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. Am J Phys Anthropol 151:339–355, 2013.© 2013 Wiley Periodicals, Inc.     

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.     

Evidence for dietary niche separation based on infraorbital foramen size variation among subfossil lemurs

The size of the infraorbital foramen (IOF) has been used in drawing both phylogenetic and ecological inferences regarding fossil taxa. Within the order Primates, frugivores have relatively larger IOFs than folivores or insectivores. This study uses relative IOF size in lemurs to test prior trophic inferences for subfossil lemurs and to explore the pattern of variation within and across lemur families. The IOFs of individuals belonging to 12 extinct lemur species were measured and compared to those of extant Malagasy strepsirhines. Observations matched expectations drawn from more traditional approaches (e.g. dental morphology and microwear, stable isotope analysis) remarkably well. We confirm that extinct lemurs belonging to the families Megaladapidae and Palaeopropithecidae were predominantly folivorous and that species belonging to the genus Pachylemur (Lemuridae) were frugivores. Very high values for relative IOF area in Archaeolemur support frugivory but are also consistent with omnivory, as certain omnivores use facial touch cues while feeding. These results provide additional evidence that the IOF can be used as an informative osteological feature in both phylogenetic and paleoecological interpretations of the fossil record.     

The carbon isotope ecology and diet of Australopithecus africanus at Sterkfontein,South Africa

The stable carbon isotope ratio of fossil tooth enamel carbonate is determined by the photosynthetic systems of plants at the base of the animal's foodweb. In subtropical Africa, grasses and many sedges have C(4)photosynthesis and transmit their characteristically enriched 13C/(12)C ratios (more positive delta13C values) along the foodchain to consumers. We report here a carbon isotope study of ten specimens of Australopithecus africanus from Member 4, Sterkfontein (ca. 2.5 to 2.0Ma), compared with other fossil mammals from the same deposit. This is the most extensive isotopic study of an early hominin species that has been achieved so far. The results show that this hominin was intensively engaged with the savanna foodweb and that the dietary variation between individuals was more pronounced than for any other early hominin or non-human primate species on record. Suggestions that more than one species have been incuded in this taxon are not supported by the isotopic evidence. We conclude that Australopithecus africanus was highly opportunistic and adaptable in its feeding habits.     

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.     

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.     

Dental microwear texture analysis and diet in the Dmanisi hominins

Reconstructions of foraging behavior and diet are central to our understanding of fossil hominin ecology and evolution. Current hypotheses for the evolution of the genus Homo invoke a change in foraging behavior to include higher quality foods. Recent microwear texture analyses of fossil hominin teeth have suggested that the evolution of Homo erectus may have been marked by a transition to a more variable diet. In this study, we used microwear texture analysis to examine the occlusal surface of 2 molars from Dmanisi, a 1.8 million year old fossil hominin site in the Republic of Georgia. The Dmanisi molars were characterized by a moderate degree of surface complexity (Asfc), low textural fill volume (Tfv), and a relatively low scale of maximum complexity (Smc), similar to specimens of early African H. erectus. While caution must be used in drawing conclusions from this small sample (n = 2), these results are consistent with continuity in diet as H. erectus expanded into Eurasia.     

Chimpanzee fauna isotopes provide new interpretations of fossil ape and hominin ecologies

Carbon and oxygen stable isotopes within modern and fossil tooth enamel record the aspects of an animal''s diet and habitat use. This investigation reports the first isotopic analyses of enamel from a large chimpanzee community and associated fauna, thus providing a means of comparing fossil ape and early hominin palaeoecologies with those of a modern ape. Within Kibale National Park forest, oxygen isotopes differentiate primate niches, allowing for the first isotopic reconstructions of degree of frugivory versus folivory as well as use of arboreal versus terrestrial resources. In a comparison of modern and fossil community isotopic profiles, results indicate that Sivapithecus, a Miocene ape from Pakistan, fed in the forest canopy, as do chimpanzees, but inhabited a forest with less continuous canopy or fed more on leaves. Ardipithecus, an early hominin from Ethiopia, fed both arboreally and terrestrially in a more open habitat than inhabited by chimpanzees.     

Craniofacial biomechanics and functional and dietary inferences in hominin paleontology

Finite element analysis (FEA) is a potentially powerful tool by which the mechanical behaviors of different skeletal and dental designs can be investigated, and, as such, has become increasingly popular for biomechanical modeling and inferring the behavior of extinct organisms. However, the use of FEA to extrapolate from characterization of the mechanical environment to questions of trophic or ecological adaptation in a fossil taxon is both challenging and perilous. Here, we consider the problems and prospects of FEA applications in paleoanthropology, and provide a critical examination of one such study of the trophic adaptations of Australopithecus africanus. This particular FEA is evaluated with regard to 1) the nature of the A. africanus cranial composite, 2) model validation, 3) decisions made with respect to model parameters, 4) adequacy of data presentation, and 5) interpretation of the results. Each suggests that the results reflect methodological decisions as much as any underlying biological significance. Notwithstanding these issues, this model yields predictions that follow from the posited emphasis on premolar use by A. africanus. These predictions are tested with data from the paleontological record, including a phylogenetically-informed consideration of relative premolar size, and postcanine microwear fabrics and antemortem enamel chipping. In each instance, the data fail to conform to predictions from the model. This model thus serves to emphasize the need for caution in the application of FEA in paleoanthropological enquiry. Theoretical models can be instrumental in the construction of testable hypotheses; but ultimately, the studies that serve to test these hypotheses - rather than data from the models - should remain the source of information pertaining to hominin paleobiology and evolution.     

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.     

Finite element,occlusal, microwear and microstructural analyses indicate that conodont microstructure is adapted to dental function

Conodonts constitute the earliest evidence of skeletal biomineralization in the vertebrate evolutionary lineage, manifest as a feeding apparatus of tooth‐like elements comprised of enamel‐ and dentine‐like tissues that evolved in parallel with these canonical tissues in other total‐group gnathostomes. As such, this remarkable example of evolutionary parallelism affords a natural experiment in which to explore the constraints on vertebrate skeletal evolution. Using finite element analysis, informed by occlusal and microwear analyses, we tested the hypothesis that coincidence of complex dental function and microstructural differentiation in the enamel‐like tissues of conodonts and other vertebrates is a consequence of functional adaptation. Our results show topological co‐variation in the patterns of stress distribution and crystallite orientation. In regions of high stress, such as the apex of the basal cavity and inner parts of the platform, the crown tissue comprises interwoven prisms, discontinuities between which would have acted to decussate cracks, preventing propagation. These results inform a general occlusal model for platform conodont elements and demonstrate that the complex microstructure of conodont crown tissue is an adaptation to the dental functions that the elements performed.     

PERSPECTIVE: EVOLUTIONARY PATTERNS IN THE FOSSIL RECORD

The study of large-scale evolutionary patterns in the fossil record has benefited from a diversity of approaches, including analysis of taxonomic data, ecology, geography, and morphology. Although genealogy is an important component of macroevolution, recent visions of phylogenetic analysis as replacing rather than supplementing other approaches are short-sighted. The ability of traditional Linnaean taxa to document evolutionary patterns is mainly an empirical rather than a theoretical issue, yet the use of these taxa has been dismissed without thorough evaluation of their empirical properties. Phylogenetic analysis can help compensate for some of the fossil record's imperfections. However, the shortcomings of the phylogenetic approach have not been adequately acknowledged, and we still lack a rigorous comparison between the phylogenetic approach and probabilistic approaches based on sampling theory. Important inferences about the history of life based on nongenealogical data have later been corroborated with genealogical and other analyses, suggesting that we risk an enormous loss of knowledge and understanding if we categorically dismiss nonphylogenetic data.     

Technical Note: Virtual reconstruction of KNM‐ER 1813 Homo habilis cranium

A very limiting factor for paleoanthropological studies is the poor state of preservation of the human fossil record, where fragmentation and deformation are considered normal. Although anatomical information can still be gathered from a distorted fossil, such specimens must typically be excluded from advanced morphological and morphometric analyses, thus reducing the fossil sample size and, ultimately, our knowledge of human evolution. In this contribution we provide the first digital reconstruction of the KNM‐ER 1813 Homo habilis cranium. Based on state of‐the‐art three‐dimensional digital modeling and geometric morphometric (GM) methods, the facial portion was aligned to the neurocranium, the overall distortion was removed, and the missing regions were restored. The reconstructed KNM‐ER 1813 allows for an adjustment of the anthropometric measurements gathered on the original fossil. It is suitable for further quantitative studies, such as GM analyses focused on skull morphology or for finite element analysis to explore the mechanics of early Homo feeding behavior and diet. Am J Phys Anthropol 153:154–160, 2014. © 2013 Wiley Periodicals, Inc.     

Hard-object feeding in sooty mangabeys (Cercocebus atys) and interpretation of early hominin feeding ecology

Morphology of the dentofacial complex of early hominins has figured prominently in the inference of their dietary adaptations. Recent theoretical analysis of craniofacial morphology of Australopithecus africanus proposes that skull form in this taxon represents adaptation to feeding on large, hard objects. A modern analog for this specific dietary specialization is provided by the West African sooty mangabey, Cercocebus atys. This species habitually feeds on the large, exceptionally hard nuts of Sacoglottis gabonensis, stereotypically crushing the seed casings using their premolars and molars. This type of behavior has been inferred for A. africanus based on mathematical stress analysis and aspects of dental wear and morphology. While postcanine megadontia, premolar enlargement and thick molar enamel characterize both A. africanus and C. atys, these features are not universally associated with durophagy among living anthropoids. Occlusal microwear analysis reveals complex microwear textures in C. atys unlike those observed in A. africanus, but more closely resembling textures observed in Paranthropus robustus. Since sooty mangabeys process hard objects in a manner similar to that proposed for A. africanus, yet do so without the craniofacial buttressing characteristic of this hominin, it follows that derived features of the australopith skull are sufficient but not necessary for the consumption of large, hard objects. The adaptive significance of australopith craniofacial morphology may instead be related to the toughness, rather than the hardness, of ingested foods.     

The Omo-Turkana Basin fossil hominins and their contribution to our understanding of human evolution in Africa

The Omo-Turkana Basin, including the hominin fossil sites around Lake Turkana and the sites along the lower reaches of the Omo River, has made and continues to make an important contribution to improving our murky understanding of human evolution. This review highlights the various ways the Omo-Turkana Basin fossil record has contributed to, and continues to challenge, interpretations of human evolution. Despite many diagrams that look suspiciously like comprehensive hypotheses about human evolutionary history, any sensible paleoanthropologist knows that the early hominin fossil record is too meager to do anything other than offer very provisional statements about hominin taxonomy and phylogeny. If history tells us anything, it is that we still have much to learn about the hominin clade. Thus, we summarize the current state of knowledge of the hominin species represented at the Omo-Turkana Basin sites. We then focus on three specific topics for which the fossil evidence is especially relevant: the origin and nature of Paranthropus; the origin and nature of early Homo; and the ongoing debate about whether the pattern of human evolution is more consistent with speciation by cladogenesis, with greater taxonomic diversity or with speciation by anagenetic transformation, resulting in less taxonomic diversity and a more linear interpretation of human evolutionary history.     

Preliminary examination of non-occlusal dental microwear in anthropoids: Implications for the study of fossil primates

Most studies of microscopic wear on non-human primate teeth have focused on the occlusal surfaces of molars. Recent analyses of the buccal surfaces of human cheek teeth have demonstrated an association between diet and dental microwear on the these surfaces as well. In the current study, we examine microwear on both the buccal and lingual surfaces of non-human primate molars to assess the potential of these surfaces to reveal information concerning anthropoid feeding behaviors. We compare frequency of microwear occurrence in 12 extant and 11 fossil anthropoid species. Among the living primates, the occurrence of microwear on non-occlusal surfaces appears to relate to both diet and degree of terrestriality. The implications of this research for the inference of feeding behaviors and substrate use in fossil cercopithecoids are discussed. © 1996 Wiley-Liss, Inc.     

Dental microwear and stable isotopes inform the paleoecology of extinct hominins

Determining the diet of an extinct species is paramount in any attempt to reconstruct its paleoecology. Because the distribution and mechanical properties of food items may impact postcranial, cranial, mandibular, and dental morphologies related to their procurement, ingestion, and mastication, these anatomical attributes have been studied intensively. However, while mechanical environments influence skeletal and dental features, it is not clear to what extent they dictate particular morphologies. Although biomechanical explanations have been widely applied to extinct hominins in attempts to retrodict dietary proclivities, morphology may say as much about what they were capable of eating, and perhaps more about phylogenetic history, than about the nature of the diet. Anatomical attributes may establish boundary limits, but direct evidence left by the foods that were actually (rather than hypothetically) consumed is required to reconstruct diet. Dental microwear and the stable light isotope chemistry of tooth enamel provide such evidence, and are especially powerful when used in tandem. We review the foundations for microwear and biogeochemistry in diet reconstruction, and discuss this evidence for six early hominin species (Ardipithecus ramidus, Australopithecus anamensis, Au. afarensis, Au. africanus, Paranthropus robustus, and P. boisei). The dietary signals derived from microwear and isotope chemistry are sometimes at odds with inferences from biomechanical approaches, a potentially disquieting conundrum that is particularly evident for several species.     

Molar microwear in Praeanthropus afarensis: evidence for dietary stasis through time and under diverse paleoecological conditions

Molar microwear fabrics in extant mammals vary with diet and, more particularly, the physical properties of the items that are consumed. Praeanthropus afarensis is well represented in the fossil record over a prolonged and radiometrically controlled temporal span, and reasonably robust paleoecological reconstructions are available for the various localities from which it is known. We therefore examined molar microwear in this species to determine whether diet varied in relation to time or in response to different ecological conditions. Of more than 70 specimens of Pr. afarensis that contain one or more worn permanent molars, only 19 were found to be suitable for microwear analysis. These derive from eight temporal horizons in the Laetolil Beds and Hadar Formation spanning approximately 400kyr (3.6-3.2Ma). Six paleoecological categories have been reconstructed for these horizons, and these were ranked on the basis of floral cover. None of the microwear variables observed for Pr. afarensis is significantly associated with either temporal or paleoecological rank. Thus, microwear and, by extension, diet does not appear to have altered significantly in Pr. afarensis through time or in response to different paleoecological circumstances. The wear pattern that appears to have characterized Pr. afarensis overlaps extensively that of Gorilla gorilla beringei and differs notably from the fabrics of extant primates (e.g., Cebus apella and Cercocebus albigena) that consume hard objects. The high proportion of scratches on Pr. afarensis molars suggests the inclusion of fine abrasives in or on the food items consumed by those individuals sampled in this study. Although Pr. afarensis may have been morphologically equipped to process hard, brittle items, the microwear data suggest that it did not necessarily do so, even in the face of varying environmental circumstances. Explanatory scenarios that describe Pr. afarensis as part of an evolutionary trajectory involving a more heavily masticated diet with an increased reliance on hard, brittle items need to be reconsidered. However, fallback foods that were consumed during relatively short, albeit critical periods may have exerted sufficient selective pressure to explain the evolution of the comparatively robust Pr. afarensis trophic apparatus. Because it is unlikely that many individuals from such restricted temporal intervals would be sampled in the paleontological record, we suggest that the most productive approach to the elucidation of paleodiet is the integration of genetic (morphological) and epigenetic (microwear and isotopic) lines of evidence.     

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     

Tool making,hand morphology and fossil hominins

Was stone tool making a factor in the evolution of human hand morphology? Is it possible to find evidence in fossil hominin hands for this capability? These questions are being addressed with increasingly sophisticated studies that are testing two hypotheses; (i) that humans have unique patterns of grip and hand movement capabilities compatible with effective stone tool making and use of the tools and, if this is the case, (ii) that there exist unique patterns of morphology in human hands that are consistent with these capabilities. Comparative analyses of human stone tool behaviours and chimpanzee feeding behaviours have revealed a distinctive set of forceful pinch grips by humans that are effective in the control of stones by one hand during manufacture and use of the tools. Comparative dissections, kinematic analyses and biomechanical studies indicate that humans do have a unique pattern of muscle architecture and joint surface form and functions consistent with the derived capabilities. A major remaining challenge is to identify skeletal features that reflect the full morphological pattern, and therefore may serve as clues to fossil hominin manipulative capabilities. Hominin fossils are evaluated for evidence of patterns of derived human grip and stress-accommodation features.