Ontogenetic biomechanics of tufted (Sapajus) and untufted (Cebus) capuchin mandibles.

OBJECTIVES: Cortical bone geometry is commonly used to investigate biomechanical properties of primate mandibles. However, the ontogeny of these properties is less understood. Here we investigate changes in cortical bone cross-sectional properties throughout capuchin ontogeny and compare captive versus wild, semi-provisioned groups. Tufted capuchins (Sapajus spp.) are known to consume relatively hard/tough foods, while untufted capuchins (Cebus spp.) exploit less mechanically challenging foods. Previous research indicates dietary differences are present early in development and adult Sapajus mandibles can resist higher bending/shear/torsional loads. MATERIALS AND METHODS: This study utilized microCT scans of 22 Cebus and 45 Sapajus from early infancy to adulthood from three sample populations: one captive Cebus, one captive Sapajus, and one semi-provisioned, free-ranging Sapajus. Mandibular cross-sectional properties were calculated at the symphysis, P3, and M1. If the tooth had not erupted, its position within the crypt was used. A series of one-way ANOVAs were performed to assess differences between and within the sample populations. RESULTS: Mandible robusticity increases across ontogeny for all three sample populations. Sapajus were better able to withstand bending and torsional loading even early in ontogeny, but no difference in shear resistance was found. Semi-provisioned, free-ranging Sapajus tend to show increased abilities to resist bending and torsional loading but not shear loading compared to captive Sapajus. DISCUSSION: This study helps advance our understanding of the primate masticatory system development and opens the door for further studies into adaptive plasticity in shaping the masticatory apparatus of capuchins and differences in captive versus free-ranging sample populations.

Tradeoffs between bite force and gape in Eulemur and Varecia.

In 1974, Sue Herring described the relationship between two important performance variables in the feeding system, bite force and gape. These variables are inversely related, such that, without specific muscular adaptations, most animals cannot produce high bite forces at large gapes for a given sized muscle. Despite the importance of these variables for feeding biomechanics and functional ecology, the paucity of in vivo bite force data in primates has led to bite forces largely being estimated through ex vivo methods. Here, we quantify and compare in vivo bite forces and gapes with output from simulated musculoskeletal models in two craniofacially distinct strepsirrhines: Eulemur, which has a shorter jaw and slower chewing cycle durations relative to jaw length and body mass compared to Varecia. Bite forces were collected across a range of linear gapes from 16 adult lemurs (suborder Strepsirrhini) at the Duke Lemur Center in Durham, North Carolina representing three species: Eulemur flavifrons (n = 6; 3F, 3M), Varecia variegata (n = 5; 3F, 2M), and Varecia rubra (n = 5; 5F). Maximum linear and angular gapes were significantly higher for Varecia compared to Eulemur (p = .01) but there were no significant differences in recorded maximum in vivo bite forces (p = .88). Simulated muscle models using architectural data for these taxa suggest this approach is an accurate method of estimating bite force-gape tradeoffs in addition to variables such as fiber length, fiber operating range, and gapes associated with maximum force. Our in vivo and modeling data suggest Varecia has reduced bite force capacities in favor of absolutely wider gapes compared to Eulemur in relation to their longer jaws. Importantly, our comparisons validate the simulated muscle approach for estimating bite force as a function of gape in extant and fossil primates.

Ontogenetic changes in jaw leverage and skull shape in tufted and untufted capuchins.

The ontogeny of feeding is characterized by shifting functional demands concurrent with changes in craniofacial anatomy; relationships between these factors will look different in primates with disparate feeding behaviors during development. This study examines the ontogeny of skull morphology and jaw leverage in tufted (Sapajus) and untufted (Cebus) capuchin monkeys. Unlike Cebus, Sapajus have a mechanically challenging diet and behavioral observations of juvenile Sapajus suggest these foods are exploited early in development. Landmarks were placed on three-dimensional surface models of an ontogenetic series of Sapajus and Cebus skulls (n = 53) and used to generate shape data and jaw-leverage estimates across the tooth row for three jaw-closing muscles (temporalis, masseter, medial pterygoid) as well as a weighted combined estimate. Using geometric morphometric methods, we found that skull shape diverges early and shape is significantly different between Sapajus and Cebus throughout ontogeny. Additionally, jaw leverage varies with age and position on the tooth row and is greater in Sapajus compared to Cebus when calculated at the permanent dentition. We used two-block partial least squares analyses to identify covariance between skull shape and each of our jaw muscle leverage estimates. Sapajus, but not Cebus, has significant covariance between all leverage estimates at the anterior dentition. Our findings show that Sapajus and Cebus exhibit distinct craniofacial morphologies early in ontogeny and strong covariance between leverage estimates and craniofacial shape in Sapajus. These results are consistent with prior behavioral and comparative work suggesting these differences are a function of selection for exploiting mechanically challenging foods in Sapajus, and further emphasize that these differences appear quite early in ontogeny. This research builds on prior work that has highlighted the importance of understanding ontogeny for interpreting adult morphology.

Seed choice differs by sex in sooty mangabeys (Cercocebus atys).

The sooty mangabey (Cercocebus atys) practices year-round durophagy. A large part of the C. atys diet consists of the oily nut of Sacoglottis gabonensis, which is accessed by post-canine crushing of the hard, protective seed coat. During a typical foraging bout, some seeds are discarded after initial crushing attempts using isometric biting, but the reason mangabeys reject some seeds and break into others is unclear. Although C. atys is sexually dimorphic, little is known about whether differences between males and females affect the selectivity of mechanically protected foods. We studied C. atys feeding on S. gabonensis in the Taï National Park,  Côte d'Ivoire, in July and August 2016. Nuts discarded after an initial crushing attempt were collected and their hardness measured using a Shore D durometer. Measurements were taken in the region of the nut where monkeys attempted to crush it. Hardness values of nuts rejected by adult male (n = 79) and adult female (n = 104) C. atys were compared to those of a control assemblage of nuts collected randomly on the forest floor (n = 69). Nuts rejected by either sex do not differ statistically from the random sample; however, they do differ from each other, with females rejecting harder nuts. This suggests that males are more effective at broaching harder seed husks, and discard seeds based on other factors.