Tuber or not tuber? Rats are the question
From a new paper by Greg Laden and Richard Wrangham:
We propose that a key change in the evolution of hominids from the last common ancestor shared with chimpanzees was the substitution of plant underground storage organs (USOs) for herbaceous vegetation as fallback foods. Four kinds of evidence support this hypothesis: (1) dental and masticatory adaptations of hominids in comparison with the African apes; (2) changes in australopith dentition in the fossil record; (3) paleoecological evidence for the expansion of USO-rich habitats in the late Miocene; and (4) the co-occurrence of hominid fossils with root-eating rodents. We suggest that some of the patterning in the early hominid fossil record, such as the existence of gracile and robust australopiths, may be understood in reference to this adaptive shift in the use of fallback foods. Our hypothesis implicates fallback foods as a critical limiting factor with far-reaching evolutionary effects. This complements the more common focus on adaptations to preferred foods, such as fruit and meat, in hominid evolution.
Tubers are not the only kinds of USOs; there are also corms, bulbs, and rhizomes. I tend to use "tuber" as an easier-to-type version of USO, though. I was practically dared to review the paper here (nota bene: I do respond to dares, albeit more carefully and slowly than for most things), and Carl Zimmer has also written a short item on the idea. The mole rats are the lede, but there is much more to it than them, and in many respects they are the least problematic part.
So here is my semi-rambling take.
Take one
In 1999, Wrangham and Laden, along with David Pilbeam, James Holland Jones, and NancyLou Conklin Brittain, suggested that tuber cooking was central to the adaptation of early Homo. The evidence for that suggestion was and remains essentially absent. As Henry Bunn put it in his comment to the paper:
Why is there abundant evidence of hunting and some form of scavenging, carcass transport, butchery, and sharing and consumption of meat and fat in the behavioral and dietary adaptations of early Pleistocene Homo (e.g., Oliver, Sikes, and Stewart 1994 and references therin)? Why are the earliest stone tool kits of the Oldowan dominated by sharp-edged cutting tools? Why is there intensive meat polish on the edges of stone flake knives studied for microwear (Keeley and Toth 1981)? Why is there not microwear evidence of grit or sediment damaged on the teeth of supposedly tuber-feeding hominids themselves, including the robust australopithecines (Kay and Grine 1988)? (Bunn 1999:580)
Additionally there is the problem of the complete lack of evidence for cooking and the weakness of evidence for early control of fire, compared to the strong and substantial evidence for both much later in the Pleistocene.
So early Homo just doesn't show any signs of having been a serious tuber-eater. Not to say it is impossible; just that there isn't any particular evidence for the idea.
Take two
Now, Australopithecus, that's another story. Robust australopithecine teeth in particular have a lot of pits and scratches on them, as if they were eating some hard, gritty foods. Underground storage organs fit that bill. Eating a lot of dirt along with them might well explain the high rate of dental wear that robust australopithecines clearly had -- many had their first molars worn almost completely flat before the third molars came into occlusion.
In this context the fallback food idea seems like an especially good one. The tooth anatomy and microwear evidence indicate that robust and nonrobust australopithecines probably did not differ in most of their dietary spectra, but instead in the accentuation of different food sources that were shared by both. If food shortages were important in the evolution of these hominids, one way that the difference between them might have been sustained was an ecological difference in fallback food utilization. Hominids like A. afarensis and A. africanus undeniably had teeth adapted to heavy grinding, fracturing off brittle foods, and intensive attrition compared to any other living or fossil primate. So it makes no sense to propose that the difference between these "gracile" australopithecines and later robust australopithecines was that the "gracile" ones lacked the high-chewing element. Rather, it makes considerably more sense to suppose that both kinds of hominids were eating the high-chewing foods, with the robust ones making a more intensive use of them, and possibly lacking some of the tough pliable foods eaten by earlier nonrobust species. A difference in fallback strategies might comprise exactly this kind of dietary prediction.
To me, the coolest thing about the hypothesis is that it explains the postcanine adaptations of australopithecines without reference to the now-well-known carbon isotope data. Indeed, the question of C4 versus C3 foods is entirely irrelevant. I discussed the carbon and other stable isotope data in an earlier post; the short story is that all kinds of australopithecines appear to have included around a 25 to 30 percent component of C4 foods, which include grasses, some sedges, and the animals who ate them.
Peters and Vogel (2005) proposed that the C4 component of the early hominid diet could be explained as a sum of several different plant and animal sources, including around 5 percent each of seeds, roots and pith, insects, small mammals and vertebrates, and large mammal meat. That does a good job of describing a diversified hominid diet without reference to tubers.
But the thing about USOs is that relatively few of them are C4 plants. If hominids did eat tubers, in other words, they still wouldn't account for the C4 fraction of the overall diet.
However, they might account for the postcanine dental adaptations of later hominids, under the assumption that they represent a substantial part of the C3 fraction. And the replacement of C3 fruits by C3 tubers would explain why robust and nonrobust hominids both have approximately the same C4 fraction, while differing so greatly in their dental adaptations and dental microwear.
As far as I can tell, nobody has mentioned this implication, but it should be the next thing to test.
The evidence
But although I think Laden and Wrangham's study has some interesting possibilities, I think the data is a bit short of where it needs to be. What about the four lines of evidence used by Laden and Wrangham? Are they to be believed?
The first thing to point out is that a reading of the paper finds little detail to go along with two of the lines of evidence. It is true that australopithecine teeth are not like ape teeth, and that robust australopithecines were different from nonrobust ones. The innovative suggestion here, although brief, is that an enlarged oral cavity in australopithecines, particularly robust ones, may be an adaptation to increase the exposure of masticated tuber to salivary digestion.
But the dental discussion appears less as two independent lines of evidence converging to one conclusion, and more as throwing up whatever seems relevant to see what will stick. A review of early hominid dental evidence also reveals plenty that is less consistent with the hypothesis that USOs were an important food for most early hominids.
For one, the comparative dental evidence is questionable. As Laden and Wrangham review the issue, Hatley and Kappelman originated the argument that the early hominid dentition was adapted to tuber-eating:
In 1980, Hatley and Kappelman pointed out parallels in dental morphology that suggested that bears, pigs, and hominids are all adapted to eating significant amounts of plant underground storage organs (USOs). They summarized their argument as follows: "We believe that postcanine similarities evident among ursids, suids, and hominids are in part an adaptation for processing this tough, fibrous, and gritty plant part. Bears, pigs, and humans are adapted to exploiting plant roots and tubers, although their methods of food gathering are functionally rather than morphologically analogous. Convergence upon the resource of belowground plant storage parts appears to make the responses of nonretractable claws, cartilaginous snout, and digging stick equivalent" (Hatley and Kappelman 1980:380, quoted in Laden and Wrangham 2005:1).
This isn't obviously true. For one thing, Pliocene pigs appear to have been mainly grazers (Harris and Cerling 2002 -- not cited by Laden and Wrangham 2005). They increased in molar size and complexity in several different lineages, as a reflection of their increased reliance on C4 vegetation. The diet of current-day suids in particular seems to share little in common with early hominids, at least as far as their stable isotope ratios are concerned. Nor are large and flat early hominid molars particularly analogous to those of most bears -- perhaps the closest are pandas, which are far from dedicated tuber-eaters.
Then there is the problem with the earliest hominids. These, like the later ones, are found alongside mole rats, at sites like Aramis and Lukeino. But they don't have the postcanine adaptations of later hominids. The essential problem with the earliest hominids is not postcanine specialization, but instead the changing role of the canine-premolar complex, and the reduction of the canines. There is no reason (at least that I can think of) to suppose that small canines are adaptive to tuber-eating (and a search of the paper finds no occurrences of the word "canine").
One way to avoid this problem is to suppose that the USO-eating adaptation was simply a feature of later hominids --- say, A. anamensis and later. Perhaps it's true, but if so, the hypothesis loses some of its punch, and possibly one of the converging lines of evidence, since the expansion of USO-rich savanna central to Laden and Wrangham's paper starts in the Miocene.
And the paper would prefer to displace the importance of tubers earlier rather than later in time:
There is growing evidence that middle to late Miocene hominoids, mainly in Europe, exploited relatively open habitats, and may have exhibited dietary adaptations (Teaford and Ungar, 2000, Smith et al., 2003 and Smith et al., 2004) that we claim here to be related to USO consumption. This lends support to our assertions that a USO niche may have emerged during the Miocene, that this niche may have been important for non-fossorial mammals, and that certain features, such as thick enamel and large teeth, can arise in response to this niche. However, we do not wish to make claims beyond the hominid taxon at this time, other than to note that this may be a fertile area of future research (Laden and Wrangham 2005:13).
If you are a student looking for a thesis topic, don't pick this one.
The most original suggestion is that hominid and mole rat remains are significantly coassociated. On the surface, this looks like fairly convincing evidence that the hominids lived in USO-rich environments, which is precisely what Laden and Wrangham conclude. And indeed, the number of sites either possessing both kinds of animals or lacking both (27) is higher than expected considering the small number that have one kind but lack the other (11).
But wait a minute. Neither "mole rats" nor "hominids" are species, they are groups composed of several species. Let's consider the same kind of comparison for other kinds of animals. How many hominid sites lack bovids? Or suids? Or crocodilians? Keep in mind that some groups are rare at early hominid sites because they hadn't diversified yet, like papionins, or hadn't yet appeared in Africa, like equids. But these groups are found at many later hominid sites. And of course, for many sites the total species list may reflect less intensity of sampling rather than the paleohabitat.
In other words, the mole rats may show that hominids had the opportunity to eat USOs -- at least, if they could compete effectively with the mole rats for them. But they don't show that the hominids actually ate USOs. At least not if we aren't equally willing to believe that the presence of crocodiles at hominid sites meant that hominids swam in rivers and ate migrating wildebeest.
The weaknesses NOT mentioned
I see two significant weaknesses in the hypothesis. The first is the simpler of the two: digging up tubers is a lot of work.
For groups like the Hadza who eat a lot of them, this work takes many hours (at least by some group members). That kind of work seems unlikely for australopithecines, even hungry ones. Especially considering the full scenario: australopithecines digging intensively for savanna-living tubers for hours at a stretch would have been highly exposed to predation and heat stress for hours at a stretch.
Might they have done it if they had nothing else to eat? Sure. But could they have done so efficiently enough to get a net return on their effort? There's a question worth answering.
Might they have banded together into large defensive groups? Maybe, but that would seem likely to decrease foraging efficiency -- how many tubers are there in any small patch of ground? However, there is slight evidence for large multimale groups (chiefly AL 333), as well as pretty good evidence that predation was high and survivorship into adulthood low. Another question worth answering.
There may be a solution for this problem: perhaps the plants themselves have evolved under intensive hominid predation. Maybe today they put their roots further underground, or maybe the plants with tougher and more fibrous roots have predominated since the Pliocene. If so, australopithecines might have had an easier time of digging them up.
The other problem is more vexing. How can we demonstrate that an extinct species was adapted to eat a food that it did not eat very often? Bone chemistry must predominantly reflect the foods that make up the majority of the diet, not those that are consumed only intermittently. Microwear also ought to reflect the majority foodstuffs, although perhaps more weakly -- especially if mortality occurs mostly during periods of dietary stress, when animals are eating more of their fallback foods than usual. This is perhaps worth looking into.
Maybe the most promising test would be variability in tooth wear. Presumably the need to rely on fallback foods would vary in accordance with climatic conditions, on a multigenerational timescale. If so, then some individuals might exhibit relatively great amounts of attrition due to their reliance on fallback foods during long periods of resource stress, while other individuals might have lived in times of relative abundance, and therefore not have experienced significant amounts of wear. This kind of heterogeneity would itself have created differences in selection on tooth size, enamel thickness, and occlusal anatomy over time: perhaps in ways that could be differentiated from alternative strategies. But even so, that kind of comparison is relatively far from the direct evidence, and may be impossible with the fossil record we have available.
Summary
Looking back at the post, I've written a balance of critical comments and supportive ones. I guess my opinion overall is that the USO hypothesis is certainly worth presenting, but it has a ways to go before it is really testable. I think there is a balance of good ideas here and evidentiary weaknesses, and it is certainly worth talking about them, perhaps with a bit more skepticism and documentation than has yet been done.
And if you are serious about tubers, as Wrangham clearly has shown himself to be, then you are going to have to choose a time when they were important. With this paper, I have now read that tubers were the key adaptation for Miocene apes, the earliest hominids, australopithecines, robust australopithecines, early Homo, and recent humans.
It can't be all of these. If it were, they would all look the same. And there wouldn't have been any reason for one to change into anything else! So you have to pick.
And making a choice means more than saying, "well, Miocene apes tasted tubers, early hominids needed them when the fruit ran out, for australopithecines they were a fallback food, robust australopithecines ate them all the time, early Homo cooked them, and recent humans pickled them with vinegar and caraway seeds. As yet, the many tuber hypotheses have been just-so-storytelling at its most self-contradictory.
If I were picking, I would put the best odds on Laden and Wrangham's current argument: USOs were important fallback foods for nonrobust australopithecines like A. afarensis and A. africanus, and equally or more important for robust australopithecines. In contrast, early Homo was adapted to meat eating, and the earliest hominids -- who lack the postcanine specializations of later hominids -- remain as yet a mystery, although a fundamentally apelike diet is a good first guess.
This post doesn't account for all the details of early hominid diets, but some previous posts review other sources of evidence, including:
Stable isotope analyses
Dental microwear
Occlusal anatomy
References:
Hatley T, Kappelman J. 1980. Bears, pigs, and Plio-Pleistocene hominids: a case for the exploitation of belowground food resources. Hum Ecol 8:371Ð387.
Laden G and Wrangham R. 2005. The rise of the hominids as an adaptive shift in fallback foods: plant underground storage organs (USOs) and australopith origins. J Hum Evol in press (online)
Wrangham RW, Jones JH, Laden G, Pilbeam D, Conklin-Brittain N. 1999. The raw and the stolen: cooking and the ecology of human origins. Curr Anthropol 40:567-594.
More microwear from South African australopithecines
Scott and colleagues (2005) examined dental microwear in some Swartkrans (A. robustus) and Sterkfontein (A. africanus) specimens. The interesting part of the study is the use of fractal analysis to quantify the complexity of scanned surfaces. They scanned a very tiny area of each tooth, around 200 micrometers on a side. Then they fed the scans through an algorithm to calculate texture.
The basic link to diet is the same as before: hard, brittle foods leave scars and pits, tough pliable foods leave directional marks like scratches.
Some results:
Fossil hominin results indicate that P. robustus (Asfc 4.29 2.150) has microwear textures more complex (chi-squared = 8.17, P < 0.005; Kruskal-Wallis test) and more variable in complexity (F = 16.82, P < 0.0005) than A. africanus (Asfc 1.686 +/- 0.52) (Fig. 2c, d). These results are consistent with the hypothesis that P. robustus incorporated more hard and brittle foods in its diet. However, some overlap in Asfc for the hominins (Fig. 3b) suggests that P. robustus was unlikely to have been a specialized hard-object feeder. It is more likely that hard, brittle foods were an occasional but important part of the diet. Previous studies have emphasized average differences between species rather than overlap, because low repeatability associated with observer error made assessments of within-species variability difficult.
In contrast, the microwear textures of Australopithecus africanus (epLsar1.8 0.0045 +/- 0.00163) show greater anisotropy (chi-squared = 3.84, P = 0.05; Kruskal-Wallis test) and epLsar variability (F = 7.38, P < 0.01) than P. robustus (epLsar1.8 0.0028 0.00060) (Fig. 2c, d). These data suggest a tougher diet on average for A. africanus compared with P. robustus, but one that is also more variable in its toughness (Scott et al. 2005:694).
The interesting thing is the overlap between the two samples. The authors also compared cebus and howler monkeys, finding extensive variation in both taxa, with minimal overlap in distributions (howlers are leaf-eaters, cebus eat a wider range of foods including some hard items). The two hominids overlap almost completely in "surface complexity" (i.e. whether they are pitted and scarred), with the main difference between the samples being an average greater complexity in A. robustus and an average greater anisotropy (i.e. grooving and scratching) in A. africanus. A third or so of each sample lie in the region of overlap in both variables.
From these measures, the diet variation within each species appears to be more extensive than the differences between them. The authors suggest this pattern of differences may represent a basically uniform diet with different fallback foods:
The greater variation in complexity for P. robustus and in anisotropy for A. africanus suggests that these species altered different components of their diet, but that there was probably substantial overlap in the fracture properties of their preferred foods. Thus, the clear differences between A. africanus and P. robustus microwear may relate, in part, to differences in critical dietary resources consumed only periodically during the year (Scott et al. 2005:695).
That would certainly be concordant with the stable isotope data. I guess it's a good thing for them that these two species weren't contemporaries.
References:
Scott RS, Ungar PS, Bergstrom TS, Brown CA, Grine FE, Teaford MF, Walker A. 2005. Dental microwear texture analysis shows within-species diet variability in fossil hominins. Nature 436:693-695. Full text (subscription required)
Robust australopithecine diet ablated
Sponheimer and colleagues (2006, link) zapped some Swartkrans teeth with lasers to measure their 13C content. I wrote quite a bit here last year about australopithecine diets, including a long review of isotopic evidence for australopithecine diets.
With respect to dietary differences between A. africanus and A. robustus (the two species with any substantial isotopic sampling), there are four essential observations:
- The apparent C4 dietary content of the two species is basically the same, and fairly high.
- High C4 foods are not so easy to come by, they include some grasses and sedges and the animals who eat them.
- The Sr/Ca ratios of the two species are fairly different.
- The postcanine teeth of A. robustus seem to be adapted to crushing and grinding, moreso than A. africanus.
One hypothesis for the difference in Sr/Ca ratios is exploitation of underground tubers (warthogs and mole rats have elevated Sr/Ca similar to A. africanus). A mix of C4 foods has been proposed to solve the grass-eating problem, including seeds, rhizomes, insects, lizards, and herbivore meat. But these don't really solve the postcanine tooth conundrum, and while they may both be true; neither is really testable.
OK, so does the new laser ablation study solve any problems? First, let's read a bit about what exactly it is, and why it might be useful. Ann Gibbons has written a ScienceNOW article:
[A] team of American and British researchers studied the teeth of four individuals of Paranthropus robustus (also known as Australopithecus robustus) from the Swartkrans Cave in South Africa. The team scanned the teeth with a sensitive laser, which did not destroy the teeth but etched them lightly enough to free carbon gases long trapped in the enamel. Because different plants absorb atmospheric carbon dioxide differently, the researchers were able to see what types of vegetation the hominids ate based on the ratio of carbon isotopes in their teeth.
An accompanying perspective by Stanley Ambrose explains:
In contrast to conventional methods, the laser ablation technique used by Sponheimer et al. barely penetrates the enamel surface of an area of less than 0.5 mm2 and is thus nearly nondestructive (2). Laser ablation also avoids the problem of time averaging in large drilled grooves. Moreover, perikymata can be counted, providing a good estimate of the minimum time interval sampled and of the duration of tooth formation.
The Paranthropus teeth studied by Sponheimer et al. show interesting patterns of seasonal variation in diet and climate. All have the isotopic composition of mixed feeders, and two show at least ca. 40% variation in the proportions of C3- and C4-based resources over 1 year. One individual had a predominantly C3-based diet and foraged in a cooler, more humid environment; it may have formed its tooth in a very wet year. The others ate more C4-based foods in a warmer, drier environment. Their average carbon-isotope ratios are similar to those of adaptively versatile savanna baboons (2). Analyses of seasonal variation in teeth of modern and fossil baboons and of other hominin species are necessary to evaluate dietary specialization in Paranthropus and niche overlap with other hominin species.
Back to me. There are two possibilities. First, the differences between 13C values for different samples might be sampling the actual dietary variability of single A. robustus individuals over the course of their tooth development (in this paper, sampled over a course of a couple hundred days).
Or second, they may just be sampling noise.
The paper presents comparative data to suggest that this is actual variability in diet and not isotopic noise. They sampled some steenbok teeth from Swartkrans with the same technique. Steenbok are consistent C3 browsers; their diet doesn't vary much in its 13C proportion over time. And the samples from the steenbok teeth didn't show very much variation across different sampling zones from the same tooth. Hence, it looks like the samples from different perikymata actually may give a consistent picture of dietary 13C composition over time.
Compared to the steenbok, the A. robustus samples show great heterogeneity in 13C content. This heterogeneity is manifested when looking at multiple samples from the same tooth, and it is also manifested when looking at different individuals. So far, that would seem to indicate dietary heterogeneity -- the A. robustus individuals ate a different mix of foods over time, and different individuals ate different foods.
On the basis of the magnitude of difference (particularly within the single specimen SKX 5939), Sponheimer et al. propose that some individuals must have gone from a diet predominantly composed of C3 foods to one predominantly C4 within the span of two years (estimated 644 days).
Here's how their paper concludes:
A dental microwear study of the earlier (3.0 to 3.7 Ma) hominin Australopithecus afarensis found no evidence that its diet changed over time or in different habitats (20). In contrast, stable carbon isotope (3, 4) and dental microwear texture analyses (1) of the slightly younger (3.0 to 2.4 Ma) hominin A. africanus demonstrated that its diet was far more variable. This suggests the possibility that a major increase in hominin dietary breadth was broadly coincident with the onset of increasing African continental aridity and seasonality after 3 Ma (21, 22) and only shortly antedated the first probable members of the genera Homo and Paranthropus (23-25) and the earliest stone tools (26). The undoubted toolmaker Homo is thought to have been a dietary generalist that consumed novel foods such as large ungulate meat and tubers that are abundant in savanna environments (27-30). Paranthropus, in contrast, with its extremely large and flat cheek teeth, thick enamel, robust mandible, and heavily buttressed facial architecture, is often portrayed as a dietary specialist (27-29). Further, it has been argued that this specialization contributed to its extinction when confronted with increasingly dry and seasonal environments later in the Pleistocene, whereas Homo's generalist adaptation was crucial for its success (28, 29). Our results suggest that Paranthropus had an extremely flexible diet, which may indicate that its derived masticatory morphology signals an increase, rather than a decrease, in its potential foods. Thus, other biological, social, or cultural differences may be needed to explain the different fates of Homo and Paranthropus (31).
We have lots of other reasons to believe that robust australopithecines were not dietary specialists, as pointed out by Wood and Strait (2004). Robust australopithecines had broad geographic ranges, were able to disperse over long distances, and persisted despite substantial climatic and environmental changes. The evidence for dietary differences across the lifespan is certainly consistent with this.
It does, however, make for an interesting conundrum: if australopithecines were selected on the basis of their ability to find different foods over the course of years, that suggests a strong role for social learning of more food types and broader geographic ranges. But if this was the path taken by robust australopithecines, what was the path taken by Homo?
References:
Ambrose SH. 2006. A tool for all seasons. Science 314:930-931. DOI link
Gibbons A. 2006. Not just nuts and berries for these hominids. ScienceNOW 9 Nov. Full text
Sponheimer M, Passey BH, de Ruiter DJ, Guatelli-Steinberg D, Cerling TE, Lee-Thorp JA. 2006. Isotopic evidence for dietary variability in the early hominin Paranthropus robustus. Science 314:980-982. DOI link
Wood B, Strait D. 2004. Patterns of resource use in early Homo and Paranthropus. J Hum Evol 46:119-162. DOI link
Chemistry and early hominid diets
The chemical analysis of bones to interpret diet rests on the observation that different foods vary in the composition of different chemical elements or isotopes. Isotopes are different forms of an element that have different numbers of neutrons in their atomic nuclei (if they had different numbers of protons, they would be different elements). The number of neutrons in the nucleus affects the atomic weight of the isotope, and for this reason different isotopes may be taken up differently by different kinds of plants or animals, or they may be more or less abundant from different natural sources, such as the different mineral compositions of local soils. The chemical composition of an animal depends on the foods that it has eaten over the course of its life. Therefore, different kinds of animals may have different chemical signatures based on their preferred diets. If these isotopes are stable, then they may be preserved in fossil remains long after the death of the individual, and paleontologists may be able to access these ratios and make interpretations about the diets of ancient species. The amount of preserved material varies depending on the type of tissue examined, so that chemical analyses are usually expressed in terms of the ratio or proportion of one isotope or element to another. The major stable isotopes that have been examined in fossil hominid remains include the ratio of strontium (Sr) to calcium (Ca) and the ratio of carbon-13 (13C) to carbon-12 (12C).
Strontium/calcium ratios
Strontium and calcium are chemically similar elements that occupy the same column on the periodic table. For this reason, strontium can be taken up by plants in the place of calcium, and the two form a ratio that depends on the environmental abundance of strontium. When herbivores eat the plants, their bodies preferentially incorporate calcium instead of strontium, so that their Sr/Ca ratio is lower than that of the plants. And when carnivores eat the herbivores, they again incorporate more calcium than strontium, so that their Sr/Ca ratio is lower than the herbivores. Taken together, this means that we could infer the general diet composition (trophic level) of a fossil hominid if we knew its ratio of strontium to calcium. This wouldn't tell everything about the diet, and in fact it leaves many blanks. But with respect to the question of whether early humans were significant meat eaters, and whether robust australopithecines and other early hominids significantly differed in diet, this technique has great potential to inform.
One thing that is worth noting about these kinds of chemical ratios is that they reflect the average diet of ancient hominids across a large part of their lifespan. This time probably varies with circumstances, but it must always have included multiple years of dietary intake. This means that these ratios may respond to different aspects of the diet than the anatomy and size of the teeth, especially if the teeth were significantly adapted to fallback foods that did not make up the majority of the dietary intake of the animal.
Analysis of strontium and calcium in fossil bones requires some background work. The amount of strontium available to the food web depends on the local soil composition, so the Sr/Ca ratio may vary among samples of the same kind of animal taken at different sites. This means that different kinds of herbivores, carnivores, and omnivores must be sampled at the same location in order to interpret their Sr/Ca ratios. Additionally, it appears that fossil bone and fossil teeth may vary in their preservation of Sr/Ca ratios. The initial work on early hominid Sr/Ca ratios was done by Andy Sillen (1992) on fossil bone from Swartkrans. But Sillen and others have shown that the process of fossilization alters composition of bones in ways that may skew or erase the endogenous ratio of strontium to calcium.
Sponheimer and colleagues (2005b) examine the ratio of strontium to calcium in the tooth enamel of fossil hominids from South African sites. Enamel is less susceptible to diagenesis (change over time) than bone, and should preserve more accurate estimates of Sr/Ca ratios. A possible issue is that enamel is mainly deposited early in life, and therefore reflects preweaning or early juvenile diets that may not be fully representative of the dietary repertoire of the animal. To examine this, Sponheimer et al. examined comparative samples of mammals from the fossil localities and from recent contexts, finding that the Sr/Ca ratios did differentiate browsers, grazers, and carnivores from each other. The differences between these animal groups are that the grazers have the highest Sr/Ca ratios, and the carnivores and browsers. Browsers eat a high proportion of leafy species that tend to have lower Sr/Ca ratios, and as a consequence their Sr/Ca ratios tend to be slightly lower than those of the carnivores.
The analysis found that the remains of A. africanus from Sterkfontein Member 4 had relatively high Sr/Ca ratios, easily within the range of or even exceeding those of the grazers. A. robustus from Swartkrans Member 1 had substantially lower Sr/Ca ratios than A. africanus, but these were within the range of all the other animals, including browsers, grazers, and carnivores.
Sponheimer and colleagues (2005b) note that the results here were different from those of Sillen (1992), who showed the robust australopithecine bones to have rather low Sr/Ca ratios. Sillen suggested that this meant that the robust australopithecines was significantly omnivorous. The tooth enamel is consistent with a broad range of diets, so it does not disprove the hypothesis that robust australopithecines were omnivores, but it does not specifically disprove the notion that they were exclusive herbivores either.
The bottom line is that it is very difficult to differentiate diets with this kind of information. One problem is the nature of the overlap among the comparison samples. The whisker plots overlap substantially among these, and since they show the 10th and 90th percentiles, the extent of overlap may have been almost complete. This is not to say that the distributions are the same, but that individual fossils that are in the area of overlap (which would include most of the robust specimens and many of the A. africanus specimens) may not be diagnosed. Fortunately the study included a large number of teeth, so that samples may be compared to each other, and these samples are significantly different from each other. Assuming that the teeth have been assigned correctly to samples, this provides some confidence in the idea of a dietary difference between these samples.
A more important problem is that very different dietary compositions may have the same Sr/Ca signature. For example, a leaf browser that included some grass seeds in its diet might have the same Sr/Ca ratio as a fruit eater that included significant meat. And the Sr/Ca ratio does not give any indication of seasonal variations that might have ecological importance.
Carbon stable isotopes
Not all plants photosynthesize in the same way. The majority of plant species use a three carbon photosynthetic pathway. These are called C3 plants. But some plants use instead a four carbon pathway, and these are called C4 plants. The C4 plants are a minority, but include a large proportion of grasses and sedges, and a few other kinds of plants.
There are two stable isotopes of carbon in nature. Most of this carbon has six neutrons, resulting in an atomic weight of 12. But a minority of carbon has seven neutrons, with an atomic weight of 13 (an additional small proportion is the radioactive carbon 14). The C3 photosynthetic pathway preferentially includes carbon 12 (12C), so that C3 plants have a ratio of 13C to 12C that is substantially lower than the 13C/12C ratio in nature. For C4 plants, this discrimination is not as great, so that C3 plants and C4 plants differ in their 13C/12C ratios. Animals obtain their carbon from the foods they eat, so that the 13C/12C ratio of a herbivore marks the proportion of C3 and C4 plants in its diet. Likewise, the 13C/12C ratio of a carnivore reflects the plant diets of its prey species.
For example, grazers tend to eat a high proportion of grasses, which in Africa are predominantly C4 plants. This means that grazers have a relatively high 13C/12C ratio compared to other herbivores. It also means that carnivores who focus on grazers as prey species also have a high 13C/12C ratio. As noted by Sponheimer et al. (2005a:302): "the tissues of zebra, which eat C4 grass, are more enriched in 13C than the tissues of giraffe, which eat leaves from C3 trees."
A number of studies have examined the 13C/12C ratio in early hominid remains, focusing on those from the South African caves (Lee-Thorp et al. 1994; Sponheimer and Lee-Thorp 1999; van der Merwe et al. 2003). These studies are reviewed along with new results by Sponheimer and colleagues (2005a). The two basic results are that A. africanus and A. robustus are indistinguishable from their 13C/12C ratios, and that both australopithecine species have 13C/12C ratios that are elevated compared to C3 consumers and intermediate between them and C4 grazers. The fact that their ratios are lower than C4 grazers is not surprising, since australopithecines clearly did not eat grass. But if they depended largely on fruits, nuts, or other C3 foods, then it is difficult to explain why they should have stable isotope ratios that reflect a partial consumption of C4 foods.
Several hypotheses might explain this observation:
- Australopithecines may have eaten underground storage organs of C4 plants, such as grass corms or tubers of certain sedges.
- They may have eaten seeds from C4 grasses.
- They may have eaten the meat from grazing species.
- They may have eaten termites that relied on grasses and other C4 species.
- Diagenesis of 13C/12C ratios in fossils may have altered the isotopic signature, which actually may have been the same as that of C3 consumers (Schoeninger et al. 2001).
Sponheimer and colleagues (2005a) address the last hypothesis by testing a greater number of australopithecine teeth, finding results consistent with earlier findings. It is not obvious that this eliminates doubt entirely, but more samples provide more confidence that a real phenomenon has been observed. A comparison of all the hominids with recent C3 consumers shows clearly that they are significantly different, with relatively little overlap. They are also very different from the fossil C3 consumers preserved at the same sites (Sterkfontein and Swartkrans), which include browsing antelopes and giraffids. They are also distinct from C4 grazers in having a lower 13C level. From these values, Sponheimer and colleagues (2005a:305, emphasis in original) write:
[T]he data suggest that Australopithecus and Paranthropus ate about 40% and 35% C4-derived foods respectively. Such a significant C4 contribution, whatever its origin, is very distinct from what has been observed for modern chimpanzees (Pan troglodytes). Schoeninger et al. (1999) found no evidence of C4 foods in chimpanzee diets even in open environments with abundant C4-grass cover.
With respect to the termites and sedges, Sponheimer and colleauges (2005a) found that termites in open environments do have a high C4 proportion, while South African sedge species were found to be predominantly C3 plants. This means that termites might have provided part of the C4 component of early hominid diets, but the underground storage organs of sedges most likely did not. This does not mean that hominids may not have used sedges as a resource, but instead that such use would not explain their relatively high C4 proportion. And a diet of 35 to 40 percent termites seems quite high, so even if these were included in the diet, there were likely other C4 sources for the early hominids.
Another factor of the observations is that A. africanus teeth were quite variable in their 13C levels. Sponheimer and colleagues (2005a) suggest that one hypothesis to explain this variability would be if the sample changed over time--for example, in response to environmental change toward more open environments. Such changes in environment may be evidenced by a difference in the stable oxygen isotope ratios of the Sterkfontein and Swartkrans hominids. But when the ages of fossils were compared to 13C/12C ratios, there was no change over time, indicating that whatever dietary changes may have occurred, they evidently did not greatly affect the C4 proportion in the diets of the australopithecines. Sponheimer and colleagues (2005a:308) conclude that the australopithecines with high variability may simply have been "extremely opportunistic primates with wide habitat tolerances that always inhabited a similarly wide range of microhabitats regardless of broad-scale environmental flux."
Combining the data
Can these different sources of evidence be put together into a single picture of ancient hominid diets? The answer is yes, but unfortunately there is more than one hypothesis that may fit the bill. The facts that must be explained are as follows:
- High Sr/Ca ratios in A. africanus
- Moderate Sr/Ca ratios in A. robustus
- High proportion of C4 sources in both A. africanus and A. robustus
- Dental anatomy unsuited to leaf or grass eating in either species
- Tooth wear and anatomy reflecting hard, brittle food consumption by robust australopithecines (Grine 1986; Grine and Kay 1988), and possibly similar but to a lesser degree in other early hominids (Ungar 2004).
Sponheimer et al. (2005b) treat the first of these observations as the most problematic, and try to account for it with hypotheses that are consistent with the other observations. One hypothesis is that early hominids were insectivorous. They indicate that modern insectivores do have higher Sr/Ca ratios than other faunivores (153). In combination with possible evidence for termite digging at Swartkrans (Backwell and d'Errico 2001), this observation might suggest that early hominids used termites and other insects as a significant food source, even moreso than living chimpanzees. Sponheimer and colleagues judge this hypothesis as problematic because the fossil hominids differ from recent insectivores in having a low ratio of barium to calcium (154). One may also add that the robust australopithecines from Swartkrans did not have especially high Sr/Ca ratios, while there has not yet been evidence of termite digging for earlier hominids.
A second hypothesis is described as follows:
We have noticed that among the modern fauna that have the unusual combination of high Sr/Ca and low Ba/Ca are warthogs (Phacochoerus africanus) and mole rats (Cryptomys hottentotus (Sponheimer, unpublished data), both of which eat diets rich in underground resources such as roots and rhizomes. Thus, the possibility of greater exploitation of underground resources by Australopithecus compared to Paranthropus requires consideration. In addition, the slightly enriched Sr/Ca of Paranthropus compared to papionins might also be evidence of increased utilization of underground resources.
This last point about A. robustus may be reaching. On the other hand, this leaves the dietary mix issue somewhat unsettled. For example, what if both A. africanus and A. robustus ate underground resources, but A. robustus also ate meat? Or if A. africanus also ate insects. And so on. It seems unclear that anything short of a clear identity of diet between an early hominid and a modern analog in the African fauna will leave the possibility of exotic mixes.
This leaves us to reflect on the full pattern of evidence more closely. How is the hard, brittle diet inferred from dental anatomy and wear reconcilable with the hypothesis that australopithecines were eating the tough, fibrous underground storage organs of C4 plants?
Peters and Vogel (2005) address the issue of C4 diet proportion by examining the range of C4 plants that may have been available to early hominids. They make a number of observations:
- C4 sedges that produce edible roots, tubers, or stems are water-reliant, and do not compete with grasses in areas where drought occurs seasonally. They are therefore limited to relatively permanent watercourses including areas that are seasonally inundated with water. The South African sites do not represent such wetlands.
- Interestingly, C4 grasses have an evolutionary origin in the late Middle Miocene, and had increased in abundance in the African flora by the origin of the hominids.
- A majority C4 food intake by early hominids seems unlikely because of the wide availability of hominid-edible C3 foods in areas where the relatively rarer C4 hominid-edible plants also exist.
- Mature tubers of C4 sedges appear to have toxicity that may have impeded their edibility by early hominids, and they could probably have been consumed only in very small amounts.
- A number of potential animals may have provided a C4 component for early hominids, beyond the relatively large C4 grazing ungulates. These would include reptiles, birds, and rodents as well as insects. Early hominids would not have competed with other large carnivores for these small animals.
This brings us to a third hypothesis for early hominid diets. Peters and Vogel (2005:232-233) support an interpretation of omnivory for the early hominids, giving the following scenario:
As a starting point we can offer the following theoretical formulation of possibilities for a 30% C4 contribution to a subadult hominid diet based on minor potential C4 food categories:This type of formulation maximizes the diversity of food species, i.e., both food-species-richness and evenness of contribution. The exact numbers are not as important as the species richness of the formulation.
- 5% C4 input from sedge stem/rootstock, green grass seed, and forb leaves
- 5% C4 input from invertebrates
- 5% C4 input from bird eggs and nestlings
- 5% C4 input from reptiles and micromammals
- 5% C4 input from small ungulates
- 5% C4 input from medium and large ungulates
A couple of things can be noted from this scenario. First, the predominant part of the C4 contribution comes from animal resources rather than plants. This conforms with Peters and Vogel's (2005) examination of C4 plant resources, only few of which are both edible by hominids and potentially available in quantity in their apparent paleoenvironments. However, this dietary component does not explain the masticatory adaptations of the australopithecines (indeed, it is not intended to explain them, since early Homo does not differ in dietary C4 contribution from earlier hominids). There is certainly nothing about the dentitions and jaw musculature of robust australopithecines to preclude an omnivorous diet of this type, but that invites the question of what fallback foods may explain that adaptation, or may explain the difference between robust and other australopithecines in that respect.
Conclusion
None of these three hypotheses really accounts for the full pattern of evidence about early hominid diets. The consensus so far appears to be that the chemical characteristics of the bones and teeth of early hominids reflect a majority diet that did not require a specialized dental adaptation. Therefore, the dental specializations of early hominids, in particular the enlargement of the postcanine dentition, reduction of the incisors and canines, and the low crowns of the molar teeth probably were adaptations to a minority of dietary intake that nevertheless was extremely important in selective terms. This would be characteristic of fallback foods eaten at times of resource scarcity, and would evidently have consisted of hard, brittle food items that could be effectively pulverized and ground by low-crowned teeth with large surface areas and thick enamel. This interpretation is supported by Ungar (2004) in an analysis of dental topography in early hominids and living hominoids (discussed in another article).
There are some remaining mysteries:
- If australopithecines had basically similar C4 dietary proportions, then what accounts for their differences in Sr/Ca ratios?
- Did any A. africanus-like hominids ever coexist with a robust australopithecine species?
- If early Homo had a C4 proportion that came in large part from hunting or scavenging grazing species, a hypothesis also supported by their dental anatomy (Ungar 2004), then did they abandon any of the C3 resources used by australopithecines?
- If australopithecines were opportunistic omnivores, were there important regional differences in their dietary composition?
These questions and others might be addressed with further sampling of dental chemistry.
References:
Backwell LR, d'Errico F. 2001. Evidence of termite foraging by Swartkrans early hominids. Proc Natl Acad Sci U S A 98:1358-1363.
Grine FE. 1986. Dental evidence for dietary differences in Australopithecus and Paranthropus: a quantitative analysis of permanent molar microwear. J Hum Evol 15:783-822.
Grine FE, Kay RF. 1988. Early hominid diets from quantitative image analysis of dental microwear. Nature 333:765-768.
Peters CR, Vogel JC. 2005. Africa's wild C4 plant foods and possible early hominid diets. J Hum Evol 48:219-236.
Schoeninger MJ, Bunn HT, Murray S, Pickering T, Moore J. 2001. Meat-eating by the fourth African ape. In: Stanford CB, Bunn HT, editors, Meat-eating and human evolution. Oxford, UK: Oxford University Press. p 179-195.
Schoeninger MJ, Moore J, Sept JM. 1999. Subsistence strategies of two savanna chimpanzee populations: The stable isotope evidence. Am J Primatol 49:297-314.
Sillen A. 1992. Strontium-calcium ratios (Sr/Ca) of Australopithecus robustus and associated fauna from Swartkrans. J Hum Evol 23:495-516.
Sponheimer M, de Ruiter D, Lee-Thorp J, Späth A. 2005b. Sr/Ca and early hominin diets revisited: New data from modern and fossil tooth enamel. J Hum Evol 48:147-156.
Sponheimer M, Lee-Thorp J, de Ruiter D, Codron D, Codron J, Baugh AT, Thackeray F. 2005a. Hominins, sedges, and termites: New carbon isotope data from the Sterkfontein valley and Kruger National Park. J Hum Evol 48:301-312.
Sponheimer M, Lee-Thorp JA. 1999. Isotopic evidence for the diet of an early hominid, Australopithecus africanus. Science 283:368-370.
Ungar P. 2004. Dental topography and diets of Australopithecus afarensis and early Homo. J Hum Evol 46:605-622.
van der Merwe NJ, Thackeray JF, Lee-Thorp JA, Luyt J. 2003. The carbon isotope ecology and diet of Australopithecus africanus at Sterkfontein, South Africa. J Hum Evol 44:581-597.
Average diet versus extreme diet in robust australopithecines
I've followed the literature on early hominid diets from the beginning of the weblog. In 2005 I discussed Peter Ungar's analyses of dental occlusal morphology in A. afarensis versus Homo, concluding:
The contrast between Homo and A. afarensis is in the same direction as the contrast in occlusal morphology between primarily meat-eating carnivores like felids and canids as opposed to more omnivorous carnivores like bears. Another observation is that meat is a major food resource of chimpanzees, although this is hardly a fallback resource. Indeed, if meat eating was indeed an important component of the behavioral repertoire of early Homo, it probably is not fair to assert that the difference in diet between Homo and Australopithecus was primarily a difference in fallback resources. It may be true that australopithecines and early Homo overlapped in their food resources, particularly in plant species consumed. But considering the likely effectiveness of early humans as predators, I think it likely that the fallback foods of early humans--when hunting was ineffective--may well have been the preferred foods of australopithecines. And when australopithecines were forced to abandon their preferred foods by early humans, they were forced to fall back upon resources that either were common or were difficult for early Homo to exploit. The disappearance of early small-bodied Homo by around 1.6 million years ago, and the ultimate extinction of the robust australopithecines after a progressive increase in their molar sizes (Wood and Lieberman 2001) indicate that this fallback strategy could not be maintained in the face of increased hunting effectiveness by large-bodied Homo.
The concept of "fallback foods" has captured a large mindshare in explaining early hominid diets. The idea is that a species may depend on preferred, staple foods for most of the year, but adopt less preferred, "fallback" foods when their staple is not available -- for instance, during the dry season.
What can fallback foods explain about early hominids? For one thing, they could explain the difference between robust and non-robust australopithecines. We know from isotope data (reviewed in this 2005 post about Matt Sponheimer's work) that A. africanus and A. robustus had similar fractions of C3 and C4 plant source foods in their diets. Across the year, they may have eaten roughly the same mix of foods. A 2005 paper by Greg Laden and Richard Wrangham (discussed here) explored the idea of underground storage organs of plants, or tubers, as fallback foods for australopithecines. Later studies of isotope data using laser ablation of small segments of the enamel (discussed here) showed that diet proportions may have substantially varied across the time that teeth were developing -- possibly concordant with the idea of seasonal or longer-period fallback foods. An earlier analysis of dental microwear in the two hominids by Scott and colleagues (discussed here) came to a similar result: there was great variability in wear properties, especially within A. robustus, although the average in the two species showed a possibly greater fraction of brittle, hard foods consumed by the robust australopithecines.
So I've written about the topic a lot, and followed it closely.
Now, Peter Ungar, Frederick Grine and Mark Teaford have examined the wear properties of the molars of Australopithecus (Paranthropus) boisei. They find that -- unlike A. robustus -- none of the seven specimens showed any evidence of having eaten hard or brittle foods:
Comparisons with the extant baseline series suggest that none of the Paranthropus boisei individuals examined consumed extremely hard or extremely tough foods in the days before death. All of these specimens lacked the extremes of Asfc evinced by Lophocebus albigena and especially Cebus apella, both known to consume hard, brittle foods. Paranthropus boisei molars also lacked the extremes of epLsar seen in Trachypithecus cristata and Alouatta palliata, both known to consume tough leaves and stems. The P. boisei individuals examined evidently avoided such metabolically challenging foods, at least in the days before death. This is notably consistent with Walker's [23] early assertion that P. boisei microwear patterns resemble those of living frugivores, and differ from those of living grazers, leaf browsers, and bone feeders.
Comparisons with the South African hominins suggest that while Paranthropus boisei may have consumed foods with similar ranges of toughness as those eaten by Australopithecus africanus, the eastern African "robust" hominin did not eat harder and brittler foods than the South African "gracile" form. Further, the patterns for P. boisei and P. robustus are very different. Paranthropus robustus likely ate foods that were on average much harder and less tough than P. boisei. The differences in both central tendencies and ranges of variation suggest different feeding strategies, and by implication, that the two species of Paranthropus probably had markedly different diets or foraging strategies (Ungar et al. 2008, italics lost).
That is very interesting that A. robustus and A. boisei are so different in their microwear patterns. It makes me wonder whether there may have been substantial habitat variation in the use of hard foods -- maybe the extant A. robustus sample, mainly drawn from a small area of South Africa, had access to some food items that were rare or absent across the larger East African range of A. boisei. But if some A. boisei populations had also depended on such hard resources some of the time, you might expect that we would have found one, or at least a bit more variability. Yet the sampled specimens, drawn from a distance from Ethiopia to Tanzania and well over a half million years of time, are pretty uniform in their microwear, showing some variability in the anisotropy dimension (here, high values have mostly parallel striations, attributed to fibrous food consumption).
So we can return to the question: the major hominid competitor of A. boisei was Homo. Both lineages appeared in the period around 2.5 million years ago, and remained sympatric throughout the next million years. Some of the dynamics of that interaction must have involved diet (considering the different dietary adaptations of the two). We can speculate that A. boisei didn't get much meat, which would then be an important difference. But what else was A. boisei eating?
Meanwhile, the data are still consistent with the idea of fallback foods in A. robustus as a driver of dental morphology, but the story for A. boisei now seems less clear. With only seven specimens, there is almost certainly not enough data to test the hypothesis -- which after all predicts that the use of hard brittle foods may be rare. But that's not positive evidence either. Is there some other food that might explain the hyperrobust craniodental morphology?
References:
Ungar PS, Grine FE, Teaford MF (2008) Dental Microwear and Diet of the Plio-Pleistocene Hominin Paranthropus boisei. PLoS ONE 3(4): e2044. doi:10.1371/journal.pone.0002044
Tooth anatomy and diet in australopithecines and early humans
Peter Ungar (2004) investigated the dietary adaptations of A. afarensis and early Homo by looking at the three-dimensional topography of their teeth. the shapes of the teeth are expected to reflect diet because the teeth themselves are adaptations for processing food. Among mammals there are some regular relationships between the morphology of an organism's teeth and the type of food it prefers. Looking specifically at primates, high-crowned teeth that interlock between the upper and lower jaws are adapted to shearing foods, in a manner analogous to the pinking shears of a seamstress. Shearing is necessary for cutting and puncturing through food items, which are the predominant actions necessary to process leaves and insects, respectively. Primates that specialize on other foods, notably fruits or harder objects like seeds, tends to have flatter teeth without high crests. These teeth useful for crushing or grinding foods. So and examination of the anatomy of the teeth is expected to give insights about the diets of ancient primates.
But direct examination of fossil tooth anatomy is complicated by the fact that the teeth wear during the course of an animal's life. The effective chewing characteristics of a tooth therefore change over time, as a result of progressive attrition on its occlusal surface. This means that it's difficult to measure the anatomy of teeth, as in the lengths of different crests or the area of shearing surfaces, because these characteristics are altered in individuals of different ages. This is a special problem among early hominids, whose teeth are generally heavily worn even among relatively young individuals. It also means that the chewing characteristics of younger individuals and older individuals may actually have been different, possibly reflecting ontogenetic differences in diet. The details of the anatomy of unworn teeth may have been largely irrelevant to the pattern of mastication throughout most of the individual's life.
Ungar (2004) applied three-dimensional modeling to assess the shape characteristics of teeth at different stages of wear. In this way he was able to quantify the surface characteristics of the teeth--that is, how flat or jagged they were, how high the cusps were, and any angulation or deviation from a horizontal occlusal surface. He applied the technique to a series of second mandibular molars (M two) of Australopithecus afarensis and early Homo (including specimens attributed to H. erectus, H. rudolfensis, and H. habilis). As a comparison, Unger also examined a series of gorillas and chimpanzees, not because their diets were probably similar, but because their molar cusp patterns are similar, yielding comparable topographic results. The topographic values derived from each of the specimens included the "average slope," which was a measure of the average vertical displacement between adjacent points on the tooth, and the "occlusal relief," which was the measurement of the three dimensional surface area scaled to the two dimensional occlusal surface area of the tooth. In principle, more jagged teeth with higher cusps will have a higher average slope and a higher occlusal relief.
The results indicated that the early Homo specimens had relatively high average slope, except in the most worn molars. These specimens had average slope near that of gorillas, which were the highest among the samples measured. The occlusal relief of early Homo molars was not as great as that of guerrillas, but was substantially larger than chimpanzees, except again among the most worn specimens.
In contrast, A. afarensis had by far the lowest average slope and occlusal relief among any of the samples. Chimpanzees were lower than early Homo, but the A. afarensis sample was still significantly flatter in its dental morphology. These results held true across a range of wear categories, degrading slightly among the most worn sample of teeth in all four species. But as teeth wore down in all four species, they tended to become flatter. His results perhaps isn't surprising but does inform about the chewing characteristics of the teeth of older individuals.
Ungar (2004) includes a discussion that addresses why the differences in surface characteristics may have come to characterize these samples. He begins with a discussion of the differences between chimpanzees and gorillas in their diets:
The differences in occlusal morphology between chimpanzees and gorillas evidently relate to differences in the material properties of the foods they eat, particularly their fallback foods. Central African common chimpanzees are primarily frugivorous, with soft fruits reported to constitute 70-80% of their diets (Kuroda, 1992; Tutin et al., 1997). Fruit is also commonly consumed by western lowland gorillas, making up about half of the food species found in their fecal remains (Williamson et al., 1990; Nishihara, 1992; Remis, 1997; Doran et al., 2002). Differences and similarities in food preferences are most obvious were these taxa are sympatric and have access to the same resources. At Lope, Gabon, for example, the dietary overlap is substantial, with gorillas reported to consume 73% of the food species eaten by chimpanzees (Tutin and Fernandez, 1985). Differences between the two taxa are notable at times of fruit scarcity though, when gorillas fall back on tougher, more fibrous foods (such as leaves and stems) than those eaten by chimpanzees (Tutin et al., 1991; Remis, 1997) (615).
It should be reiterated that differences in occlusal morphology between P. t. troglodytes and G. g. gorilla evidently reflect differences in fallback resources rather than preferred foods. While both tax evidently prefer soft fruits when available, differences in occlusal morphology apparently allow the gorillas to take advantage of fallback foods that are less accessible to the chimpanzees (615)
For the case of A. afarensis, Ungar concludes that the differences in occlusal morphology from chimpanzees are not as great as the differences between chimpanzees and gorillas, although in the opposite direction. In his view this implies that A. afarensis included more brittle, less deformable foods, possibly as a fallback strategy in contrast to chimpanzees.
For the case of early Homo, the conclusion is that the molars were intermediate between chimpanzees and gorillas in their occlusal characteristics. This means that, compared to chimpanzees and compared to A. afarensis, early Homo was better adapted to chewing "tough, pliant foods" (616). This has important implications for dietary reconstruction in early humans:
[T]ubers, especially larger ones (Baritelle and Hyde, 1999) are often fairly brittle, whereas mammalian soft tissues tend to be tough and elastic (Lucas and Peters, 2000). Thus, meat seems more likely to have been a key tough-food resource for early Homo then would have USOs. It has also been noted that USOs those are of limited nutritional value (Schoeninger et al., 2001), and so would not have made very good keystone resources (616-617)
Ungar does not mention a number of other arguments that might also favor this interpretation. The contrast between Homo and A. afarensis is in the same direction as the contrast in occlusal morphology between primarily meat-eating carnivores like felids and canids as opposed to more omnivorous carnivores like bears. Another observation is that meat is a major food resource of chimpanzees, although this is hardly a fallback resource. Indeed, if meat eating was indeed an important component of the behavioral repertoire of early Homo, it probably is not fair to assert that the difference in diet between Homo and Australopithecus was primarily a difference in fallback resources. It may be true that australopithecines and early Homo overlapped in their food resources, particularly in plant species consumed. But considering the likely effectiveness of early humans as predators, I think it likely that the fallback foods of early humans--when hunting was ineffective--may well have been the preferred foods of australopithecines. And when australopithecines were forced to abandon their preferred foods by early humans, they were forced to fall back upon resources that either were common or were difficult for early Homo to exploit. The disappearance of early small-bodied Homo by around 1.6 million years ago, and the ultimate extinction of the robust australopithecines after a progressive increase in their molar sizes (Wood and Lieberman 2001) indicate that this fallback strategy could not be maintained in the face of increased hunting effectiveness by large-bodied Homo.
References:
Ungar P. 2004. Dental topography and diets of Australopithecus afarensis and early Homo. J Hum Evol 46:605-622.
Other references therein.
John Hawks Department of Anthropology
University of Wisconsin—Madison
Copyright © 2007 John Hawks