A paleontological perspective on the evolution of human diet.
Peter Ungar1 and Mark Teaford2
1Department of Anthropology, Old Main 330, University of Arkansas, Fayetteville, AR 72701.
2Department of Cell Biology and Anatomy, Johns Hopkins University School of Medicine, 725 North Wolfe Street, Baltimore, MD 21205.
Since the discovery of Australopithecus afarensis, many researchers have emphasized the importance of bipedality in scenarios of human origins (e.g., Lovejoy, 1975; Susman et al., 1984). Surprisingly, less attention has been focused on the role played by diet in the ecology and evolution of the early hominids. Because diet is the most important parameter underlying behavioral and ecological differences among living primates, it is clearly critical to understanding hominid paleobiology. We need to focus not just on how the earliest hominids moved between food patches, but also on what they ate when they got there!
New and important fossil finds from the early Pliocene raise new questions concerning the role that dietary changes may have played in the origins and early evolution of the Hominidae. The discovery of thin molar enamel for Ardipithecus ramidus (White et al., 1994), and unique aspects of the mandible and dentitions of Australopithecus anamensis (Ward et al., in press) lead us to new questions, and highlight the importance of this type of research.
In this presentation, we review the fossil evidence for the diets of the earliest hominids. We also trace what has been inferred concerning the diets of the "gracile" australopithecines through time to put changes in Pliocene hominid diets into some temporal perspective. Such evidence has come in basically five categories: tooth size, tooth shape, enamel structure, dental microwear and jaw biomechanics. These lines of evidence suggest a dietary shift in the early australopithecines indicating an improved ability to consume hard, abrasive foods compared with their hominoid forebearers. Changes in diet-related adaptations from Australopithecus anamensis to A. afarensis to A. africanus suggest that hard, abrasive foods became increasingly important through the Pliocene.
In 1970, Jolly noted that australopithecines had relatively small incisors compared with molars, and speculated that this might be associated with terrestrial seed-eating, as seen in Theropithecus today. While this idea has been the subject of some controversy (e.g., Dunbar, 1976), Jolly's efforts have stimulated considerable research on relative incisor size in a wide variety of living and fossil primates. Most notably, Hylander (1975) examined the relationship of incisor row length (relative to body size) in a range of living anthropoids, and found that those species with larger incisors tend to consume larger, tougher fruits, whereas those with smaller front teeth tend to feed on smaller foods, or those that require less extensive incisa1 preparation, such as leaves or berries. Since then, numerous workers have looked to incisor size in early hominids and other fossil primates for clues concerning diet.
What can front tooth size tell us of the diets of Miocene apes? Unfortunately, not as much as we'd like. Ideally, to consider relative incisor sizes among taxa, we need estimates of species body weight means based on attributes independent of the dentition. Such estimates are unavailable for most taxa. Further, Miocene apes as a whole evidently had small incisors compared with extant hominoids, in much the same way as platyrrhines as a whole have relatively smaller incisors than catarrhines do independent of diet (Kay and Ungar, 1997). Such phylogenetic effects make it difficult to find an extant comparative baseline series with which to compare these basal taxa of uncertain phyletic affinities.
On the other hand, incisor size might give us some clues to diet and tooth use for the early australopithecines, and we have good, consistent weight estimates from independent studies (Junger, 1988; McHenry, 1992) for many of these taxa.
If we look at a regression of maxillary central incisor breadth on body size for species representing a variety of catarrhine genera, we see a nice separation of cercopithecines (with relatively larger incisors) above the line and colobines below (Figure 1). Further, more frugivorous chimpanzees and orangutans fall above the line, whereas gibbons and gorillas fall close to the line, with relatively smaller incisors. Indeed, values for the living frugivorous great apes fall above the 95% confidence limits of expected incisor size for these taxa. The human values falls out below the 95% confidence limits, indicating that we have very small incisors relative to body size.
Relative incisor sizes for the three "gracile" australopithecines are remarkably similar, and both fall very close to the regression line, much like the gorilla. These results are similar to those reported by Kay (1984) and Ungar and Grine (1991), and suggest that these hominids used their incisors in ingestion to a similar degree, though they all probably used these teeth less than either the chimpanzee or orangutan. As an interesting side note, australopithecine relative incisor size is very similar to those of both gorillas and gibbons, so these data cannot distinguish folivorous from frugivorous adaptations. On the other hand, they can give us some idea of whether a taxon often eats foods that require incisal preparation. For instance, while lar gibbons have much smaller incisors than orangutans (and they spend more of their day eating fruits on average), they depend on smaller fruits requiring little incisal preparation (Ungar, 1994, 1996a). From this perspective, the australopithecines probably put less emphasis on foods that require considerable incisor use, such as those with thick husks or hard shells, and those with flesh adherent to large, hard seeds. Body weight estimates and incisor size data for Ardipithecus ramidus should provide more insights into this issue.
One of the hallmarks of the australopithecines has always been their large, relatively flat molars (Kay, 1985; McHenry, 1984; Robinson, 1956; Suwa et al., 1994; Wood and Abbott, 1983; Wolpoff, 1973). There may well be differences in the amount of occlusal relief between gracile and robust australopithecines (Grine, 1981). However, by comparison with other primates, the australopithecines' molars are flat and huge. Even in the earliest hominids, this can be seen in a simple plot of postcanine tooth area (MD x BL), where most taxa have teeth larger than those of the modern orangutan (Figure 2).
The only exception is Ardipithecus, which is more chimp-sized in the P4 - M1 region, but intermediate between chimpanzees and orangutans in the M2 - M3 region. Again, interpretations of such differences are hampered by the lack of body size estimates for Ardipithecus, but if a body size estimate of 51 kg is used for Australopithecus anamensis (the average of the two different estimates based on the tibia), McHenry's "megadontia quotient" for this taxon is essentially identical to that for A. afarensis.
In other words, its molars are large for a hominoid, but smaller than those of A. africanus or the "robust" australopithecines.
As one might expect, the Miocene hominoids show a tremendous range of tooth sizes. Many have postcanine tooth areas larger than that of Ardipithecus, and some (such as Ouranopithecus) even have larger postcanine tooth areas than that of A.anamensis, but as all body size estimates for them have been computed from dental remains, a megadontia quotient cannot be computed for them. The main message from a simple look at postcanine tooth size is that the earliest hominids make a nice progression leading into subsequent hominids, but they do not have larger postcanine teeth than all of the mid-late Miocene hominoids. So what does this mean?
It might just mean that there are a variety of body sizes sampled in these taxa. However, as shown by the work of Lucas and colleagues, variations in tooth size are a means of adapting to changes in the external characteristics of foods such as their size, shape, abrasiveness, and stickiness. Clearly, some of these food characteristics were changing during the evolution of the earliest hominids, as postcanine teeth got relatively larger and larger. However, evidence from the mid-to-late Miocene shows that tooth size, by itself, cannot pinpoint the initial change to a hominid diet, at least not with the samples at-hand.
One other way of looking at postcanine tooth size is to look at the ratio of the areas of M1 and M3. Lucas et al (1986) showed that this ratio was inversely related to the percentage of leaves, flowers, and shoots in the diet, that is, anthropoids with a high ratio of M1 to M3 area consumed more fruit than did those with a low M1 to M3 ratio. When this is computed for the earliest hominids, plus a sample of Miocene apes, a clear separation is evident, with the early hominids, including Ardipithecus, showing higher ratios than the Miocene apes.
So, does this indicate more fruit in the diet of the earliest hominids? To begin to answer that question, we must look at analyses of tooth shape.
Natural selection dictates that primate tooth shape should reflect the mechanical properties of foods. As shown by numerous workers, variations in tooth shape are a means of adapting to changes in the internal characteristics of foods such as their strength, toughness, and deformability (Lucas and Teaford, 1994; Spears and Crompton, 1996; Strait, 1997; Yamashita, 1998). Clearly, foods are complicated structures; thus it is impossible to describe all of the internal characteristics that might have confronted the earliest hominids' teeth. However, another approach is to describe the capabilities of those teeth.
For example, tough foods are sheared between the leading edges of sharp crown crests whereas hard, brittle foods are crushed between planar surfaces. As such, reciprocally concave, highly crested teeth have the capability of efficiently processing tough items such as insect exoskeletons and leaves, whereas rounder and flatter cusped teeth are best suited for a more frugivorous diet. Kay (1984) has devised a "shearing quotient" (SQ) as a measure of relative shear potential of a molar tooth. He and colleagues have demonstrated that more folivorous species have the longest crests, followed by those that prefer brittle, soft fruits. Finally, hard-object feeders have the shortest crests and bluntest molars (Kay, 1984; Meldrum and Kay, 1997).
Shearing crest studies have been conducted on early Miocene African apes and middle to late Miocene European apes. Such studies show a considerable range of diets very much consistent with microwear results for these same taxa. For example, Rangwapithecus and Oreopithecus have relatively long shearing crests suggesting folivory, Ouranopithecus has extremely short crests suggesting a hard-object specialization, whereas most other Miocene taxa studied, such as Proconsul, and Dryopithecus have the intermediate length crests of a frugivore (Kay and Ungar, 1997; Ungar and Kay, 1995). Thus, shearing crest study results suggest that Miocene apes, especially those from the later Miocene of Europe, show a substantial range of diets.
As for the early hominids, Grine (1981) has noted differences between Australopithecus africanus and Paranthropus robustus in molar form, such that the "gracile" species had more occlusal relief than did the "robust" form, suggesting a dietary difference. While no shearing crest length studies have been conducted on early hominids, all australopithecines have relatively flat, blunt molar teeth and lack the long shearing crests seen in some extant hominoids (e.g., Kay, 1985). By itself, this indicates that the earliest hominids would have had difficulty breaking down tough, pliant foods, such as soft seed coats and the veins and stems of leaves -- although they probably were capable of processing buds, flowers, and shoots.
Interestingly, as suggested by Lucas and Peters (in press) another tough pliant food they would have had difficulty in processing is meat. In other words, the early hominids were not dentally preadapted to eat meat - they simply did not have the sharp, reciprocally-concave shearing blades necessary to retain and cut such foods. By contrast, given their flat, blunt teeth, they were admirably equipped to process hard brittle objects. What about soft fruits? It really depends on the toughness of those fruits. If they were tough, then they would also need to be precisely retained and sliced between the teeth. Again, early hominids would be very inefficient at it. If they were not tough, then the hominids could certainly process soft fruits.
In sum, Miocene ape molars show a range of adaptations including folivory, soft-fruit eating and hard-object feeding. This range exceeds that of living hominoids, and especially the early hominids. While comparable shearing crest length studies have not been conducted on early hominids, australopithecines certainly have relatively flat molar teeth compared with many living and fossil apes. These teeth were well-suited to breaking down hard, brittle foods including some fruits and nuts, and soft, weak foods such as flowers and buds; but again, they were not well-suited to breaking-down tough pliant foods like stems, soft seed pods, and meat.
Another area of interest regarding dental functional anatomy is the study enamel thickness. There are certainly methodological differences between studies (e.g., Beynon and Wood, 1986; Beynon et al. 1991; Grine and Martin, 1988; Macho and Thackeray 1992; Martin 1985; Spoor et al. 1993); but the consensus still seems to be that the australopithecines had relatively thick enamel compared with living primates, and that many of the Miocene apes also had thick enamel (Andrews and Martin, 1991; Beynon et al. 1997; Beynon and Wood, 1986; Gantt, 1986; Grine and Martin, 1988; Kay, 1985; Macho and Thackeray 1992; Robinson, 1956) . Interestingly, this perspective may be changing as we get glimpses of more and more new taxa. For instance, Conroy et al. (1995) have noted that Otavipithecus may have had thin enamel, and White et al. (1994) have made the same observation for Ardipithecus. Granted, in neither case do we have a detailed series of measurements over the tooth crown, but still, the figures that have been quoted (less than 1 mm. for Otavipithecus and 1.1-1.2 mm. for Ardipithecus) are far less than those quoted for the australopithecines.
So what might be the functional significance of enamel thickness? A number of ideas have been put forth (see Andrews and Martin (1991), and Martin (1983) for reviews), but the most frequently cited correlation is that between the consumption of hard food items and thick molar enamel (Dumont, 1995; Kay, 1981). There are many potential complicating factors (such as differences in enamel thickness within, and between, teeth) (Dumont, 1995; Macho & Berner, 1993; Macho and Thackeray 1992). Thus it is perhaps not surprising that the correlation between enamel thickness and hard-object feeding isn't a perfect one. Moreover, thick enamel by itself doesn't necessarily provide protection against hard objects - which commonly cause fracture of enamel. The best protection against that is prism or crystallite decussation. Workers are now beginning to study the functional implications of variations in enamel prism (and crystallite) arrangements throughout the dentition. Unfortunately, as that work generally requires the sectioning and etching of teeth, it has rarely been done on fossil apes and hominids. The work of Maas, Rensberger, and others has shown that prism and crystallite orientations can give clues to intricate details of dental function, and that decussation (or inter-weaving) can be an effective crack-stopping mechanism in many animals. Only anecdotal references to this phenomenon in Miocene apes and early hominids have been made thus far. Still, after some discussion and debate (Beynon and Wood, 1986; Gantt 1986; Grine and Martin, 1988), a consensus now seems to be that they did have a significant degree of prism decussation. Thus, it may well turn out in the end that the thick enamel of the early hominids was both a means to resist breakage during the consumption of hard objects and an adaptation to prolong the life of the tooth given an abrasive diet.
Numerous workers have recognized that microscopic patterns of wear on the incisors and molar teeth of primates reflect tooth use and diet. For example, those primates that use their front teeth often in ingestion have higher densities of microwear striations on their incisors than those that do not. Further, folivores have higher incidences of long narrow microwear scratches on their molar teeth whereas frugivores have more pits on those surfaces. Among frugivores, hard-object feeders have even higher pit incidences than soft-fruit eaters. These and other relationships between microwear and feeding behaviors in living primates have been used to infer diet in fossil forms.
Much of this work has focused on Miocene apes. To this point, microwear studies have been published for a diverse array of taxa from the early to middle Miocene of Africa, and the middle to late Miocene of Eurasia.. While none of these may be the last common ancestor of humans and African apes, they can (especially the late Miocene forms) give us some clues as to the diversity of adaptations of apes that lived around the time of, if not just before the divergence.
Miocene apes have a remarkable range of microwear patterning, greatly exceeding that of living hominoids. For example, relatively high scratch densities suggest that Micropithecus, Rangwapithecus and especially Oreopithecus (Ungar et al, 1996; Ungar, 1996b) included more leaves in their diets. In contrast, high pit percentages suggest that Griphopithecus, and Ouranopithecus (King, 1998; Ungar, 1996b) were hard-object specialists. Finally, intermediate microwear patterns suggest that most other species studied, such as Gigantopithecus, Dendropithecus, Proconsul, Dryopithecus and perhaps Sivapithecus (Daegling and Grine, 1994, Teaford and Walker, 1984; Ungar, 1996b; Ungar et al, 1996) had diets dominated by soft fruits. These microwear data give us a glimpse at the extraordinary variation that must have characterized the diets of Miocene apes. It is from this range of variation that the last common ancestor evidently came.
So, what is known of the microwear of early australopithecines? Precious little! No microwear research has yet been published for either A. ramidus or A. anamensis, though there has been some done on A. afarensis and A. africanus. The work done on A. afarensis has been largely qualitative and focused on the anterior teeth. Most of this research has used a baboon analogy to argue that these hominids were beginning to exploit savanna resources. For example, Puech and Albertini (1984) argued upper canines from Laetoli and Hadar show wear crenulations comparable to those seen on baboons. They also argued that A. afarensis incisors show labiolingually oriented furrows related to stripping and clamping small, hard vegetable materials in open savanna habitats. Further, Ryan and Johanson (1989) argued that Australopithecus afarensis had a mosaic of gorilla-like fine wear striae and baboon-like pits and microflakes indicating the use of incisors to strip gritty plant parts such as seeds, roots and rhizomes. These authors also suggested that wear striae and marked pitting on the flattened distal edges of the canine and occlusal surface of P3 suggest a functional shift in this complex from ape-like slicing and cutting to hominid puncture-crushing.
Work done on A. africanus has been more quantitative, but focused on comparing this taxon to Paranthropus robustus rather than to an extant comparative baseline series. Grine (1986) found for example, that A. africanus molars have lower incidences of pitting on their molars than seen for Paranthropus
A. africanus scratches are also longer and narrower, and show more homogeneity in orientation. Grine argued that compared with the "robust" forms, A. africanus ate more soft fruits and leaves. Comparisons with work from Teaford places A. africanus between Cebus olivaceus on one hand, and Pan troglodytes on the other, though different techniques were used to collect the microwear data. Work on A. africanus incisors has shown that this taxon has higher microwear feature densities on all surfaces examined than does Paranthropus (Ungar and Grine, 1991).
This suggests that A. africanus processed a greater variety of foods with their front teeth, including larger, more abrasive ones, than were encountered by Paranthropus. Comparisons with an extant baseline series examined by Ungar (in press) puts Australopithecus between Pongo pygmaeus and the seed predator/folivore Presbytis thomasi in degree of anterior tooth use in ingestion.
In sum then, what can be said of the microwear data? These data indicate that by the end of the Miocene, hominoids had a wide range of diets. Preliminary work on Australopithecus afarensis suggests that these hominids may have already begun to incorporate some abrasive, terrestrial resources that required incisal stripping into their diets. Quantitative work on Australopithecus africanus microwear suggests that this taxon may have still focused attention on soft fruit, particularly that which required a moderate amount of incisal preparation. Clearly however, considerably more work is needed on these and other early hominids to put together a reasonable picture of diet based on microwear evidence.
Finally, there are other lines of evidence beyond teeth that we can examine to look for evidence of diet. Mandibular fragments are among the most common bony remains found in assemblages of australopithecines and other fossil primates. It makes sense then, that many researchers have focused attention on the functional anatomy of the lower jaw. The basic idea is that the architecture of this bone has been adapted to withstand stresses and strains associated with oral food processing and thus, should reflect some aspects of diet. While studies of early primate jaws have focused on symphyseal fusion, analyses of australopithecine mandibular biomechanics have concentrated more on corpus size and shape.
Comparisons of australopithecine and extant hominoid jaws have shown some qualitative differences. Hylander (1988) and Daegling and Grine (1991) independently found, for example, that A. afarensis and A. africanus respectively have relatively thick mandibular corpora compared with extant catarrhines. These authors also found this pattern for Paranthropus boisei and P. robustus. Figure X shows mandibular robusticity index values for extant great apes, some Miocene apes and early australopithecines. The values represent a ratio of corpus breadth to height at the level of the first molar. Thus, larger numbers indicate a relatively thicker corpus. The early hominids show relatively thicker mandibular corpora than both extant great apes and Miocene catarrhines, suggesting a morphological shift in the former.
Both functional and non-functional interpretations have been offered to explain this phenomenon. For example, it may simply be that a thick mandibular corpus is an effect of large cheek teeth, or a reduced canine. These are not likely explanations however, as australopithecines still have relatively broad mandibles when considered relative to molar size, and there appears to be no relationship between mandibular robusticity and relative canine size among the australopithecines (Daegling and Grine, 1991).
It seems more likely that the unique shape of the australopithecine mandibular corpus relates to the functional demands of mastication. Thickened mandibles can act to resist extreme stresses associated with transverse bending (that is, "wishboning") and torsion. Because wishboning stresses decline towards the back of the corpus, torsion is likely a more important explanation. Corpus torsion can result from bite force and muscle activity during mastication. Therefore, it may be that australopithecine mandibular morphology reflects elevated stresses associated with unusual mechanical demands. Daegling and Grine (1991) suggest that australopithecines may have eaten fibrous, coarse foods that required repetitive loading. While this fails to explain why colobines do not have thick corpora, it does suggest a fundamental difference between australopithecines and living great apes that may reflect a shift in diet in the early hominids.
Studies of corpus shape in A. anamensis and A. ramidus will likely provide further clues regarding differences in mandibular architecture between great apes and later australopithecines. Corpus robusticity indices for A. anamensis below M1 are 53.1 and 55.8 for female and male mandibles respectively (computed from cast data supplied by Alan Walker). These values fall near the upper range for extant hominoids (Pan = 39.2-57.8; Gorilla = 43.5 - 59.7; Pongo = 35.7-52.0) and near the lower end of the range for later fossil hominids (A. afarensis = 49.8-79.5, A. africanus = 54.8-79.0) (data from Daegling and Grine, 1991).
It may also be of some significance that A. anamensis is intermediate between great apes and later australopithecines in that their maxillary postcanine tooth rows are set nearly parallel. This contrasts with the condition seen in extant hominoids, where the rows converge slightly posteriorly and those of later australopithecines, wheren the rows tend to diverge toward the back. The functional significance of this change in configuration is not yet clear, but according to Walker (pers com), it may also be related to the way in which masticatory stresses are dissipated..
In sum, the architecture of the mandibular corpus suggests that Australopithecus afarensis and A. africanus differed from living apes in their abilities to dissipate masticatory stresses. Taken with other lines of evidence, this certainly suggests of a shift in diet. Further analyses of earlier hominid materials may help us place this shift in time, but it already looks likely that Australopithecus anamensis is intermediate between the African ape and later australopithecine conditions.
The australopithecines exhibited a complex of morphological features related to diet that are unique compared with living hominoids or Miocene apes. These early hominids all had small-to-moderate sized incisors; large, flat molars with little shear potential; a ratio of first to third molar area low compared with extant apes, but generally higher than those of Miocene apes; thick tooth enamel; and thick mandibular corpora. This suite of traits is distinctive of australopithecines, and suggests a dietary shift at or near the stem of hominid evolution. Their thick-enameled, flattened molars would have had great difficulty propagating cracks through tough foods, suggesting that the australopithecines were not well-suited for eating tough fruits, leaves or meat. The dental microwear data agree with this, as the australopithecine patterns documented to date are most similar to those of modern-day seed predators and soft fruit eaters. Further, given their comparatively small incisors, these hominids probably did not specialize on large, husked fruits or those requiring extensive incisal preparation. Instead, the australopithecines would have been easily able to break down hard, brittle foods. Their large flat molars would have served well for crushing, and their thick enamel would have withstood abrasion and fracture. Their mandibular corpora would probably have conferred an advantage for resisting failure given high occlusal loads. In essence, for much of their history, the australopithecines had an adaptive package that allowed them ready access to hard objects, plus soft foods that were not particularly tough. These hominids could have eaten both abrasive and non-abrasive foods.
So, does this mean we can talk of a characteristic "australopithecine" dietary pattern? Perhaps to some extent, but while the australopithecines shared many features in common, they also differed from one another, suggesting a change in diet through time. Such morphological changes occurred as a mosaic, much as that seen for locomotor anatomy.
Much of the evidence for Ardipithecus ramidus is not yet available, but despite its thin molar enamel and absolutely smaller teeth than those of later hominids, it shows molar size proportions that may hint at dietary changes to come. Australopithecus anamensis shows the first indications of thicker molar enamel in a hominid, and its molar teeth were equivalent in size to those of A. afarensis. Still, its mandibular corpus is intermediate in robusticity between those of living great apes and later australopithecines. This combination of features suggests that A. anamensis might have been the first hominid to be able to effectively withstand the functional demands of hard and perhaps abrasive objects in its diet whether or not such items were frequently eaten, or only an important occasional food source. Australopithecus afarensis was similar to A. anamensis in relative tooth sizes and probably enamel thickness, yet it did show a large increase in mandibular robusticity. This may be due to changes in peak force magnitude or degree of repetitive loading in mastication. Either way, hard and perhaps abrasive foods may have become even more important components of the diet of A. afarensis. Australopithecus africanus shows yet another increase in postcanine tooth size, which by itself, would suggest an increase in the sizes and abrasiveness of foods. However, its molar microwear does not show the degree of pitting one might expect from a classic hard-object feeder. As the subsequent "robust" australopithecines do show such patterns, the divergence of Paranthropus probably represents another substantial dietary change, with even greater specialization on hard, abrasive foods.
In sum, diet was probably an important factor in the origin and early evolution of our family. The earliest australopithecines show a unique suite of diet-related features unlike those of Miocene apes or living hominoids. Such features suggest that the earliest hominids may have begun to experiment with harder, more brittle foods at the expense of softer, tougher ones early on. This does not mean that all of the australopithecines were specialized hard-object feeders. Still, such foods probably became increasingly important in hominid diets through the Pliocene, culminating with the specializations seen in Paranthropus. Another important aspect of early hominid trophic adaptations is evident from data presented here -- the dietary shift from apes to early hominids did not involve an increase in the consumption of tough foods, and so, the australopithecines were not pre-adapted for eating meat.
Investigators have tried to relate patterns of hominid evolution with patterns of climatic change for some time (see for example Potts 1996 and Vrba 1995). The focus of recent work has been on the origin of the genus Homo. Can the dietary shifts in the earliest hominids be tied to such changes? While there is some evidence of large-scale climatic changes around the Mediterranean (Bernor, 1983) and unusual faunal turnover in parts of western Asia ( Barry 1995), there are no large-scale changes evident in sub-Saharan Africa until after the earliest hominids have come and gone (1.5 - 2.5 Ma). There is the slow and inexorable cooling and drying of the Miocene, but perhaps the crucial resultant of that is the increase in microhabitat variability. In other words, after Ardipithecus, the early hominids are almost always found in lake and river margin habitats, often in the vicinity of a mixture of woodland and bushland and even grassland. In such a land of variable opportunities, the generalized craniodental tool kit of the very earliest hominids may have had a distinct advantage.
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