Enamel chipping in Taï Forest cercopithecids: Implications for diet reconstruction in paleoanthropological contexts.

Antemortem enamel chipping in living and fossil primates is often interpreted as evidence of hard-object feeding (i.e., 'durophagy'). Laboratory analyses of tooth fracture have modeled the theoretical diets and loading conditions that may produce such chips. Previous chipping studies of nonhuman primates tend to combine populations into species samples, despite the fact that species can vary significantly in diet across their ranges. Chipping is yet to be analyzed across population-specific species samples for which long-term dietary data are available. Here, we test the association between enamel chipping and diet in a community of cercopithecid primates inhabiting the Taï Forest, Ivory Coast. We examined fourth premolars and first molars (n = 867) from naturally deceased specimens of Cercocebus atys, Colobus polykomos, Piliocolobus badius,Procolobus verus, and three species of Cercopithecus. We found little support for a predictive relationship between enamel chipping and diet across the entire Taï monkey community. Cercocebus atys, a dedicated hard-object feeder, exhibited the highest frequencies of (1) chipped teeth and (2) chips of large size; however, the other monkey with a significant degree of granivory, Co. polykomos, exhibited the lowest chip frequency. In addition, primates with little evidence of mechanically challenging or hard-food diets-such as Cercopithecus spp., Pi. badius, and Pr. verus-evinced higher chipping frequencies than expected. The equivocal and stochastic nature of enamel chipping in the Taï monkeys suggests nondietary factors contribute significantly to chipping. A negative association between canopy preference and chipping suggests a role of exogenous particles in chip formation, whereby taxa foraging closer to the forest floor encounter more errant particulates during feeding than species foraging in higher strata. We conclude that current enamel chipping models may provide insight into the diets of fossil primates, but only in cases of extreme durophagy. Given the role of nondietary factors in chip formation, our ability to reliably reconstruct a range of diets from a gradient of chipping in fossil taxa is likely weak.

On the vital role of enamel prism interfaces and graded properties in human tooth survival.

Teeth of omnivores face a formidable evolutionary challenge: how to protect against fracture and abrasive wear caused by the wide variety of foods they process. It is hypothesized that this challenge is met in part by adaptations in enamel microstructure. The low-crowned teeth of humans and some other omnivorous mammals exhibit multiple fissures running longitudinally along the outer enamel walls, yet remain intact. It is proposed that inter-prism weakness and enamel property gradation act together to avert entry of these fissures into vulnerable inner tooth regions and, at the same time, confer wear resistance at the occlusal surface. A simple indentation experiment is employed to quantify crack paths and energetics in human enamel, and an extended-finite-element model to evaluate longitudinal crack growth histories. Consideration is given as to how tooth microstructure may have played a vital role in human evolution, and by extension to other omnivorous mammals.

Simulation of enamel wear for reconstruction of diet and feeding behavior in fossil animals: A micromechanics approach.

The deformation and wear events that underlie microwear and macrowear signals commonly used for dietary reconstruction in fossil animals can be replicated and quantified by controlled laboratory tests on extracted tooth specimens in conjunction with fundamental micromechanics analysis. Key variables governing wear relations include angularity, stiffness (modulus), and size of the contacting particle, along with material properties of enamel. Both axial and sliding contacts can result in the removal of tooth enamel. The degree of removal, characterized by a "wear coefficient," varies strongly with particle content at the occlusal interface. Conditions leading to a transition from mild to severe wear are discussed. Measurements of wear traces can provide information about contact force and particle shape. The potential utility of the micromechanics methodology as an adjunct for investigating tooth durability and reconstructing diet is explored.

Primate dietary ecology in the context of food mechanical properties.

Substantial variation exists in the mechanical properties of foods consumed by primate species. This variation is known to influence food selection and ingestion among non-human primates, yet no large-scale comparative study has examined the relationships between food mechanical properties and feeding strategies. Here, we present comparative data on the Young's modulus and fracture toughness of natural foods in the diets of 31 primate species. We use these data to examine the relationships between food mechanical properties and dietary quality, body mass, and feeding time. We also examine the relationship between food mechanical properties and categorical concepts of diet that are often used to infer food mechanical properties. We found that traditional dietary categories, such as folivory and frugivory, did not faithfully track food mechanical properties. Additionally, our estimate of dietary quality was not significantly correlated with either toughness or Young's modulus. We found a complex relationship among food mechanical properties, body mass, and feeding time, with a potential interaction between median toughness and body mass. The relationship between mean toughness and feeding time is straightforward: feeding time increases as toughness increases. However, when considering median toughness, the relationship with feeding time may depend upon body mass, such that smaller primates increase their feeding time in response to an increase in median dietary toughness, whereas larger primates may feed for shorter periods of time as toughness increases. Our results emphasize the need for additional studies quantifying the mechanical and chemical properties of primate diets so that they may be meaningfully compared to research on feeding behavior and jaw morphology.

Sea otter dental enamel is highly resistant to chipping due to its microstructure.

Dental enamel is prone to damage by chipping with large hard objects at forces that depend on chip size and enamel toughness. Experiments on modern human teeth have suggested that some ante-mortem chips on fossil hominin enamel were produced by bite forces near physiological maxima. Here, we show that equivalent chips in sea otter enamel require even higher forces than human enamel. Increased fracture resistance correlates with more intense enamel prism decussation, often seen also in some fossil hominins. It is possible therefore that enamel chips in such hominins may have formed at even greater forces than currently envisaged.

Inferring biological evolution from fracture patterns in teeth.

It is hypothesised that specific tooth forms are adapted to resist fracture, in order to accommodate the high bite forces needed to secure, break down and consume food. Three distinct modes of tooth fracture are identified: longitudinal fracture, where cracks run vertically between the occlusal contact and the crown margin (or vice versa) within the enamel side wall; chipping fracture, where cracks run from near the edge of the occlusal surface to form a spall in the enamel at the side wall; and transverse fracture, where a crack runs horizontally through the entire section of the tooth to break off a fragment and expose the inner pulp. Explicit equations are presented expressing critical bite force for each fracture mode in terms of characteristic tooth dimensions. Distinctive transitions between modes occur depending on tooth form and size, and loading location and direction. Attention is focussed on the relatively flat, low-crowned molars of omnivorous mammals, including humans and other hominins and the elongate canines of living carnivores. At the same time, allusion to other tooth forms - the canines of the extinct sabre-tooth (Smilodon fatalis), the conical dentition of reptiles, and the columnar teeth of herbivores - is made to highlight the generality of the methodology. How these considerations impact on dietary behaviour in fossil and living taxa is discussed.

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.

Tooth chipping patterns in Archaeolemur provide insight into diet and behavior.

OBJECTIVES: Archaeolemur is a recently extinct genus of lemur that is often compared to some Cercopithecidae, especially baboons. This is due in part to their derived dentition, with large anterior teeth and reduced bilophodont molars. Research involving comparative morphology, analysis of coprolites, isotopes, and enamel structure, have suggested Archaeolemur had an omnivorous diet involving mechanically challenging items. Yet, microwear analysis of posterior teeth does not necessarily support this conclusion. MATERIALS AND METHODS: In this macroscopic study, dental chipping was recorded on permanent teeth of Archaeolemur from different localities (53 individuals; 447 permanent teeth; including both A. edwardsi and A. majori specimens). This study aimed to compare chipping patterns across the dentition of Archaeolemur with chipping in other primates. RESULTS: The results show enamel chipping was prevalent on the anterior teeth of Archaeolemur (38.9% of anterior teeth showed at least one fracture) yet rare in posterior teeth (9%). There was a decrease in chipping frequency across the dentition, moving distally from incisors (50%; 20/40), through caniniform teeth (30%; 15/50), premolars (9.5%; 16/169), and molars (8.5%; 16/188). DISCUSSION: The results support previous research suggesting Archaeolemur had a varied omnivorous diet in which the anterior dentition was used for extensive food processing. This likely included mechanically challenging items such as tough/hard large fruits, small vertebrates, and crustaceans. Such a high rate of chipping in the anterior dentition is uncommon in other primates, with exception of hominins.

Microwear, mechanics and the feeding adaptations of Australopithecus africanus.

Recent studies of dental microwear and craniofacial mechanics have yielded contradictory interpretations regarding the feeding ecology and adaptations of Australopithecus africanus. As part of this debate, the methods used in the mechanical studies have been criticized. In particular, it has been claimed that finite element analysis has been poorly applied to this research question. This paper responds to some of these mechanical criticisms, highlights limitations of dental microwear analysis, and identifies avenues of future research.

The role of tooth enamel mechanical properties in primate dietary adaptation.

Primate teeth adapt to the physical properties of foods in a variety of ways including changes in occlusal morphology, enamel thickness, and overall size. We conducted a comparative study of extant primates to examine whether their teeth also adapt to foods through variation in the mechanical properties of the enamel. Nanoindentation techniques were used to map profiles of elastic modulus and hardness across tooth sections from the enamel-dentin junction to the outer enamel surface in a broad sample of primates including apes, Old World monkeys, New World monkeys, and lemurs. The measured data profiles feature considerable overlap among species, indicating a high degree of commonality in mechanical properties. These results suggest that differences in the load-bearing capacity of primate molar teeth are more a function of morphology-particularly tooth size and enamel thickness-than of underlying mechanical properties.

Remarkable resilience of teeth.

Tooth enamel is inherently weak, with fracture toughness comparable with glass, yet it is remarkably resilient, surviving millions of functional contacts over a lifetime. We propose a microstructural mechanism of damage resistance, based on observations from ex situ loading of human and sea otter molars (teeth with strikingly similar structural features). Section views of the enamel implicate tufts, hypomineralized crack-like defects at the enamel-dentin junction, as primary fracture sources. We report a stabilization in the evolution of these defects, by "stress shielding" from neighbors, by inhibition of ensuing crack extension from prism interweaving (decussation), and by self-healing. These factors, coupled with the capacity of the tooth configuration to limit the generation of tensile stresses in largely compressive biting, explain how teeth may absorb considerable damage over time without catastrophic failure, an outcome with strong implications concerning the adaptation of animal species to diet.

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.

Adaptation to hard-object feeding in sea otters and hominins.

The large, bunodont postcanine teeth in living sea otters (Enhydra lutris) have been likened to those of certain fossil hominins, particularly the 'robust' australopiths (genus Paranthropus). We examine this evolutionary convergence by conducting fracture experiments on extracted molar teeth of sea otters and modern humans (Homo sapiens) to determine how load-bearing capacity relates to tooth morphology and enamel material properties. In situ optical microscopy and x-ray imaging during simulated occlusal loading reveal the nature of the fracture patterns. Explicit fracture relations are used to analyze the data and to extrapolate the results from humans to earlier hominins. It is shown that the molar teeth of sea otters have considerably thinner enamel than those of humans, making sea otter molars more susceptible to certain kinds of fractures. At the same time, the base diameter of sea otter first molars is larger, diminishing the fracture susceptibility in a compensatory manner. We also conduct nanoindentation tests to map out elastic modulus and hardness of sea otter and human molars through a section thickness, and microindentation tests to measure toughness. We find that while sea otter enamel is just as stiff elastically as human enamel, it is a little softer and tougher. The role of these material factors in the capacity of dentition to resist fracture and deformation is considered. From such comparisons, we argue that early hominin species like Paranthropus most likely consumed hard food objects with substantially higher biting forces than those exerted by modern humans.

Fundamental mechanics of tooth fracture and wear: implications for humans and other primates.

Until recently, there had been little attempt in the literature to identify and quantify the underlying mechanics of tooth durability in terms of materials engineering concepts. In humans and most mammals, teeth must endure a lifetime of sustained occlusal mastication-they have to resist fracture and wear. It is well documented that teeth are resilient, but what are the unique features that make this possible? The present article surveys recent materials engineering research aimed at addressing this fundamental question. Elements that determine the mechanics and micromechanics of tooth fracture and wear are analysed: at the macrostructural level, the geometry of the enamel shell and cuspal configuration; and at the microstructural level, interfacial weakness and property gradients. Inferences concerning dietary history in relation to evolutionary pressures are discussed.

Tooth chipping can reveal the diet and bite forces of fossil hominins.

Mammalian tooth enamel is often chipped, providing clear evidence for localized contacts with large hard food objects. Here, we apply a simple fracture equation to estimate peak bite forces directly from chip size. Many fossil hominins exhibit antemortem chips on their posterior teeth, indicating their use of high bite forces. The inference that these species must have consumed large hard foods such as seeds is supported by the occurrence of similar chips among known modern-day seed predators such as orangutans and peccaries. The existence of tooth chip signatures also provides a way of identifying the consumption of rarely eaten foods that dental microwear and isotopic analysis are unlikely to detect.

Dental enamel as a dietary indicator in mammals.

The considerable variation in shape, size, structure and properties of the enamel cap covering mammalian teeth is a topic of great evolutionary interest. No existing theories explain how such variations might be fit for the purpose of breaking food particles down. Borrowing from engineering materials science, we use principles of fracture and deformation of solids to provide a quantitative account of how mammalian enamel may be adapted to diet. Particular attention is paid to mammals that feed on 'hard objects' such as seeds and dry fruits, the outer casings of which appear to have evolved structures with properties similar to those of enamel. These foods are important in the diets of some primates, and have been heavily implicated as a key factor in the evolutionary history of the hominin clade. As a tissue with intrinsic weakness yet exceptional durability, enamel could be especially useful as a dietary indicator for extinct taxa.

Phytoliths can cause tooth wear.

Comparative laboratory sliding wear tests on extracted human molar teeth in artificial saliva with third-body particulates demonstrate that phytoliths can be as effective as silica grit in the abrasion of enamel. A pin-on-disc wear testing configuration is employed, with an extracted molar cusp as a pin on a hard disc antagonist, under loading conditions representative of normal chewing forces. Concentrations and sizes of phytoliths in the wear test media match those of silica particles. Cusp geometries and ensuing abrasion volumes are measured by digital profilometry. The wear data are considered in relation to a debate by evolutionary biologists concerning the relative capacities of intrinsic mineral bodies within plant tissue and exogenous grit in the atmosphere to act as agents of tooth wear in various animal species.

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.

The influence of fallback foods on great ape tooth enamel.

Lucas and colleagues recently proposed a model based on fracture and deformation concepts to describe how mammalian tooth enamel may be adapted to the mechanical demands of diet (Lucas et al.: Bioessays 30 2008 374-385). Here we review the applicability of that model by examining existing data on the food mechanical properties and enamel morphology of great apes (Pan, Pongo, and Gorilla). Particular attention is paid to whether the consumption of fallback foods is likely to play a key role in influencing great ape enamel morphology. Our results suggest that this is indeed the case. We also consider the implications of this conclusion on the evolution of the dentition of extinct hominins.