Limb muscle mass ratios in newborn primates

Abstract

Adult nonhuman primates achieve locomotion in a variety of ways including large vertical leaps, bounding movements, and quadrupedal walking and running. As neonates, however, primates may be left in a nest, carried orally, or cling to a caregiver's fur. Because of this, the initial distribution of muscles mass between limb segments (e.g., leg/thigh) may not reflect the requirements of adult locomotion. Here, we investigate the distribution of muscle mass between and within limbs in neonates. We compare muscle distribution ratios between neonates and adults in selected species. We used nine primate species (n = 18 individuals) including two monkeys, one tarsier, five lemurs and one galago. Limb muscles were removed in groups (e.g., quadriceps, thigh adductors, etc.) and wet weights of muscle groups were recorded. In neonates of all species, the thigh is > 50% of the total (thigh + leg) hindlimb mass, whereas the arm is < 50% of the total forelimb mass. The thigh becomes proportionally bigger during adulthood in all species, whereas the distribution within the forelimb is unchanged between age groups. This suggests that the functional emphasis in forelimb muscular compartments may change less than in hindlimb compartments. Muscle group weights indicate that neonates have a significantly larger leg:thigh muscle mass ratio than their corresponding adults, with Propithecus characterized by the largest shift (0.51 to 0.27). There are two distinct patterns of age-related change within the posterior compartment of the leg. In Cheirogaleus and Microcebus, the deep:superficial flexor mass ratio increases with age (i.e., deep flexors become proportionally larger over time). In all other species the ratio decreases (indicating that superficial flexors outpace deep flexors in growth), although only in leaping specialists is the adult ratio < 1 (i.e., superficial flexors larger than deep flexors). Results are consistent with hypothesis that hindlimb muscle mass distribution shifts as locomotor behavior matures towards the adult state. For most primates, this reflects an early emphasis on grip strength of the foot among neonates versus propulsion in mature individuals. Intriguingly, both exceptions (Microcebus and Cheirogaleus) are arboreal quadrupeds that are nest-bound at birth. Thus, they may lack an early emphasis on grip strength, and later gain deep flexor mass as they begin to climb and run on relatively small supports. Observed ratios also indicate that neonates do not display adequate proximal hindlimb musculature at birth for adult locomotion and require a shift in mass from distal to proximal musculature throughout growth. Support or Funding Information School of Physical Therapy, Slippery Rock University, Slippery Rock PA 16057 Department of Anatomy and Neurobiology Northeast Ohio Medical University Relative Muscle Mass Percentages Upper Extremity Muscle Mass Cheirogaleus and G. Moholi Cmedius Gmoholi Neo Adult Neo Adult arm flexors 0.01 0.34 0.013 0.28 arm extensors 0.018 0.61 0 021 0.45 Forearm, ant. comp. 0.017 0.7 0.028 0.71 Forearm, post. comp. 0.013 0.31 0.019 0.28 Brachioradialis 0.005 0.17 0.007 0.13 A+FA 0.063 2.13 0.088 1.85 A 0.028 0.95 0.034 0.73 %arm of overall MM 44.44 44.60 38.64 39.46 intermembral index 89.4 68.8 65 52.8 (forelimb bone lengths (H+R)*100/hindlimb bone lengths (F+T) limb mm mass index (forelimb mm *100/hin 101.61 46.92 37.77 18.54 Lower Extremity Muscle Mass Values from Atzeva or Baker Cmedius Gmoholi Mmurinus Tsyrichta Pcoquereli Vvariegata neo adult neo adult neo adult neo adult neo adult neo adult Ham 0.011 0.98 0.04 1.35 0.015733 0.483633 0.113 0.55 0.414 22 0.404 36.9 sartorius 0.002 0.14 0.008 0.5 0.002167 0.056767 0.027 0.13 0.199 9 0.067 4.4 quads 0.017 1.18 0.109 5.48 0.0192 0.638333 0.347 2.39 1.525 129.2 0.762 59.2 adds 0.008 0.68 0.018 0.98 0.011667 0.263183 0.059 0.41 0.436 25.1 0.271 25.9 sup flex 0.01 0.4 0.019 0.63 0.007367 0.182933 0.057 0.35 0.3 12.1 0.177 14.9 deep flex 0.006 0.45 0.018 0.41 0.006433 0.192417 0.05 0.25 0.472 18 0.28 16.4 ant 0.005 0.44 0.013 0.37 0.005133 0.13845 0.041 0.21 0.316 9 0.173 9.7 lat 0.003 0.27 0.008 0.26 0.005967 0.095983 0.031 0.14 0.232 7.8 0.121 6.5 T+L 0.062 4.54 0.233 9.98 0.073667 2.0517 0.725 4.43 3.894 232.2 2.255 173.9 T 0.038 2.98 0.175 8.31 0.048767 1.441917 0.546 3.48 2.574 185.3 1.504 126.4 % thigh of overall MM 61.29 65.64 75.11 83.27 66.20 70.28 75.31 78.56 66.10 79.80 66.70 72.69 deep/superficial flex ratio 0.60 1.13 0.95 0.65 0.87 1.05 0.88 0.71 1.57 1.49 1.58 1.10 Lower Extremity Muscle Mass Catta, Francois, Anancymaae Neonates L catta neo Tfrancoisi Anancymaae Ham 0.232 2.799 0.3323 Sartorius 0.0725 0.278 0.043 Quads 0.4215 3.705 0.381 Adductors 0.1953 3.477 0.334 sup flex 0.1194 1.3415 0.265 deep flex 0.1828 1.565 0.1065 ant 0.122 1.4391 0.21 lat 0.0647 0.582 0.0705 Deep/Superficial Ratio 1.53 1.17 0.4 This abstract is from the Experimental Biology 2019 Meeting. 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