Thursday, 23 November 2017

The lost rice of South America

One of my pet interests is lost crops, or largely forgotten ones-- species that were important in the past which are either completely lost from cultivation today or very nearly so. They serve to remind us that the ethnographic present does not provide a full range of potential economic activities nor the full range of crops. They demonstrate that archaeobotanical evidence can provide important broadening of our list of potential crops to consider in future breeding and sustainability efforts. An endemic rice of South America can now be added to the list of lost crops.

This exciting find, that received quite a bit of media attention (e.g. in Science) was the recent report of a rice that was apparently undergoing morphological change, i.e. domestication. The archaeobotanical evidence, published in Nature Ecology and Evolution last month by Hilbert, Iriarte and colleagues as part of the ERC Pre-Colombian Amazon Scale Transformations project, comes 

from  phytolith anaylses through a stratigraphic sequence at the site of Monte Castelo in southwest Amazonia, dating to between 5300 BP and 700 BP, which includes rice husk phytoliths (the double-peaked cells) and bulliform throughout. The proportion of rice increased somewhat in the past 4000 years, but shifted especially towards a much higher ratio of husk types to bulliforms, suggesting the concerntration of husk phytoliths that one might expect from dehusking or harvested rice spikelets. It is at this stage that the shape of the husk phytoiths also starts to change, with phytoliths getting wider, taller and with more pronounced peaks. These are the kinds of changes that may be indicative of a domestication process and be a proxy for increasing grain size. The change takes places somewhere in the upper levels of the site, which are unfortunately not well constrained in dating, except being younger than 4000 BP and up to 700 BP or so. This suggests that the inferred domestication process took place or was even ongoing upto shortly before Colombian arrival from Europe and Amazonian population decimation.


One can quibble over whether changes in husk and inferred grain size increases must be human caused. The classic case of such a change in Chinese rice is decidedly NOT about domestication, as it takes place in sites South of Yangtze at the transition from the LGM to much warmer conditions, i.e. around 18,000-16,000 years ago. A full 10,000 years before the appearance on non-shattering rice spikelet bases appear-- domesticated by definition. When originally published by Zhao (1998 Antiquity) this was mistakenly dated to the Holocene, and thus inferred to represent domestication, but this falled a false equations (domestication because change is start of Holocene; start of Holocene because advent of ceramics could not possibly be any earlier). We now know the advent of ceramics transition in China took place around 18,000 years ago at Yuchanyan and possibly even earlier at Xianrendong, as already discussed for at least 7 years (e.g. Fuller et al. 2010). while domesticate rice, i.e. that was dependent on humans for dispersal, evolved during the middle Holocene, with the earliest large assemblage of non-shattering spikelet bases at Baligang by ca. 6500 BC and predominance in the Lower Yangtze as late as ca. 4000 BC (for a updated summary see here). It now appears most likley that the morphological change in husk phytoliths in South China was driven by the rapid climate change and especially the increase in carbondioxide which has major repercussions on plant productivity and morphology (see experimental work by Cunniff et al 2010), and thus the near doubling of carbondioxide that took place in the millennia just after the LGM (along with increasing temperature) ought to have hade major effects on rice productivity and aspects of morphology).

However, in the past 4000 years it seems unlikely that there were any climate or carbon dioxide shifts on quite the necessary scale, which makes the inference of a local rice domestication process much more likely.  A shift in grain size, however, would be expected to be accompanied by some selection for reduced shattering-- as this co-evolves in all of our better documented cereal domestications, most notably in Asian rice. Thus good flotation samples, with the required fine mesh of ca. 250 or 300 microns, ought to produce small charred rice spikelet bases. Recent experience suggests that everywhere we look, and do the requisite flotation, in tropical Asia, we find now that rice spikelet bases greatly outnumber charred grains and this tells us that they survive well and are archaeobotanically recoverable. This is also true to the major rice growing areas along the ancient Niger river. Some macro-remains would seem the obvious next step to pinning down more details about the evolution of this lost rice of South America. It would be highly unexpected if selection for larger grains did not take place alongside increases of indehiscent spikelet bases, as these co-evolve in other well documented cereals (as illustrated in a PNAS 2014 article).

It is also highly likely that increase in grain size implies management of soils, i.e. some sort of cultivation. This is contrary to the novel, but rather unconvincing, hypothesis of the authors that grains would have been encased in clay and dropped into the water. They cite as an ethnographic parallel systems of reseeding American wild rice (Zizania palustris) stands in the Great Lakes region of North America. But in that context there is no evidence for prehistoric grain size increase or domestication processes.The rice represented at Monte Castelo was likely a productive annual, as the authors note, and could have been encouraged by burning of competing vegetation after seeds are shed, in which case selection for seed size increase can be expected from the levelled playing field conditions of freshly cleaned fields which put a premium on rapid seedling establishment against competition from conspecific seedlings. 

South America boasts 4 indigenous wild rice species, Oryza alta, O. latifolia, O. grandiglumis, and O. glumaepatula, and only the last has annual ecotypes. South America's O. glumaepatula is also an AA genome, like domesticated Oryza sativa or Oryza glaberrima, and thus this suggests something inherently attractive for, or conducive to, domestication in the AA wild rices. Like Oryza species everywhere these are water-loving grasses, but there are still two ends of a spectrum from perennials in deeper water and annuals and places that are seasonally dry. Oryza alta, which can form mats along river margins, is a perennial (see, for example the photo at left lifted from Duncan Vaughan's 1994 monograph on the wild rices). Annual Oryza are prolific seasonal grain producers, and thus lent themselves easily to forager intensification, and it was such annuals that were ancestral of the early cultivars of Asian indica and aus rices, or African glaberimma (from wild annual O. barthii). By contrast perennial rices are less prolific grain producers due to investment in perennating stems, roots and more leaves. Thus Asian rices when available ought perhaps be expected to be used resources. The other continent with annual AA genome wild rices in Australia, where these are found in the northern parts. Lets see some archaeobotanical work carried out there, in the region of Oryza meridionalis, as one might expect parallel evolution for utilization and even management there.


Tuesday, 21 November 2017

Using big machines to look at the finer aspects of seeds

This year has seen three studies on high resolution x-ray computed tomography applied to archaeobotany, one using ct-scanning to recovered chaff hidden in ceramics (see Finding Rice Domestication in Clay), and two using a synchrotron to peer inside seeds, including soybeans and horsegram.

http://www.diamond.ac.uk/Home/About.htmlThis past summer, I published with colleague Charlene Murphy, a Scientific Reports article on domestication of the Indian crop horsegram. While this article represents an important contribution on the domestication history of a major crop in India, and evidence for evolution of morphological change during that crops domestication in South India (see also our GRCE paper, reviewing all that is known about horsegram origins), this is really more significant for the methodological contribution to the archaeobotanical documentation of domestication. We were able to put our small archaeological seeds in a very large machine, the Diamond Light synchrotron (shown at left). which allowed us to non-destructively capture the the internal structure of the entire seed (not as straightfoward as it sounds as it takes a lot of computing time). And from this we could measure seed coat thickness on any of the 1000s of cross-section slices through our seeds (like that below/right)
horsegramOne of the well-known domestication syndrome traits in pulses is the thinning of the seed coat, tied to loss of germination inhibition. But it has been difficult to document this archaeologically. Seed coats are often destroyed in charring, but even if preserved they study on charred seeds would require destructive breaking of seeds. And even if damaged, it might only be possible to document the seed coat thickness in one or two places with an SEM or high powered normal microscope. As a result this has been rarely documented, which has lead to a fair degree of speculation on the evolution of thin-seedcoat, readily germinating pulses, as the result of conscious selection of the readymade mutants in the wild (although none have been documented in the present day)-- the domestication before cultivation hypothesis applied to lentils-- or positing a rapid conscious selection by those who initiated cultivation-- lets call this the pea breeding before agriculture hypothesis. The truth appears to be, however, a gradual evolutionary process as seed coats thinned over time, much like the evolution of increasing seed size or the non-shattering in cereals-- at least in horsegram. This can be seen in the chart below showing the thinning seed coat along side a trend in seed size increase in horsegram. Further work is needed on additional pulses to see if this pans out as typical of the pulses domestication processes, or whether there was variation, or indeed any cases of plucking domesticated types from the wild-- of which I am doubtful. At least now we have a method for approaching this.
This is actually, quite logical: established stands of pulses could be maintained and wild-type dormant seeds would constitute an established seed, and would recurrently add new plants to the the stand over a series of years. But due to annual human harvests mutations that reduced dormancy would get selected, and would be particularly important for any new populations planted in areas without existing wild populations. In this context we can expect the gradual evolution for thinner coated, more easily germinating seeds through selection across what are presumably multiple loci, as is evident in our archaeological horsegram data (shown left).

Soybean oil content in charred seeds?
The claim for earliest use of a synchrotron to look at charred archaeological pulse seeds, however, goes to our colleagues in China, in collaboration with Prof. Gary Carwford, Shandong archaeobotanist Xuexiang Chen. They argue that soybean underwent selection for increased oil content in prehistory during domestication-- undoubtedly true-- and that this can be tracked archaeological through a change in the number and size of pores visible on the inside of charred soybeans viewed through the synchrotron and High-Resolution Computed Tomography. I remain unconvinced on this last point, and although the paper reports on examination of modern soybeans and, other oily crop seeds, and experimentally charred seeds none of these are illustrated or really described so as to support this interpretation. The authors infer that more small pore is a product of more oil whereas large pores represent burned out protein, but is this true. The differences look to me more like artefacts of carbonization processes, and not a good proxy for the internal anatomy of the original uncharred soybeans. As the few illustrated example suggest larger and irregular pore are present in seeds with more distorted external surface anatomy (e.g. c), whereas small pores are more evident in better preserved examples (e.g. f).

Unfortunately, the central claim in this paper does not really add up, or at least are not well justified and explained in the text. This makes me very nervous about accepting the main conclusion of the paper, i.e. that the authors have demonstrated an increase in oil content in soybean during domestication by measuring the quantity of bubbles (voids) of different sizes in charred archaeological soybeans. Small voids are attributed to oil content and large voids to protein—but this is never demonstrated (for example in modern and experimental charred examples) or backed up by citations on soybean anatomy, as to why these voids should differ between oil and protein. That soybeans are oily, in contrast to most pulses is clear, but this also has major implications for the nature of archaeological finds. Most carbonized archaeological soybean are poorly preserved, distorted, full of large voids and small voids and very shiny on their interior. This is contrast to pretty much every other pulse I have seen archaeobotanically, from Vigna spp. to lentils and peas to Lablab. Even in the Chinese samples, presumably subjected to similar formation processes Vigna angularis seed present typical features of carbonized pulses, including a dense charred matrix with distinct cotyledons. In Glycine cotyledons are rarely evident and their interiors are heavily distorted by voids and bubbles. The obvious deduction is that this state of things is the result of the oil content in soybeans, and of course many other oily seeds, from cotton to sesame, also tend to show similar levels of bubbling and porosity when charred. If large voids in soybean are due to protein burning up during carbonization then surely one would expect to see this in any pulse, all of which have at least 20% protein content. It is true that the oil in soybean is contained in fresh seeds in many small droplets/sacs but upon charring things are likely to end up being very different. Oils are going to burn to more readily to gas than carbohydrates or proteins and thus create more bubbles and explosions of expanding gas. As this progresses and cracks to the outside of the seed allow penetration of gas (and some oxygen) from the exterior, one would expect this to speed up. The persistence of small voids then might be predicted to be the result of less oxidation, less temperature and perhaps other variables of charring conditions of a given seed. Cracking and penetration of gases into the charring seed may indeed be affected by aspects of domestication—thinning of seed coat, increase in seed size. Indeed, larger seeds seem likey to leave larger parts of their interior cotyledons unexposed to exterior cracks and oxygen; and in this context would be expected to preserved more small oil bubbles as a side effect of seed volume increase: i.e. the difference over time would reflect preservation artefacts rather than selection for genetic change. It is hard to see how at this stage we can deduce difference in underlying phenotype and genetics from this sort of data—at least until we have much better grasp on who charring conditions affect the distribution of seed contents, and this calls for some systematic experiments.
Undoubtedly soybeans were selected for oil content, but when and how this took place in relation to other domestication traits remains sadly unclear. I find I have to reject to conclusions of Zong et al., although their paper doe illustrate the potential analytical power of using a synchrotron to peer inside archaeological seeds

Sunday, 29 October 2017

Finding rice domestication in clay (new methods in archaeobotany)

One of the more exciting methodological developments in archaeobotany I have seen lately is the use of ct-scanning to look into chaff tempered ceramics and to extract in virtual terms the invisible plant remains therein. Aleese Baron, Tim Denham working with a range of colleagues have applied ct-scanning and computed tomography to produce images of rice chaff and rice spikelet bases from Neolithic sherds from three Neolithic sites in Vietnam published in Nature's Scientific Reports.
The sites are An Son, Loc Giang and Rach Nui. In all cases, conventional archaeobotanical evidence through macro-remains has been limited, although rice and millet as well as various wild taxa were reported from flotation at Rach Nui earlier this year. This makes the potential to recover plant remains from ceramic tempering quite tempting as an additional source of evidence on past plant use. As demonstrated by new evidence on sorghum domestication found in old sherds. However, while traditional we may cast impressions of those remains that are haphazardly represented on the surface, ct scanning allows full three-dimensional voids to be recovered from the interior of the ceramic fabric.
While patience and skill required to get such images is impressive, the results are breath-taking, with images of domesticated type, non-shattering rice spikelet bases pretty much as good as those found through flotation emerging (see left). It is not any surprise that these Neolithic folks in Vietnam were already dehusking fully domesticated rice and using the chaff to temper their ceramics-- this very much fits current hypotheses for the spread of fully domesticated rice into mainland southeast Asia from the end the Third Millennium BC (e.g. the recent review by Castillo in the journal Man in India). Methodologically, however, opens up the possibility for studying old ceramic collections from sites that may no longer be amenable to sampling through flotation or which lack good stratigraphy, at least so long as some ceramics are chaff tempered. This could prove quite useful for any earlier, less sedentary phases in the spread of rice, just as sherd impressions have proved so useful in Africa, right across the Sahara and sub-Sahara. Studying sherd impressions just got powerful new tool.

Thursday, 26 October 2017

Earlier Sorghum in Sudan (2017)





A few years ago I posted a blog on Earlier sorghum in Sudan highlighting the work by Alemseged Beldados and Constatini on sherd impressions from Kasala from the early Second Millennium BC. At the time I raised the question as to whether or not these impressions were wild or domesticasted. At the time I bemoaned the lack of SEMs and attention to spikelet base remains. That blog post attracted the attention of Frank Winchell (see his comments at the time), and around the same time Frank had met Michael Brass, then a PhD student at UCL. Through these interactions, online and eventually in person, we started a collaboration to re-examine ceramics that Frank has collected and studied from a site of Kasm el Girba 23, to the southwest of Kasala, from field work over 30 years ago. Frank has long been impressed by the present of a large number of apparently seed or chaff tempered ceramics in a ware type called Kharadag Plain, and through extensive examination in the UCL archaeobotany laboratory, casting impressions and SEM study, as well as re-assessing our reference material of domesticated and wild sorghum.


The results are highly significant, and have now been published in Current Anthropology. Domesticated sorghum morphologies were present much earlier than previously found, i.e before 3000 BC, more than a millennium earlier than the Kasala finds or finds in India. In addition the material represents a mix of almost equal parts morphologically wild (smooth spikelet base) and domesticated (torn rachilla). This suggests that the Kasm el Girba material is around midway in the domestication process, and by analogy with the protracted domestication now well documented for rice, wheat and barley, we should be considering this as an advanced stage of pre-domestication cultivation, and seeking the beginnings of pre-domestication cultivation sometime before 4000 BC. This has received some science journalism attention from Nature and Science News.

One of the other highly significant patterns is the Kasm el Girba faunal evidence, as previously published by Joris Peters: it represents a wild hunted savanna fauna. It lacks the evidence for sheep, goat or cattle, in contrast to the evidence for some pastoral component to the economies of the Neolithic around Khartoum from the Fifth Millennium BC at least. This calls into questions the widely accepted notion of "cattle before crops" in Africa (as per Marhsall and Hildebrand 2002). Certainly pastoralism gets established in parts of the Sahara around 6000 BC, long before any evidence for cultivation. It is also true that the earliest evidence for domestication of pearl millet, reported by Manning et al (2011), occurs alongside evidence for cattle and caprine pastoralism. But in this case we seem to see evidence for cultivation of early sorghum and sorghum domestication taking place among fairly sedentary hunter-gatherers and not their Sahelian pastoralist neighbours. This raises some exciting questions for further research in Sudan, and calls for renewed efforts in zooarchaeology and archaeobotany of the Early to Middle Holocene in northern Sudan, etc.

Wednesday, 23 September 2015

A tribute to Alice Berger, a research student lost too soon

A personal tribute from Alice’s PhD supervisors at UCL

This week we learned the sad and shocking news of Alice Berger’s passing. As Alice’s PhD supervisors at the Institute of Archaeology, UCL, we extend our deepest sympathies to her family and friends. Alice came to the Institute from the Department of Archaeology and Ancient Near Eastern Cultures at Tel Aviv University. Her Masters thesis on “Plant Economy and Ecology in Early Bronze Age Tel Bet Yerah” won the prestigious John Evans postgraduate prize, awarded by the Association for Environmental Archaeology, and her achievements were recognized by the further award of UCL’s Overseas Research Scholarship and Graduate Research Scholarship to support her PhD research.
Alice was a fiercely independent researcher of extraordinary capacity, breadth, and originality. She possessed a flair for environmental archaeology that was quite unusual, mastering techniques of botanical and zoological analysis that are often treated as isolated specialisms, and reminding us all that these are simply vehicles in a wider project of understanding the human past, and its changing relationships to the non-human world. Her doctoral project, teasing out the environmental correlates of Early Bronze Age urbanisation and migration in the southern Levant, was producing exciting results, presented by Alice at conferences around the world with a style and confidence that always rose to the surface when she spoke in public. She was deeply passionate about her research, which was attracting widespread praise and attention.
Alice was also a gifted and natural teacher, seeming happiest and calmest when instructing students. While some specialists are intellectual hoarders, Alice’s approach to knowledge was democratic to the core. She excelled as a teaching assistant at the Institute, and in the field at Tel Bet Yerah she transformed her laboratory into a centre of learning, taking pride and delight in the ability of undergraduates to identify prehistoric animal remains after just a short time in her company. Anyone who had the privilege to know or work alongside Alice will also know the struggles she faced on a daily basis, and the courage with which she confronted them. One always had the feeling that, whatever the obstacle, Alice would eventually emerge, smiling, resolute, and in search of her next challenge. Hers is a dreadful loss to our subject and our community, and we will miss her terribly.
But we also feel sure that Alice would not want our brief tribute to end on a sombre note. So we will finish with a recollection that perhaps captures something of Alice, and the intensity with which she seized life, both inside and outside the laboratory. It relates to Alice’s first encounter with the Institute in London, when she undertook Dorian’s intense short-course in archaeobotany. David Wengrow, her host at the time, recalls her coming to his office within a few days of arrival, to explain that she had suffered a concussion while attending a Rob Zombie concert. ‘But don’t worry’, she reassured him, ‘I actually find that as a result I can stare down the microscope for much longer periods of time’. May you rest in peace, dear Alice.  



Many more posts from Alice's friends and colleagues can be found on her facebook wall.

Early Rice Project symposium last week

Last week we hosted in London a symposium for the Early Rice Project, 
Investigating the evolution and impact of rice cultivation through the later prehistory of monsoon Asia. We brought in colleagues and collaborators on the archaeology of India, Southeast Asia and China, from countries across several continents, and had a success full exchange, not just on the archaeobotany of the region and new data (much of it generated at UCL through our NERC and ERC projects), but also on the stories of domesaticated fauna, our current understanding of Neolithic spread processes, Mesolithic persistence, demographic growth and the emergence of complex societies and irrigation. What is clear is that there is much new to say about rice, when it first arrived in several regions of monsoon Asia, and as it was transformed into the cornerstone species in the subsistence base of large complex societies. Nevertheless the meeting highlighted also the major gaps in empirical evidence, both geographically and chronologically. We hope to be able to pull this together for publication to further broaden out our dialogue on what we know and what we need to know. There has certainly been a rapid increase in data as the chart (below) of published, or recently counted archaeological spikelet bases indicates (from my introduction presentation)..


Some recent outputs from the Early Rice Project include publication of ancient DNA from charred rice grains from sites in Thailand and India (Castillo, Tanaka et al.), which add some flesh on the skeleton of the Proto-indica hypothesis; and publication of the first of a new generation spatial modelling of the early geography of rice, this one aimed at deducing the most like region (or regions) from which rice originated and spread, in particular the originals of early japonica rice that was so important to the Neolithic developments in China and throughout Southeast Asia (Silva et al. in PLOSone).  See also, the paper on phytoliths as a reflection of weed flora (Weisskopf et al 2014), the first of several in the pipeline that will illustrate new and more robust approaches to determining past rice ecology.

Friday, 27 February 2015

Mesolithic cereal trade in Europe?

This week's Science includes in ancient sedimentary DNA study by Oliver Smith, Robin Allaby and colleagues from sediments from an archaeological site sealed beneath the English Channel, with evidence that wheat was decomposing on this Mesolithic site 8000 years ago. Such a claim is obvioulsy a big deal for archaeologists, it is counter to our accepted narrative of the introduction of cereals with Neolithic farming immigrants around 6000 years ago. No surprisingly it has received science media attention, both in Science and in New Scientist, as well as a learned commentary from Gregor Larson; and despite a busy teaching week I have been asked for comments. Here I give my full extended comment. While I agree that we really need more evidence to clinch this from additional sites, and I would prefer directly radiocarbon dated grains, I also don't think this requires a complete overhaul of what we know about the introduction of sustained farming around 4000 BC.

This paper is methodologically impressive. They have developed a robust phylogenetic approach to cautiously ID sedimentary aDNA. The deposits seem well dated and sealed by rising sea-levels. So we are left with the challenge of fitting this to our world view as archaeologists. 


This report is sure to be heavily debated, and I guess many archaeologists will reject this out of hand. But that is perhaps like the ostrich with its head in the sand. I would certainly be happier with an AMS-dated cereal grain, but this new evidence tells us we need to be actively looking for those Pre-Neolithic traded grains.

I suppose this will reopen the debate about claims for Mesolithic cereal pollen grains, which have been claimed from sites here and there in Britain and France. Most archaeologists have rightly tended to follow the critical assessment of these, represented for example by the writings of Prof Behre, a senior archaeobotanist and doyen of anthropogenic pollen indicators (e.g. Behre 2007). I expect new scrutiny of such finds, as they could also relate to a pioneer phase of small scale cereal adoption.

From Larson 2015
This find does not mean the Neolithic needs to redated. The Neolithic in Britian is well dated to about 4000 BC which sees a rapid rise in human population together with evidence for emmer wheat, barley and livestock. This follows a spread of agricultural populations, uniformly with big demographic booms across central and western Europe (e.g work by Shennan et al. in Nature Comms, 2013). This I think is still clear. But the New wheat DNA from the English channel requires us to think in terms of small scale pioneers operating beyond the frontier of farming spread and trading with Foragers, and beyond that foragers trading with each other. Mesolithic foragers were well adapted to their environments given their population density so this would not have been about trading food as needed calories but about foodstuffs that were rare, exotic and valuable. I would guess these early cereals would have been symbolically charged as exotica much like spices in much later times. In regions with obsidian we know Mesolithic populations had long distance trade networks. This new evidence suggests long distance networks also moved perishables, including edibles.

I think we can see this as on par with the food "globalization" episodes in much later prehistory, such as the Bronze Age. When sorghum and other African crops arrived in India 4000 years ago, or wheat arrived in China in the third millennium BC, these edibles proceeded any other material evidence for trade. This implies long distance small scale exchanges in exotica, including what seem to us today as mundane edibles, were highly valued, presumably in part because of the symbolic associations with distance and the exotic. I have written about this in a few places, e.g Fuller et al 2011 in Antiquity or Boivin et al 2012 in World Archaeology (blogged here).

So perhaps what we are seeing is evidence for an early Holocene equivalent-- the Neolithic grain as the tastey exotica in a the Mesolithic world