Barth W. Wright

Mechanical and Nutritional Properties of Food as Factors in Platyrrhine Dietary Adaptations

Platyrrhines face a vast array of potential food resources in the Neotropics. Ecological challenges associated with finding, ingesting, masticating, and digesting foods are influenced by food availability and accessibility. Food availability is influenced by seasonal variation in forest productivity, fruiting synchrony, and crop size (e.g., Stevenson 2001; Chapman et al. 2003, but see Milton et al. 2005). Accessibility, on the other hand, is related to such factors as fruit and seed size, the ability to breach mechanically challenging tissues, to tolerate secondary chemical compounds, and to balance nutrient intake. Our goal in this chapter is to examine the diversity of platyrrhine responses to this second variable – gaining access to and processing foods. All platyrrhine genera include fruit in their diets, but the annual percentage of fruit intake ranges widely from 8% in Cebuella to 86% in Ateles (Table 11.1). A wide variety of other resources including exudates, fungi, leaves, flowers, nectar and insect or vertebrate prey make up the balance, or at times the bulk, of annual diets. Some particularly interesting feeding behaviors seen in platyrrhines signal the evolution of specific adaptations. These include the ability to extract and digest plant resources such as gums by Cebuella and Callithrix (Nash 1986; Power and Oftedal 1996), fungi by Callimico (Porter 2001; Porter and Garber 2004; Hanson et al. 2006; Rehg 2006), and seeds by the pitheciins (van Roosmalen et al. 1988; Ayres 1989; Kinzey and Norconk 1990; Kinzey 1992; Peetz 2001; Norconk and Conklin-Brittain 2004). Although gums, seeds and fungi are ingested by other primate species [especially lemurs (Nash 1989; Hemingway 1998) and colobines (Waterman and Kool 1994; Kirkpatrick 1998)], they are used very intensively by these platyrrhines, composing either a majority of their diet during a single season, a subset of the annual diet, or are routinely and extensively used throughout the year.

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. Anat Rec, 293:583–593, 2010.

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.

The Feeding Biomechanics and Dietary Ecology of Paranthropus boisei

The African Plio‐Pleistocene hominins known as australopiths evolved derived craniodental features frequently interpreted as adaptations for feeding on either hard, or compliant/tough foods. Among australopiths, Paranthropus boisei is the most robust form, exhibiting traits traditionally hypothesized to produce high bite forces efficiently and strengthen the face against feeding stresses. However, recent mechanical analyses imply that P. boisei may not have been an efficient producer of bite force and that robust morphology in primates is not necessarily strong. Here we use an engineering method, finite element analysis, to show that the facial skeleton of P. boisei is structurally strong, exhibits a strain pattern different from that in chimpanzees (Pan troglodytes) and Australopithecus africanus, and efficiently produces high bite force. It has been suggested that P. boisei consumed a diet of compliant/tough foods like grass blades and sedge pith. However, the blunt occlusal topography of this and other species suggests that australopiths are adapted to consume hard foods, perhaps including grass and sedge seeds. A consideration of evolutionary trends in morphology relating to feeding mechanics suggests that food processing behaviors in gracile australopiths evidently were disrupted by environmental change, perhaps contributing to the eventual evolution of Homo and Paranthropus. Anat Rec, 298:145–167, 2015.

The Global Impact of Sutures Assessed in a Finite Element Model of a Macaque Cranium

The biomechanical significance of cranial sutures in primates is an open question because their global impact is unclear, and their material properties are difficult to measure. In this study, eight suture‐bone functional units representing eight facial sutures were created in a finite element model of a monkey cranium. All the sutures were assumed to have identical isotropic linear elastic material behavior that varied in different modeling experiments, representing either fused or unfused sutures. The values of elastic moduli employed in these trials ranged over several orders of magnitude. Each model was evaluated under incisor, premolar, and molar biting conditions. Results demonstrate that skulls with unfused sutures permitted more deformations and experienced higher total strain energy. However, strain patterns remained relatively unaffected away from the suture sites, and bite reaction force was likewise barely affected. These findings suggest that suture elasticity does not substantially alter load paths through the macaque skull or its underlying rigid body kinematics. An implication is that, for the purposes of finite element analysis, omitting or fusing sutures is a reasonable modeling approximation for skulls with small suture volume fraction if the research objective is to observe general patterns of craniofacial biomechanics under static loading conditions. The manner in which suture morphology and ossification affect the mechanical integrity of skulls and their ontogeny and evolution awaits further investigation, and their viscoelastic properties call for dynamic simulations. Anat Rec 293:1477–1491, 2010.

It’s Tough Out There: Variation in the Toughness of Ingested Leaves and Feeding Behavior Among Four Colobinae in Vietnam

Colobines are similar in their exploitation of a high percentage of leaf matter. However, this observation obfuscates interesting differences among genera of Southeast Asian colobines in morphology and behavior that may be reflected in the degree to which they rely on mastication or gut volume and gut retention time when ingesting and digesting leaves. We detail the use of a laboratory-based method to measure the mechanical properties of foods selected and processed by 4 captive species of Southeast Asian Colobinae —Pygathrix nemaeus, Pygathrix cinerea, Trachypithecus delacouri, and Trachypithecus laotum hatinhensis— at the Endangered Primate Rescue Center (EPRC), Vietnam. We also detail a field method that quantifies chewing rates and chewing behavior via a consumer-grade video camera and laptop computer. Observations in the captive setting permit a degree of experimental control that is not possible in the wild, and the location of the EPRC in the primates’ habitat country permitted us to provide leaves that they encounter and eat in the wild. We collected toughness data with a portable tester designed by Lucas et al. The average toughness of selected leaves does not differ among the taxa, nor does the length of time spent chewing foods. However, there are differences in feeding rate, with Trachypithecus spp. chewing foods twice as fast as Pygathrix spp. Our findings suggest that Trachypithecus spp. emphasize comminution of food by mastication, while Pygathrix spp. emphasize the comminution of leaf matter in the stomach. The hypothesis is supported by data on molar size, gut mass, and gut morphology. We provide new insights into dietary variation among primate species and detail methods that are typically conducted only in a laboratory setting. We augment the findings with additional data on activity, feeding rates, and tooth morphology.

The Importance of Fallback Foods in Primate Ecology and Evolution

The role of fallback foods in shaping primate ranging, socioecology, and morphology has recently become a topic of particular interest to biological anthropologists. Although the use of fallback resources has been noted in the ecological and primatological literature for a number of decades, few attempts have been made to define fallback foods or to explore the utility of this concept for primate evolutionary biologists and ecologists. As a preface to this special issue of the American Journal of Physical Anthropology devoted to the topic of fallback foods in primate ecology and evolution, we discuss the development and use of the fallback concept and highlight its importance in primatology and paleoanthropology.

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.

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.

Craniofacial Strain Patterns During Premolar Loading: Implications for Human Evolution

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