Elsevier

Journal of Human Evolution

Volume 51, Issue 3, September 2006, Pages 297-319
Journal of Human Evolution

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

https://doi.org/10.1016/j.jhevol.2006.04.004Get rights and content

Abstract

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 400 kyr (3.6–3.2 Ma). 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.

Introduction

Diet is central to a species' ecology and behavior. The seasonal availability of items that constitute the dietary repertoire of a species can impact attributes such as mobility patterns, population size, and social organization. In addition, the distribution and mechanical properties of these items may impact postcranial and cranial morphologies related to their procurement, ingestion, and mastication. It is understandable, therefore, that considerable effort has been expended to elucidate the dietary proclivities of our extinct hominin relatives. Paleodietary reconstructions have been attempted from a number of disparate sources of information, including 1) the archaeological record, 2) biomechanical models of cranial and mandibular morphology, 3) tooth size and morphology, 4) isotope chemistry, and 5) dental microwear. Each of these approaches has its own strengths, and each is beset with its own problems.

The archaeological record is, of course, relevant only if there is one. At present, lithic flakes and/or cores that are identifiable as having been purposefully manufactured and animal bones with stone-tool cutmarks are known only as far back as about 2.5 Ma (Kimbel et al., 1996, Semaw et al., 1997, de Heinzelin et al., 1999, Semaw, 2000, Semaw et al., 2003, Domínquez-Rodrigo et al., 2005). This leaves well over half of the hominin fossil record devoid of any durable artifacts that might be informative of dietary habits. Even when there is an archaeological record, it is pertinent only if particular artifact assemblages can be attributed to a specific species.

Biomechanical models are appealing because the material properties of dietary items almost certainly influence cranial and mandibular morphology. However, the exact relationships between loading environments and particular morphologies are unclear (Hylander and Johnson, 2002, Daegling and Grine, in press). Indeed, because it is the mechanical properties of ingested items rather than diet per se that impacts jaw morphology, even a full appreciation of cranial and mandibular design can provide only limited insight into diet.

Aspects of dental morphology—such as molar cusp height and alignment, and enamel thickness and structure—are appealing for the same reason that biomechanical models of cranial and mandibular design have attracted such interest (Kay, 1984, Ungar, 2004, Macho et al., 2005). Morphological attributes may reflect the efficiency with which teeth can process different types of food, and inform us about the range of foods a species is capable of fracturing, but they do not provide direct evidence for what an animal actually ate. Dental adaptations may reflect preferred dietary items, fallback resources, or both, but they will be biased towards those foods that are difficult to fracture or puncture. The oftentimes imprecise functional relationship between form and diet is even more difficult to decipher when analyzing morphologies (or combinations of morphologies) that are unique to the fossil record (Ross et al., 2002). In essence, the anatomical record may speak to specific adaptations of a species or lineage, but these may or may not be germane to what individuals actually consumed at any given time.

In contrast to biomechanical/adaptive models of jaw and tooth design, isotope chemistry and microwear preserve epigenetic signals directly related to an individual's diet. Isotope chemistry and trace-element analysis are extremely promising avenues of paleodietary research (Sillen and Kavanagh, 1991, Lee-Thorpe et al., 1994, Sillen et al., 1995, Sponheimer and Lee-Thorpe, 1999, Bocherens and Drucker, 2003, Drucker and Bocherens, 2004, Sponheimer et al., 2005a, Sponheimer et al., 2005b). Problems besetting this approach include diagenetic alteration of tooth and (especially) bone chemistry, and the temporal/preservation limitations imposed by elements (e.g., nitrogen) that are restricted to the organic phases of these hard tissues (Schoeninger and DeNiro, 1982, Nelson et al., 1986). In addition, particular food sources can yield different results depending upon the environment from which they come, and different types of foods can yield similar chemical signatures. Moreover, trophic levels can influence interpretations, where, for example, carnivorous and/or insectivorous behaviors result in the ingestion of the chemical components of the foliage eaten by the prey. Thus, while knowledge of environmental parameters and diet may predict isotope ratios in hominin fossils, the reverse is not necessarily the case (Burton and Wright, 1995). Unfortunately, to date, isotopic studies have not been undertaken on the Plio-Pleistocene hominin fossils from eastern Africa.

Dental microwear has been extensively studied in attempts to elucidate the dietary habits of extinct hominin species (Grine, 1981, Grine, 1986, Walker, 1981, Puech and Albertini, 1983, Puech and Albertini, 1984, Puech et al., 1983, Grine and Kay, 1988, Ryan and Johanson, 1989, Ungar and Grine1991, Teaford et al., 2002, Scott et al., 2005, Ungar et al., 2006). Studies of dental microwear have demonstrated a relationship between occlusal surface texture and the types of dietary items that constitute a species' diet (Walker et al., 1978, Scott et al., 2005). Occlusal molar microwear is capable of distinguishing among broad dietary categories that correspond to differences in the fracture properties of their included food items (Teaford and Walker, 1984, Teaford, 1985, Teaford, 1986, Teaford, 1988a, Teaford and Glander, 1991, Teaford and Glander, 1996, Daegling and Grine, 1999, Nelson et al., 2005). It is also capable of identifying subtle differences in the diets of closely related species, as well as short-term variations in diet, permitting the detection of seasonal and other ecological differences (Teaford, 1986, Teaford and Oyen, 1989a, Teaford and Robinson, 1989, Teaford and Glander, 1991, Teaford and Glander, 1996).

However, while microwear fabrics may vary with diet, they actually vary with the physical properties (fracture toughness and hardness) of the foods or abrasives that are chewed. Moreover, the ability of microwear fabrics to indicate subtle, short-term variations in diet means that they may only preserve information pertaining to the meals consumed in the days or weeks prior to an individuals death. This is the so-called “Last Supper Effect” (Grine, 1986). It is potentially a confounding influence in the analysis of fossil assemblages that may accumulate over a prolonged period of time and thus sample different seasons in unequal abundance. Finally, taphonomic artifacts, including environmental erosion or etching, as well as damage inflicted through physical and/or mechanical preparation of fossils, have the potential to confound microwear interpretations if they are not properly diagnosed (Teaford, 1988b, King et al., 1999). In particular, such artifacts may severely limit available samples, especially where the fossil assemblages comprise surface collections from fluvial channel-sand deposits (e.g., the Shungura Formation). Thus, in a recent study of molar microwear in early Homo, only 18 of 83 molars from Plio-Pleistocene deposits in eastern and southern Africa were found to be suitable for analysis (Ungar et al., 2006). Taphonomic limitations on available sample sizes may exacerbate the “Last Supper Effect.”

Notwithstanding these caveats, dental microwear analysis, like the study of hard-tissue chemistry, can provide important information relating to the dietary proclivities of extinct individuals because it can provide evidence of what they were eating. Thus, one important question that microwear has the potential to address is that of changes in a species' diet over time or in response to different environmental or ecological conditions.

Towards this end, we investigated permanent molar microwear in Praeanthropus afarensis,1 a hominin species that is well represented in the fossil record over a prolonged and radiometrically controlled temporal span. Moreover, reasonably robust paleoecological reconstructions are available for the various localities and stratigraphic horizons from which specimens attributable to Pr. afarensis have been recovered.

There have been several previous studies of dental microwear in Pr. afarensis. However, these have been limited to qualitative assessments of incisor wear (Puech and Albertini, 1984) and canine/premolar function (Puech and Albertini, 1983, Ryan and Johanson, 1989). Ryan and Johanson (1989) undertook a quantitative analysis of incisal wear in a sample of 15 teeth from the Hadar Formation, but the only study of molar wear (Puech et al., 1983) was based upon observations at low magnification (from 50× to 100×) of varnish replicas of an undetermined number of specimens.

In the present study, we examined all permanent maxillary and mandibular molars that we accept as belonging to Pr. afarensis. We recorded quantitative data relating to occlusal microwear in those specimens found suitable for such investigation, and analyzed these data in relation to time and the paleoenvironmental reconstructions that have been proffered for the particular localities and/or horizons from which the teeth derive. Additionally, comparisons were made with microwear patterns exhibited by extant primates with well-documented dietary habits.

Section snippets

The Praeanthropus afarensis hypodigm

This species is well represented at a number of sites in eastern Africa that date from about 4.0 Ma to about 3.0 Ma. The bulk of the Pr. afarensis hypodigm derives from the Hadar Formation, Ethiopia, and the Laetolil Beds, Tanzania, although fossils that are attributable to it are known from additional localities in Ethiopia and Kenya. We here review these attributions insofar as they pertain to specimens with permanent molar teeth, whose inclusion in the hypodigm of the species potentially

Paleoenvironmental reconstructions of Pr. afarensis-bearing localities

Paleoenvironmental reconstructions have been proffered for all but one of the localities from which Pr. afarensis fossils have been recovered. The majority of these are based on associated vertebrate faunas, although palynological and paleobotanical records, as well as data from paleosols and stable isotopes, have featured in many interpretations. In order to investigate whether molar microwear (and thus, diet) in Pr. afarensis was affected by environmental variables, it is necessary to review

Materials and methods

High-resolution replicas of all permanent tooth crowns that are attributable to Pr. afarensis (Table 2) were made following established procedures (Teaford and Oyen, 1989b). The occlusal surfaces were cleaned with cotton swabs soaked in ethyl alcohol or acetone to remove dirt and/or preservatives, and impressions were then made using polysiloxane vinyl impression material (President's Jet Regular Body; Coltène-Whaledent Corp., Mawah, NJ), and allowed to degas before casting. Replicas of

Results

The microwear data obtained for individual Pr. afarensis specimens are recorded in Table 4. In only one instance—the Hadar A.L. 333 locality3—is there a sample that is even marginally adequate for the purpose of

Discussion

Praeanthropus afarensis possesses large, robustly constructed mandibles and has been characterized as megadont for its inferred body size (McHenry, 1984). Moreover, its cheek teeth are thickly enameled, with low, rather bulbous cusps (White et al., 2000, Ungar, 2004). These morphological characteristics have led to the conclusion that Pr. afarensis had an “enhanced masticatory apparatus” compared to extant African apes and earlier hominins (White et al., 2000: 66). This, in turn, has led to the

Conclusions

Molar microwear in Pr. afarensis was examined to determine whether diet varied in relation to time or the different ecological conditions that it experienced. The 19 molars of this species that are suitably preserved for microwear analysis derive from eight discrete stratigraphic horizons in the Laetolil Beds and Hadar Formation, spanning close to 500 kyr (3.65–3.18 Ma). Six paleoecological categories have been reconstructed for these horizons from paleontological and paly-nological records, and

Acknowledgements

We thank Frank Brown, Craig Feibel, Eric Delson, Bernard Wood, Terry Harrison and William Kimbel for information. In particular, Terry graciously allowed us to quote from his unpublished notes on the provenience of the Laetoli hominin fossils. We thank E. Mbua, National Museums of Kenya, and A.J. Haile Mariam and W/t Mamitu Yilma, National Museum of Ethiopia, for permission to examine the fossil specimens in those institutions. We are grateful to W.H. Kimbel and D.C. Johanson, who granted us

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