The functional correlates of jaw‐muscle fiber architecture in tree‐gouging and nongouging callitrichid monkeys

Abstract

Common (Callithrix jacchus) and pygmy (Cebuella pygmaea) marmosets and cotton-top tamarins (Saguinus oedipus) share broadly similar diets of fruits, insects, and tree exudates. Marmosets, however, differ from tamarins in actively gouging trees with their anterior dentition to elicit tree exudates flow. Tree gouging in common marmosets involves the generation of relatively wide jaw gapes, but not necessarily relatively large bite forces. We compared fiber architecture of the masseter and temporalis muscles in C. jacchus (N = 18), C. pygmaea (N = 5), and S. oedipus (N = 13). We tested the hypothesis that tree-gouging marmosets would exhibit relatively longer fibers and other architectural variables that facilitate muscle stretch. As an architectural trade-off between maximizing muscle excursion/contraction velocity and muscle force, we also tested the hypothesis that marmosets would exhibit relatively less pinnate fibers, smaller physiologic cross-sectional areas (PCSA), and lower priority indices (I) for force. As predicted, marmosets display relatively longer-fibered muscles, a higher ratio of fiber length to muscle mass, and a relatively greater potential excursion of the distal tendon attachments, all of which favor muscle stretch. Marmosets further display relatively smaller PCSAs and other features that reflect a reduced capacity for force generation. The longer fibers and attendant higher contraction velocities likely facilitate the production of relatively wide jaw gapes and the capacity to generate more power from their jaw muscles during gouging. The observed functional trade-off between muscle excursion/contraction velocity and muscle force suggests that primate jaw-muscle architecture reflects evolutionary changes related to jaw movements as one of a number of functional demands imposed on the masticatory apparatus.

Allometry and Evolution in the Galago Skull

“…3 ). This latter finding also constitutes evidence against the suggestion that exudativores necessarily generate larger bite forces than their sister taxa [Williams et al, 2002;Taylor and Vinyard, 2004;Taylor et al, 2009]. These observations are consistent with interspecific analyses of mandibular morphology in primate and non-primate exudativores, which are also found to possess anteroposteriorly elongated TMJ condyles and glenoid fossae [Dumont, 1997;Vinyard et al, 2003].…”

The morphology of the masticatory apparatus facilitates muscle force production at wide jaw gapes in tree-gouging common marmosets (Callithrix jacchus)

“…There are differences in the tendon to fiber length ratios in the masseter and temporalis of C. jacchus and S. oedipus (Taylor et al, 2009b). This is important because tendons represent a source of series elasticity in a muscle-tendon unit.…”

“…Gouging trees to elicit exudates is hypothesized to provide marmosets with specific ecological benefits, such as a source of carbohydrates and calcium, a stable food supply and access to an under-exploited food source (Coimbra-Filho and Mittermeier, 1977;Nash, 1986;Power, 1996;Sussman and Kinzey, 1984). These divergent ingestive behaviors between marmosets and tamarins provide a natural experiment for studying the influence of anterior tooth biting on marmoset masticatory apparatus form and function (Taylor and Vinyard, 2004;Taylor et al, 2009a;Taylor et al, 2009b;Vinyard et al, 2003;Vinyard et al, 2009).…”

“…Compared with cotton-top tamarins, tree-gouging marmosets have relatively longer masseter and temporalis fibers but relatively smaller physiological cross-sectional areas (PCSA) (Taylor and Vinyard, 2004;Taylor et al, 2009a;Taylor et al, 2009b). Because fiber length is a measure of the number of sarcomeres in series, and the absolute excursion of a fiber is equivalent to the unit excursions achieved by each sarcomere in series (Gans, 1982;Williams and Goldspink, 1978;Williams and Goldspink, 1971), the relatively longer jaw-muscle fibers of treegouging marmosets reduce the amount of muscle stretch per angular degree of gape.…”

Predicting bite force in mammals: two-dimensional versus three-dimensional lever models

“…A common measure of muscle area is physiological cross-sectional area (PCSA) which can only be gathered from detailed dissections of fresh or preserved muscles. Not surprisingly, these data are available for only a handful of mammal species Perry, 2008;Santana et al, 2010;Taylor et al, 2009). Nevertheless, the widespread interest in bite force and its implications for organismal performance has lead to development of methods for estimating PCSA.…”