Dental microwear and diet of the Plio-Pleistocene hominin Paranthropus boisei

The Plio-Pleistocene hominin Paranthropus boisei had enormous, flat, thickly enameled cheek teeth, a robust cranium and mandible, and inferred massive, powerful chewing muscles. This specialized morphology, which earned P. boisei the nickname "Nutcracker Man", suggests that this hominin could have consumed very mechanically challenging foods. It has been recently argued, however, that specialized hominin morphology may indicate adaptations for the consumption of occasional fallback foods rather than preferred resources. Dental microwear offers a potential means by which to test this hypothesis in that it reflects actual use rather than genetic adaptation. High microwear surface texture complexity and anisotropy in extant primates can be associated with the consumption of exceptionally hard and tough foods respectively. Here we present the first quantitative analysis of dental microwear for P. boisei. Seven specimens examined preserved unobscured antemortem molar microwear. These all show relatively low complexity and anisotropy values. This suggests that none of the individuals consumed especially hard or tough foods in the days before they died. The apparent discrepancy between microwear and functional anatomy is consistent with the idea that P. boisei presents a hominin example of Liem's Paradox, wherein a highly derived morphology need not reflect a specialized diet.     

Experimental perspective on fallback foods and dietary adaptations in early hominins

The robust jaws and large, thick-enameled molars of the Plio–Pleistocene hominins Australopithecus and Paranthropus have long been interpreted as adaptations for hard-object feeding. Recent studies of dental microwear indicate that only Paranthropus robustus regularly ate hard items, suggesting that the dentognathic anatomy of other australopiths reflects rare, seasonal exploitation of hard fallback foods. Here, we show that hard-object feeding cannot explain the extreme morphology of Paranthropus boisei. Rather, analysis of long-term dietary plasticity in an animal model suggests year-round reliance on tough foods requiring prolonged postcanine processing in P. boisei. Increased consumption of such items may have marked the earlier transition from Ardipithecus to Australopithecus, with routine hard-object feeding in P. robustus representing a novel behaviour.     

Seasonal Mortality Patterns in Primates: Implications for the Interpretation of Dental Microwear

The microscopic traces of use wear on teeth have been extensively studied to provide information that will assist in elucidating the dietary habits of extinct hominin species. 1 - 13 It has been amply documented that dental microwear provides information pertaining to diet for living animals, where there is a strong and consistent association between dental microwear patterns and different types of foods that are chewed. The details of occlusal surface wear patterns are capable of distinguishing among diets when the constituent food items differ in their fracture properties. 14 - 20 For example, the microwear traces left on the teeth of mammals that crush hard, brittle foods such as nuts are generally dominated by pits, whereas traces left on the teeth of mammals that shear tough items such as leaves tend to be characterized by scratches. These microwear features result from and thus record actual chewing events. As such, microwear patterns are expected to be variably ephemeral, as individual features are worn away and replaced or overprinted by others as the tooth wears down in subsequent bouts of mastication. Indeed, it has been demonstrated, both in the laboratory and the wild, that short‐term dietary variation can result in the turnover of microwear. 17 , 21 - 23 Because occlusal microwear potentially reflects an individual's diet for a short time (days, weeks, or months, depending on the nature of the foods being masticated), tooth surfaces sampled at different times will display differences that relate to temporal (for example, seasonal) differences in diet. 24     

Dental microwear texture and anthropoid diets

Dental microwear has long been used as evidence concerning the diets of extinct species. Here, we present a comparative baseline series of dental microwear textures for a sample of 21 anthropoid primate species displaying interspecific and intraspecific dietary variability. Four dental microwear texture variables (complexity, anisotropy, textural fill volume, and heterogeneity) were computed based on scale-sensitive fractal analysis and high-resolution three-dimensional renderings of microwear surfaces collected using a white-light confocal profiler. The purpose of this analysis was to assess the extent to which these variables reflect variation in diet. Significant contrasts between species with diets known to include foods with differing material properties are clearly evident for all four microwear texture variables. In particular, species that consume more tough foods, such as leaves, tended to have high levels of anisotropy and low texture complexity. The converse was true for species including hard and brittle items in their diets either as staples or as fallback foods. These results reaffirm the utility of dental microwear texture analysis as an important tool in making dietary inferences based on fossil primate samples.     

Playing 'possum: A microwear experiment

A recent experiment to evaluate the reliability of dental microwear as an indicator of diet seems to show that differences in diets fed to laboratory animals are not reflected by their tooth wear. We feel that these results are misleading, and reflect not so much the limits of microwear analysis per se, but rather result from the problems of design and execution inherent in any experimental simulation of natural feeding behavior. The experiment in question was flawed in several respects, and we think that changes in the methods and assumptions of the study are necessary before the experimental approach can yield meaningful results with which to test hypotheses about microwear analyses.     

Dietary Abrasiveness Is Associated with Variability of Microwear and Dental Surface Texture in Rabbits

Dental microwear and 3D surface texture analyses are useful in reconstructing herbivore diets, with scratches usually interpreted as indicators of grass dominated diets and pits as indicators of browse. We conducted feeding experiments with four groups of rabbits (Oryctolagus cuniculus) each fed a different uniform, pelleted diet (lucerne, lucerne & oats, grass & oats, grass). The lowest silica content was measured in the lucerne and the highest in the grass diet. After 25 weeks of exposure to the diets, dental castings were made of the rabbit''s lower molars. Occlusal surfaces were then investigated using dental microwear and 3D areal surface texture analysis. In terms of traditional microwear, we found our hypothesis supported, as the grass group showed a high proportion of (long) “scratches” and the lucerne group a high proportion of “pits”. Regardless of the uniform diets, variability of microwear and surface textures was higher when silica content was low. A high variability in microwear and texture analysis thus need not represent dietary diversity, but can also be related to a uniform, low-abrasion diet. The uniformity or variability of microwear/texture analysis results thus might represent varying degrees of abrasion and attrition rather than a variety of diet items per se.     

Viewpoints: Feeding mechanics,diet, and dietary adaptations in early hominins

Inference of feeding adaptation in extinct species is challenging, and reconstructions of the paleobiology of our ancestors have utilized an array of analytical approaches. Comparative anatomy and finite element analysis assist in bracketing the range of capabilities in taxa, while microwear and isotopic analyses give glimpses of individual behavior in the past. These myriad approaches have limitations, but each contributes incrementally toward the recognition of adaptation in the hominin fossil record. Microwear and stable isotope analysis together suggest that australopiths are not united by a single, increasingly specialized dietary adaptation. Their traditional (i.e., morphological) characterization as “nutcrackers” may only apply to a single taxon, Paranthropus robustus. These inferences can be rejected if interpretation of microwear and isotopic data can be shown to be misguided or altogether erroneous. Alternatively, if these sources of inference are valid, it merely indicates that there are phylogenetic and developmental constraints on morphology. Inherently, finite element analysis is limited in its ability to identify adaptation in paleobiological contexts. Its application to the hominin fossil record to date demonstrates only that under similar loading conditions, the form of the stress field in the australopith facial skeleton differs from that in living primates. This observation, by itself, does not reveal feeding adaptation. Ontogenetic studies indicate that functional and evolutionary adaptation need not be conceptually isolated phenomena. Such a perspective helps to inject consideration of mechanobiological principles of bone formation into paleontological inferences. Finite element analysis must employ such principles to become an effective research tool in this context. Am J Phys Anthropol 151:356–371, 2013.© 2013 Wiley Periodicals, Inc.     

Hominins, sedges, and termites: new carbon isotope data from the Sterkfontein valley and Kruger National Park

Stable carbon isotope analyses have shown that South African australopiths did not have exclusively frugivorous diets, but also consumed significant quantities of C4 foods such as grasses, sedges, or animals that ate these foods. Yet, these studies have had significant limitations. For example, hominin sample sizes were relatively small, leading some to question the veracity of the claim for australopith C4 consumption. In addition, it has been difficult to determine which C4 resources were actually utilized, which is at least partially due to a lack of stable isotope data on some purported australopith foods. Here we begin to address these lacunae by presenting carbon isotope data for 14 new hominin specimens, as well as for two potential C4 foods (termites and sedges). The new data confirm that non-C3 foods were heavily utilized by australopiths, making up about 40% and 35% of Australopithecus and Paranthropus diets respectively. Most termites in the savanna-woodland biome of the Kruger National Park, South Africa, have intermediate carbon isotope compositions indicating mixed C3/C4 diets. Only 28% of the sedges in Kruger were C4, and few if any had well-developed rhizomes and tubers that make some sedges attractive foods. We conclude that although termites and sedges might have contributed to the C4 signal in South African australopiths, other C4 foods were also important. Lastly, we suggest that the consumption of C4 foods is a fundamental hominin trait that, along with bipedalism, allowed australopiths to pioneer increasingly open and seasonal environments.     

Diet of upper paleolithic modern humans: Evidence from microwear texture analysis

This article presents the results of the occlusal molar microwear texture analysis of 32 adult Upper Paleolithic modern humans from a total of 21 European sites dating to marine isotope stages 3 and 2. The occlusal molar microwear textures of these specimens were analyzed with the aim of examining the effects of the climatic, as well as the cultural, changes on the diets of the Upper Paleolithic modern humans. The results of this analysis do not reveal any environmentally driven dietary shifts for the Upper Paleolithic hominins indicating that the climatic and their associated paleoecological changes did not force these humans to significantly alter their diets in order to survive. However, the microwear texture analysis does detect culturally related changes in the Upper Paleolithic humans' diets. Specifically, significant differences in diet were found between the earlier Upper Paleolithic individuals, i.e., those belonging to the Aurignacian and Gravettian contexts, and the later Magdalenian ones, such that the diet of the latter group was more varied and included more abrasive foods compared with those of the former. Am J Phys Anthropol 153:570–581, 2014. © 2014 Wiley Periodicals, Inc.     

Potential hominin plant foods in northern Tanzania: semi-arid savannas versus savanna chimpanzee sites

Savanna chimpanzees are useful as referential models for early hominins, and here potential differences between chimpanzee and early hominin ecology is the focus. Whereas chimpanzees inhabit only a handful of modern African savannas, there is evidence that early hominins occupied relatively more open and arid savannas than those in which chimpanzees live. In order to help expand potential models of early hominin palaeoecology beyond savanna chimpanzee-like scenarios, and to provide a basis for future modeling and testing of actual hominin diets, this study compares the types of plant foods available in modern semi-arid savannas of northern Tanzania to plant foods at savanna chimpanzee sites. The semi-arid savannas are not occupied by modern chimpanzees, but are potentially similar to environments occupied by some early hominins. Compared to savanna chimpanzee habitats, the northern Tanzania semi-arid savanna has a lower density and fewer species of trees that produce fleshy fruits. Additionally, the most abundant potential hominin plant foods are seasonally available Acacia seeds/pods and flowers, grass seeds, and the underground parts of marsh plants, as evidenced by vegetation surveys and by studies of the diets of baboons that forage in similar areas. The information from this study should be useful for framing hypotheses about hominin diets for sites with palaeoenvironmental contexts similar to those of the northern Tanzania semi-arid savannas and for contextualising tests of actual hominin diets (e.g., those based on dental microwear or isotopes).     

Ecogeographic variation in Neandertal dietary habits: evidence from occlusal molar microwear texture analysis

In the late Middle and early Late Pleistocene, Neandertals inhabited a wide variety of ecological zones across western Eurasia during both glacial and interglacial times. To elucidate the still poorly understood effects of climatic change on Neandertal subsistence patterns, this study employs dental microwear texture analysis to reconstruct the diets of Neandertal individuals from various sites across their wide temporal and geographic ranges. The results of this study reveal environmentally-driven differences in the diets of Neandertal groups. Significant differences in microwear signatures, correlated with paleoecological conditions, were found among Neandertal groups that lived in open, mixed, and wooded environments. In comparison to recent hunter-gatherer populations with known, yet diverse diets, the occlusal molar microwear signatures of all the Neandertal groups indicate that their diet consisted predominantly of meat. However, the results of this study suggest that plant foods did form an important part of the diet of at least some Neandertal groups (i.e., those that lived in mixed and wooded habitats). Overall, the proportion of plant foods in the Neandertal diet appears to have increased with the increase in tree cover.     

In vivo and in vitro turnover in dental microwear

Given the potential usefulness of dental microwear analyses in interpretations of archaeological and paleontological material, it is surprising how little we know about changes in individual microwear features through time. The purpose of this study was to document the turnover in primate dental microwear through in vivo dental studies of monkeys raised on different diets, and through in vitro studies of the abrasive effects of monkey chow biscuits on isolated monkey teeth. As in previous studies, epoxy replicas were prepared from dental impressions and examined under a scanning electron microscope. Results indicate that, under certain conditions, the turnover in primate dental microwear can be on the order of days, hours, or even minutes. Individual microscopic wear features can be obliterated within 24 hours on the molars of laboratory monkeys, and monkey chow biscuits can easily scratch the enamel of isolated monkey teeth. Monkeys raised on a hard diet showed more rapid turnover in dental microwear than monkeys raised on a soft diet. However, paired-sample tests revealed that, for all animals, the molar shearing facets were being abraded at a significantly slower rate than molar crushing/grinding facets. In light of these results, investigators should make every effort to use large samples in interspecific comparisons of dental microwear involving species with variable diets. Another implication of these results is that changes in dental microwear might be useful indicators of changes in oral behavior over relatively short periods of time.     

Incisor microwear of Sumatran anthropoid primates

Several studies have suggested that incisor microwear reflects diet and feeding adaptations of anthropoids. However, such studies have been largely qualitative, and interpretations have relied on anecdotal references to diet and tooth use reported in the socioecology literature. The current study relates incisor microwear in four anthropoid primates to specific ingestive behaviors and food types. Central incisor casts of wild-shot museum specimens of Hylobates lar, Macaca fascicularis, Pongo pygmaeus, and Presbytis thomasi were examined by scanning electron microscopy, and analyzed using a semiautomated image analysis procedure. Microwear patterns were used to generate predictions regarding diet and anterior tooth use. These predictions were evaluated using data collected during a 1 year study of feeding behavior of these same taxa in the wild (Ungar, 1992, 1994a, b). Results suggest that (1) enamel prism relief is associated with the effectiveness of etching reagents in foods, (2) dental calculus buildup results from a lack of incisor use and perhaps the ingestion of sugar-rich foods, (3) striation density varies with degree of anterior tooth use in the ingestion of abrasive food items, (4) striation breadth is proposed to relate to the ratio of exogenous grit to phytoliths consumed; and (5) preferred striation orientation indicates the direction that food items are pulled across the incisors during ingestion. It is concluded that incisor microwear studies can contribute to the understanding of diets and feeding behaviors of extinct primates. © 1994 Wiley-Liss, Inc.     

Technical note: An in vitro study of dental microwear formation using the BITE Master II chewing machine

Dental microwear has been used for decades to reconstruct the diets of fossil hominins and bioarchaeological populations. The basic theory has been that hard‐brittle foods (e.g., nuts, bone) require crushing and leave pits as they are pressed between opposing cheek‐tooth surfaces, whereas soft‐tough foods (e.g., grass blades, meat) require shearing and leave scratches as they are dragged along opposing surfaces that slide past one another. However, recent studies have called into question the efficacy of microwear as an indicator of diet. One issue has been the limited number of in vitro studies providing empirical evidence for associations between microwear pattern and chewing behavior. We here describe a new study using a chewing simulator, the BITE Master II, to examine the effects of angle of approach between opposing teeth and food consistency on microwear surface texture. Results indicate that opposing teeth that approach one another: 1) perpendicular to the occlusal plane (crushing) result in pits; 2) parallel to the occlusal plane (shearing) result in striations in the direction of movement; and 3) oblique to the occlusal plane (45°) result in both striations and pits. Results further suggest that different food types and abrasive loads affect the propensity to accumulate microwear features independent of feature shapes. Am J Phys Anthropol 158:769–775, 2015. © 2015 Wiley Periodicals, Inc.     

Dental microwear and diets of African early Homo

Conventional wisdom ties the origin and early evolution of the genus Homo to environmental changes that occurred near the end of the Pliocene. The basic idea is that changing habitats led to new diets emphasizing savanna resources, such as herd mammals or underground storage organs. Fossil teeth provide the most direct evidence available for evaluating this theory. In this paper, we present a comprehensive study of dental microwear in Plio-Pleistocene Homo from Africa. We examined all available cheek teeth from Ethiopia, Kenya, Tanzania, Malawi, and South Africa and found 18 that preserved antemortem microwear. Microwear features were measured and compared for these specimens and a baseline series of five extant primate species (Cebus apella, Gorilla gorilla, Lophocebus albigena, Pan troglodytes, and Papio ursinus) and two protohistoric human foraging groups (Aleut and Arikara) with documented differences in diet and subsistence strategies. Results confirmed that dental microwear reflects diet, such that hard-object specialists tend to have more large microwear pits, whereas tough food eaters usually have more striations and smaller microwear features. Early Homo specimens clustered with baseline groups that do not prefer fracture resistant foods. Still, Homo erectus and individuals from Swartkrans Member 1 had more small pits than Homo habilis and specimens from Sterkfontein Member 5C. These results suggest that none of the early Homo groups specialized on very hard or tough foods, but that H. erectus and Swartkrans Member 1 individuals ate, at least occasionally, more brittle or tough items than other fossil hominins studied.     

Functional morphology,biomechanics and the retrodiction of early hominin diets

A fundamental axiom that underlies evolutionary biomechanics maintains that natural selection has adapted skeletal and dental morphologies to facilitate function in intelligible ways. Because selection is held to result in the improvement of functional design, it is thought possible to predict the adaptive significance of a morphological feature from a design criterion. This rationale has been widely applied to the interpretation of morphological complexes in the paleontological record for which no strict extant analogues exist. In particular, biomechanical models have been used to infer the dietary habits of extinct hominin taxa from aspects of craniodental morphology. Many of these models are hampered by missing data and loosely justified assumptions. Craniodental morphologies may indicate more about what an extinct species was capable of processing intra-orally – and probably more about its phylogenetic history – than the constitution of its diet. Even a dedicated leaf-eating hominin cannot be expected to have possessed bilophodont molars. The dietary retrodictions based on comparative anatomical that have been proffered for Plio-Pleistocene hominin species are reviewed here. We argue that the application of finite element analysis to these fossils has not revealed convincing evidence of specific feeding behaviors. Indeed, the conclusions from these biomechanical models are often incongruent with data from stable light isotopes, microwear and phytolith analysis; nor do they conform with observations on the dietary repertoires and feeding behaviors of extant primates. For example, the sooty mangabey (Cercocebus atys) is a committed hard object feeder, but suffers no deleterious consequences from the “poor design” of its facial skeleton for processing hard foods. Because primates are adept at behaviorally circumventing mechanical problems, it is perhaps useful to consider the breadth of any fossil hominin's feeding repertoire in the context of behaviors that enable mechanical problems to be dealt with prior to ingestion.     

Kinematic parameters inferred from enamel microstructure: new insights into the diet of Australopithecus anamensis

The dietary adaptations of Australopithecus anamensis are contentious, with suggestions that range from soft fruits to hard, brittle, tough, and abrasive foods. It is unlikely that all propositions are equally valid, however. Here we extend recent finite element (FE) analyses of enamel microstructure (Shimizu and Macho, 2008) to enquire about the range of loading directions (i.e., kinematics) to which A. anamensis enamel microstructure/molars could safely be subjected. The rationale underlying this study is the observation that hard brittle foods are broken down in crush, while tough foods require shear. The findings are compared with those of Pan and Gorilla.Eighteen detailed FE models of enamel microstructure were created and analysed. The results highlight the uniqueness of A. anamensis dental structure and imply that mastication in this species included a greater shear component than in Pan, as well as a wider range of loading directions; it is similar to that in Gorilla in this respect. These findings are in accord with microwear studies (Grine et al., 2006a). Unlike either of the great apes, however, enamel microstructure of A. anamensis was found to be poorly equipped to withstand loading parallel to the dentino-enamel junction; such loading regimes are associated with mastication of soft fleshy fruits. This, together with broader morphological considerations, raises doubts as to whether A. anamensis was essentially a frugivore that expanded its dietary niche as a result of fluctuations in environmental conditions, e.g., during seasonal food shortages. Instead, it is more parsimonious to conclude that the habitual diet of A. anamensis differed considerably from that of either of the extant African great apes.     

Microwear evidence for Plio-Pleistocene bovid diets from Makapansgat Limeworks Cave, South Africa

Makapansgat Limeworks Cave is a well-known Australopithecus africanus bearing locality that has spawned a considerable amount of paleoecological research because of its hominin component. Most recently, the paleoecology of this Plio-Pleistocene site has been studied by determining the diet and habitat of other extinct taxa, particularly the bovids. The diets of seven bovids (Aepyceros sp., Gazella vanhoepeni, Makapania broomi, Parmularius braini, Redunca darti, Tragelaphus sp. aff. T. angasii, and Tragelaphus pricei) have now been classified using taxonomic uniformitarianism, ecomorphology, stable carbon isotopes, and mesowear analysis. Here, dental microwear is applied to the same bovids for additional comparison and to further elucidate the strengths and weaknesses of each method. The different dietary proxy methods noted provide a temporal continuum, with genetic signals such as ecomorphology and taxonomic uniformitarianism indicating behavioral adaptations over geologic time, while nongenetic data such as stable carbon isotopes and mesowear reflect different aspects of average diet over extended portions of an animal's life, and dental microwear provides dietary snapshots.Microwear separated an extant baseline of ten bovid species into expected dietary categories and the Makapansgat bovids clearly fell into two groups with the same degree of separation as between extant grazers and browsers. The results indicate that a multidisciplinary approach produces a more accurate and robust reconstruction of past diets. In sum, the microwear analysis is in-line with the isotope and mesowear results, which suggest a stronger browsing component than either taxonomic uniformitarianism or ecomorphology imply.     

The Hadropithecus conundrum reconsidered, with implications for interpreting diet in fossil hominins

The fossil 'monkey lemur' Hadropithecus stenognathus has long excited palaeontologists because its skull bears an astonishing resemblance to those of robust australopiths, an enigmatic side branch of the human family tree. Multiple lines of evidence point to the likelihood that these australopiths ate at least some 'hard', stress-limited food items, but conflicting data from H. stenognathus pose a conundrum. While its hominin-like craniofacial architecture is suggestive of an ability to generate high bite forces, details of its tooth structure suggest that it was not well equipped to withstand the forces imposed by cracking hard objects. Here, we use three-dimensional digital reconstructions and finite-element analysis to test the hard-object processing hypothesis. We show that Archaeolemur sp. cf. A. edwardsi, a longer-faced close relative of H. stenognathus that lacked hominin convergences, was probably capable of breaking apart large, stress-limited food items, while Hadropithecus was better suited to processing small, displacement-limited (tougher but more compliant) foods. Our suggestion that H. stenognathus was not a hard-object feeder has bearing on the interpretation of hominin cranial architecture; the features shared by H. stenognathus and robust australopiths do not necessarily reflect adaptations for hard-object processing.     

Technical note: Dental microwear textures of "Phase I" and "Phase II" facets

The power stroke of mastication has been traditionally divided into two parts, one which precedes centric occlusion, and the other which follows it-"Phase I" and "Phase II," respectively. Recent studies of primate mastication have called into question the role of Phase II in food processing, as they have found little muscle activity or accompanying bone strain following centric occlusion. That said, many researchers today look to Phase II facets to relate diet to patterns of dental microwear. This suggests the need to reevaluate microwear patterns on Phase I facets. Here we use texture analysis to compare and contrast microwear on facets representing both phases in three primate species with differing diets (Alouatta palliata, Cebus apella, and Lophocebus albigena). Results reaffirm that microwear patterns on Phase II facets better distinguish taxa with differing diets than do those on Phase I facets. Further, differences in microwear textures between facet types for a given taxon may themselves reflect diet. Some possible explanations for differences in microwear textures between facet types are proposed.