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Comparative Study
. 2021 Feb;238(2):321-337.
doi: 10.1111/joa.13314. Epub 2020 Oct 4.

The forearm and hand musculature of semi-terrestrial rhesus macaques (Macaca mulatta) and arboreal gibbons (fam.Hylobatidae). Part II. Quantitative analysis

Marie J M Vanhoof  1 , Timo van Leeuwen  1 , Lorenzo Galletta  2 , Evie E Vereecke  1
Affiliations
Comparative Study

The forearm and hand musculature of semi-terrestrial rhesus macaques (Macaca mulatta) and arboreal gibbons (fam.Hylobatidae). Part II. Quantitative analysis

Marie J M Vanhoof et al. J Anat. 2021 Feb.

Abstract

Nonhuman primates have a highly diverse locomotor repertoire defined by an equally diverse hand use. Based on how primates use their hands during locomotion, we can distinguish between terrestrial and arboreal taxa. The 'arboreal' hand is likely adapted towards high wrist mobility and grasping, whereas the 'terrestrial' hand will show adaptations to loading. While the morphology of the forearm and hand bones have been studied extensively, functional adaptations in the forearm and hand musculature to locomotor behaviour have been documented only scarcely. In this paper, we investigate the forelimb musculature of the highly arboreal gibbons (including Hylobates lar,Hylobates pileatus,Nomascus leucogenys,Nomascus concolor and Symphalangus syndactylus) and compare this with the musculature of the semi-terrestrial rhesus macaques (Macaca mulatta). Anatomical data from previous dissections on knuckle-walking bonobos (Pan paniscus) and bipedal humans (Homo sapiens) are also included to further integrate the analyses in the scope of catarrhine hand adaptation. This study indicates that the overall configuration of the arm and hand musculature of these primates is very similar but there are some apparent differences in relative size which can be linked to differences in forelimb function and which might be related to their specific locomotor behaviour. In macaques, there is a large development of wrist deviators, wrist and digital flexors, and m. triceps brachii, as these muscles are important during the different phases of palmi- and digitigrade quadrupedal walking to stabilize the wrist and elbow. In addition, their m. flexor carpi ulnaris is the most important contributor to the total force-generating capacity of the wrist flexors and deviators, and is needed to counteract the adducting torque at the elbow joint during quadrupedal walking. Gibbons show a relatively high force-generating capacity in their forearm rotators, wrist and digital flexors, which are important muscles in brachiation to actively regulate forward movement of the body. The results also stress the importance of the digital flexors in bonobos, during climbing and clambering, and in humans, which is likely linked to our advanced manipulation skills.

Keywords: adaptation; anatomy; hylobatids; locomotion; macaques; primates.

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Figures

FIGURE 1
FIGURE 1
Boxplot of the scaled fascicle length (FL) of the (a) flexors, (b) extensors, (c) deviators and (d) rotators. Within the hylobatid family, the triangles represent the siamangs. For none of these groups, there is a significant difference between macaques, gibbons and bonobos. (e) In macaques, the scaled FL of the rotators is significantly different from that of their flexors (p < .001), extensors (p < .001) and deviators (p < .01). In gibbons (f) and bonobos (g), the scaled FL of the functional muscle groups are not significantly different from one another (p > .05)
FIGURE 2
FIGURE 2
(a) Boxplot of the ratio of elbow flexors over elbow extensors is low in macaques compared to gibbons (p < .001). (b, c) Boxplots of the relative PCSA of the biceps and triceps brachii. Within the hylobatid group, the triangles represent the siamangs. (b) The m. triceps brachii has a significantly higher PCSA in macaques compared to gibbons (p < .001). (c) The m. biceps brachii has a slightly higher relative PCSA in gibbons compared to macaques (p < .05)
FIGURE 3
FIGURE 3
Boxplot of the relative size of the flexors in the forearm. Within the hylobatid group, the triangles represent the siamangs. (a) The ratio of flexors over extensors is significantly higher in gibbons compared to humans (p < .05); (b) the relative PCSA of the wrist flexors is similar in macaques and gibbons (p > .05), while significant differences can be observed between the other primate taxa; (c) the ratio of digital flexors over digital extensors is similar in gibbons, macaques and bonobos; (d) the relative PCSA of the digital flexors is significantly higher in gibbons compared to macaques (p < .001) and bonobos (p < .01)
FIGURE 4
FIGURE 4
Boxplot of the relative size of the radioulnar deviators. Within the hylobatid group, the triangles represent the siamangs. (a) The wrist deviators have a significantly higher PCSA in macaques compared to gibbons (p < .001) and bonobos (p < .05); (b) the ratio of radial deviators over ulnar deviators of gibbons is significantly higher than the ratio observed in macaques (p < .001) and bonobos (p < .05)
FIGURE 5
FIGURE 5
Boxplot of the relative PCSA of the forearm rotators. Within the hylobatid group, the triangles represent the siamangs. The proportion of the rotator PCSA is significantly higher in gibbons compared to macaques (p < .01)
FIGURE 6
FIGURE 6
Results on tendonization of the flexor muscles. Within the hylobatid family, the triangles represent the siamangs. (a) The relative length of the tendons is significantly longer in gibbons compared to bonobos (p < .05) but not to macaques (p > .05); (b) within the hylobatid family, there is no significant difference between the relative length of the tendons between the different genera (Nomascus, Hylobates, Symphalangus) (p > .05)
FIGURE 7
FIGURE 7
The composition of the intrinsic hand muscles is very similar in gibbons and macaques, with a dominant development (%PCSA) of the intermediate hand muscles (~59% and ~51% respectively), the thenar PCSA taking up approximately 30% of the total intrinsic PCSA and the hypothenar muscle PCSA amounting to only 10% and 18%. In bonobos, the intermediate hand muscles take up a larger proportion of the total intrinsic PCSA (~66%), while in humans, the thenar PCSA is relatively more prominent (~47%). The proportion of the intrinsic hand muscle PCSA relative to total forearm muscle PCSA is 14.7% in macaques, 14.5% in gibbons and humans and 18.4% in bonobos (p > .05)
FIGURE 8
FIGURE 8
Overview of the different muscle parameters that were measured for this study and the corresponding values for macaques, gibbons, bonobos and humans. Significant differences are only shown between macaques and gibbons
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References

    1. Alexander, R.M.N. (2002) Tendon elasticity and muscle function. Comparative Biochemistry and Physiology ‐ A Molecular and Integrative Physiology, 133(4), 1001–1011. - PubMed
    1. Almécija, S. , Smaers, J.B. & Jungers, W.L. (2015) The evolution of human and ape hand proportions. Nature Communications, 6(1), 1–11. - PMC - PubMed
    1. Anapol, F. & Gray, J.P. (2003) Fiber architecture of the intrinsic muscles of the shoulder and arm in semiterrestrial and arboreal guenons. American Journal of Physical Anthropology, 122(1), 51–65. - PubMed
    1. Aversi‐Ferreira, T.A. , Maior, R.S. , Carneiro‐e‐Silva, F.O. , Aversi‐Ferreira, R.A. , Tavares, M.C. , Nishijo, H. et al. (2011) Comparative anatomical analyses of the forearm muscles of Cebus libidinosus (Rylands et al. 2000): Manipulatory behavior and tool use, PLoS One, 6(7), 1–8. - PMC - PubMed
    1. Bartlett, T.Q. , Light, L.E.O. & Brockelman, W.Y. (2016) Long‐term home range use in white‐handed gibbons (Hylobates lar) in Khao Yai National Park, Thailand. American Journal of Primatology, 78(2), 192–203. - PubMed

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