Ingestive behaviors in bearded capuchins (Sapajus libidinosus)

Abstract

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.

Figure 1

(A) Sample feeding events for ‘piaçava’ nuts (Obrignya sp.) captured from a video. Manual food processing behaviors take place outside of the oral cavity and involve using the limbs and, in some cases, tools in various combinations. In contrast, ingestive behaviors are defined as food passing into the oral cavity and can exclusively include the oral cavity or a combination of the limbs and oral cavity. Ingestion is typically followed by mastication, which takes place on the postcanine teeth and is characterized by cyclic jaw movements, presumably associated with upward, medial, and anterior movements of the lower teeth relative to the upper teeth during the slow close phase of the gape cycle. A chewing sequence typically begins when the food enters the oral cavity (ingestion) and continues until the food is swallowed or discarded. (B) However, chewing sequences may be discontinuous. For example, primates may ingest a food item then later remove it from the oral cavity, then engage in manually processing before ingesting it for a second time. Importantly, not all ingested materials undergo manual processing before ingestion and not all ingested materials are masticated and swallowed. Some food items may be ingested and subsequently discarded. Feeding sequences and feeding events end when the food item is swallowed or discarded.

Figure 2

(A) Photos of manual, oral-manual ingestive, and masticatory behaviors in Sapajus libidinosus taken at Fazenda Boa Vista by Mariana Dutra Fogaça. (B) Boxplot of variation in food toughness between manual and ingestive behaviors. (C) Boxplot of variation in food elastic modulus between manual and ingestive behaviors, and (D) boxplot of variation in the duration of manual, ingestive, and masticatory behaviors. For all plots, the upper and lower bound of the boxes corresponds with the 25th and 75th percentiles and the whiskers extend 1.5 times the interquartile range in either direction. The median is represented by a horizontal line inside the boxes. A significance level, p < 0.01, is indicated by three asterisks. Figure generated in R (2017; https://www.R-project.org).

Figure 3

(A) Photos of oral and oral-manual ingestive behaviors in Sapajus libidinosus taken at Fazenda Boa Vista by Mariana Dutra Fogaça. (B) Boxplot of variation in food toughness between oral and oral-manual ingestive behaviors. (C) Boxplot of variation in food elastic modulus between oral and oral-manual ingestive behaviors, and (D) boxplot of variation in the duration of oral and oral-manual ingestive behaviors. The upper and lower bound of the boxes corresponds with the 25th and 75th percentiles and the whiskers extend 1.5 times the interquartile range in either direction. The median is represented by a horizontal line inside the boxes. The sample size of toughness and elastic modulus measures for oral-manual behaviors is small and the median line corresponding with lower bound of the box. A significance level, p < 0.01, is indicated by three asterisks. Figure generated in R (2017; https://www.R-project.org).

Figure 4

(A) Photos of oral and oral-manual ingestive behaviors at the anterior and posterior dentition in Sapajus libidinosus taken at Fazenda Boa Vista by Mariana Dutra Fogaça. (B) Boxplot of variation in food toughness between oral and oral-manual ingestive behaviors on the anterior and posterior dentition. (C) Boxplot of variation in food elastic modulus between oral and oral-manual ingestive behaviors on the anterior and posterior dentition, and (D) boxplot of variation in the duration of oral and oral-manual ingestive behaviors on the anterior and posterior dentition. The upper and lower bound of the boxes corresponds with the 25th and 75th percentiles and the whiskers extend 1.5 times the interquartile range in either direction. The median is represented by a horizontal line inside the boxes. The sample size of toughness and elastic modulus measures for each behavior location is small, and the median line corresponds with upper or lower bound of the box. A significance level, p < 0.01, is indicated by three asterisks. Figure generated in R (2017; https://www.R-project.org).