Dating rice remains through phytolith carbon-14 study reveals domestication at the beginning of the Holocene

Edited by Dolores R. Piperno, Smithsonian Institution, Fairfax, VA, and approved April 19, 2017 (received for review March 16, 2017)
May 30, 2017
114 (25) 6486-6491

Significance

When the domestication of rice began in its homeland, China, is an enduring and important issue of debate for researchers from many different disciplines. Reliable chronological and robust identification criteria for rice domestication are keys to understanding the issue. Here, we first use phytolith dating to constrain the initial occupation of Shangshan, an important site with early rice remains located in the Lower Yangtze region of China. We then identify the rice phytoliths of Shangshan as partly domesticated based on their morphological characteristics. The results indicate that rice domestication may have begun at Shangshan in the Lower Yangtze during the beginning of the Holocene.

Abstract

Phytolith remains of rice (Oryza sativa L.) recovered from the Shangshan site in the Lower Yangtze of China have previously been recognized as the earliest examples of rice cultivation. However, because of the poor preservation of macroplant fossils, many radiocarbon dates were derived from undifferentiated organic materials in pottery sherds. These materials remain a source of debate because of potential contamination by old carbon. Direct dating of the rice remains might serve to clarify their age. Here, we first validate the reliability of phytolith dating in the study region through a comparison with dates obtained from other material from the same layer or context. Our phytolith data indicate that rice remains retrieved from early stages of the Shangshan and Hehuashan sites have ages of approximately 9,400 and 9,000 calibrated years before the present, respectively. The morphology of rice bulliform phytoliths indicates they are closer to modern domesticated species than to wild species, suggesting that rice domestication may have begun at Shangshan during the beginning of the Holocene.

Continue Reading

Acknowledgments

We thank Prof. Dolores R. Piperno for her important suggestions, which subsequently improved this paper; Mr. Darden Hood and Ron Hatfield for their advice about phytolith dating; Prof. Chunxia Zhang and Ms. Bin Hu for their assistance with X-ray diffraction of the phytolith; Dr. Saihong Yang for her assistance with scanning electron microscopy and energy-dispersive spectrometer analysis; and Prof. Yunfei Zheng for providing several images of pottery sherds from Shangshan. This work was funded jointly by the 973 Program Grant 2015CB953801; the National Natural Science Foundation of China Grants 41230104, 41401230, 41430103, and 41472154; and the China Postdoctoral Science Foundation-funded project Grant 2014M561050.

Supporting Information

Supporting Information (PDF)

References

1
; International Rice Research Institute Bringing Hope, Improving Lives: Strategic Plan 2007–2015 (IRRI, Manila, Philippines), pp. 1–61 (2006).
2
S-i Nakamura, The origin of rice cultivation in the Lower Yangtze Region, China. Archaeol Anthropol Sci 2, 107–113 (2010).
3
DQ Fuller, et al., The domestication process and domestication rate in rice: Spikelet bases from the Lower Yangtze. Science 323, 1607–1610 (2009).
4
X Wei, et al., Domestication and geographic origin of Oryza sativa in China: Insights from multilocus analysis of nucleotide variation of O. sativa and O. rufipogon. Mol Ecol 21, 5073–5087 (2012).
5
F Silva, et al., Modelling the geographical origin of rice cultivation in Asia using the rice archaeological database. PLoS One 10, e0137024 (2015).
6
Z Zhao, DR Piperno, Late Pleistocene/Holocene environments in the middle Yangtze River valley, China and rice (Oryza sativa L.) domestication: The phytolith evidence. Geoarchaeology 15, 203–222 (2000).
7
X Wu, et al., Early pottery at 20,000 years ago in Xianrendong Cave, China. Science 336, 1696–1700 (2012).
8
DQ Fuller, Pathways to Asian civilizations: Tracing the origins and spread of rice and rice cultures. Rice (N Y) 4, 78–92 (2011).
9
HY Lu, et al., Rice domestication and climatic change: Phytolith evidence from East China. Boreas 31, 378–385 (2002).
10
L Jiang, L Liu, New evidence for the origins of sedentism and rice domestication in the Lower Yangzi River, China. Antiquity 80, 355–361 (2006).
11
BL Gross, Z Zhao, Archaeological and genetic insights into the origins of domesticated rice. Proc Natl Acad Sci USA 111, 6190–6197 (2014).
12
L Liu, G-A Lee, L Jiang, J Zhang, Evidence for the early beginning (c. 9000 cal. BP) of rice domestication in China: A response. Holocene 17, 1059–1068 (2007).
13
DQ Fuller, E Harvey, Q Ling, Presumed domestication? Evidence for wild rice cultivation and domestication in the fifth millennium BC of the Lower Yangtze region. Antiquity 81, 316–331 (2007).
14
ZI Gilmore, Direct radiocarbon dating of Spanish moss (Tillandsia usneoides) from early fiber-tempered pottery in the southeastern U.S. J Archaeol Sci 58, 1–8 (2015).
15
LP Wilding, RE Brown, N Holowaychuk, Accessibility and properties of occluded carbon in biogenetic opal. Soil Sci 103, 56–61 (1967).
16
DR Piperno, Phytolith radiocarbon dating in archaeological and paleoecological research: A case study of phytoliths from modern Neotropical plants and a review of the previous dating evidence. J Archaeol Sci 68, 54–61 (2016).
17
DR Piperno, Standard evaluations of bomb curves and age calibrations along with consideration of environmental and biological variability show the rigor of phytolith dates on modern neotropical plants: Review of comment by Santos, Alexandre, and Prior. J Archaeol Sci 71, 59–67 (2016).
18
Y Asscher, S Weiner, E Boaretto, A new method for extracting the insoluble occluded carbon in archaeological and modern phytoliths: Detection of 14C depleted carbon fraction and implications for radiocarbon dating. J Archaeol Sci 78, 57–65 (2017).
19
MJ Hodson, The development of phytoliths in plants and its influence on their chemistry and isotopic composition. Implications for palaeoecology and archaeology. J Archaeol Sci 68, 62–69 (2016).
20
S Soter, Radiocarbon anomalies from old CO2 in the soil and canopy air. Radiocarbon 53, 55–69 (2011).
21
D Piperno Phytoliths: A Comprehensive Guide for Archaeologists and Paleoecologists (Altamira Press, Lanham, MD), pp. 1–21 (2006).
22
X Zuo, et al., Radiocarbon dating of prehistoric phytoliths: A preliminary study of archaeological sites in China. Sci Rep 6, 26769 (2016).
23
H Jin, et al., A primary study on AMS 14C dating of phytolith at Tianluoshan site, Zhejiang Province. Quat Sci 34:1–7. Chinese. (2014).
24
Y Ma, et al., Rice bulliform phytoliths reveal the process of rice domestication in the Neolithic Lower Yangtze River region. Quat Int 426, 126–132 (2016).
25
X Huan, et al., Bulliform phytolith research in wild and domesticated rice paddy soil in South China. PLoS One 10, e0141255 (2015).
26
L Jiang, The early Neolithic age of the Qiantangjiang Basin and its cultural lineage. Southeast Culture, 44–53. Chinese. (2013).
27
Y Zheng, GW Crawford, L Jiang, X Chen, Rice domestication revealed by reduced shattering of archaeological rice from the Lower Yangtze valley. Sci Rep 6, 28136 (2016).
28
DQ Fuller, et al., Consilience of genetics and archaeobotany in the entangled history of rice. Archaeol Anthropol Sci 2, 115–131 (2010).
29
T Ball, et al., Phytoliths as a tool for investigations of agricultural origins and dispersals around the world. J Archaeol Sci 68, 32–45 (2016).
30
Y Wu, L Jiang, Y Zheng, C Wang, Z Zhao, Morphological trend analysis of rice phytolith during the early Neolithic in the Lower Yangtze. J Archaeol Sci 49, 326–331 (2014).
31
Y Zheng, A Matsui, H Fujiwara, Phytoliths of rice detected in the Neolithic sites in the Valley of the Taihu Lake in China. Environ Archaeo 8, 177–183 (2003).
32
D Pearsall, et al., Distinguishing rice (Oryza sativa Poaceae) from wild Oryza species through Phytolith analysis: Results of preliminary research. Econ Bot 49, 183–196 (1995).
33
YS Gu, ZJ Zhao, DM Pearsall, Phytolith morphology research on wild and domesticated rice species in East Asia. Quat Int 287, 141–148 (2013).
34
Y Ge, DM Jie, JX Guo, HM Liu, LX Shi, Response of phytoliths in Leymus chinensis to the simulation of elevated global CO2 concentrations in Songnen Grassland, China. Chin Sci Bull 55, 3703–3708 (2010).
35
I Issaharou-Matchi, et al., Intraspecific biogenic silica variations in the grass species Pennisetum pedicellatum along an evapotranspiration gradient in South Niger. Flora 220, 84–93 (2016).
36
DQ Fuller, Contrasting patterns in crop domestication and domestication rates: Recent archaeobotanical insights from the Old World. Ann Bot (Lond) 100, 903–924 (2007).
37
DQ Fuller, L Qin, Archaeobotany in the origin of the rice agriculture. Southern Cultural Relics, 38–45. Chinese. (2009).
38
PE Reyerson, et al., Unambiguous evidence of old soil carbon in grass biosilica particles. Biogeosciences 13, 1269–1286 (2016).
39
GM Santos, et al., Possible source of ancient carbon in phytolith concentrates from harvested grasses. Biogeosciences 9, 1873–1884 (2012).
40
J Yin, X Yang, Y Zheng, Influence of increasing combustion temperature on the AMS 14C dating of modern crop phytoliths. Sci Rep 4, 6511 (2014).
41
L Janz, JK Feathers, GS Burr, Dating surface assemblages using pottery and eggshell: Assessing radiocarbon and luminescence techniques in Northeast Asia. J Archaeol Sci 57, 119–129 (2015).
42
RE Taylor, O Bar-Yosef Radiocarbon Dating: An Archaeological Perspective (Left Coast Press, 2nd Ed, Walnut Creek, CA, 2014).
43
X Yang, et al., Barnyard grasses were processed with rice around 10000 years ago. Sci Rep 5, 16251 (2015).
44
J Wang, L Jiang, A primary analysis on use-wear and residues of flaked stone tools from the Shangshan site, Zhejiang Province. Southern Cultural Relics, 117–121. Chinese. (2016).
45
G Larson, et al., Current perspectives and the future of domestication studies. Proc Natl Acad Sci USA 111, 6139–6146 (2014).
46
X Yang, et al., Early millet use in northern China. Proc Natl Acad Sci USA 109, 3726–3730 (2012).
47
H Lu, et al., Earliest domestication of common millet (Panicum miliaceum) in East Asia extended to 10,000 years ago. Proc Natl Acad Sci USA 106, 7367–7372 (2009).
48
Z Zhao, The process of origin of agriculture in China: Archaeological evidence from flotation results. Quat Sci 34, 73–84 (2014).
49
Z Zhao, New archaeobotanic data for the study of the origins of agriculture in China. Curr Anthropol 52, S295–S306 (2011).
50
MA Zeder, The origins of agriculture in the Near East. Curr Anthropol 52, S221–S235 (2011).
51
DR Piperno, The origins of plant cultivation and domestication in the New World Tropics: Patterns, process, and new developments. Curr Anthropol 52, S453–S470 (2011).
52
JD Shakun, et al., Global warming preceded by increasing carbon dioxide concentrations during the last deglaciation. Nature 484, 49–54 (2012).
53
J Dong, et al., A high-resolution stalagmite record of the Holocene East Asian monsoon from Mt Shennongjia, central China. Holocene 20, 257–264 (2010).
54
DJ Cohen, The beginnings of agriculture in China. Curr Anthropol 52, S273–S293 (2011).
55
X Zuo, H Lu, Z Gu, Distribution of soil phytolith-occluded carbon in the Chinese Loess Plateau and its implications for silica–carbon cycles. Plant Soil 374, 223–232 (2014).
56
GM Santos, et al., The phytolith 14C puzzle: A tale of background determinations and accuracy tests. Radiocarbon 52, 113–128 (2010).
57
JA Carter, Atmospheric carbon isotope signatures in phytolith-occluded carbon. Quat Int 193, 20–29 (2009).
58
R Corbineau, PE Reyerson, A Alexandre, GM Santos, Towards producing pure phytolith concentrates from plants that are suitable for carbon isotopic analysis. Rev Palaeobot Palynol 197, 179–185 (2013).
59
C Bronk Ramsey, S Lee, Recent and planned developments of the program OxCal. Radiocarbon 55, 720–730 (2013).
60
PJ Reimer, et al., IntCal13 and marine13 radiocarbon age calibration curves 0–50,000 years cal BP. Radiocarbon 55, 1869–1887 (2013).
61
A Alexandre, et al., Direct uptake of organic carbon by grass roots and allocation in leaves and phytoliths: 13C labeling evidence. Biogeosciences 15, 1693–1703 (2016).
62
WH Casey, SD Kinrade, CTG Knight, DW Rains, E Epstein, Aqueous silicate complexes in wheat, Triticum aestivum L. Plant Cell Environ 27, 51–54 (2004).

Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 114 | No. 25
June 20, 2017
PubMed: 28559349

Classifications

Submission history

Published online: May 30, 2017
Published in issue: June 20, 2017

Keywords

  1. rice domestication
  2. radiocarbon dating
  3. Shangshan
  4. chronology
  5. phytolith-occluded carbon

Acknowledgments

We thank Prof. Dolores R. Piperno for her important suggestions, which subsequently improved this paper; Mr. Darden Hood and Ron Hatfield for their advice about phytolith dating; Prof. Chunxia Zhang and Ms. Bin Hu for their assistance with X-ray diffraction of the phytolith; Dr. Saihong Yang for her assistance with scanning electron microscopy and energy-dispersive spectrometer analysis; and Prof. Yunfei Zheng for providing several images of pottery sherds from Shangshan. This work was funded jointly by the 973 Program Grant 2015CB953801; the National Natural Science Foundation of China Grants 41230104, 41401230, 41430103, and 41472154; and the China Postdoctoral Science Foundation-funded project Grant 2014M561050.

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Key Laboratory of Cenozoic Geology and Environment, Institute of Geology and Geophysics, Chinese Academy of Sciences, 100029 Beijing, China;
Key Laboratory of Cenozoic Geology and Environment, Institute of Geology and Geophysics, Chinese Academy of Sciences, 100029 Beijing, China;
Center for Excellence in Tibetan Plateau Earth Science, Chinese Academy of Sciences, 100101 Beijing, China;
University of Chinese Academy of Sciences, Beijing 100049, China;
Leping Jiang
Zhejiang Provincial Institute of Relics and Archaeology, 310014 Hangzhou, China;
Jianping Zhang1 [email protected]
Key Laboratory of Cenozoic Geology and Environment, Institute of Geology and Geophysics, Chinese Academy of Sciences, 100029 Beijing, China;
Center for Excellence in Tibetan Plateau Earth Science, Chinese Academy of Sciences, 100101 Beijing, China;
Key Laboratory of Land Surface Pattern and Simulation, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China
Xiujia Huan
Key Laboratory of Cenozoic Geology and Environment, Institute of Geology and Geophysics, Chinese Academy of Sciences, 100029 Beijing, China;
University of Chinese Academy of Sciences, Beijing 100049, China;
Keyang He
Key Laboratory of Cenozoic Geology and Environment, Institute of Geology and Geophysics, Chinese Academy of Sciences, 100029 Beijing, China;
University of Chinese Academy of Sciences, Beijing 100049, China;
Can Wang
Key Laboratory of Cenozoic Geology and Environment, Institute of Geology and Geophysics, Chinese Academy of Sciences, 100029 Beijing, China;
Naiqin Wu
Key Laboratory of Cenozoic Geology and Environment, Institute of Geology and Geophysics, Chinese Academy of Sciences, 100029 Beijing, China;
University of Chinese Academy of Sciences, Beijing 100049, China;

Notes

1
To whom correspondence may be addressed. Email: [email protected] or [email protected].
Author contributions: H.L. and J.Z. designed research; X.Z., H.L., and X.H. performed research; X.Z., L.J., and X.Y. contributed new reagents/analytic tools; X.Z., H.L., J.Z., X.Y., K.H., C.W., and N.W. analyzed data; X.Z., H.L., L.J., X.H., and K.H. collected samples; and X.Z. and H.L. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

Metrics & Citations

Metrics

Note: The article usage is presented with a three- to four-day delay and will update daily once available. Due to ths delay, usage data will not appear immediately following publication. Citation information is sourced from Crossref Cited-by service.


Citation statements

Altmetrics

Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

Cited by

    Loading...

    View Options

    View options

    PDF format

    Download this article as a PDF file

    DOWNLOAD PDF

    Login options

    Check if you have access through your login credentials or your institution to get full access on this article.

    Personal login Institutional Login

    Recommend to a librarian

    Recommend PNAS to a Librarian

    Purchase options

    Purchase this article to access the full text.

    Single Article Purchase

    Dating rice remains through phytolith carbon-14 study reveals domestication at the beginning of the Holocene
    Proceedings of the National Academy of Sciences
    • Vol. 114
    • No. 25
    • pp. 6413-6544

    Media

    Figures

    Tables

    Other

    Share

    Share

    Share article link

    Share on social media