Structure and scale of the mechanics of mammalian dental enamel viewed from an evolutionary perspective.

Mammalian enamel, the contact dental tissue, is something of an enigma. It is almost entirely made of hydroxyapatite, yet exhibits very different mechanical behavior to a homogeneous block of the same mineral. Recent approaches suggest that its hierarchical composite form, similar to other biological hard tissues, leads to a mechanical performance that depends very much on the scale of measurement. The stiffness of the material is predicted to be highest at the nanoscale, being sacrificed to produce a high toughness at the largest scale, that is, at the level of the tooth crown itself. Yet because virtually all this research has been conducted only on human (or sometimes "bovine") enamel, there has been little regard for structural variation of the tissue considered as evolutionary adaptation to diet. What is mammalian enamel optimized for? We suggest that there are competing selective pressures. We suggest that the structural characteristics that optimize enamel to resist large-scale fractures, such as crown failures, are very different to those that resist wear (small-scale fracture). While enamel is always designed for damage tolerance, this may be suboptimal in the enamel of some species, including modern humans (which have been the target of most investigations), in order to counteract wear. The experimental part of this study introduces novel techniques that help to assess resistance at the nanoscale.

Novel developments in field mechanics.

Our aim is general: we want to illustrate how much can be gleaned from mechanical measurement in the field. We ask how mechanics may constrain foraging and feeding on both plants and animals, and how various aspects of mechanical behavior could affect the feeding choices that primates make. Here, we present novel methods for the measurement of the material properties and also the employment of tried and tested methods in novel settings. This review demonstrates how mechanical investigation methods can quantify the environmental factors affecting primate locomotion to and from food, which makes up a large part of a primate's daily energy budget. We indicate that, despite the accumulation of much data on the material properties of primate foods, the introduction of new methods is allowing researchers to pursue new avenues of research and change paradigms in primate feeding ecology. Field methods are presented that could aid in the understanding of the extra-oral processing of foodstuffs by primates and enrich further studies into cognition and culture surrounding these types of behavior. We conclude that the use of in-field measurements and a greater understanding of the physics of primate environments are vital and exciting themes integral to the continued understanding of primate evolution and biology.

Membrane-plate transition in leaves as an influence on dietary selectivity and tooth form.

Primates need accurate sensory signals about food quality to forage efficiently. Current evidence suggests that they target leaf foods based on color at long-range, reinforcing this with post-ingestive sensations relating to leaf toughness evoked during chewing. Selection against tough leaves effectively selects against high fiber content, which in turn gives a greater opportunity of acquiring protein. Here we consider a novel intermediate mechanical factor that could aid a folivore: leaves may transform mechanically from membranes (sheets that cannot maintain their shape under gravitational loads and thus 'flop') early on in development into plates (that can maintain their shape) as they mature. This transformation can be detected visually. Mechanical tests on two species of leaf eaten by southern muriqui monkeys (Brachyteles arachnoides) in Southern Atlantic Forest, Brazil, support a membrane-to-plate shift in turgid leaves during their development. A measure of this mechanical transition, termed lambda (λ), was found to correlate with both leaf color and toughness, thus supporting a potential role in leaf selection. Muriquis appear to select membranous leaves, but they also eat leaves that are plate-like. We attribute this to the degree of cresting of their molar teeth. A dietary choice restricted to membranous leaves might typify the type of 'fallback' leaf that even frugivorous primates will target because membranes of low toughness are relatively easily chewed. This may be relevant to the diets of hominins because these lack the bladed postcanine teeth seen in mammals with a specialized folivorous diet. We suggest that mammals with such dental adaptations can consume tougher leaf 'plates' than others.

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.

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.

Stiffness characteristics of splints for fixation of traumatized teeth.

BACKGROUND/AIM: Traumatic dental injuries (TDI) are treated by repositioning and splinting. Ideally, injured teeth should possess some mobility for optimal periodontal and pulp healing. Splints should be easy to apply in emergencies, affordable, and esthetically acceptable. The aims were to compare some clinically used splints with regard to stiffness (measured in Nm(-1)), esthetics, cost, and ease of application. MATERIALS AND METHODS: Six splints were applied to dental models using an acid-etched bonding technique. One central incisor was adjusted to give 1 mm of horizontal movement at the incisal edge. The mobilized tooth was then connected to adjacent teeth with either twistflex wire (TF), titanium trauma splint (TTS), single (SFG) and double fiberglass (DFG), nylon (fishing) line (FL), or power chain (PC). A horizontal force was then gradually applied to the incisor in a standardized manner with a spherical probe (1.65 mm radius), monitoring force with a 50N load cell and displacement with a linear variable differential transformer (LVDT). Signals were amplified, converted digitally (14-bit analog-to-digital converter), and displayed in real time to show the splint stiffness. Splints were also ranked with regard to esthetics, application time needed, and ease of application cost. RESULTS: FL and PC were the least stiff, averaging 5.7 and 6.3 Nm(-1), respectively. TTS averaged 6.9 Nm(-1), while SFG and TF averaged 18.5 and 18.4 Nm(-1), respectively. DFG was the stiffest, averaging 24.3 Nm(-1). PC and SFG were the fastest to apply. FL showed the best esthetic score, followed by TTS and PC. TTS was the most expensive splint, while FL, PC, SFG, DFG, and TF showed similar costs. CONCLUSIONS: Of these TDI splints, DFG should be avoided for flexible splinting because it is too stiff. PC may be an interesting novel alternative, affording sufficient mobility due to its low stiffness.

The wear and tear of teeth.

A review is presented of the mechanical damage suffered by tooth crowns. This has been the subject of much recent research, resulting in a need to revise some of the thinking about the mechanisms involved. Damage is classified here by scale into macro-, meso- and microfracture. The focus is on the outer enamel coat because this is the contact tissue and where most fractures start. Enamel properties appear to be tailored to maximize hardness, but also to prevent fracture. The latter is achieved by the deployment of developmental flaws called enamel tufts. Macrofractures usually appear to initiate as extensions of tufts on the undersurface of the enamel adjacent to the enamel-dentine junction and extend from there into the enamel. Cracks that pass from the tooth surface tend to be deflected by an enamel region of high toughness; if they find the surface again, a chip (mesofracture) is produced. The real protection of the enamel-dentine junction here is the layer of decussating inner enamel. Finally, a novel analysis of mechanical wear (microfracture) suggests that the local toughness of the enamel is very important to its ability to resist tissue loss. Enamel and dentine have contrasting behaviours. Seen on a large scale, dentine is isotropic (behaving similarly in all directions) while enamel is anisotropic, but vice versa on a very small scale. These patterns have implications for anyone studying the fracture behaviour of teeth.

Food material properties and early hominin processing techniques.

Although early Homo is hypothesized to have used tools more than australopiths to process foods prior to consumption, it is unknown how much the food processing techniques they used altered the material properties of foods, and therefore the masticatory forces they generated, and how well they were able to comminute foods. This study presents experimental data on changes to food material properties caused by mechanical tenderization (pounding with a stone tool) and cooking (dry roasting) of two foods likely to have been important components of the hominin diet: meat and tubers. Mechanical tenderization significantly decreased tuber toughness by 42%, but had no effect on meat toughness. Roasting significantly decreased several material properties of tubers correlated with masticatory effort including toughness (49%), fracture stress (28%) and elastic modulus (45%), but increased the toughness (77%), fracture stress (50%-222%), and elastic modulus of muscle fibers in meat (308%). Despite increasing many material properties of meat associated with higher masticatory forces, roasting also decreased measured energy loss by 28%, which likely makes it easier to chew. These results suggest that the use of food processing techniques by early Homo probably differed for meat and tubers, but together would have reduced masticatory effort, helping to relax selection to maintain large, robust faces and large, thickly enameled teeth.

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.

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.

How cellulose-based leaf toughness and lamina density contribute to long leaf lifespans of shade-tolerant species.

Cell wall fibre and lamina density may interactively affect leaf toughness and leaf lifespan. Here, we tested this with seedlings of 24 neotropical tree species differing in shade tolerance and leaf lifespan under standardized field conditions (140-867 d in gaps; longer in shade). We quantified toughness with a cutting test, explicitly seeking a mechanistic linkage to fibre. Lamina density, but not fracture toughness, exhibited a plastic response to gaps vs shade, while neither trait was affected by leaf age. Toughness corrected for lamina density, a recently recognized indicator of material strength per unit mass, was linearly correlated with cellulose content per unit dry mass. Leaf lifespan was positively correlated with cellulose and toughness in shade-tolerant species but only weakly in gap-dependent species. Leaf lifespan was uncorrelated with lamina thickness, phenolics and tannin concentrations. In path analysis including all species, leaf lifespan was directly enhanced by density and toughness, and indirectly by cellulose via its effect on toughness. Different suites of leaf traits were correlated with early seedling survival in gaps vs shade. In conclusion, cellulose and lamina density jointly enhance leaf fracture toughness, and these carbon-based physical traits, rather than phenolic-based defence, explain species differences in herbivory, leaf lifespan and shade survival.

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.

Global patterns of leaf mechanical properties.

Leaf mechanical properties strongly influence leaf lifespan, plant-herbivore interactions, litter decomposition and nutrient cycling, but global patterns in their interspecific variation and underlying mechanisms remain poorly understood. We synthesize data across the three major measurement methods, permitting the first global analyses of leaf mechanics and associated traits, for 2819 species from 90 sites worldwide. Key measures of leaf mechanical resistance varied c. 500-800-fold among species. Contrary to a long-standing hypothesis, tropical leaves were not mechanically more resistant than temperate leaves. Leaf mechanical resistance was modestly related to rainfall and local light environment. By partitioning leaf mechanical resistance into three different components we discovered that toughness per density contributed a surprisingly large fraction to variation in mechanical resistance, larger than the fractions contributed by lamina thickness and tissue density. Higher toughness per density was associated with long leaf lifespan especially in forest understory. Seldom appreciated in the past, toughness per density is a key factor in leaf mechanical resistance, which itself influences plant-animal interactions and ecosystem functions across the globe.

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.

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.