diet

Last week, Nature published a paper by Christine Austin and colleagues, in which they developed a new approach to understand how breastfeeding affects the elemental content of tooth enamel [1]. Barium and strontium are chemically similar to calcium (all three are in the same column of the periodic table of elements), and a small fraction of both elements are incorporated into enamel and dentine in place of calcium. The fractions of barium and strontium incorporated in teeth depend on an individual's diet; different food sources have different concentrations of these elements. So the concentrations of these elements in tooth enamel give some indication of the diet sources that an individual relied upon when her teeth were developing.

Two of the most significant diet changes occur early in life -- the change at birth when an infant begins relying upon mother's milk, and the change at weaning from milk to other kinds of foods. Austin and colleagues set out to examine whether they could reliably determine the timing of these two transitions, based upon knowledge of the enamel deposition process:

We propose that micro-spatial analysis of barium/calcium ratios (Ba/Ca) in dental tissues represents a powerful approach to assess dietary transitions. Whereas prenatal Ba transfer is restricted by the placenta, marked enrichment occurs immediately after birth from mother’s milk or infant formulas, which contain higher Ba levels than umbilical cord sera. In response to these variations in dietary Ba exposure, Ba/Ca in enamel and dentine should increase at birth, remain elevated for the duration of exclusive breastfeeding and rise further with introduction of infant formula. Circulating Ba levels are expected to change at weaning as Ba (and Ca) content and bioavailability is markedly different across plant and animal food sources. To test this hypothesis, we investigated Ba/Ca patterns in teeth from human children for whom early life diets were recorded prospectively, and in teeth from captive macaques in which maternal milk was collected and suckling behaviour observed.

They applied their method to deciduous teeth that came from children whose mothers had participated in the Center for the Health Assessment of Mothers and Children of Salinas (CHAMACOS) study in Monterey County, California. This allowed Austin and colleagues to examine the fraction of barium in enamel and dentin, layer by layer, within children whose diets had been recorded including the dates of exclusive breastfeeding, supplemented breastfeeding, transition to infant formula and full weaning. The sample of teeth is not very large (only 25 individuals) but the barium signals within the teeth tracked very well with the dates reported for birth, breastfeeding and transition off milk. Additionally, Austin and colleagues considered the teeth of four macaques whose record of suckling and weaning had been recorded. The macaques did not have the confounding influence of formula supplementation, and their barium/calcium signatures gave quite clear records of natural, gradual weaning versus abrupt weaning upon the separation of mother and juvenile.

Although both barium and strontium may provide a signal of these diet changes, Austin and colleagues focused on barium because strontium is more likely to be shifted within ancient tooth enamel after it has been buried in the ground. The goal of the paper was not only to show that the signature of breast feeding is consistent within living populations (in this case, macaques and humans) but also to provide a way to infer these dietary transitions in ancient primates. To that end, they examined the pattern within a Neandertal tooth from Scladina, Belgium:

Chemical and temporal mapping of Neanderthal first molar enamel (Fig. 3) revealed a transition pattern similar to the macaque that weaned abruptly. After approximately 13 days of prenatal enamel formation, Ba/Ca near the enamel–dentine junction increased and remained elevated until approximately 227 days of age (~7.5 months), followed by intermediate values until 435 days of age (1.2 years). After this age Ba/Ca rapidly returned to prenatal levels for the final 1.15 years of crown formation.

They infer that the Neandertal child was moved off exclusive breastfeeding to partial supplemented breastfeeding at around 7.5 months of age, which the authors suggest is consistent with the pattern in other primates. Then, they suggest that the extended period of breastfeeding in conjunction with solid food supplementation was "abruptly" cut off at the unusually low 1.2 years. After that time, the child continued to grow, apparently without mother's milk.

Katie Hinde, one of the authors of the research paper, has written a blog post giving a lucid explanation of the research and its background: "Teeth and Weaning and Neanderthal… OH MY!" She discusses whether the Scladina tooth is sufficient to make inferences about Neandertal life history more generally:

So do we think we know the species typical pattern of Neanderthal weaning? Not at all. The precipitous decrease of barium at 1.2 years of age pretty clearly suggests that the Scladina Neanderthal was abruptly weaned in a non-typical fashion.

...

We have a really powerful way to investigate the period of exclusive milk feeding and the weaning process with high precision and resolution. For the first time we have a method to look at individual differences in these parameters in primates “collected” by old school naturalists gathering dust in natural history museums or skeletal material recovered at primate field sites. And we can do this in well-preserved fossil hominins... if colleagues are willing to share.

I think this research is really great, and I was talking about it the other day as an example of how we are uncovering evidence about ancient people that was previously invisible to us. Obviously, I'd like to see the same kind of analysis extended to much larger samples of teeth. This paper is a very promising start to the research, but we need to understand what variation there may be within living humans who are eating a broader range of diets, and who may have somewhat different patterns of tooth development.

What I think is most encouraging about this line of research is that breastfeeding may give a natural chemical tracer that will allow researchers to confirm the periodicity of enamel formation in people of known breastfeeding history. A problem in earlier research on tooth development has been the lurking possibility that the deposition process varies among people in ways that make inferences about life history and diet transitions in prehistoric humans somewhat doubtful. A more extensive record of comparative work on breastfeeding and tooth development, with large human and primate samples, has the potential to test whether between-population and within-population variation in developmental processes is important here.

As the research develops, I keep reflecting on the plasticity of childhood development. Here we see breastfeeding as an influence upon the stable isotopes represented in teeth, but the teeth grow with or without that food source. One of the macaques showed a pulse of increased barium after being weaned entirely, which the authors suggest may have been caused by the release of barium and calcium from the skeleton and incorporation in the teeth. Our bodies use stored minerals within the skeleton as a reservoir for later biochemical needs, and acquisition of nutrients from the mother's bodily stores is an important part of that process. Human development relies upon buffers against environmental variability, and in certain physiological processes -- such as enamel formation -- we see a complex trace of those buffers interacting with extreme shifts in environmental resource availability.

This is a really complicated way of saying that our bodies have to cope with losing people, because our ancestors lost their parents much more often than we do today. The Scladina child was part of this heritage of survival.

References

Joseph Ferraro and colleagues have done some neat analyses of the faunal remains from Kanjera South, Kenya [1]. Kanjera South is an archaeological assemblage of Oldowan artifacts and associated animal bones from around 2 million years ago. The site was once a plain next to a lake, and gradually built up clay and silt sediments over years and years of flooding and soil formation. Stone tools and bones stand out in the sediments, representing recurrent activities of ancient humans over a few hundreds or thousands of years. As a result, the site has a good statistical representation of fauna that were hunted by early humans, relatively early in the evolution of our genus.

This is not the earliest site with evidence for meat acquisition by stone toolmakers. We know that people were butchering animals with stone tools around 2.6 million years ago. But the first really good evidence for hunting strategies is much more recent -- around 1.8 million years ago at Olduvai Gorge. There are actually very few Oldowan-era faunal assemblages large enough to study hunting behaviors. Kanjera South shows that the activities documented at Olduvai Gorge were happening a bit earlier, and the site helps to clarify the kind of context in which we might expect to find more evidence of hunting behavior.

Hunting versus scavenging is the tiredest chestnut in anthropologists' Oldowan arsenal. Were early hunters really competent enough to bring down a duiker on their own? Or did they steal away pieces of half-eaten zebra carcases when the lions took a break?

In reality, there is no contradiction here. Undefended meat doesn't last a day in the open, whether on the plains or near waterholes. So scavenging meat from other carnivores usually means facing them down -- not a job for an incompetent killer. Meanwhile, present-day peoples who hunt and gather rely quite a lot on "power scavenging", or taking advantage of other carnivores' successes. The present value of a dead carcass is higher than that of a live animal, as long as it may still escape you. Whether the hunter has to predict prey behavior, or the scavenger has to predict competitors' behavior, both strategies require a depth of planning. So, when it comes to Oldowan-era sites, we should expect to see a mixture of hunted and scavenged remains.

In that context, we can make some inferences about hominin hunting practices by assessing which kinds of animals they hunted, and which they scavenged. Looking at tooth mark and cutmark evidence is not a perfect way of sorting hunting and scavenging -- because both kinds of marks are rare on faunal elements in archaeological contexts. But sometimes those comparisons lead to clear results. For example, here is the chart showing the number of tooth-marked midshaft fragments from long bones at Kanjera South, in comparison to experimental bone assemblages:

Figure 3 from Ferraro et al. 2013. Original caption: Tooth-marked mid-shaft fragments: results from experimental assemblages and excavations at KJS. Figure follows a published model [26]. Hominin-first assemblages refer to remains initially defleshed and demarrowed by hominins, then subsequently exposed to large-bodied carnivores (primarily hyenas). Carnivore-first assemblages refer to remains initially defleshed and/or demarrowed by large-bodied carnivores (primarily hyenas and/or lions). Data for body sizes 1–4 [21]. Modern data (with single standard deviations where available) derived from the literature [23]–[26], [56]–[58]. KJS frequencies are from Table 2 and Table S1. Multiple symbols for KJS indicate the results of multiple analysts. X’s indicate minimum and maximum estimates of damage (see Table S1). doi:10.1371/journal.pone.0062174.g003

These are cool data. Carnivores who get to chew on bones for a while tend to leave the middle of them covered in tooth marks. If humans get access to the carcass early, they will strip off the meat from those midshafts, break them into bits, and otherwise prevent the taphonomic pathway to carnivore tooth marking. And in the graph we see that the Kanjera South faunal assemblage looks like cases where humans were the agents of defleshing and butchering.

If humans had primary access to the carcasses, then the transport decisions of ancient hunters should have shaped the bone assemblage at Kanjera South. It is very common in analyses of the fauna from African Oldowan-era sites to divide the prey animals into three size classes -- small, medium and large. The majority of prey species were bovids, ranging from small antelopes to water buffalo, although most were in the small and medium size categories at Kanjera South. Ferraro and colleagues show that for medium-sized bovids, the hominins were taking two strategies. These bovids were too big to carry wholesale to a central place for sharing. So the hunters disarticulated the animals and carried back the legs, leaving the axial skeleton for the most part behind.

Except for the heads:

But why acquire, transport, and process an abundance of medium-sized heads? In living animals, these remains contain a wealth of fatty, calorie-packed, nutrient-rich tissues: a rare and valuable food resource in a grassland setting where alternate high-value foodstuffs (fruits, nuts, etc.) are often unavailable [2], [3], [29], [49], [52], [63], [76]–[78]. Medium-sized heads are also relatively dense and durable elements, and their internal contents are generally inaccessible to all but hyenas and tool-wielding hominins [63], [79], [80]. As a result, they are often seasonally-available as scavengable resources in East African grasslands [63], [76], [79]–[83]. Additionally, bone surface modification studies at KJS clearly demonstrate that hominins accessed internal head contents: several cranial vault and mandibular fragments bear evidence of percussion striae. Considered in sum, the presumed availability of these isolated remains across the landscape, the relative abundance of these remains in the KJS assemblages, and unambiguous material evidence that hominins exploited their contents on-site is most parsimoniously interpreted as reflecting very early archaeological evidence of a distinct hominin scavenging strategy – one that included a strong focus on acquiring and exploiting fatty, nutrient-rich, energy-dense within-head food resources (e.g., brain matter, mandibular nerve and marrow, etc.) [e.g., 24,63,76,82,84–86].

This is John Speth's scenario for fat acquisition from lean animals. The brain is the last part of the body to become fat-depleted during times of stress. If hunters are energy-limited, further lean meat is not going to be valuable to them because protein takes energy to digest. What they need most is fat, and the most ready source of fat is the brain. Accumulation of head elements, whether from hunted or scavenged sources, is an effective behavioral strategy in those circumstances. It's one that we think Neandertals pursued at the end of winter in some parts of Europe, and a strategy followed by hunters in ethnographic and historic contexts as well.

The paper's conclusion is well-framed as a summary of the overall value of evidence from Kanjera South.

With regard to evolutionary ecology, the relative uniformity of hominin activities documented through the KJS sequence indicates an evolved foraging adaptation well-tuned to local ecological contexts. This point implies that hominin involvement with, and their presumed consumption of, animal remains had substantial fitness implications. In turn, sufficiently strong selective pressures are implicated as having favored the evolution of persistent hominin carnivory no later than 2.0 million years ago. This date is approximately 200,000–500,000 years earlier than previously documented [11], [20], [33], [45], and increases the known time depth of this adaptation within the hominin lineage (range of dates reflects varied interpretations of faunal materials from Olduvai [20]–[42]).

This one was fun to read, because the data being built up at Kanjera South are really capable of testing hypotheses about hunting behavior in a way that some of the Oldovai Gorge assemblages have done up to now. Putting the faunal exploitation together with the stone tool evidence, we see a really interesting picture. As I reported a few years ago ("Plant processing with early Oldowan tools"), Kanjera South is one of the locations where we have good evidence of plant exploitation of some kind by Oldowan peoples. The site has also provided evidence about stone material transport decisions and the planning depth of stone flaking ("Technological sophistication of the earliest toolmakers". It is a good illustration of how deep knowledge of a single site, with teams returning to excavations over multiple seasons, can yield a richness of statistical information about hominin behavior.

References