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.

Fig 1. Shape analysis.

(A) Cranium of Pithecia pithecia (MCZ 30719) in anterior, lateral, and inferior view showing fixed landmarks (red) and sliding semi-landmarks (black) used in the shape analysis. Plots show results for the PCA of cranial shape in (B) Callicebus, (C) Pithecia, (D) Chiropotes, and (E) Cacajao. For each plot, crania at the positive and negative ends of the PC1 and PC2 axes describe shape change along these axes, warped onto the specimen closest to the group centroid (i.e., shortest distance from group centroid). The specimens with the most positive and most negative principal component scores along PC1 were selected for use in FEA. In Callicebus, PC1 mainly captures variation in neurocranial height and length and facial length, with longer and lower crania with slightly longer faces toward negative scores. PC2 explains some differences in facial width and orbit, with wider faces toward minimum scores. In Pithecia, PC1 describes differences in facial and neurocranial width, with wider crania toward positive scores. PC2 reflects aspects of neurocranial and facial variation, with the neurocranium extended superoinferiorly and face extended inferoanteriorly toward positive scores. In Chiropotes, PC1 captures some differences in neurocranial shape and facial projection, with longer crania and faces toward positive scores. Faces are slightly wider toward positive scores along PC2. Cacajao is similar to Chiropotes, except that longer crania and face are found along the negative end of PC1.

Fig 2. Digital dissection and jaw adductor muscle areas.

(A) Surface model of Chiropotes satanas specimen showing digitally dissected temporalis and masseter muscles used to calculated forces applied to FEMs. (B) Lateral view of the Chiropotes PC1- surface model showing origin and insertion areas for the temporalis (red) and masseter (purple) muscles. (C) Sagittal section showing origin and insertion for the medial pterygoid (blue-green). Note that muscle tractions were only applied to origins (i.e., those attachments on the cranium), whereas the insertions (i.e., on the mandible) were used to guide the orientation of muscle force vectors.

Fig 3. Color mapping of Batch 1 strain results.

Color maps of von Mises microstrain (με) distributions in FEMs of Callicebus, Pithecia, Chiropotes, and Cacajao using Batch 1 muscle forces (without species-specific force ratios) for (A) canine and (B) M² biting. “Cool” colors represent areas of low strain, whereas “warm” colors indicate larger strain magnitudes. White regions exceed 750 με. Models are shown at roughly the same facial height (i.e., not to scale) to accentuate similarities and differences in strain distribution.

Fig 4. Plot of Batch 1 strain data from sampled regions.

The von Mises microstrain (με) magnitudes sampled from 20 craniofacial sites in FEMs of Callicebus, Pithecia, Chiropotes, and Cacajao for Batch 1 during (A) canine and (B) M² biting.

Fig 5. Color mapping of Batch 2 strain results.

Color maps of von Mises microstrain (με) distributions in FEMs of Callicebus, Pithecia, Chiropotes, and Cacajao using Batch 2 muscle forces (including species-specific force ratios) for (A) canine and (B) M² biting. “Cool” colors represent areas of low strain, whereas “warm” colors indicate larger strain magnitudes. White regions exceed 750 με. Models are shown at roughly the same facial height (i.e., not to scale) to accentuate similarities and differences in strain distribution.