Biting mechanics and niche separation in a specialized clade of primate seed predators

Abstract

We analyzed feeding biomechanics in pitheciine monkeys (Pithecia, Chiropotes, Cacajao), a clade that specializes on hard-husked unripe fruit (sclerocarpy) and resistant seeds (seed predation). We tested the hypothesis that pitheciine crania are well-suited to generate and withstand forceful canine and molar biting, with the prediction that they generate bite forces more efficiently and better resist masticatory strains than the closely-related Callicebus, which does not specialize on unripe fruits and/or seeds. We also tested the hypothesis that Callicebus-Pithecia-Chiropotes-Cacajao represent a morphocline of increasing sclerocarpic specialization with respect to biting leverage and craniofacial strength, consistent with anterior dental morphology. We found that pitheciines have higher biting leverage than Callicebus and are generally more resistant to masticatory strain. However, Cacajao was found to experience high strain magnitudes in some facial regions. We therefore found limited support for the morphocline hypothesis, at least with respect to the mechanical performance metrics examined here. Biting leverage in Cacajao was nearly identical (or slightly less than) in Chiropotes and strain magnitudes during canine biting were more likely to follow a Cacajao-Chiropotes-Pithecia trend of increasing strength, in contrast to the proposed morphocline. These results could indicate that bite force efficiency and derived anterior teeth were selected for in pitheciines at the expense of increased strain magnitudes. However, our results for Cacajao potentially reflect reduced feeding competition offered by allopatry with other pitheciines, which allows Cacajao species to choose from a wider variety of fruits at various stages of ripeness, leading to reduction in the selection for robust facial features. We also found that feeding biomechanics in sympatric Pithecia and Chiropotes are consistent with data on food structural properties and observations of dietary niche separation, with the former being well-suited for the regular molar crushing of hard seeds and the latter better adapted for breaching hard fruits.

Computational biomechanical analyses demonstrate similar shell-crushing abilities in modern and ancient arthropods

“…The widely applied comparative FEA method that yields relative as opposed to absolute predictions was therefore used and the role of geometry in determining mechanical performance was explored [37,[47][48][49]. The left L. polyphemus coxa model was imported as a Nastran (NAS) file into STRAND7 (Strand7 Pty Ltd, Sydney, Australia) FEA software [50]. The model was treated as isotropic with Young's modulus of 867 N mm 22 (for sclerotized cuticle [51]) and a Poisson ratio of 0.3 (for isometric cuticle [35]).…”

“…Muscle origins were tessellated as plate elements onto the meshed surface and modelled as 3D membrane (thickness ¼ 0.0001 mm). Forces for each muscle, directed toward their respective insertion sites, were then applied to plate elements using Boneload [50,52]. Muscle insertions were treated as single points and identified using the 'point coordinates' tool in GEOMAGIC STUDIO.…”

Investigating the effect of endocranial volume on cranial shape in platyrrhines and the relevance of this relationship to interpretations of the fossil record

“…While according to our EQ data, Pithecia , Chiropotes , and Cacajao all have relatively large brains, their food processing strategy is so extreme that growth of a sagittal crest is still required, particularly in the smaller‐bodied Pithecia . These taxa are seed predators that have specialized incisors and canines and are capable of generating large bite forces during extractive foraging, or “sclerocarp harvesting,” of hard‐skinned, unripe fruits (i.e., Anapol & Lee, ; Kinzey, ; Ledogar, Luk, Perry, Neaux, & Wroe, ; Norconk, ; Norconk, Wright, Conklin‐Brittain, & Vinyard, ; Taylor, Yuan, Ross, & Vinyard, ). Pithecia has been described as more gracile in their canine teeth, perhaps illustrating a primitive expression of the complex, and they depart further from the Chiropotes and Cacajao pattern in having large molar teeth as well (Anapol & Lee, ; Kinzey, ; Rosenberger, ).…”

Analyzing the sclerocarpy adaptations of the Pitheciidae mandible

“…They found that pitheciines have higher biting leverage and are generally more resistant to masticatory strain as compared to Callicebus . However, they found limited support for the morphocline hypothesis since Cacajao showed higher strain magnitudes in various facial regions when compared with the other analyzed taxa (Ledogar et al, ). This study also found that biting leverage in Cacajao was slightly less than in Chiropotes , and that strain values during canine biting (i.e., one of the main mechanisms to open unripe fruits) followed a strength trend described as Cacajao–Chiropotes–Pithecia , rather than the proposed morphocline hypothesis (Kinzey, ).…”

“…In spite of all these valuable studies, most of these investigations have been restricted to morphological comparisons, and simple biomechanical comparisons (i.e., comparing lever arms and MA), with fewer studies using modern virtual functional morphology techniques or experimental approaches applied to analyze platyrrhine mandibles (Ross et al, ; Ross, Iriarte‐Diaz, Reed, Stewart, & Taylor, ). Only recently, one study analyzed feeding biomechanics in pitheciine monkeys, by applying finite element analysis (FEA) to assess cranial biting mechanics (Ledogar et al, ). They found that pitheciines have higher biting leverage and are generally more resistant to masticatory strain as compared to Callicebus .…”