Sterkfontein

The New York Times has given over free access to its e-archives, normally behind the "Times Select" paywall. It is a great opportunity to institute a new series, "(Best) forgotten tales of paleoanthropology," where I link to great (or not-so-great) moments in the field.

For my first installment, here's an osteodontokeratic flashback from 1948:

Baboon Killers' Method 1,000,000 Years Ago Traced in Recent Tactics of African Tribe

By PHIL RAY

JOHANNESBURG, South Africa, Dec. 24 -- For those who like their mystery stories steeped in the ages, we present a plot that may be 1,000,000 years old: "Who bashed the baboons of ancient Africa, and how?"

...

Baboon skulls have been found in abundance in the rocks and fill of South Africa's ancient caves, and the great majority of these skulls are found to be fractured as if by a blow on the top of the head. The fracture is usually neat and distinct, indicating that whoever gave the blow did so expertly and with an instrument suited to killing baboons with speed and efficiency.

Prof. Charles L. Camp and Dr. Frank Peabody of the University of California expedition now working in South Africa have uncovered a large number of baboon skulls at Taungs, finding six fine specimens in a single chunk of rock less than two feet across its largest dimension. All showed the same evidence of a sudden and violent end -- and a neat fracture about an inch and a half in diameter. Many others have been unearthed by Dr. Robert Broom at Sterkfontein and still others have been found at Makapoans [sic], generally showing the same neat fracture.

At this point the story discusses Dart's well-known view that australopithecines had killed the baboons with clubs. And then:

New evidence was uncovered by Professor Camp during his recent trip to South-West Africa. He discovered that the Klip Kaffir tribesmen, or Bergdaramas, who live in the Waterberg region, once hunted baboons with clubs. According to his aged native informant, a "knob-kerrie," or light stick about half as long as a walking stick and with a knob head was used.

As far as I can tell, the "neat fracture" argument never returned in print.

For a recent discussion of the accumulating agents for the South African caves (focused on Swartkrans), I suggest my colleague Travis Pickering's paper, "Beyond leopards: tooth marks and the contribution of multiple carnivore taxa to the accumulation of the Swartkrans Member 3 fossil assemblage". Berger and Clarke (1995) discuss the hypothesis that eagles were involved in the accumulation of the Taung fauna, including those baboons.

References:

Pickering TR, Domínguez-Rodrigo M, Egeland CP, Brain CK. 2004. Beyond leopards: tooth marks and the contribution of multiple carnivore taxa to the accumulation of the Swartkrans Member 3 fossil assemblage. J Humn Evol 46:595-604. doi:10.1016/j.jhevol.2004.03.002

Berger LR, Clarke RJ. 1995. Eagle involvement in the accumulation of the Taung child fauna. J Hum Evol 29:275-299.

Rex Dalton has a great two-page article in Nature about the bush vs. ladder dispute. It keys off of the Middle Awash Australopithecus anamensis article by White and colleagues from a couple of weeks ago.

If you recall that one, White et al. posited that Ardipithecus was likely ancestral to Au. anamensis, and that the two did not overlap in time. Here's the key exchange in the Dalton piece:

This month's Nature paper makes a bold argument, and shows the Awash team seeking to put its mark on the record. Others in the
field are impressed. "When you find 30 new hominid fossils, you are allowed a certain amount of conjecture," says Bernard Wood, a palaeoanthropologist at George Washington University in Washington DC. "As always, they have done a fantastic job."

But he and others are unconvinced by the Awash team's conclusion: "This is only the first half of the rugby match," says Wood. Meave Leakey, lead author on the Au. anamensis discoveries in Kenya, is more blunt. "I don't believe this," she says. "We do not have the specimens to fill the gaps."

Leakey and Wood are among those who believe that other, as yet undiscovered hominid species may have lived at this time, from 4.4 million to 2.9 million years ago. The existence of other species would cloud or eliminate the argument for a direct lineage. "My prejudice is there are more lineages rather than fewer -- more diversity," says Wood. "I have to concede these new data are dramatic. But we should beware coming out with a complete explanation when we don't have all the
evidence."

This argument frustrates White. "There were Martians there back then too," he says. "And spacecraft all over the Pliocene -- we just haven't found them yet."

Waiting for Monte Cassino

In a series of articles since 2000, White and colleagues have laid out a systematic attack on the "bushy" phylogeny model. Their arguments have extended across four million years and seven species, with a breadth that rivals the Allies breaking the Winter Line.

Consider the angles of attack:

1. Au. anamensis -- Au. afarensis. Everyone basically accepts that Au. anamensis is a direct ancestor of Au. afarensis. And the two species are really not very different from each other -- for instance, they are more alike than either is to Ardipithecus. The transition between these species would look to be a simple case of anagenesis, except...

...for Kenyanthropus (Leakey et al. 2001). This small-toothed, flat faced hominid needs an ancestor, too. Au. anamensis might have been the common ancestor of Kenyanthropus and Au. afarensis. If so, then both these later species originated by cladogenesis from Au. anamensis. A similar argument might be made for other species, like Australopithecus bahrelghazali (Brunet et al. 1996) or the Sterkfontein Member 2 hominids. But Au. bahrelghazali is only known from a partial mandible and only differs from Au. afarensis by a three-rooted premolar, which is considered by many to be weak evidence, and the Sterkfontein Member 2 sample has not yet been taxonomically assigned -- they might turn out to be Au. afarensis, for example. Kenyanthropus remains the strongest case for cladogenesis (i.e., a "bush"). Yet...

...White (2003) denied that the Lomekwi skull KNM-WT 40000 was a distinct species. In particular, he argued that the extensive postmortem deformation of the skull made it impossible to substantiate an anatomical difference from Au. afarensis, and even if it was different, the anatomical diversity of living hominoid species is so great that it would probably encompass the difference between KNM-WT 40000 and known Au. afarensis crania.

2. Earliest hominids. At the moment, the earliest putative hominids include three genera: Orrorin (Senut et al. 2000), Sahelanthropus (Brunet et al. 2002), and Ardipithecus, represented in the Late Miocene by Ar. kadabba (Haile-Selassie 2001, Haile-Selassie et al. 2004). Evidence for obligate bipedality has been challenged (by different researchers) for each of these three (I'm one of those who has questioned bipedality for Sahelanthropus).

So far the only comparable anatomical parts from all three samples are teeth...

...which were examined by Haile-Selassie, Suwa and White (2004). They concluded that the variation among these three genera

is no greater in degree than that seen within extant ape genera. Despite claims of molar enamel thickness differences among these late Miocene fossils, we question the interpretation that these taxa represent three separate genera or even lineages. Given the limited data currently available, it is possible that all of these remains represent specific or subspecific variation within a single genus (Haile-Selassie et al. 2004:1505).

Additionally, Ohman, Lovejoy and White (2005) challenged the interpretation of the internal anatomy of the Orrorin femur, which had been suggested to be more derived than that of Au. afarensis. They wrote:

We agree that the Lukeino femur's external morphology suggests some form of bipedality. Yet the more detailed original scans appear to show a distinct superior cortex different from Australopithecus and humans, with the cortex distribution being more primitive than that seen in any other hominid, including Australopithecus.

The relevance of this argument to the phylogenetic diversity of early hominids depends on the anatomy of the Ardipithecus femur, which none of the rest of us are in a position to know. But one may speculate that if all these early "hominids" had femora with similar morphology, it would further reinforce the interpretation that they belong to a single lineage.

3. Ardipithecus -- Au. anamensis. This is the current example. Here's how Dalton discusses it:

The latest Afar discovery is exciting experts because it shows that the three hominids existing in the same area, but in successive time periods. Tim White of the University of California, Berkeley, co-leader of the Awash team, believes this points to a direct lineage between the three -- a process called phyletic evolution. The new Au. anamensis fossils are only 300,000 years younger than Ar. ramidus, meaning that if one became the other, the changes would have had to happen that fast. But the key point, says White, is that fossils of Au. anamensis and Au. afarensis have never been found in sediments the same age as those containing Ar. ramidus. If fossils of the different species were found together, that could show that they belonged to multiple lineages existing simultaneously.

Finding remains of all three species in the same area but not from the same time period suggests they did not coexist, says White.

...

The specimens also provide anatomical clues to evolutionary history. "The new Au. anamensis fossils are anatomically intermediate between the earlier Ar. ramidus and the later Au. afarensis," says White. For example, the teeth of the newly discovered Au. anamensis fossils seem adapted to chew tougher and more abrasive foods than Ar. ramidus. The researchers believe this shows that Au. anamensis had a broader diet. "All this strengthens the view that there is phyletic evolution from Ar. ramidus through Au. anamensis," says White. He believes he has nailed down the relationship between the two later species, although he says that further specimens are needed to prove the earlier link (Dalton 2006:1100).

Of course, it would help matters if we knew in more detail what Ardipithecus looked like. But one must imagine that the stage is being set for its revelation. The unilineal interpretation places Ardipithecus at the critical point as an ancestor to the major mid-Pliocene australopithecine lineage. Extending the unilineal interpretation earlier into the Late Miocene would make Ardipithecus the earliest hominid as well.

It is not necessary to think that taxonomic uniformity means anatomical uniformity, though. Ardipithecus already encompasses a trend of decreasing canine size and less sectorial P₃ for example. A trend toward fuller skeletal adaptation to bipedality may also be imagined. But in that context, it is important to note that the time interval between the Orrorin femur and the unpublished Aramis skeleton is longer than the time between Aramis and Hadar. Those relative times may become quite important in thinking about the evolution of those postcrania.

The Winter Line was broken at Monte Cassino, after many failed attempts from different approaches. The Aramis fossils are either the heavy shoe waiting to drop, or they are the uncomfortable foot that all this talk about phyletic evolution is meant to shoehorn into place.

Commentary

If all these cases are added together, they imply a single evolving lineage encompassing at least four anagenetic taxa, Ar. kadabba -- Ar. ramidus -- Au. anamensis -- Au. afarensis. This last would presumably be followed by a cladogenesis into a robust australopithecine species (Australopithecus aethiopicus) and Australopithecus africanus.

One could add Homo erectus to this list, since White and colleagues argued in their description of the Daka skull (Asfaw et al. 2002) that the Asian and African samples represent one cosmopolitan species.

But then one species sticks out as a surprising exception to the pattern: Australopithecus garhi (Asfaw et al. 1999). It will be interesting to see a close argument showing why this species is really different from South African Au. africanus. Say, more different than KNM-WT 40000 is from the Hadar crania. It's quite glaring, really, that this species should be there mucking up such a simple phylogeny.

I have to say, after reviewing all these papers in one sitting -- this entire bush vs. ladder thing is getting very tiresome! I mean, isn't there something else that we could organize early hominid discoveries by? These are all papers in the top journals, and this is the (fairly specialized) discussion that has been promoted as the central issue in the field!

The subtitle of the Dalton piece suggests that it is merely a philosophical difference:

Deciding whether our ancestors evolved as a single lineage may depend more on philosophy than fossils.

But that's not really true. There is a clear null hypothesis here, quite directly drawn from William of Ockham:

entia non sunt multiplicanda praeter necessitatem

Which of course means:

Sometimes fossil samples really do form ancestor-descendant relationships.*

(*) It doesn't really. It means "Entities should not be multiplied beyond necessity."

References:

Asfaw B, Gilbert WH, Beyene Y, Hart WK, Renne PR, WoldeGabriel G, Vrba ES, White TD. 2002. Remains of Homo erectus from Bouri, Middle Awash, Ethiopia. Nature 416:317-320. DOI link

Asfaw B, White T, Lovejoy O, Latimer B, Simpson S, Suwa G. 1999. Australopithecus garhi: A new species of early hominid from Ethiopia. Science 284:629-635. DOI link

Begun DR. 2004. The earliest hominins -- is less more? Science 202:1478-1480. DOI link

Brunet M. and 37 others. 2002. A new hominid from the Upper Miocene of Chad, Central Africa. Nature 418:145-151. DOI link

Brunet M, Beauvillain A, Coppens Y, Heintz E, Moutaye AHE, Pilbeam D. 1995. The first australopithecine 2,500 kilometres west of the Rift Valley (Chad). Nature 378:273-275. DOI link

Dalton R. 2006. Feel it in your bones. Nature 440:1100-1101. DOI link

Haile-Selassie Y. 2001. Late Miocene hominids from the Middle Awash, Ethiopia. Nature 412:178-181. DOI link

Haile-Selassie Y, Suwa G, White TD. 2004. Late Miocene teeth from Middle Awash, Ethiopia, and early hominid dental evolution. Science 303:1503-1505. DOI link

Leakey MG, Spoor F, Brown FH, Gathogo PN, Kiarie C, Leakey LN, McDougall I. 2001. New hominin genus from eastern Africa shows diverse middle Pliocene lineages. Nature 410:433-440. DOI link

Ohman JC, Lovejoy CO, White TD. 2005. Questions about the Orrorin femur. Science 307:845. DOI link

Senut B, Pickford M, Gommery D, Mein P, Cheboi K, Coppens Y. 2001. First hominid from the Miocene (Lukeino formation, Kenya). Comptes Rendus 332:137-144.

White T. 2003. Early hominids -- diversity or distortion? Science 299:1994-1996. DOI link

Tim White and colleagues (2006) report on new fossils from Aramis and a new site, Asa Issie, with estimated dates between 4.1 and 4.2 million years ago.

In addition to the paper, there are articles in the New York Times (by John Noble Wilford), the Associated Press (by Seth Borenstein), and BBC (by Paul Rincon).

The story is being played as another "missing link" -- this one between Ardipithecus and Australopithecus. From the Times:

Tim D. White, a paleontologist at the University of California, Berkeley, who was a leader of the team, and his colleagues said the 4.1-million-year-old fossils were anatomically intermediate between the earlier species Ardipithecus ramidus and the later species Australopithecus afarensis, the Lucy family. The newfound bones and teeth are the earliest remains of the most primitive Australopithecus, known as anamensis.

"This new discovery closes the gap between the fully blown australopithecines and earlier forms we call Ardipithecus," Dr. White said in a statement. "We now know where Australopithecus came from before four million years ago."

The fossil specimens are a partial maxilla from Aramis, ARA-VP-14/1; two partial maxillary dentitions from Asa Issie numbered ASI-VP-2/2 and ASI-VP-2/334; and a large femur shaft fragment, ASI-VP-5/154. There are also several postcranial bones -- phalanges, vertebrae, a metatarsal -- that are pictured in some of the press accounts and briefly discussed but not pictured or numbered in the paper. The postcanine teeth in the maxillary specimens are larger than the known sample of Ardipithecus, but the canines are larger and more mesiodistally elongated than in Australopithecus afarensis. The best anatomical match for these features is with the Kanapoi and Allia Bay samples assigned to Australopithecus anamensis, and White and colleagues assign the new fossils to that species.

So why are these fossils important? On the surface, there isn't very much to them. Three piecemeal upper dentitions don't tell much. They have big molars and big canines, both within the range of Au. anamensis. Neither they nor the femur shaft extend the known range of variation in early hominids.

Remembering that every fossil fragment is a precious relic of a bygone age, the main importance of these is that they may address hypotheses about the biogeography of Early Pliocene hominids. The maxillae show that a large-molared hominid existed in the same geographic location at a later time than the small-molared Ardipithecus. That could be interesting, and it is the hook for the news stories and the team's press statement.

The strongest part of this story is the geographic -- finding them in the Middle Awash instead of Kenya -- and the paleoenvironmental. There is some suggestion in the paper that there may be a paleoenvironmental difference at the sites that currently have evidence of Au. anamensis:

Palaeoenvironmental circumstances surrounding Au. anamensis ~1,000 km to the south in Kenya have been described for Allia Bay as a mixed assemblage sampling aquatic, forest, grassland and bushland. Nearby Kanapoi conspecifics were found in another mix of environments described as dry, possibly open, wooded, or bushland conditions with a wide gallery forest in the vicinity. Habitat preferences in such mixed assemblages are difficult to ascertain despite the assertion that the hominids "favored mosaic settings". In contrast, the Ethiopian occurrence of Au. anamensis described here allows its tight spatial and temporal placement in a vertebrate assemblage with taphonomic integrity. Its relative abundance suggests that it was a regular occupant of a wooded biome that appears to have persisted in this part of the Afar during the 200,000-yr interval subsequent to Ar. ramidus at Aramis (White et al. 2006:887-888).

This points to two salient facts about the Australopithecus lineage: they were able to disperse effectively across relatively long distances, and occupy at least those habitats where wooded cover and resources were available.

On the other hand, the fossils don't really "fill a gap" between Ardipithecus and Australopithecus, because they are pretty firmly within the time range of known Au. anamensis, being around the same age as the Au. anamensis sample from the Lake Turkana area -- the oldest Kanapoi hominids may be between 4.1 and 4.2 million years old also. The paper points out the other East African examples of Australopithecus at or above 4 million years ago; but it omits the Sterkfontein Member 2 remains, which are also conceivably in the age range of Au. anamensis. Or, for that matter, the Lothagam mandible, which might be the earliest australopithecine even if its date weren't as high as the >5 Ma estimate.

The paper attempts to close off -- for the moment -- the idea that there were allopatric species of early (ca. 4 Ma) australopithecines with differing dietary adaptations. But the paper cannot reject this hypothesis without caveats:

Two phylogenetic hypotheses concerning the origin of Australopithecus can be offered to account for the available data. The first hypothesis derives Au. anamensis phyletically from Ar. ramidus within a 200,000-yr interval [i.e., between 4.4 and 4.2 Ma]. The second involves cladogenesis of Au. anamensis from an ancestor (presumably Ardipithecus or some close relative) even deeper in the Pliocene or Late Miocene. Under the latter hypothesis, Ar. ramidus would represent a relict species in an ecological refugium (White et al. 2006:888).

This latter alternative is the only "bushy" interpretation -- the idea that known species of Ardipithecus can't really be the direct ancestors of Australopithecus, but that there must be some as-yet-undiscovered hominid (or better yet, hominids) that are the common ancestors, cousins, and other bushy relatives of the known species. White and colleagues cannot reject it, but they clearly do not favor it.

In its place, they suggest Ardipithecus ramidus as a lineal, possibly anagenetic ancestor of Au. anamensis, and Au. anamensis as the anagenetic ancestor of Au. afarensis. It's a ladder from primitive to derived, small-molared to big-molared, big-canined to small-canined.

I tend to think this is the null hypothesis -- we have sampled adaptations that differ because of evolution in what is essentially a single lineage of successive species. I say "essentially" because there was not necessarily a wholesale transformation of one species to another across its entire range. Instead, dispersals of new adaptive packages by population movements were probably important biogeographic aspects of evolution in these early hominids. But I think it important to recognize that one species can indeed be the ancestor of a later species.

People who like their phylogenies bushy and their speciations punctuated can take solace in that 200,000-year gap. The finding of Au. anamensis within the already-known time range of Au. anamensis means that the new fossils haven't really added much to the question of phylogenetic diversity in early hominids.

As a postscript, I have a nomination for "most significant sentence" in the paper:

At Aramis, the lone hominoid and largest primate was Ar. ramidus (109 of 6,156 identified specimens so far) (White et al. 2006:888, emphasis added).

References:

White TD and 21 others. 2006. Asa Issie, Aramis and the origin of Australopithecus. Nature 440:883-889. DOI link

Speaking of Phillip Tobias, The Sunday Independent is carrying a long interview of Tobias discussing his autobiography. Google says the site is subscription-only, but I got it without a problem, and I'm no subscriber.

At 80, Tobias is the dean of South African paleoanthropologists. He oversaw excavations in South Africa for many years, had a huge research output, named Homo habilis and worked closely with many other leaders in the field. The article touches on the beginnings of his career:

His brilliant career was ridden with personal conflict. Some colleagues left the country because they found apartheid untenable. He declined several invitations to take up chairs at universities overseas. He opted for Wits and assumed his position in the chair of anatomy in January 1959, the year in which apartheid legislation in education was passed in parliament - "a dark time".

To leave the university and the country would be intellectual suicide, he wrote in his journal. And in our interview he remarks: "And how close that would have been to physical suicide."

And so he stayed the course and fought against apartheid from within.

And on the "ultimate messages" of it all:

I try to get past the bigger questions Tobias poses in his memoir, for instance: do we owe our success as bipeds to anatomical adjustments of our skeleton, or to a more exquisitely developed proprioceptive system?

He has written about his continuing search for Sterkfontein's "ultimate messages" and the need for synthesis: between ancient and modern peoples; genetics and evolution; long-term and short-term development; brain, mind and behaviour.

I call on the professor to make his personal story more, well, human. In this way we move past some of the contradictions of his nature, modesty coupled with insistent probing, public with private - only to discover further, great contradictions.

The article says that next week The Independent will run an excerpt of the memoir, Into the Past.

Several articles in the South African press have covered the opening of the new visitors' center at the Cradle of Humankind World Heritage site. The one with the most detail is in the Mining Weekly.

The neatest part is the dedication of the center to Phillip Tobias:

The centre was named after Professor Phillip Tobias, who has worked at the caves for about 60 years conducting scientific research on fossils.

...

Professor Tobias, who celebrated his 80th birthday on Friday, told BuaNews that there were times when years passed without any fossils being discovered.

"We just kept optimism and faith," he reminisced. "But there were also times when fossils came pouring like an avalanche." Gauteng Premier Mbhazima Shilowa said more than R160-million had been invested in the Sterkfontein area through tourism, among others.

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)

In a 2002 paper on cranial remains from Sterkfontein, Lockwood and Tobias write the following in a section called "Are there multiple hominin species from Sterkfontein Member 4?":

The Group C specimens (Stw 183 and Stw 255) arguably represent a phenon, as they deviate from the A. africanus sample in the same direction. Each exhibits some derived characters of A. aethiopicus, A. robustus, and/or A. boisei. Moreover, based on dental size and morphology, Stw 252 probably belongs in this group (Clarke, 1988).

Stw 183 is the strongest craniofacial evidence for a second species of Member 4, though it is not by itself definitive (Lockwood, 1997). Stw 183 is an immature individual, and a full interpretation of this specimen relies on a comparative framework of early hominin ontogeny that is at present incomplete. Despite its youth, it possesses characters typically found in A. robustus, such as an incipient maxillary trigon and a rounded lateral portion of the inferior orbital margin (not present in any other specimen from Sterkfontein Member 4).

The temporal bones catalogued at Stw 255 (including Stw 266a) resemble A. africanus in essentially one autapomorphic character: the prominent eustachian process. Otherwise, this individual shows traits corresponding to A. boisei, especially in the relationship of the tympanic to the postglenoid and mastoid processes. On the whole, Stw 255 suggests the appearance of the temporal bone in KNM-WT 17000 of A. aethiopicus. Moreover, Spoor (1993) showed that Stw 255 has a combination of features regarding the orientation of the posterior petrosal surface that may correspond to the external anatomy of KNM-WT 17000: an unflexed cranial base combined with a petrous axis that is relatively coronally oriented in the transverse plane. Fossils catalogued as Stw 255 may also be associated with the various specimens that make up Stw 252, but this is uncertain, as a second individual (Stw 265) of similar preservation was found in close proximity to Stw 252 (Lockwood and Tobias 2002:446-447, citations in original).

They go on to say they do not think that these specimens are sufficient evidence that another species was present, and they note details of a few other fragments that are different from the sample as a whole. They differ from Clarke (e.g. 1988), who would have divided the relatively complete cranial specimens into two samples.

Some other workers have suggested that individual specimens from Sterkfontein Member 4 might represent other species besides A. africanus. Kimbel and Rak (1993) proposed that Sts 19 probably represents Homo, and that the inclusion of the specimen into A. africanus inflates the variation within that species. This proposition was tested by Ahern (1998), who found the Sterkfontein Member 4 specimens to be quite variable without Sts 19 also. In other words, this site preserves a variable sample -- especially considering nonmetric traits observed on individual specimens.

The traits of Stw 183 and Stw 255 may fall in that category of variation, and Lockwood and Tobias (2002) suggest that possibility. I think the specimens are interesting because of whose traits they share. Studying A. africanus not as a branch of a cladogram, but as a real species with possible ancestors and descendants, the occasional presence of characters of earlier and later species is to be expected. The question is whether these characters document an ancestor-descendant relation for A. africanus and the robust taxa, or whether they might be shared by collateral taxa by virtue of common ancestry alone. The half-million years preceding the origins of Homo may have been just as interesting for the study of populations as the last half-million years.

References:

Ahern JCM. 1998. Underestimating intraspecific variation: the problem with excluding Sts 19 from Australopithecus africanus. Am J Phys Anthropol 105:461-480.

Clarke RJ. 1988. A new Australopithecus cranium from Sterkfontein and its bearing on the ancestry of Paranthropus. In (Grine FE, ed) Evolutionary history of the robust australopithecines. Aldine de Gruyter, New York. p. 285-292.

Kimbel WH and Rak Y. 1993. The importance of species taxa in paleoanthropology and an argument for the phylogenetic concept of the species category. In (Kimbel WH and Martin LB, eds) Species, species concepts, and primate evolution. Plenum Press, New York. p. 461-484.

Lockwood CA and Tobias PV. 2005. Morphology and affinities of new hominin cranial remains from Member 4 of the Sterkfontein Formation, Gauteng Province, South Africa. J Hum Evol 42:389-450.

A recent spate of articles has carried on a debate about the age of the Sterkfontein hominids. Sterkfontein is a complicated site, including several distinct caverns and deposition layers, called members. The dating of these layers is a serious problem because of their complex stratigraphy and the lack of volcanics that could be subjected to radiometric dating. Until recently the only insights into the age of the fossils came from uranium-series dating and paleomagnetic analysis of calcite deposits in the caves.

The Sterkfontein deposits are divided into six members, and hominid have been recovered from Member 5, Member 4, and Member 2. Most of the hominid remains assigned to Australopithecus africanus come from Member 4, which was long thought to date to between 2.8 million and 2.6 million years. Before Member 5 was deposited, there was erosion on the top of Member 4, and the two are separated by an unknown period of time. This deposit is generally thought to be less than 2 million years in age, perhaps extending as recently as 1.4 million years (Kuman and Clarke 2000). In recent years, excavations lower in the deposit, including the Jacovec cavern and the Silberberg grotto, have produced hominid fossils attributable to Member 2. These were initially believed to be around 3.5 million years old.

The most important fossils from Member 2 belong to the specimen StW 573. The foot bones of this skeleton were initially found in a dump of breccia outside the cave (Clarke and Tobias 1995). The origin of the bones was traced to Member 2, and they were matched to the broken end of a tibia still in situ in the Silberberg grotto. The skeleton is now known to be largely complete, including a skull and mandible, forelimb and hindlimb elements, and much else. It appears to be considerably more complete than the "Lucy" skeleton from Hadar, AL 288-1, or any other australopithecine, but it is not yet fully excavated from the overlying breccia and flowstone. The idea that this skeleton might date to 3.5 million years was potentially very important. At this date, it would be a contemporary of A. afarensis from Laetoli and Maka (it would be earlier than the Hadar deposits). It is not clear yet whether StW 573 anatomically resembles A. afarensis or is more similar to later South African hominids, but this would certainly be an important question to answer from the respect of early hominid phylogeny.

Making Sterkfontein later

McKee (1996) suggested that Member 2 was likely immediately earlier than Member 4. His argument was that the fauna of Member 2 were all found in Member 4, but several species were absent from Makapansgat Member 3 and 4, which date to between 3.2 and 2.9 million years. He proposed that this could be explained by the chance lack of these species at Makapansgat, but viewed that possibility as less likely than the hypothesis that the species appeared after Makapansgat Member 4, to be found in the later Sterkfontein deposits.

Clarke and Tobias (1996) responded to this argument by noting the long stratigraphy of Member 3 between the Member 2 and 4 sequences, with several flowstones that must have taken a long time to deposit. They note that although Makapansgat does not preserve all the Member 2 fauna, the species that are absent are known from other African sites prior to 3.5 million years, and therefore are not of use in dating the deposits. The exception is one baboon species, Papio izodi, which is known only from Member 4 and Taung, and may therefore be rare enough to be absent from other sites.

Berger and colleagues (2002) argued that the entire Sterkfontein sequence is substantially later than had previously been thought. They base their argument on biostratigraphic and paleomagnetic considerations. They have a number of reasons for this:

1. The presence of Equus in the deposit, which is not radiometrically dated in Africa earlier than 2.36 million years ago.
2. In addition to Equus, several other taxa are found in Member 4 that do not have secure radiometric dates above 2.5 million years anywhere in Africa.
3. A later date for Member 4 would suggest that the sequence of magnetic samples from the site should be displaced earlier by a reversal cycle. This would place the top of Member 2 within the Olduvai subchron, and the StW 573 hominid would then date to between 2.15 and 3.04 million years ago. If this is displaced by another cycle more recently, StW 573 would date to as recently as 1.07 to 1.95 million years.

As far as Equus, Kuman and Clarke (2000) are at pains to show that it actually may not occur in Member 4. According to them, only one equine tooth has been excavated from Member 4 in situ, with the remaining bones taken from fill that may derive from Member 5. They argue that the one tooth is insufficient evidence of the presence of the genus, considering the possibility of erosion from later deposits.

Making Sterkfontein earlier

Partridge and colleagues (2003) dated the Sterkfontein Member 2 deposits by using the radioactive decay of cosmogenic isotopes. These are created when cosmic rays from outer space interact with the elements in quartz grains near the earth's surface. In particular, aluminum-26 and beryllium-10 accumulate in quartz grains at a predictable ratio. These two isotopes have different half-lifes (²⁶Al = 1.02 million years, ¹⁰Be = 1.93 million years), which means that once the quartz grain is buried and no longer exposed to cosmic rays, the ratio of the two isotopes changes.

Sediments near the StW 573 specimen gave a date estimate of 4.17 million years, while the orange breccia in the Jacovec Cavern gave an estimate of around 4.02 million years. These date estimates are substantially earlier than were previously estimated for these localities at the site.

It was not possible to date Member 4 in this way, because it is shallow enough that cosmic rays can still affect the quartz grains used for dating.

Partridge et al. (2003) do not present a response to Berger et al. (2002), except to note that their earlier dating "is unsustainable on stratigraphic and faunal as well as on paleomagnetic grounds" (612, note 12). In any event, there seems to be no strong biostratigraphic reason to place Member 2 at either an earlier or later date; the preserved fauna is not specific as to age.

Member 5 stratigraphy

Kuman and Clarke (2000) review the stratigraphy of Member 5. The most important hominid specimen that has been attributed to Member 5 is StW 53, a nearly complete skull that has been variably attributed to A. africanus or Homo habilis. Kuman and Clarke (2000) show that the skull derives from an area that likely is intermediate in age between Members 4 and 5 proper. They call this area the "StW 53 Infill." No artifacts derive from this area. The authors argue that the infill is likely more recent than Member 4 because of the presence in the deposit of Theropithecus oswaldi, a species found in the later Swartkrans Members 1--3, and associated with drier open grassland habitats. On this basis, they place the StW 53 Infill between 2 million years ago and 2.4 million years, which marks the earliest appearance of T. oswaldi in East Africa.

According to Kuman and Clarke (2000), Member 5 can be divided by the presence of two distinct tool industries. The Oldowan Infill dates to between around 2 million and 1.7 million years ago, and preserves 3245 excavated artifacts (Field 1999). The paleoenvironment seems to indicate a grassland. The later phase is referred to the Acheulean because of the presence of bifaces, and is placed between 1.7 and 1.4 million years ago. Like the earlier Oldowan infill, the Acheulean infill represents a predominantly grassland fauna, similar to Swartkrans.

Kuman and Clarke (2000) provide a list of hominid fossils with their probable associations in the stratigraphy. They also discuss the taxonomy of the fossils and their resemblances with elements of the earlier Member 4 and Swartkrans remains.

More on Sterkfontein

More on Makapansgat

References:

Berger LR, Lacruz R, de Ruiter DJ. 2002. Brief communication: Revised age estimates of Australopithecus-bearing deposits at Sterkfontein, South Africa. Am J Phys Anthropol 119:192-197.

Clarke RJ, Tobias PV. 1995. Sterkfontein Member 2 foot bones of the oldest South African hominid. Science 269:521-524.

Clarke RJ, Tobias PV. 1996. Faunal evidence and Sterkfontein Member 2 foot bones of early hominid. Science 271:1301-1302.

Field AS. 1999. An analytic and comparative study of the Earlier Stone Age archaeology of the Sterkfontein Valley. MasterÕs thesis, University of the Witswatersrand.

Kuman K, Clarke RJ. 2000. Stratigraphy, artefact industries and hominid associations for Sterkfontein Member 5. J Hum Evol 38:827-847.

McKee JK. 1996. Faunal evidence and Sterkfontein Member 2 foot bones of early hominid. Science 271:1301.

Partridge TC, Granger DE, Caffee MW, Clarke RJ. 2003. Lower Pliocene hominid remains from Sterkfontein. Science 300:607-612.

Pickering and colleagues (2004) examine the fauna from Sterkfontein Member 2, coming to the following conclusion:

In summary, the mammalian fauna from Member 2 indicates a paleohabitat that was probably typified by rolling, rock-littered and brush- and scrub-covered hills (suitable for caracals and Makapania, and also commonly exploited by papionins). The valley bottom might have retained standing water year-round, and perhaps supported a tree line or restricted riverine forest, fringed by open woodland or grassland -- a setting appropriate for Alcelaphini, the abundant monkeys, and ambush predators, such as leopards (292).

The authors find this paleoenvironmental reconstruction to be basically similar to other contemporary hominid sites, such as Kanapoi (Wynn 2000), as well as the fauna from the Jacovec cavern. All of these contrast with earlier hominid sites, which were predominantly closed woodlands (WoldeGabriel et al. 2001; Pickford and Senut 2001). Indeed, WoldeGabriel and colleagues (2001:177) conclude that:

The demonstration that the earliest hominids consistently derive from strata bearing indicators of wooded environments may explain their rarity at some sites. It therefore seems increasingly likely that early hominids did not frequent open habitats until after 4.4 Myr. Before that, they may have been confined to woodland and forest habitats.

The final conclusion of Pickering and colleagues (2004) is about the relative abundance of hominid fossils, which are much rarer in the overall composition of the fauna than at sites like Kanapoi. They consider that this relative absence of hominids may either result from a relative scarcity of hominids in the environment, or instead from taphonomic biases that may have led hominids to be underrepresented in Member 2 in particular. They point out that the Member 2 hominids are relatively unaffected by carnivores, with an absence of toothmarks or other indicators of predation. This contrasts with the hominid fossils from the open-air sites in East Africa, where marks from carnivores and other predators are common In their view, the hominids mainly got into the deposit by walking in and dying. This is not as common as carnivores carrying in prey to eat it, but both recent papionins and hominids are known to enter caves -- in the case of the baboons, apparently because caves are cool places to escape the sun. They do not evaluate whether predation may have been higher in Member 4, but are apparently open to the possibility that differences in the taphonomy are mainly consequences of differences in hominid behavior.

More on Sterkfontein

More on A. africanus

References:

Barrett L, Gaynor D, Rendall D, Mitchell D, Henzi SP. 2004. Habitual cave use and thermoregulation in chacma baboons (Papio hamadryas ursinus). J Hum Evol 46:215-222.

Leakey MG, Feibel CS, McDougall I, Ward C, Walker A. 1998. New specimens and confirmation of an early age for Australopithecus anamensis. Nature 393:62-66.

Pickering TR, Clarke RJ, Heaton JL. 2004. The context of Stw 573, an early hominid skull and skeleton from Sterkfontein Member 2: Taphonomy and paleoenvironment. J Hum Evol 46:279-297.

Pickford M, Senut B. 2001. The geological and faunal context of Late Miocene hominid remains from Lukeino, Kenya. C R Acad Sci Paris Sciences de la Terre et des planetes 332:145-152.

Ward CV, Leakey MG, Walker A. 2001. Morphology of Australopithecus anamensis from Kanapoi and Allia Bay, Kenya. J Hum Evol 41:255-368.

WoldeGabriel G, Haile-Selassie Y, Renne PR, Hart WK, Ambrose SH, Asfaw B, Heisken G, White TD. 2001. Geology and paleontology of the late Miocene Middle Awash Valley, Afar Rift, Ethiopia. Nature 412:175-178.

Wynn JG. 2000. Paleosols, stable carbon isotopes, and paleoenvironmental interpretation of Kanapoi, northern Kenya. J Hum Evol 39:411-432.

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:

1. Australopithecines may have eaten underground storage organs of C₄ plants, such as grass corms or tubers of certain sedges.
2. They may have eaten seeds from C₄ grasses.
3. They may have eaten the meat from grazing species.
4. They may have eaten termites that relied on grasses and other C₄ species.
5. 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:

1. High Sr/Ca ratios in A. africanus
2. Moderate Sr/Ca ratios in A. robustus
3. High proportion of C₄ sources in both A. africanus and A. robustus
4. Dental anatomy unsuited to leaf or grass eating in either species
5. 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:

1. 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.
2. 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.
3. 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.
4. 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.
5. 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:

• 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

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.

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:

1. If australopithecines had basically similar C₄ dietary proportions, then what accounts for their differences in Sr/Ca ratios?
2. Did any A. africanus-like hominids ever coexist with a robust australopithecine species?
3. 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?
4. 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.

I (and others) have had about a week to reflect on this new skeleton and its significance. There is little question that this is one of the most vexing discoveries ever.

To understand why, compare the situation with that surrounding a major find like Lucy (AL 288-1). Lucy (and the Hadar sample as a whole) presented little new or interesting information about the morphology of australopithecines. The Sterkfontein sample, which had emerged over the thirty years prior to the Hadar discoveries, demonstrated nearly everything important about the australopithecine adaptive pattern--including body size, dental characteristics, evidence for bipedality, and brain size. The story from Hadar was that it was older than everything else then known, and that there was a relatively complete skeleton that associated much of the important morphology into a single specimen. This is why Lucy now has such importance in our textbooks, but the fact is that almost everything interesting was known long before.

One might say some of the same things about Liang Bua. It looks in many respects like we know some early hominids looked (although admittedly with many differences in detail). But here the differences in time and place are a much greater story, because they upset so much more. A "new earliest hominid" does little but push back the date of hominid origins, especially since none of the "new earliests" have been particularly informative about the ancestral condition (they are all obligate bipeds so far, and none of them is very chimpanzee-like, notwithstanding the dentition of Ardipithecus). But Liang Bua is striking because it has no obvious ancestor. If it is an australopithecine, where are the earlier Asian australopithecines that it descends from? Meganthropus? If it descended from early Javan humans like Sangiran, then what accounts for the necessary selection for smaller brains leading to this specimen?

Only if LB1 can be attributed to pathology are these questions less pressing. In that case, it represents just one of (potentially) many human populations that lived on Flores or passed through it on the way to Sahul, Melanesia, and points east. The pathology hypothesis has not yet been refuted, and it is important to keep that in mind.

Do the tools belong to LB1 or its ilk?

With a 380 mL brain, LB1 is at the bottom of the range of australopithecine brain sizes. After the advent of stone tools 2.6 million years ago, no known hominid has a brain size of less than 400 mL, and most paleoanthropologists have assumed that the manufacture of stone was accomplished by species with brain sizes that averaged 500 mL or more. It is not at all clear to what extent the mass of neural tissue is related to tool manufacture or any other capabilities. Perhaps it is the case that the essential changes affected the structure of the brain rather than its size, and a smaller brain might well have the circuitry to accomplish many advanced cognitive tasks. It is certainly true that chimpanzees are capable of tool use, the mastery of rudimentary symbol manipulation, and cooperative foraging, despite having brains that average 400 mL or less.

On the other hand, modern humans reached Australia by 50,000 years ago, and were present in island Melanesia by 30,000 years ago. The route to both of these places passes through Flores, so it is highly probable that modern humans were present on Flores 18,000 years ago, when the LB1 lived.

In this context, I think we can reasonably assume that the stone tools, fire, and evidence of Stegodon hunting can be attributed to these modern people. Colin Groves has sent me a reference to an ABC News story where he makes much the same argument.

This leaves the two main hypotheses about LB1:

1. it was a pathological member of this modern human population
2. it was part of an earlier hominid population alongside these modern humans

In the second case, we can speculate about the relationship of these populations. Perhaps LB1 was a victim of the modern humans: i.e. it is in the cave for the same reason the Stegodon remains are in the cave. Perhaps the tiny-bodied population avoided the modern humans in the same way as today orangutans avoid modern people on Borneo and Sumatra. This might imply a very different ecological role for these smaller hominids, considering the ecological breadth and travel potential of the modern humans alongside them.