Mechanical compensation in the evolution of the early hominin feeding apparatus.

Australopiths, a group of hominins from the Plio-Pleistocene of Africa, are characterized by derived traits in their crania hypothesized to strengthen the facial skeleton against feeding loads and increase the efficiency of bite force production. The crania of robust australopiths are further thought to be stronger and more efficient than those of gracile australopiths. Results of prior mechanical analyses have been broadly consistent with this hypothesis, but here we show that the predictions of the hypothesis with respect to mechanical strength are not met: some gracile australopith crania are as strong as that of a robust australopith, and the strength of gracile australopith crania overlaps substantially with that of chimpanzee crania. We hypothesize that the evolution of cranial traits that increased the efficiency of bite force production in australopiths may have simultaneously weakened the face, leading to the compensatory evolution of additional traits that reinforced the facial skeleton. The evolution of facial form in early hominins can therefore be thought of as an interplay between the need to increase the efficiency of bite force production and the need to maintain the structural integrity of the face.

Unexpected hard-object feeding in Western lowland gorillas.

OBJECTIVES: Gorilla diets are characterized by large amounts of fruit and tough fibrous plant material. Hard-object feeding is not generally associated with this genus as the high crests on their molar teeth would be at risk of damage from the mechanically challenging woody endocarp. This study aims to demonstrate that at least one population of western lowland gorillas are seasonal hard-object feeders, orally processing the seeds of Coula edulis. MATERIALS AND METHODS: Feeding behavior of habituated western lowland gorillas and phenology of fruiting trees was observed over a 4-year period to determine the extent they exploited the seeds of C. edulis. Additionally, the endocarps of C. edulis were subjected to testing to determine their mechanical properties. RESULTS: Our results demonstrate that during the fruiting season (January, February, and December) gorillas consistently opened the seeds of C. edulis using their postcanine dentition. The protective endocarp is composed of a very stiff material, presenting a substantial mechanical challenge to a gorilla. However, the high ratio between elastic modulus and toughness will facilitate brittle, cataclysmic fracture of the seed shell given a high enough load. DISCUSSION: Although a rich energy source, C. edulis likely tax gorilla dentitions to their upper limit. The rarity of such behavior at sites where it could be observed may indicate a degree of social learning or culture driving its occurrence. This shows a greater breadth of gorilla diets than previously described and suggests gorillas may be a useful model for interpreting the dietary mechanics that necessitated robust craniodental morphology in australopiths.

Taking a big bite: Working together to better understand the evolution of feeding in primates.

The study of adaptation requires the integration of an array of different types of data. A single individual can find such integration daunting, if not impossible. In an effort to clarify the role of diet in the evolution of the primate craniofacial and dental apparatus, we assembled a team of researchers that have various types and degrees of expertise. This interaction has provided a range of insights for all contributors, and this has helped to refine questions, clarify the possibilities and limitations that laboratory and field settings offer, and further explore the ways in which laboratory and field data can be suitably integrated. A complete and accurate picture of dietary adaptation cannot be gained in isolation. Collaboration provides the bridge to a more holistic view of primate biology and evolution.

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.

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.

Feeding and oral processing behaviors of two colobine monkeys in Tai Forest, Ivory Coast.

We collected frequency data on oral processing behaviors during feeding in habituated groups of Western red colobus, Piliocolobus badius, and Western black and white, Colobus polykomos, ranging in the Ivory Coast's Tai National Park. During the sampling period, the diet of red colobus consisted of approximately 75% leaves compared to approximately 47% leaves and buds in black and white colobus. Black and white colobus chewed more frequently per ingestive event than did red colobus. Black and white colobus also employed their anterior teeth much more frequently than did red colobus, a difference attributed to the frequent consumption by C. polykomos of Pentaclethra macrophylla seeds and pods. A material analysis of these food items reveals that both the seed coating and seed flesh are quite soft; however, the pod housing the seeds is very tough. We argue that the pod's toughness, geometry, and fiber orientation collectively result in a food that is very difficult to process, resulting in long handling times and frequent, aggressive use of the incisors. We compare these data with those collected on another Tai primate-the sooty mangabey, Cercocebus atys-and demonstrate that during feeding, both colobine species use their incisors less than the mangabey, but that the cercopithecine chews less than either colobine. Combining data on oral processing behaviors with those on the material properties of items being ingested should lead to more informed interpretations of dentognathic morphology.

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.

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.

Ingestive behaviors in bearded capuchins (Sapajus libidinosus).

The biomechanical and adaptive significance of variation in craniodental and mandibular morphology in fossil hominins is not always clear, at least in part because of a poor understanding of how different feeding behaviors impact feeding system design (form-function relationships). While laboratory studies suggest that ingestive behaviors produce variable loading, stress, and strain regimes in the cranium and mandible, understanding the relative importance of these behaviors for feeding system design requires data on their use in wild populations. Here we assess the frequencies and durations of manual, ingestive, and masticatory behaviors from more than 1400 observations of feeding behaviors video-recorded in a wild population of bearded capuchins (Sapajus libidinosus) at Fazenda Boa Vista in Piauí, Brazil. Our results suggest that ingestive behaviors in wild Sapajus libidinosus were used for a range of food material properties and typically performed using the anterior dentition. Coupled with previous laboratory work indicating that ingestive behaviors are associated with higher mandibular strain magnitudes than mastication, these results suggest that ingestive behaviors may play an important role in craniodental and mandibular design in capuchins and may be reflected in robust adaptations in fossil hominins.

Hard plant tissues do not contribute meaningfully to dental microwear: evolutionary implications.

Reconstructing diet is critical to understanding hominin adaptations. Isotopic and functional morphological analyses of early hominins are compatible with consumption of hard foods, such as mechanically-protected seeds, but dental microwear analyses are not. The protective shells surrounding seeds are thought to induce complex enamel surface textures characterized by heavy pitting, but these are absent on the teeth of most early hominins. Here we report nanowear experiments showing that the hardest woody shells - the hardest tissues made by dicotyledonous plants - cause very minor damage to enamel but are themselves heavily abraded (worn) in the process. Thus, hard plant tissues do not regularly create pits on enamel surfaces despite high forces clearly being associated with their oral processing. We conclude that hard plant tissues barely influence microwear textures and the exploitation of seeds from graminoid plants such as grasses and sedges could have formed a critical element in the dietary ecology of hominins.

The Materials of Mastication: Material Science of the Humble Tooth.

Dental functional morphology, as a field, represents a confluence of materials science and biology. Modern methods in materials testing have been influential in driving the understanding of dental tissues and tooth functionality. Here we present a review of dental enamel, the outermost tissue of teeth. Enamel is the hardest biological tissue and exhibits remarkable resilience even when faced with a variety of mechanical threats. In the light of recent work, we progress the argument that the risk of mechanical degradation across multiple scales exhibits a strong and continued selection pressure on the structural organization of enamel. The hierarchical nature of enamel structure presents a range of scale-dependent toughening mechanisms and provides a means by which natural selection can drive the specialization of this tissue from nanoscale reorganization to whole tooth morphology. There has been much learnt about the biomechanics of enamel recently, yet our understanding of the taxonomic diversity of this tissue is still lacking and may form an interesting avenue for future research.

Food mechanical properties and isotopic signatures in forest versus savannah dwelling eastern chimpanzees.

Chimpanzees are traditionally described as ripe fruit specialists with large incisors but relatively small postcanine teeth, adhering to a somewhat narrow dietary niche. Field observations and isotopic analyses suggest that environmental conditions greatly affect habitat resource utilisation by chimpanzee populations. Here we combine measures of dietary mechanics with stable isotope signatures from eastern chimpanzees living in tropical forest (Ngogo, Uganda) and savannah woodland (Issa Valley, Tanzania). We show that foods at Issa can present a considerable mechanical challenge, most saliently in the external tissues of savannah woodland plants compared to their tropical forest equivalents. This pattern is concurrent with different isotopic signatures between sites. These findings demonstrate that chimpanzee foods in some habitats are mechanically more demanding than previously thought, elucidating the broader evolutionary constraints acting on chimpanzee dental morphology. Similarly, these data can help clarify the dietary mechanical landscape of extinct hominins often overlooked by broad C3/C4 isotopic categories.

Evidence that metallic proxies are unsuitable for assessing the mechanics of microwear formation and a new theory of the meaning of microwear.

Mammalian tooth wear research reveals contrasting patterns seemingly linked to diet: irregularly pitted enamel surfaces, possibly from consuming hard seeds, versus roughly aligned linearly grooved surfaces, associated with eating tough leaves. These patterns are important for assigning diet to fossils, including hominins. However, experiments establishing conditions necessary for such damage challenge this paradigm. Lucas et al. (Lucas et al. 2013 J. R. Soc. Interface10, 20120923. (doi:10.1098/rsif.2012.0923)) slid natural objects against enamel, concluding anything less hard than enamel would rub, not abrade, its surface (producing no immediate wear). This category includes all organic plant matter. Particles harder than enamel, with sufficiently angular surfaces, could abrade it immediately, prerequisites that silica/silicate particles alone possess. Xia et al. (Xia, Zheng, Huang, Tian, Chen, Zhou, Ungar, Qian. 2015 Proc. Natl Acad. Sci. USA112, 10 669-10 672. (doi:10.1073/pnas.1509491112)) countered with experiments using brass and aluminium balls. Their bulk hardness was lower than enamel, but the latter was abraded. We examined the ball exteriors to address this discrepancy. The aluminium was surfaced by a thin rough oxide layer harder than enamel. Brass surfaces were smoother, but work hardening during manufacture gave them comparable or higher hardness than enamel. We conclude that Xia et al.'s results are actually predicted by the mechanical model of Lucas et al. To explain wear patterns, we present a new model of textural formation, based on particle properties and presence/absence of silica(tes).

Dental abrasion as a cutting process.

A mammalian tooth is abraded when a sliding contact between a particle and the tooth surface leads to an immediate loss of tooth tissue. Over time, these contacts can lead to wear serious enough to impair the oral processing of food. Both anatomical and physiological mechanisms have evolved in mammals to try to prevent wear, indicating its evolutionary importance, but it is still an established survival threat. Here we consider that many wear marks result from a cutting action whereby the contacting tip(s) of such wear particles acts akin to a tool tip. Recent theoretical developments show that it is possible to estimate the toughness of abraded materials via cutting tests. Here, we report experiments intended to establish the wear resistance of enamel in terms of its toughness and how friction varies. Imaging via atomic force microscopy (AFM) was used to assess the damage involved. Damage ranged from pure plastic deformation to fracture with and without lateral microcracks. Grooves cut with a Berkovich diamond were the most consistent, suggesting that the toughness of enamel in cutting is 244 J m(-2), which is very high. Friction was higher in the presence of a polyphenolic compound, indicating that this could increase wear potential.

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.