Jaw-muscle fiber architecture in tufted capuchins favors generating relatively large muscle forces without compromising jaw gape

摘要

Cebus apella is renowned for its dietary flexibility and capacity to exploit hard and tough objects. Cebus apella differs from other capuchins in displaying a suite of craniodental features that have been functionally and adaptively linked to their feeding behavior, particularly the generation and dissipation of relatively large jaw forces. We compared fiber architecture of the masseter and temporalis muscles between the tufted capuchin (C. apella; n = 12 ) and two “untufted” capuchins (C. capuchinus, n = 3; C. albifrons, n = 5). These three species share broadly similar diets, but tufted capuchins occasionally exploit mechanically challenging tissues. We tested the hypothesis that C. apella exhibits architectural properties of their jaw muscles that facilitate relatively large forces, including relatively greater physiologic cross-sectional areas (PCSA), more pinnate fibers, and lower ratios of mass to tetanic tension (Mass/P0). Results show some evidence supporting these predictions, as C. apella has relatively greater superficial masseter, whole masseter, and temporalis PCSAs, significantly so only for the temporalis following Bonferroni adjustment. Capuchins did not differ in pinnation angle or Mass/P0. As an architectural trade-off between maximizing muscle force and muscle excursion/contraction velocity, we also tested the hypothesis that C. apella exhibits relatively shorter muscle fibers. Contrary to our prediction, there are no significant differences in relative fiber lengths between tufted and untufted capuchins. Therefore, we attribute the relatively greater PCSAs in C. apella primarily to their larger muscle masses. These findings suggest that relatively large jaw-muscle PCSAs can be added to the suite of masticatory features that have been functionally linked to the exploitation of a more resistant diet by C. apella. By enlarging jaw-muscle mass to increase PCSA, rather than reducing fiber lengths and increasing pinnation, tufted capuchins appear to have increased jaw-muscle and bite forces without markedly compromising muscle excursion and contraction velocity. One performance advantage of this morphology is that it promotes relatively large bite forces at wide jaw gapes, which may be useful for processing large food items along the posterior dentition. We further hypothesize that this morphological pattern may have the ecological benefit of facilitating the dietary diversity seen in Cebus apella. Lastly, the observed feeding on large objects, coupled with a jaw-muscle architecture that facilitates this behavior, raises concerns about utilizing C. apella as an extant behavioral model for hominins that might have specialized on small objects in their diets.