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

Abstract

Common marmosets (Callithrix jacchus) generate wide jaw gapes when gouging trees with their anterior teeth to elicit tree exudate flow. Closely related cotton-top tamarins (Saguinus oedipus) do not gouge trees but share similar diets including exudates. Maximizing jaw opening theoretically compromises the bite forces that marmosets can generate during gouging. To investigate how jaw-muscle architecture and craniofacial position impact muscle performance during gouging, we combine skull and jaw-muscle architectural features to model muscle force production across a range of jaw gapes in these two species. We incorporate joint mechanics, resting sarcomere length and muscle architecture estimates from the masseter and temporalis to model muscle excursion, sarcomere length and relative tension as a function of joint angle. Muscle excursion from occlusion to an estimated maximum functional gape of 55 deg. was smaller in all regions of the masseter and temporalis of C. jacchus compared with S. oedipus except the posterior temporalis. As a consequence of reduced muscle excursion distributed over more sarcomeres in series (i.e. longer fibers), sarcomere length operating ranges are smaller in C. jacchus jaw muscles across this range of gapes. This configuration allows C. jacchus to act on a more favorable portion of the length-tension curve at larger gapes and thereby generate relatively greater tension in these muscles compared with S. oedipus. Our results suggest that biting performance during tree gouging in common marmosets is improved by a musculoskeletal configuration that reduces muscle stretch at wide gapes while simultaneously facilitating comparatively large muscle forces at the extremes of jaw opening.

Fig. 1.

The tree-gouging common marmoset (Callithrix jacchus) shown generating a wide jaw gape while gouging in a laboratory setting. Adapted from Vinyard and Schmitt (Vinyard and Schmitt, 2004).

Fig. 2.

Maximum bite forces can occur at relatively large jaw gapes during tree gouging. (A) The solid arrows show peak force whereas the broken arrows indicate maximum jaw gape. Force trace showing that resultant forces are relatively low at maximum gape (broken arrows). (B) Plot of gapes, for the same two gouges as in A, illustrating that peak forces can occur at relatively large jaw gapes (solid arrows). The intermittent nature of linear gape results from teeth not being visible for digitizing in all frames (C.J.V., unpublished).

Fig. 3.

This schematic demonstrates the relationship between moment arm and muscle fiber length and the consequences for a muscle's operating range. Increasing the moment arm increases the amount of stretch imposed on the muscle, thereby increasing its operating range for a given amount of angular rotation (compare elongated red lines estimating operating range in A and B with those in C and D). Increasing the muscle fiber length increases the number of sarcomeres to take up the imposed stretch, decreasing the operating range (compare shortened red lines estimating operating range in B and D with those in A and C).

Fig. 4.

Sagittal view of Callithrix jacchus (A) and Saguinus oedipus (B) skulls with the masseter and temporalis muscles removed. The origin and insertion points of the anterior (AT), middle (MT) and posterior temporalis (PT; yellow circles) as well as the anterior superficial (ASM; red circles), deep (DM; blue circles) and posterior superficial (PSM: green circles) masseter are shown. Markings were made on the skulls as muscles were removed to approximate muscle paths.

Fig. 5.

A custom jig was used to measure muscle excursion. The cranium was secured to the jig using Steinmann pins. Sutures were used to approximate the path of each muscle as the jaw was opened from occlusion to a pre-determined maximum gape (data collection for the anterior temporalis is shown here). A 3-0 nylon suture was secured to the coronoid process and placed through a custom eyelet over the marked insertion of the anterior temporalis muscle. The proximal end of the suture was pre-tensioned with a 40 g weight and placed over a potentiometer. The mandible was opened incrementally and in-plane images were used to measure joint angle while muscle excursion was measured with a potentiometer.

Fig. 6.

Excursion as a function of joint angle in the (A) anterior superficial (ASM), (B) deep (DM) and (C) posterior superficial (PSM) masseter as well as the (D) anterior (AT), (E) middle (MT) and (F) posterior (PT) temporalis in Callithrix jacchus (blue squares) and Saguinus oedipus (yellow triangles). Data are presented as means ± s.e.m. Significant differences (P<0.05) between C. jacchus and S. oedipus at a given joint angle are indicated with an asterisk (*).

Fig. 7.

Sarcomere length operating ranges of masseter and temporalis muscle regions in Callithrix jacchus (blue) and Saguinus oedipus (yellow) from occlusion to our maximum gape estimate (55 deg.). Sarcomere operating ranges are superimposed on a sarcomere length—relative tension curve. The sarcomere length operating ranges of the anterior superficial masseter as well as anterior and middle temporalis in S. oedipus are significantly greater compared with C. jacchus as a function of longer moment arms (i.e. greater excursion) and shorter fibers.

Fig. 8.

Muscle force as a function of joint angle in the (A) anterior superficial (ASM), (B) deep (DM) and (C) posterior superficial (PSM) masseter as well as the (D) anterior (AT), (E) middle (MT) and (F) posterior (PT) temporalis in Callithrix jacchus (blue squares) and Saguinus oedipus (yellow triangles). Data are presented as means ± s.e.m. Significant differences (P<0.05) between C. jacchus and S. oedipus at a given joint angle are indicated with an asterisk (*).