Age-related variation in the mechanical properties of foods processed by Sapajus libidinosus.

OBJECTIVES: The diet of tufted capuchins (Sapajus) is characterized by annual or seasonal incorporation of mechanically protected foods. Reliance on these foods raises questions about the dietary strategies of young individuals that lack strength and experience to access these resources. Previous research has demonstrated differences between the feeding competencies of adult and juvenile tufted capuchins. Here we test the hypothesis that, compared to adults, juveniles will process foods with lower toughness and elastic moduli. MATERIALS AND METHODS: We present data on variation in the toughness and elastic modulus of food tissues processed by Sapajus libidinosus during the dry season at Fazenda Boa Vista, Brazil. Food mechanical property data were collected using a portable universal mechanical tester. RESULTS: Results show that food tissues processed by the capuchins showed significant differences in toughness and stiffness. However, we found no relationship between an individual's age and mean or maximum food toughness or elastic modulus, indicating both juvenile and adult S. libidinosus are able to process foods of comparable properties. DISCUSSION: Although it has been suggested that juveniles avoid mechanically protected foods, age-related differences in feeding competence are not solely due to variation in food toughness or stiffness. Other factors related to food type (e.g., learning complex behavioral sequences, achieving manual dexterity, obtaining physical strength to lift stone tools, or recognizing subtle cues about food state) combined with food mechanical properties better explain variation in juvenile feeding competency.

Viewpoints: diet and dietary adaptations in early hominins: the hard food perspective.

Recent biomechanical analyses examining the feeding adaptations of early hominins have yielded results consistent with the hypothesis that hard foods exerted a selection pressure that influenced the evolution of australopith morphology. However, this hypothesis appears inconsistent with recent reconstructions of early hominin diet based on dental microwear and stable isotopes. Thus, it is likely that either the diets of some australopiths included a high proportion of foods these taxa were poorly adapted to consume (i.e., foods that they would not have processed efficiently), or that aspects of what we thought we knew about the functional morphology of teeth must be wrong. Evaluation of these possibilities requires a recognition that analyses based on microwear, isotopes, finite element modeling, and enamel chips and cracks each test different types of hypotheses and allow different types of inferences. Microwear and isotopic analyses are best suited to reconstructing broad dietary patterns, but are limited in their ability to falsify specific hypotheses about morphological adaptation. Conversely, finite element analysis is a tool for evaluating the mechanical basis of form-function relationships, but says little about the frequency with which specific behaviors were performed or the particular types of food that were consumed. Enamel chip and crack analyses are means of both reconstructing diet and examining biomechanics. We suggest that current evidence is consistent with the hypothesis that certain derived australopith traits are adaptations for consuming hard foods, but that australopiths had generalized diets that could include high proportions of foods that were both compliant and tough.

A finite element analysis of masticatory stress hypotheses.

Understanding how the skull transmits and dissipates forces during feeding provides insights into the selective pressures that may have driven the evolution of primate skull morphology. Traditionally, researchers have interpreted masticatory biomechanics in terms of simple global loading regimes applied to simple shapes (i.e., bending in sagittal and frontal planes, dorsoventral shear, and torsion of beams and cylinders). This study uses finite element analysis to examine the extent to which these geometric models provide accurate strain predictions in the face and evaluate whether simple global loading regimes predict strains that approximate the craniofacial deformation pattern observed during mastication. Loading regimes, including those simulating peak loads during molar chewing and those approximating the global loading regimes, were applied to a previously validated finite element model (FEM) of a macaque (Macaca fascicularis) skull, and the resulting strain patterns were compared. When simple global loading regimes are applied to the FEM, the resulting strains do not match those predicted by simple geometric models, suggesting that these models fail to generate accurate predictions of facial strain. Of the four loading regimes tested, bending in the frontal plane most closely approximates strain patterns in the circumorbital region and lateral face, apparently due to masseter muscle forces acting on the zygomatic arches. However, these results indicate that no single simple global loading regime satisfactorily accounts for the strain pattern found in the validated FEM. Instead, we propose that FE models replace simple cranial models when interpreting bone strain data and formulating hypotheses about craniofacial biomechanics.

The structural rigidity of the cranium of Australopithecus africanus: implications for diet, dietary adaptations, and the allometry of feeding biomechanics.

Australopithecus africanus is an early hominin (i.e., human relative) believed to exhibit stress-reducing adaptations in its craniofacial skeleton that may be related to the consumption of resistant food items using its premolar teeth. Finite element analyses simulating molar and premolar biting were used to test the hypothesis that the cranium of A. africanus is structurally more rigid than that of Macaca fascicularis, an Old World monkey that lacks derived australopith facial features. Previously generated finite element models of crania of these species were subjected to isometrically scaled loads, permitting a direct comparison of strain magnitudes. Moreover, strain energy (SE) in the models was compared after results were scaled to account for differences in bone volume and muscle forces. Results indicate that strains in certain skeletal regions below the orbits are higher in M. fascicularis than in A. africanus. Moreover, although premolar bites produce von Mises strains in the rostrum that are elevated relative to those produced by molar biting in both species, rostral strains are much higher in the macaque than in the australopith. These data suggest that at least the midface of A. africanus is more rigid than that of M. fascicularis. Comparisons of SE reveal that the A. africanus cranium is, overall, more rigid than that of M. fascicularis during premolar biting. This is consistent with the hypothesis that this hominin may have periodically consumed large, hard food items. However, the SE data suggest that the A. africanus cranium is marginally less rigid than that of the macaque during molar biting. It is hypothesized that the SE results are being influenced by the allometric scaling of cranial cortical bone thickness.

Mechanical impact of incisor loading on the primate midfacial skeleton and its relevance to human evolution.

The midfacial skeleton in the human lineage demonstrates a wide spectrum of variation that may be the consequence of different environmental and mechanical selective pressures. However, different facial configurations may develop under comparable selective regimes. For example, the Neanderthal high and projected face and the Inuit broad and flat face are hypothesized to be the consequence of (1) life in a cold climate, and (2) excessive paramasticatory stresses focused on the anterior dentition. In this study, the second of these two hypotheses is tested using finite element analyses of a monkey skull. Results indicate that incisor loading induces heavy stress in the anterior midface of macaques. Additional analyses using incremental increases in the anteroinferior tilt of the skull to simulate different magnitudes of facial projection revealed that comparable muscular force generates less stress in a less-projected face. However, the findings of our final analyses, which attempted to combine biting with the incisors and pulling with the hands, differed from the analyses that mimicked only incisor loading (without any sort of anterior pulling component). These findings suggest that shortening the face may be the most effective way to compensate for anterior dental loading but not necessarily offset the forces incurred when using the anterior dentition as a vice for various paramasticatory behaviors. Although Neanderthals may have frequently loaded their anterior dentition, countervailing selection pressures, such as the inclusion of tough foods in the diet that demanded molar grinding, may have selected for a longer face with a lower load- to lever-arm ratio.

Indentation as a technique to assess the mechanical properties of fallback foods.

A number of living primates feed part-year on seemingly hard food objects as a fallback. We ask here how hardness can be quantified and how this can help understand primate feeding ecology. We report a simple indentation methodology for quantifying hardness, elastic modulus, and toughness in the sense that materials scientists would define them. Suggested categories of fallback foods-nuts, seeds, and root vegetables-were tested, with accuracy checked on standard materials with known properties by the same means. Results were generally consistent, but the moduli of root vegetables were overestimated here. All these properties are important components of what fieldworkers mean by hardness and help understand how food properties influence primate behavior. Hardness sensu stricto determines whether foods leave permanent marks on tooth tissues when they are bitten on. The force at which a food plastically deforms can be estimated from hardness and modulus. When fallback foods are bilayered, consisting of a nutritious core protected by a hard outer coat, it is possible to predict their failure force from the toughness and modulus of the outer coat, and the modulus of the enclosed core. These forces can be high and bite forces may be maximized in fallback food consumption. Expanding the context, the same equation for the failure force for a bilayered solid can be applied to teeth. This analysis predicts that blunt cusps and thick enamel will indeed help to sustain the integrity of teeth against contacts with these foods up to high loads.

Fallback foraging as a way of life: using dietary toughness to compare the fallback signal among capuchins and implications for interpreting morphological variation.

The genus Cebus is one of the best extant models for examining the role of fallback foods in primate evolution. Cebus includes the tufted capuchins, which exhibit skeletal features for the exploitation of hard and tough foods. Paradoxically, these seemingly "specialized" taxa belong to the most ubiquitous group of closely related primates in South America, thriving in a range of different habitats. This appears to be a consequence of their ability to exploit obdurate fallback foods. Here we compare the toughness of foods exploited by two tufted capuchin species at two ecologically distinct sites; C. apella in a tropical rainforest, and C. libidinosus in a cerrado forest. We include dietary data for one untufted species (C. olivaceus) to assess the degree of difference between the tufted species. These data, along with information on skeletal morphology, are used to address whether or not a fallback foraging species exhibits a given suite of morphological and behavioral attributes, regardless of habitat. Both tufted species ingest and masticate a number of exceedingly tough plant tissues that appear to be used as fallback resources, however, C. libidinosus has the toughest diet both in terms of median and maximal values. Morphologically, C. libidinosus is intermediate in absolute symphyseal and mandibular measurements, and in measures of postcranial robusticity, but exhibits a higher intermembral index than C. apella. We propose that this incongruence between dietary toughness and skeletal morphology is the consequence of C. libidinosus' use of tools while on the ground for the exploitation of fallback foods.

The feeding biomechanics and dietary ecology of Australopithecus africanus.

The African Plio-Pleistocene hominins known as australopiths evolved a distinctive craniofacial morphology that traditionally has been viewed as a dietary adaptation for feeding on either small, hard objects or on large volumes of food. A historically influential interpretation of this morphology hypothesizes that loads applied to the premolars during feeding had a profound influence on the evolution of australopith craniofacial form. Here, we test this hypothesis using finite element analysis in conjunction with comparative, imaging, and experimental methods. We find that the facial skeleton of the Australopithecus type species, A. africanus, is well suited to withstand premolar loads. However, we suggest that the mastication of either small objects or large volumes of food is unlikely to fully explain the evolution of facial form in this species. Rather, key aspects of australopith craniofacial morphology are more likely to be related to the ingestion and initial preparation of large, mechanically protected food objects like large nuts and seeds. These foods may have broadened the diet of these hominins, possibly by being critical resources that australopiths relied on during periods when their preferred dietary items were in short supply. Our analysis reconciles apparent discrepancies between dietary reconstructions based on biomechanics, tooth morphology, and dental microwear.