and ab-adductor muscles marks a dramatic simplification of the intrinsic foot musculature in B. variegatus, the extent to which varies across extant species of two- and three-toed tree sloths and likely is related to substrate preference/use.

Keywords: flexors; hindlimb; mass; muscle; suspension; suspensory support.

FIGURE 1

Muscle maps of the ventral (A) and dorsal (B) pelvis for Bradypus variegatus. Muscle nomenclature abbreviations are given in Table 2

FIGURE 2

Muscle maps of the caudal (A) and lateral (B) pelvis for Bradypus variegatus. Muscle nomenclature abbreviations are given in Table 2. Colored in light gray and unlabeled is the acetabulum

FIGURE 3

Muscle maps of the cranial (A) and caudal (B) femur as well as the cranial (C) and caudal (D) tibia‐fibula for Bradypus variegatus. Muscle nomenclature abbreviations are given in Table 2. Encircled on the medial epicondyle of the tibia in panel B is the alternative insertion for m. semitendinosus

FIGURE 4

Lateral view of the hindlimb musculature for Bradypus variegatus. Muscles: (a) m. iliopsoas; (b) m. tensor fasciae latae; (c) m. gluteus superficialis; (d) mm. gemelli; (e) m. rectus femoris; (f) m. vastus lateralis; (g) m. semimembranosus; (h) m. biceps femoris‐ischial head; (i) m. biceps femoris‐femoral head; (j) m. flexor digitorum superficialis (or m. plantaris); (k) m. gastrocnemius‐lateral head; (l) m. soleus; (m) m. extensor digitorum longus; (n) m. fibularis longus; (o) m. fibularis quartus; (p) m. quadratus plantae; (q) m. extensor digitorum brevis; (r) m. interosseous lateralis. Colored in black is the sciatic nerve. Note: all superficial fibers of the m. biceps femoris‐ischial head that inserts onto crural fascia of the lateral leg is not illustrated to show the proximal bellies of the m. flexor digitorum superficialis and m. soleus

FIGURE 5

Illustration of the deep hip muscles for Bradypus variegatus. Muscles: (a) m. gluteus medius; (b) m. piriformis; (c) m. gemellus superior; (d) m. gemellus inferior; (e) m. quadratus femoris; (f) m. obturatorius externus

FIGURE 6

Medial view of the hindlimb musculature for Bradypus variegatus. Muscles: (a) m. sartorius; (b) m. pectineus‐adductor brevis; (c) m. adductor longus‐cranial head; (d) m. adductor longus‐caudal head; (e) m. adductor magnus; (f) m. vastus medialis; (g) m. semitendinosus; (h) m. semimembranosus; (i) m. gracilis‐external part; (j) m. gastrocnemius‐medial head; (k) m. flexor digitorum (profundus) medialis; (l) m. tibialis cranialis; (m) m. quadratus plantae; (n) m. extensor digitorum brevis; (o) m. interosseous medius. Hatched regions indicate the origins of m. gracilis (belly for the internal part not illustrated). Colored in gray proximally is the femoral artery and in black distally is the tibial nerve

FIGURE 7

Muscle maps of the dorsal (A) and plantar (B) pes for Bradypus variegatus. The medial and lateral most metatarsals are remnants of digits I and V, respectively. Muscle nomenclature abbreviations are given in Table 2

FIGURE 8

Illustrations of superficial (A) and deep (B) caudal leg musculature as well as cranial leg muscles (C) for Bradypus variegatus. Muscles: (a) m. flexor digitorum superficialis (or m. plantaris); (b) m. gastrocnemius‐lateral head; (c) m. gastrocnemius‐medial head; (d) m. soleus; (e) m. popliteus; (f) m. flexor digitorum (profundus) medialis; (g) m. flexor digitorum (profundus) lateralis; (h) m. tibialis caudalis; (i) m. extensor digitorum longus; (j) m. tibialis cranialis‐tibial head; (k) m. tibialis cranialis‐fibular et tibial head; (l) m. tibialis cranialis‐fibular head; (m) m. extensor digitorum brevis. Note: m. quadratus plantae is not illustrated to show details of the deep flexor tendons in the plantar aspect of the pes

FIGURE 9

Pelvic limb muscle mass as a percentage of body mass (A) and scaled with body mass (B) across seven individuals of Bradypus variegatus sampled. Total limb muscle mass (TLMM) was calculated as the summed mass of all muscles studied for each individual. The results of a Model I regression indicate that TLMM scaled with slight positive allometry largely due to the influence of one adult individual (Bv8) with hypertrophied muscles

FIGURE 10

Distribution of functional group muscle mass to total limb muscle mass (TLMM) in three species of a tree sloth. Proximal‐to‐distal muscle group mass is expressed as a percentage, with bars representing means for each functional group. Error bars represent the SD (standard deviation) across N = 7 individuals of Bradypus variegatus (Bv). Muscles with synergistic functions are combined in one functional group. Bi‐articular muscles are included in more than one functional group (i.e., combined mass is greater than 100%). Data for Bradypus tridactylus (Bt: Mackintosh, 1875a) and Choloepus didactylus (Cd: Mackintosh, 1875b) are taken from the literature