Ontogenetic changes in bite force and gape in tufted capuchins.

Bite force and gape are two important performance metrics of the feeding system, and these metrics are inversely related for a given muscle size because of fundamental constraints in sarcomere length-tension relationships. How these competing performance metrics change in developing primates is largely unknown. Here, we quantified in vivo bite forces and gapes across ontogeny and examined these data in relation to body mass and cranial measurements in captive tufted capuchins, Sapajus spp. Bite force and gape were also compared across geometric and mechanical properties of mechanically challenging foods to investigate relationships between bite force, gape and food accessibility (defined here as the ability to breach shelled nuts). Bite forces at a range of gapes and feeding behavioral data were collected from a cross-sectional ontogenetic series of 20 captive and semi-wild tufted capuchins at the Núcleo de Procriação de Macacos-Prego Research Center in Araçatuba, Brazil. These data were paired with body mass, photogrammetric measures of jaw length and facial width, and food geometric and material properties. Tufted capuchins with larger body masses had absolutely higher in vivo bite forces and gapes, and animals with wider faces had absolutely higher bite forces. Bite forces and gapes were significantly smaller in juveniles compared with subadults and adults. These are the first primate data to empirically demonstrate the gapes at which maximum active bite force is generated and to demonstrate relationships to food accessibility. These data advance our understanding of how primates meet the changing performance demands of the feeding system during development.

The effects of feeding frequency on jaw loading in two lemur species.

OBJECTIVES: Studies on oral processing are often snapshots of behaviors that examine feeding through individual bouts. In this study, we expand on our previous work comparing bite/chew variables per feeding bout to summed daily biting, chewing, and food intake to interpret loading that could have potential morphological effects. MATERIALS AND METHODS: We observed sympatric Lemur catta and Propithecus verreauxi over two field seasons in the dry forest of Bezà Mahafaly Special Reserve in southwestern Madagascar. Bite and chew rates determined from videos filmed during observations were multiplied with time spent feeding on specific foods during focal follows to calculate daily values for each feeding bout. Food mechanical properties (FMPs) were tested on dietary items with a portable tester. We contrasted daily bite/chew numbers and intake with FMPs, species, season, and food shape. RESULTS: Daily bite and chew numbers increased with maximum, but not average, food toughness. Daily intake decreased with average and maximum toughness. Season had a strong effect on daily bites and chews, but not on intake. Food shape influenced intake and total bite and chew numbers. The lemur species did not differ in our models. DISCUSSION: Maximum food toughness impacted feeding behaviors and intake, which is consistent with higher loads having a greater effect on morphology. In contrast to feeding per bout, cumulative biting and chewing did not differ between species; taking feeding frequency into consideration affects interpretation of jaw loading. Finally, biting, as much as chewing, may generate strains that impact morphology.

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.

Comparing effects of food mechanical properties on oral processing behaviors in two sympatric lemur species.

OBJECTIVES: The link between diet and the masticatory apparatus in primates is complex. We investigated how food mechanical properties (FMPs) and food geometry affect feeding behaviors and subsequent jaw loading. We compared oral processing in two sympatric lemur species with distinct diets and mandibular morphologies. MATERIALS AND METHODS: All-day focal follows of Lemur catta (Lc) and Propithecus verreauxi (Pv) were conducted in both the dry and wet seasons at Beza Mahafaly Special Reserve. We collected activity budget data, filmed feeding bouts, and collected food items to measure their mechanical properties with an FLS-1 portable tester. Feeding videos for the top food items they spent the most time consuming were analyzed frame-by-frame to assess bite and chew numbers and rates. RESULTS: Lc bite more and at a slower rate on tougher (maximum) foods, chew more for tougher (average) foods, and chew less for stiffer leaves. Pv initially increase chew number for tougher (average) foods, but their behavior is less affected as food toughness increases. Pv chew less and more slowly but spend more of the day feeding than Lc. Additionally, they have a tougher (maximum) diet than Lc. DISCUSSION: Lc adjust their feeding behaviors depending on the FMPs of their top food items, while Pv feed more consistently. The more robust masticatory apparatus of Pv may not require them to adjust their feeding behaviors for more mechanically challenging foods. Furthermore, the two species show distinct differences in chewing. Exploring chewing on a daily scale could aid in understanding its impact on the loading of the masticatory apparatus.

Ingestive behaviors in bearded capuchins (Sapajus libidinosus).

The biomechanical and adaptive significance of variation in craniodental and mandibular morphology in fossil hominins is not always clear, at least in part because of a poor understanding of how different feeding behaviors impact feeding system design (form-function relationships). While laboratory studies suggest that ingestive behaviors produce variable loading, stress, and strain regimes in the cranium and mandible, understanding the relative importance of these behaviors for feeding system design requires data on their use in wild populations. Here we assess the frequencies and durations of manual, ingestive, and masticatory behaviors from more than 1400 observations of feeding behaviors video-recorded in a wild population of bearded capuchins (Sapajus libidinosus) at Fazenda Boa Vista in Piauí, Brazil. Our results suggest that ingestive behaviors in wild Sapajus libidinosus were used for a range of food material properties and typically performed using the anterior dentition. Coupled with previous laboratory work indicating that ingestive behaviors are associated with higher mandibular strain magnitudes than mastication, these results suggest that ingestive behaviors may play an important role in craniodental and mandibular design in capuchins and may be reflected in robust adaptations in fossil hominins.