The Functional Morphology of Ingestion in the Platyrrhine Sclerocarpic Harvesters (Platyrrhini, Primates)

The identification of anatomical correlates of diet and feeding behavior in nonhuman primates is an important area of research in biological anthropology. The morphology of the jaws and teeth reflects the phylogeny and adaptations that distinguish taxa and their different ecological niches. Studying the form-function relationships of jaws and teeth in modern species provides a framework for interpreting the diets of extinct species and for inferring the ecological pressures that may have contributed to the evolutionary diversification of primate craniodental morphology. Previous work on modeling primate jaw mechanics has focused largely on the functional context of a closed jaw. Little attention has been given to the biomechanical arrangement of the system’s ingestive morphology whereby the anterior teeth and the musculoskeletal anatomy function in open-jaw positions. This dissertation advances the state of knowledge of the evolution of the primate feeding apparatus by considering the functional significance of the morphology of the anterior teeth, masticatory muscles and the jaws as they would operate in an open-gape context. The taxonomic focus of this thesis is a group of platyrrhines characterized by an intensive form of ingestion. These “sclerocarpic harvesters” include the pitheciids Cacajao, Chiropotes,Pithecia,andCallicebus, and also the cebid Aotus. These primates feed on fruits with hard or tough outer coverings, and the pitheciins (Cacajao, Chiropotes, Pithecia) frequently prey on the variably soft seeds within. By comparing these taxa with other platyrrhines, this research aims to to shed light on the possibility of biomechanical tradeoffs favoring either the ingestion or mastication of foods that may reflect adaptive priorities in the feeding complex, optimized for a particular set of functions. As a group, the sclerocarpic harvesters exhibit deep mandibles with expanded gonial regions where two adductors of the jaw insert, i.e., the superficial masseter and medial pterygoid muscles. These taxa are distinguished dentally from similarly-sized platyrrhines by their relatively large incisors, tall and narrow among the pitheciids, broad in Aotus, similarly used for scraping and scoring the outer protective rinds and/or gouging out the soft flesh from within hard-skinned fruits. The pitheciins are further distinguished in having robust triquetrous canine teeth – approximately triangular in cross-section – that are used to breach and pry open relatively large whole fruit with wide open jaws. Together the mandible and the canine teeth are two structures in the feeding complex that particularly distinguish the sclerocarpic harvesters and form the basis of this research. Jaw shape is routinely used in discussions of relationships among living and extinct platyrrhines, though few efforts have aimed to parse the phylogenetic and functional signals that affect the variability in this morphology. Chapter 3 of this dissertation begins the analytical section of this work by testing for functional correlates of the mandibular morphology that largely distinguish the pitheciids from the predominately-frugivorous, and similarly-sized cebids (except Aotus). 3D geometric morphometrics (3DGM) and principal components analysis was used to identify the leading sources of the variability in the shapes of 145 landmarked mandibles of pitheciids (Cacajao, Chiropotes, Pithecia, Callicebus) and cebids (Sapajus, Cebus, Aotus, Saimiri). Biomechanically-significant measurements of the mandibles were derived from the landmark coordinates, i.e., inter-landmark distances were calculated that span morphological features that aid in the mitigation of stress in the jaw during loading. These functional signals were regressed against the PCA shape components to test for correspondence between the phylogenetic and functional signals in the shapes of the jaws. Results of the 3DGM mandible study in Chapter 3 link the variability in the study sample with jaw function and distinguish these taxa in terms of feeding strategies more consistently than phylogeny. These results are support a new mechanical explanation for the diversity in jaw shape whereby Aotusand the pitheciids are unified as sclerocarpic harvesters, i.e., a group that emphasizes anterior-tooth loading during the first phase of feeding – ingestion – while the jaws of pitheciins and Sapajusoverlap in values associated with support for eccentric loading during the second phase – mastication – e.g., cracking and masticating seeds. This two-phase mechanical explanation for jaw shape diversity poses a problem for the use of mandible shape for phylogenetic analyses, particularly in platyrrhines wherein the cebids Aotusand Sapajusboth exhibit patterns of mandibular morphology that appear to reflect a process of convergence on the pitheciid-like emphasis on ingestion. However, this success in characterizing jaw shape diversity as a composite response to challenges associated with both phases of feeding suggests that a similar approach to evaluating the feeding behavior of extinct platyrrhines from fossil mandibles may add significant definition to what is known about the paleobiology of this radiation. Another component of the feeding apparatus is the musculature of the jaws, and aspects of the shape of the mandible are related to the organization the muscles. Broadly, the musculoskeletal anatomy of primate jaws is understood to be influenced by feeding behavior, phylogeny, and body size. Jaw shape and muscle anatomy act together in life but are typically studied apart, and while the discrete components of the masticatory complex provide useful insights into feeding adaptations and trends in primates, the interaction of components may not be obvious when studied in isolation. In Chapter 4, the skeletal morphology and muscle performance are integrated to study the effect of variability in jaw shape on muscle force with changes in gape. To consider the effect of body size, two larger-bodied platyrrhines were added to the comparative sample for this study, i.e., Atelesand Alouatta. Patches of virtual landmarks were applied to the attachment sites of jaw-closing muscles on 3D models of skulls using Landmark Editor software. The distances between attachments were measured with skulls set to different gape configurations, then length-tension formulas and muscle physiological cross-section area (PCSA) data from the literature were used to model maximum muscle force in each position. The results reported in Chapter 4 show that variation in muscle position with respect to the jaw joint produces a pattern of heterogeneous excursion that distinguishes each muscle, and together form patterns that are differ across the taxa studied. The relative rate of decline in muscle force outputs with increasing gape varies in the platyrrhines modeled with body size driving this relationship such that the sum of jaw muscle forces declines more gradually with increasing gape in smaller taxa while in larger taxa the decline is more acute. The scaling of the force-gape relationship with body size may therefore constitute a baseline strategy among platyrrhines to cope with the physical properties of foods that is most limiting to their ecological niche. The jaws of smaller primates favor the retention of muscle forces at higher gapes, which is consistent with the expectation that relative fruit size poses a more significant challenge for ingestion in these taxa. Conversely, larger platyrrhines exhibit a pattern that favors greater force production at lower gapes in support of diets that incorporate mastication of tougher foods that are relatively smaller on account of their greater body size. In the second half of this dissertation, the definition and functional significance of canine robusticity is explored. Robust canines are a hallmark of the pitheciin seed predators and prospective pitheciids in the fossil record exhibit similarly-robust, but more conical canines beginning in the early middle Miocene of Patagonia. Canine tooth crown height is understood more generally to correspond with diverse competitive regimes and mating strategies among primates, but little is known about the potential function of canine tooth robustness, i.e., whether proportionally wider canine teeth confer some social or dietary advantage over a more gracile crown. Canine bending strength is believed to correspond with canine tooth robusticity but does not vary with social factors such as group size and antagonism among primate species. In contrast, bending strength is higher in the robust-toothed pitheciins and capuchins (Cebusand Sapajus), several of which use these teeth for mechanically-intensive challenges associated with feeding on protected fruits and seeds. As a result, it was presumed that canine tooth robusticity is an evolutionary response to fracture risk, and it was predicted that the pitheciins and capuchins experience a lower risk of canine fracture than in other primates. In Chapter 5, the prediction that variability in canine bending strength and canine tooth robusticity corresponds with fracture risk was tested by surveying museum collections of wild caught platyrrhines of seven genera (i.e., Cacajao, Chiropotes, Pithecia, Cebus, Sapajus, Saimiri, and Ateles) for canine teeth broken before death, and then fracture rates were compared with those published for carnivores. Results demonstrate the rarity of fractured canine teeth in platyrrhines including both seed-eating and non-seed-eating species; on average one in twenty individuals exhibit one or more broken canine teeth. This consistently low prevalence of fractures among platyrrhines suggests that higher canine bending strength does not lessen the risk of breaking a canine tooth. Alternatively, it might be argued that more robust, stronger canines serve to retain a comparatively-low frequency of fracture on platyrrhines rely on these teeth to access more resistant foods. However, published surveys of carnivore fracture rates suggest that the fracture rate may vary a great deal in taxa that depend on their canine teeth for prey capture, and thus it is unlikely that primates should have resolved this problem more perfectly than carnivores. Further, primates were reported to have higher bending strength values in their canine teeth than carnivores, but the prevalence of fracture does not strictly fit this generalization. Overall the results of this study suggest that previously-reported bending strength values do not predict risk of fracture in canine teeth, and an explanation for any functional significance of variability in canine tooth robusticity is lacking. In Chapter 6, finite elements analysis (FEA) was used to evaluate an alternative hypothesis for the constraints on canine tooth shape, i.e., that the width of the cementoenamel junction (CEJ) is a response to the buildup of stresses in the surrounding alveolar tissue when the tooth is loaded during biting. A geometrically-simplified digital model of a canine crown was constructed and set in a virtual jaw bone and loaded with simulated forces, then modified in its dimensions and tested again to study the effect of changes in CEJ dimensions on the peak stresses in the modeled alveolus. Estimates of bite forces derived from published platyrrhine muscle PCSA data were used in conjunction with canine tooth measurements to model the effect of taxon-specific forces on the canine tooth model with an array of different geometry that approximates the dimensions in the platyrrhine sample (i.e., Cacajao, Chiropotes, Pithecia, Cebus, Sapajus, Saimiri, andAteles). An optimization program was run using an iterative approach to simulate the effects of different geometry and loading conditions in the modeled canines. The program identifies the geometry that best balances between the goal of minimizing the CEJ diameter (to facilitate greater mechanical advantage for penetration) while not exceeding a set stress criterion in the alveolar bone (i.e., critical failure resulting from stresses exceeding yield strength). Finally, optimized model results are compared with the dimensions of the platyrrhine sample to consider the expectation that the geometry in these taxa are the result of similar drivers and constraints as those specified in the FEA simulations. The results of FEA simulations in Chapter 6 suggest that canine shape reflects the optimization of competing pressures to maximize mechanical advantage for penetration while minimizing the stresses in the alveolar bone in which the tooth is rooted, particularly during moderate to high-gape biting. The optimized canine models generated are sensitive to the magnitude and orientation of forces applied to simulate canine biting. The models that were vertically-loaded resulted in a narrow-crowned optimal output because the stresses in these models are easily dissipated along the tooth root surface, permitting an unnaturally narrow crown without damaging the alveolar tissue. Oblique loads used to simulate biting during open-gape functions on these models produce an uneven distribution of stress in the alveolus where compressive stresses are concentrated opposite of where the oblique load is positioned. To mitigate the concentration of stresses in the alveolus, the CEJ diameter is broadened during the automated optimization process, resulting in more geometrically robust optimal output that closely approximate the dimensions of the canines from the sampled platyrrhine taxa. Strong correlations between the real geometry of the platyrrhine sample and the optimal model outputs for the obliquely-loaded trials provide support for the hypothesis that canine robusticity is a response to stress in the alveolar tissues, not the canine tooth itself. Taken together, the results of the four analytical chapters of this thesis add definition to the gross morphological patterns in the anterior teeth and jaws among the sclerocarpic harvesters, principally the pitheciins, that have been presumed to have evolved in support of their specialization on large, hard-skinned fruits and seeds. The mandibles of the pitheciids and cebids signal a malleability of mandible shape that is sensitive to mechanical challenges during both ingestion and mastication phases of feeding. However, the sclerocarpic harvesters are not exceptional in the organization of their musculature in support of ingestion at high gapes, and instead they follow a trend in the organization that scales with body size. Caveats to this observation include the special roles that canine teeth of the pitheciins and Callicebusplay as potentially different approaches to the similar problem breaching relatively large foods (i.e., tall laterally-splayed in pitheciins and shortened upright crowns in Callicebus) that may modify the force-gape relationship in the jaws by increasing the clearance and facilitating less stretch and more muscle force when biting a food of a given size. Additionally, the shape of the canine teeth themselves appear to be responses to the stresses produced during loading in the first ingestive steps when the resistant outer components of whole foods found in nature present the most intense mechanical challenges to alveolar tissue around the canines as the food is opened. Finally, while the anatomical diversity of pitheciins is related to functions that are specific to the feeding strategies among these taxa, the mechanistic relationships and biomechanical constraints on the morphology identified here are common factors in the evolution of the feeding apparatus in all primates, e.g., the yield characteristics of cortical bone and enamel, the diversity of loading regimes at different gapes, and the effect of muscle length and position on the excursion and force in jaw muscles. Thus, advances to the understanding of interactions between these factors bears significance for the evolution of feeding mechanics on a broader scale and may also benefit the evaluation of the functional morphology of the feeding complex throughout the order Primates and mammals more broadly