Phytolith evidence for human-plant subsistence in Yahuai (Guangxi, South ) over the past 30000 years Yan WU, Guangmao XIE, Limi MAO, Zhijun ZHAO and Miriam BELMAKER Citation: SCIENCE CHINA Earth Sciences; doi: 10.1007/s11430-020-9640-3

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Phytolith evidence for human-plant subsistence in Yahuai Cave (Guangxi, South China) over the past 30000 years Yan WU1,2*, Guangmao XIE3,4†, Limi MAO5, Zhijun ZHAO6 & Miriam BELMAKER7

1 Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China; 2 CAS Center for Excellence in Life and Paleoenvironment, Beijing 100044, China; 3 College of History, Culture and Tourism, Guangxi Normal University, Guilin 541001, China; 4 Guangxi Institute of Cultural Relic Protection and Archaeology, Nanning 530022, China; 5 State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China; 6 Institute of Archaeology, Chinese Academy of Social Sciences, Beijing 100710, China; 7 Department of Anthropology, University of Tulsa, Tulsa, Oklahoma 74104, USA

Received January 27, 2020; revised April 23, 2020; accepted June 6, 2020; published online July 29, 2020

Abstract South China preserves a rich archaeological record elucidating the evolution of early modern humans during the Late Pleistocene. However, few studies on plant utilization were conducted in this region. We used phytolith analysis from Yahuai Cave, Guangxi, to infer human use of plant resources over the past 30000 years. AMS 14C dating was used to constrain the chronological framework. Results indicate that several economically essential species were present throughout the sequence including Urticineae (cf. Ulmus sp.), which appears in the lower layers of the sequence (Marine Isotope Stage 3 through Heinrich 1); bamboo and palm which appear throughout the sequence, and wild rice which appears in a clear archaeological context dating to 16000 years ago. This is the earliest record of wild rice in South China and a prerequisite for rice domestication. The unique stone tool assemblages, which resemble those in north China as opposed to South China, point to the possibility that humans, seeking refuge from the colder north, brought their tool kit with them and utilized familiar northern taxa. Warmer South China would have served as a refuge for human populations escaping the cold, harsh climate in the north with more ameliorate conditions in the south. Keywords Phytolith, Wild rice, South China, Bamboo, Late Pleistocene

Citation: Wu Y, Xie G, Mao L, Zhao Z, Belmaker M. 2020. Phytolith evidence for human-plant subsistence in Yahuai Cave (Guangxi, South China) over the past 30000 years. Science China Earth Sciences, 63, https://doi.org/10.1007/s11430-020-9640-3

1. Introduction eral renowned discoveries of human remains from this per- iod, including the modern human skulls from Qilinshan and Abundant archaeological sites from South China provide Liujiang (Woo and Peng, 1959), human dental and skeletal insight into the adaptive strategies of humans in the Late remains from Bailiandong (Bailian Cave), Baojiyan (Yuan Pleistocene (Chi and Hung, 2010). Indeed, the Guangxi and Wei, 2015), Zengpiyan (Fangwu and Weisan, 1997; Zhuang autonomous region in South China is home to sev- Zhang M L et al., 2011) and Dingshishan (Fu et al., 1998), which highlights the critical role of this region as a focal point for the evolution of modern humans in China. * Corresponding author (email: [email protected]) Yahuai Cave, Guangxi Zhuang autonomous region in † Corresponding author (email: [email protected])

© Science China Press and Springer-Verlag GmbH , part of Springer Nature 2020 earth.scichina.com link.springer.com http://engine.scichina.com/doi/10.1007/s11430-020-9640-3 2 Wu Y, et al. Sci China Earth Sci

South China (Figure 1a), yielded a long archaeological se- millet and rice (Luo et al., 2019). quence with a total of over 50 layers, the upper layers dating Here we present phytolith evidence of the economically to the Holocene and lower layers dating to the Late Pleis- significant plant remains from Yahuai Cave, Guangxi tocene. The extensive lithic collections are attributed to the Zhuang autonomous region, South China over the past flake industry, which is common in North China. The fauna 30000 years in the context of human population dynamics. includes both large and small vertebrate remains currently under study (Belmaker et al., 2018). However, despite the evidence that the Guangxi region was significant for Late 2. Materials and methods Pleistocene humans, little work has explored human-plant utilization. 2.1 The site of Yahuai Cave Phytoliths are microscopic silica particles that precipitate Yahuai cave is located in Long’an County, Guangxi Zhuang in or between cells in a wide range of plant tissues. They autonomous region, South China (107°45′35″E, 23°6′25″N), preserve well in the fossil record and across a wide range of 100 km northwest from Nanning (Figure 1a and 1b). It environments, and thus are rapidly becoming an invaluable consists of a rock-shelter and an inner cave, covering a total tool for studying past vegetation human used and plant area of more than 100 m2. Three seasons of excavation at this communities (Albert et al., 2015; Piperno, 2006; Rashid et site were carried out between 2015 and 2018 by the Guangxi al., 2019; Strömberg, 2005). Phytoliths may be identified to Institute of Cultural Relic Protection and Archaeology. Ex- taxa, based on morphology and morphometrics, and also cavations in each area were conducted in 1 m×1 m squares, allow for distinguishing between wild vs. domestic coun- and at 5 cm vertical interval spits. All cultural remains were terparts of the same species. For example, phytolith evidence recorded on-site using a total station to document the three- played a vital role in the study of agricultural origins such as dimensional coordinates of the finds, in addition to drawing, maize in central America (Piperno, 1984) and bananas in photography, and video. Small remains were collected by southeast Asia (Ball et al., 2006). In recent years, increased sieving and flotation. phytolith studies have been reported from Chinese archae- The excavation was divided into four areas: A, B, C, and ological contexts focusing primarily on the agricultural ori- D, with a total exposure of 50 m2 (Appendix Figure S1, gins, cultivation and domestication of foxtail millet, common https://link.springer.com). In this study, we focus on Area B.

Figure 1 Yahuai Cave site. (a) Location of the site. (b) Panoramic view of the site. (c)–(e) Stratigraphic profile of Area B denoting the location of AMS 14C and phytolith samples. M1 denotes the location where the skull was found. http://engine.scichina.com/doi/10.1007/s11430-020-9640-3 Wu Y, et al. Sci China Earth Sci 3

Area B is 17 m2 in size with 24 stratigraphic layers throu- different layers in area B (layers 3, 5, 7 through 9, 18, 17, and ghout 4.2 m of deposits (Figure 1c–1e). Area B (Figure 2a) is 21 from units 4 through 2). The ages of samples were rich with stone artifacts (Figure 2b and 2c), a complete hu- measured by Beta Analytic Radiocarbon Dating Laboratory man skull with a partial mandible discovered in layer 8 and Peking University Dating Laboratory following pub- which dates to 16000 cal yr B.P. (Figure 2d), a (Figure lished procedures. The eight AMS 14C ages obtained were 2e), and a rich vertebrate faunal assemblage (Figure 2f). The calibrated based on the dataset INTCAL13 (Reimer et al., lithic assemblage from Yahuai Cave site is dominated by 2013). small amorphous flakes, with some bearing evidence of utilization, manufactured on quartzite, sandstone, flint, tek- 2.3 Sampling and phytolith extraction tite, or crystal. The retouched tools, namely scrapers, points, and knives, are simple and unifacially retouched, often re- As part of a more extensive research program to study the stricted to one side or end of the flakes and without alteration archaeobotanical remains in this area, we conducted flotation of the original blank form (Xie et al., 2018). and pollen sampling to identify paleobotanical remains. Unfortunately, only a few macrobotanical remains were 2.2 Chronostratigraphy found. Pollen was found only in layer 21. The thickest cul- tural depositional profile of Area B was chosen for phytolith Eight charred material samples for AMS 14C were taken from sampling. Twenty-one soil samples, 10 g each, were col-

Figure 2 Human fossil and cultural remains from the Yahuai cave. (a) Area B section with human burial; (b) stone artifacts; (c) perforated stones; (d) human skull; (e) hearth; (f) faunal remains. http://engine.scichina.com/doi/10.1007/s11430-020-9640-3 4 Wu Y, et al. Sci China Earth Sci lected from the stratified deposits across different squares 1987, 1992; Twiss et al., 1969; Wang and Lu, 1993). (Figure 1c–1e). The archaeological samples were processed using a pro- 2.4.2 Oryza sp. cedure slightly modified from Piperno (2006) and Lu et al. Rice (Oryza) produces three types of phytoliths: bilobate (2007). The soil samples, consisting of compact clay, were (leaves), double peak (husks), and bulliform phytoliths dried and ground into powder. The dry powder samples were (leaves). Only double peak and bulliform phytoliths have treated with 30% H2O2 and heated, followed by 10% HCl been shown to discriminate between wild and domesticate treatment, and washed with distilled water three times. The varieties. Double peak phytoliths are rare in prehistoric se- samples were subjected to heavy liquid flotation with a dense diments, but Oryza-type bulliform phytoliths are common −1 solution of ZnBr2 (d=2.4 g mL ) to separate opal silica and may be used to distinguish between the two varieties phytoliths from non-opal silica particles by centrifuging at (Huan et al., 2015). 2500 rpm for five minutes. Fujiwara and Kaner (1993) reported that the number of fish To extract phytoliths, we followed the standard dry-ashing scale-like decorations of Oryza-type bulliform phytoliths method at 550°C lasting 12 hours. Then, the ash was trans- could distinguish between wild and domestic varieties. Lu et ferred to the test tube. 6 mL of 10% hydrochloric acid was al. (2002) reported that while there is a broad diversity in added to the test tube, which was shaken for 5 min. Distilled total numbers of decorations, and specifically scale-like water was added to the test tube, and the mixture was cen- decorations, wild rice commonly has less than nine decora- trifuged at 3000 rpm for 10 min. The above steps were re- tions while those of domesticated rice display eight to peated until the supernatant fluid was clear. fourteen decorations (Lu et al., 2002). Huan et al. (2015) The extracted samples were mounted in glycerin to rotate indicated that the proportion of Oryza-type bulliform phy- them if necessary and to obtain more accurate measurements. toliths with <9 decorations was 17.46±8.29% in wild rice balsam acted as the medium to obtain better identi- samples, while in domesticated samples, the corresponding fication and for photographic procedures. proportion was 63.70±9.22%, suggesting that the proportion of phytoliths with <9 decorations can be used as a criterion to 2.4 Phytolith identification discriminate wild species of rice. Ma et al. (2018) pointed out that the number of scale-like Phytoliths identification and counting were conducted under decorations on the phytoliths is due to water supply and a Nikon Eclipse LV100POL microscope based on published cultivation practices. Rice leaves roll their leaves as an keys (Piperno and Pearsall, 1998a) and our modern reference adaptive response to water deficit to maintain a favorable collection stored in the Key Laboratory of Vertebrate Evo- water balance (Cal et al., 2019). The formation of the fish lution and Human Origins of the Chinese Academy of Sci- scale-like decoration on the Oryza-type bulliform phytoliths ences, Institute of Vertebrate Paleontology and is related to the extrusion between cells in rice leave epi- Paleoanthropology (IVPP), Chinese Academy of Sciences dermis. Leaf rolling leads to an increase in fish scale-like (CAS). At least 200 phytoliths were counted for each sample. decorations. Wild rice grows in areas with permanent water For the Oryza type, percentage of wild vs. domesticated was inundation with a lower probability of leaf rolling, and thus a calculated based on a count of 100 Oryza phytoliths. The lower number of fish scale-like decorations. In contrast, diagram of phytolith counts for main types was graphed domesticated rice is often subjected to drainage of rice using software TILIA (Grimm, 1991). Phytolith nomen- paddies, leading to a water deficit, and an increase in the clature followed the nomenclature of the International Code probability of leaf rolling, leading to an increase of fish for Phytoliths Nomenclature 2.0 (Neumann et al., 2019). scale-like decorations (Ma et al., 2018). The percentage of domesticated vs. wild Oryza-type bul- 2.4.1 Grasses liform phytoliths per sample was determined by scanning Monocotyledonous phytoliths were dominant in all samples each sample until 100 individual Oryza-type bulliform compared to dicotyledonous (Figure 3a–3m). Phytoliths phytoliths were extracted, and identified as wild or domes- from grass silica short cell phytoliths (GSSCP) occur in all ticated as presented in Figure 3n–3r). samples with Chloridoideae (Short saddle) and Panicoideae (bilobate) comprising a majority of the phytoliths within the 2.4.3 Urticineae (cf. Ulmus sp.) assemblages with rare Pooideae (rondel). Other phytolith Hair base phytoliths are very common in eudicots, often morphotypes such as acute bulbosus, blocky, elongate entire, strictly adhering to hair cells, can be useful in discriminating trapezoid, elongate dentate and elongate, and bulliform fla- between taxa (Piperno, 2006). Hair base phytoliths are pro- bellate are not as diagnostic and can only be assigned to duced in both leaves and seeds but are much more common unspecific grasses (Fredlund and Tieszen, 1994; Gu et al., in the former (Kealhofer and Piperno, 1998; Piperno, 1989, 2016; Mulholland, 1989; Piperno and Pearsall, 1998b; Twiss, 2006). Their morphology is distinct, specifically the adorn- http://engine.scichina.com/doi/10.1007/s11430-020-9640-3 Wu Y, et al. Sci China Earth Sci 5 ment features and size. Urticaceae and Moraceae (Zhang S D et al., 2011). To Layer 21 contained a few specimens of flattish spheres, identify the family of Urticineae present in Yahuai, phyto- often with a circular mark in the center surrounded by liths from 12 species of extant Urticineae (Table 1) collected spherical inclusions, hair base phytoliths consistent with from Beijing Botanical Garden, Institute of Botany, Chinese phytoliths extracted from subord. Urticineae (order Rosales) Academy of Sciences, were extracted following the proce- and which include the families of Ulmaceae, Cannabaceae, dure outlined in Section 2.3. Unfortunately, the morphology

Figure 3 Phytolith types extracted from Yahuai cave site: (a) bilobate; (b) acicular hair cell; (c) short saddle; (d) bilobate; (e) rondel; (f) long saddle; (g) spheroid echinate; (h) Bambusoideae-type bulliform; (i) Bambusoideae-type bulliform; (j) irregular elongate; (k) hair base; (l) Blocky; (m) rectangular; ((n) through (r)) Oryza-type bulliform ((n) through (q)) Oryza-type bulliform phytoliths with <9 fish-scale decorations, (r) Oryza-type bulliform phytoliths with >9 fish-scale decorations.

Table 1 Specimens of 12 plant species from modern Urticineae used in the comparative database Family Genus Species English name Cannabis C. sativa L. Medicinal marijuana Celtis C. bungeana Blume Bunge’s hackberry Celtis C. koraiensis Nakai Korean hackberry Cannabaceae Humulus H. lupulus L. Common hop Humulus H. scandens (Lour.) Merr. Wild hop Pteroceltis P. tatarinowii Maxim. Blue Sandalwood Moraceae Morus M. alba L. White mulberry Ulmus U. davidiana Planch. David elm Ulmus U. lamellosa C. Wang & S.L. Chang Hebei elm Ulmaceae Ulmus U. macrocarpa Hance Large fruited elm Ulmus U. pumila L. Siberian elm Urticaceae Boehmeria B. nivea (L.) Gaudich. Ramie http://engine.scichina.com/doi/10.1007/s11430-020-9640-3 6 Wu Y, et al. Sci China Earth Sci of the hair base phytoliths did not distinguish the different position with little post-depositional disturbance. Unit 5 is Urticineae families. However, as diagnostic Ulmus sp. pollen recorded in layers 1–4. Cultural remains from layers 3–4 was discovered in layer 21, we suggest a tentative identifi- contain potsherds and ground stone tools attributed to the cation of the phytoliths to this genus (Figure S2). Neolithic age. However, a single 14C dates from layer 3 suggests a younger date of 1262–1052 cal yr B.P. There is a 2.4.4 Palm gap in the stratigraphic deposits where unit 5 overlies unit 4 Echinate phytoliths (Piperno, 2006; Strömberg et al., 2007) unconformably, and deposits dating from ~15000–6000 B.P. are spheroid shaped (or nearly so) beset with prickles. They are missing. Layers 1–3 are present, but they are limited in have been observed most commonly in palm (Arecaceae) their horizontal distribution (less than one square meter) and species (Albert et al., 2009, 2015; Albert and Bamford, 2012; very thin. Bamford et al., 2006; Fenwick et al., 2011). Identification Unit 4 is recorded in layers 5–8. 14C dates from layers 5, 7, resolution below the family level seems unlikely without and 8 of 16366–15850 cal yr B.P. are consistent with the further morphological study. previous data obtained from the skull discovered in layer 8 and dated to 16000 cal yr B.P. Heinrich events are Pleisto- 2.4.5 Bamboo cene periods of rapid cooling. Two peaks of cold climate Cuneiform or fan shape bulliform cell phytoliths that are not represent the Heinrich 1 event (~20–16.1 ka). The current identified as Sasa- and Pleioblastus bamboo types are clas- date estimates are ~16.1 (H1.1) and ~15 ka (H1.2) (Hodell et sified as Bambusoideae-type bulliform phytoliths (Okunaka al., 2017). Unit 4 may be attributed to Heinrich 1 event, and et al., 2012). Bambusoideae-type bulliform phytoliths are specifically the older cold peak H1.1. common throughout the sequence in Yahuai, albeit with Unit 3 is recorded from layers 9–17. 14C dates from layers varying proportions. 9, 16, and 17 suggest a date of 25693–24120 cal yr B.P. consistent with a hearth dated to 24000 cal yr B.P. This unit 2.5 Statistical analysis can be attributed to the Last Glacial Maximum (LGM), dated between 31000 and 16000 cal yr B.P. To identify phytolith zones, we applied a classical hierarchal Unit 2 is recorded from layers 18–23. 14C date from layer cluster analysis using a UPGMA algorithm with Gower 21 is 36359–35310 cal yr B.P. This unit can be assigned to dissimilarity index and stratigraphic constraints. Statistical the end of Marine Isotope Stage 3 (MIS 3), dated between analysis was conducted using PAST 4.01 software (Hammer 60000 and 30000 years B.P. et al., 2001). Unit 1 is observed in layer 24. No radiocarbon dates were obtained for this layer, and it is assigned to the Pleistocene.

3. Results 3.2 Phytolith zones

3.1 Yahuai Cave chronostratigraphy Figure 4 exhibits the temporal distribution of each phytolith The stratigraphy was divided into units 5 through 1 (from top morphotype. The majority of phytoliths (morphotypes acute to bottom) based on geomorphology, cultural analysis, and bulbosus, blocky, elongate entire, trapezoid, elongate dentate where possible, radiometric dating. Unit 5 is the only Ho- and elongate, and bulliform flabellate) can only be attributed locene unit, while units 4 through 1 include Late Pleistocene to grasses (Poaceae). Other phytolith morphotypes that can deposits. be identified to lower taxonomic levels: Hair base (Urtici- All radiocarbon dates are in linear and stratigraphic order neae cf. Ulmus sp.), spheroid echinate (Arecaceae), Bam- (Table 2). The chronostratigraphy suggests a sequential de- busoideae-type bulliform (Bambusoideae), saddle

Table 2 AMS 14C dates and information on the measured materials from selected layers Conventional radiocarbon age 2 Sigma calibrated age Sample code Laboratory number Dated material (yr B.P.) (cal yr B.P.) BT0910-3 BA160131 charred material 1205±40 1262–1052 BT1206-5 BA160128 charred material 13340±50 16238–15850 BT1206-7 Beta-444301 charred material 13500±50 16355–16130 BT1206-8 BA170399 charred material 13445±50 16366–15976 BT1106-9 BA170401 charred material 20310±70 24618–24120 BT0907-16 Beta-444303 charred material 20470±70 24880–24410 BT0908-17 BA170404 charred material 21100±100 25693–25189 BT1006-21 Beta-495504 charred material 32050±190 36359–35510 http://engine.scichina.com/doi/10.1007/s11430-020-9640-3 Wu Y, et al. Sci China Earth Sci 7

Figure 4 Diagram showing phytolith counts of key types extracted from the layers 1–21, 14C dates and dendrogram based on cluster analysis. Red line denotes the cutoff defining a cluster (dissimilarity=0.20).

(Chloridoideae), bilobate (Panicoideae), and rondel (Pooi- ther Urticineae (cf. Ulmus sp.) nor Pooideae phytoliths. deae). There are no Oryza type bulliform phytoliths in this layer. Table 3 presents the percentage of each phytolith mor- Cluster IV covers phytolith assemblages from layers 14 to photype. Figure 4 shows the results of cluster analysis pre- 10 from unit 3 dating to the LGM. Overall, these assem- sented by a dendrogram with numbers within the blages are dominated by high percentages of unspecified dendrogram representing 9999 iterations. The higher the grasses (>70%), which preclude any significant analysis. number, the more robust the clustering. Phytolith clusters However, it is interesting to note that layer 14 has 1% of had a cophenetic correlation coefficient of 0.6322. We also Urticineae (cf. Ulmus sp.), suggesting that its absence in the tested several other clustering algorithms and indices with other layers of this cluster may be an artifact of preservation comparable results suggesting the clustering is robust. Eight and sampling. clusters were identified. Cluster V comprises the phytolith assemblages from layer Cluster I contains the phytolith assemblage from layer 21 9 from unit 3 dated to 24618–24120 cal yr B.P. and layer 8 unit 2, dated to the end of MIS 3. The phytoliths in this from unit 4 dated to 16366–15976 cal yr B.P. The clustering cluster are dominated by Bambusoideae-type bulliform results are particularly interesting since the carbon 14 dates (18%), Chloridoideae (around 11%), and Panicoideae position each layer in different non-overlapping chron- (4.21%). Pooideae (4.51%) and Urticineae cf. Ulmus sp. ological periods. Moreover, there is only a low percentage (3.01%) are present in the layer in low proportions. There are of unidentified grasses in these two layers, so this clustering no spheroid echinate Arecaceae phytoliths in this cluster as pattern cannot be associated with low proportions of iden- well as no Oryza type bulliform phytoliths. tified phytoliths—the nearly 5000 years between layers 9 Cluster II has the phytolith assemblages from layers 20–18 and 8 points to a possible unconformity in the sediments. from unit 2 and layers 16–17 from unit 3, spanning the end of The phytolith assemblages of the two layers are similar, MIS 3 and the beginning of the LGM. These assemblages are with 17% Bambusoideae, 4% Chloridoideae, and 6.5% dominated by a high percentage of unspecified grasses Panicoideae. However, they differ in the percentage of (>85%), which preclude any significant analysis and prob- Arecaceae phytoliths: 21% in layer 9 and 47% in layer 8. ably account for the clustering of layers from different units. Layer 9 also includes 0.7% of Urticineae (cf. Ulmus sp.), Thus, the grouping of layers from units 2 and 3 is probably suggesting that its absence in previous layers may be an an artifact of the low proportions (< less than 10%) of di- artifact of the preservation or sampling rather than an actual agnostic phytoliths. absence. Cluster III includes the phytolith assemblage from layer 15 Cluster VI includes layer 7 dated to 16355–16130 cal yr B.P. from unit 3, dating to the LGM. This cluster has nearly equal and associated with the Older Dryas (Heinrich 1 event). percentages of spheroid echinate Arecaceae phytoliths (14%) This assemblage is dominated by a high proportion of un- and Bambusoideae-type bulliform (12%), Chloridoideae specified grasses (>85%), which preclude any significant (13%) and Panicoideae (10%) phytoliths. This unit has nei- analysis. http://engine.scichina.com/doi/10.1007/s11430-020-9640-3 8 Wu Y, et al. Sci China Earth Sci

Table 3 Phytolith morphotypes percentages across Yahuai archeological layer

No. Grasses Spheroid Hair base Bambusoideae-type Oryza-type Saddle Bilobate Rondel echinate bulliform bulliform 1 90.42 0.00 0.00 6.20 0.00 2.25 1.13 0.00 2 72.37 18.74 0.00 6.56 0.00 1.17 1.17 0.00 3 70.39 23.03 0.00 3.07 0.00 1.54 1.97 0.00 4 66.09 11.53 0.00 7.84 11.53 1.73 1.27 0.00 5 68.37 5.85 0.00 9.39 10.44 1.67 2.19 2.09 6 73.96 6.58 0.00 5.78 7.32 4.10 1.10 1.17 7 85.15 7.37 0.00 0.59 0.00 3.93 1.18 1.77 8 25.75 47.31 0.00 17.37 0.00 3.59 5.99 0.00 9 48.06 20.93 0.78 17.83 0.00 5.43 6.98 0.00 10 89.77 2.08 0.00 3.41 0.00 2.84 1.89 0.00 11 89.08 3.07 0.00 3.75 0.00 4.10 0.00 0.00 12 69.03 3.54 0.00 18.58 0.00 8.85 0.00 0.00 13 74.77 6.54 0.00 7.01 0.00 6.07 5.61 0.00 14 78.50 5.61 0.93 4.67 0.00 10.28 0.00 0.00 15 51.09 14.13 0.00 11.96 0.00 13.04 9.78 0.00 16 88.64 8.06 0.00 0.37 0.00 0.73 2.20 0.00 17 93.05 2.14 0.00 2.41 0.00 0.27 2.14 0.00 18 92.86 0.00 0.00 5.26 0.00 0.38 1.50 0.00 19 86.97 1.15 0.00 3.07 0.00 5.75 3.07 0.00 20 91.95 0.00 0.00 8.05 0.00 0.00 0.00 0.00 21 59.04 0.00 3.01 18.07 0.00 11.14 4.22 4.52

Cluster VII consists of the phytolith assemblages from by a high proportion of unspecified grasses (>70%), which layers 6 and 5 from unit 4 dated to 16238–15850 cal yr B.P. preclude any significant analysis. and layer 4 from unit 5. While there is no chronometric date for layer 4, the lithic assemblage is comprised of flake tools, which differ significantly from the lithic assemblages in the 4. Discussion older units. The phytolith assemblages of the two layers are similar: 8% Bambusoideae, 3% Chloridoideae, and 1.5% The deposition and accumulation of phytoliths in archae- Panicoideae. However, they differ in the percentage of ological sites are related to anthropic behavior as well as a Arecaceae phytoliths: 6% in layers 6 and 5 and 11% in layer host of abiotic depositional processes such as water and air 4. Layers 5 and 6 also include 1–2% Pooideae, while layer 4 (Madella and Powers-Jones, 1998). Nonetheless, phytolith does not. In all three layers, Oryza type bulliform proportions assemblages in archaeological sites are primarily created by are between 7–11%. However, 60% of Oryza type bulliform the decay of plants that humans brought into the site. Human phytoliths from layer 4 (Holocene) can be classified as do- selective processes, i.e., collecting specific plant species, mesticated Oryza, while in layers 5–6 (Pleistocene), 90% of may affect the composition of phytolith assemblages. Oryza type bulliform can be classified as wild rice (i.e., <9 Commonly selected species include plants used for food or fish-scale decorations) (Figure 3n–3q). In these layers, only raw material for construction (bedding, furniture) and ten percent of Oryza type bulliform may be classified as household items (baskets, ropes, bowls). domesticated Oryza based on the numbers of scale-like decorations (Figure 3r). The difference in the proportion of 4.1 Plant utilization in Yahuai wild vs. domesticated rice would suggest that this cluster needs to be divided into two sub-clusters: Cluster VIIa layers In Yahuai, the identified phytoliths derived from economic- 6 and 4 and Cluster VIIb with layer 4. This classification is ally important plants include rice, elm, bamboo, and palm also consistent with the chronostratigraphy. together with general unspecified grasses, as well as Chlor- Cluster VIII has the phytolith assemblages from layer 3 to idoideae, Panicoideae and Pooideae grasses, which may have 1, dating to the Holocene. These assemblages are dominated been used as raw material. We can identify several trends in http://engine.scichina.com/doi/10.1007/s11430-020-9640-3 Wu Y, et al. Sci China Earth Sci 9 plant utilization in Yahuai. Zhao and Piperno, 2000; Zong et al., 2007; Zuo et al., 2017). While rice has been an important staple across Asia, pa- 4.1.1 Palm and Bamboo leoethnobotanical evidence for its utilization in the Late Palms (Arecaceae) are one of the most diverse and eco- Pleistocene has been missing. Some areas, such as North nomically essential families growing in tropical and sub- China, have been extensively sampled, while others, such as tropical climate condition (Albert et al., 2009), and they are South China, have not (Fuller et al., 2016). also one of the oldest monocotyledonous flowering plants Classification of rice as wild or domestic in the arche- with 184 genera with ca. 2500 species described worldwide ological record depends on morphological characteristics of (Wang et al., 2015). Palms comprise several species present macrobotanical remains such as charred seeds and spikelet in Guangxi today, including (among others) Guihaia sp. (4–5 bases as well as microbotanical remains phytoliths (Ma et al., species) Raphis humilis, Calmus melanochorus, and Arenga 2018). Domesticated rice has been dated to 6.5–8.5 ka in the westerhoutii (Henderson, 2009; Luo et al., 2016). Starch Lower and Middle Yangtze River basin (Choi et al., 2017). granules derived from palm were retrieved from stone tools Single nucleotide polymorphism (SNP)-based molecular in the Neolithic site of Xincun (ca. 5500–4470 B.P.) and phylogenetic analysis showed that the middle region of the included fishtail palm (Caryota sp.), tailpot palm (Corypha Pearl River Delta in Guangxi province, South China, is umbraculifera) and Arenga palm (Arenga sp.) known today probably the origin of cultivated rice (Huang et al., 2012), from the tropics and sub-tropic of South China where they while a geospatial model has identified the wider Yangtze are processed for starch (Yang et al., 2013). River basin as the oldest center for rice domestication (Silva The subfamily Bambusoideae comprises 37 genera and et al., 2015). 500 species in China alone (Gu et al., 2016). Bamboo has Before the cultivation and domestication of rice, there been a critical economic plant in many human communities. would have been intensive rice gathering practices (Ander- Its uses are––but not limited to––a substitute for wood in son, 1999). Thus, the presence of wild rice is one of the most construction, furniture, scaffolding, and flooring (Yuming et substantial pieces of evidences to pinpoint the potential al., 2004). Bamboo has also been a source of food and origin of rice cultivation and domestication. It has been hy- medicine in China since ancient times (Nirmala et al., 2018). pothesized that during Pleistocene glacial periods in which Plant parts used for food includes the shoots as well as the climate was cold and dry, wild rice populations would have fibers. From a medicinal perspective, all parts of the bamboo been restricted to wetter tropical refuges. With the shift to plant, such as shoots, leaves, roots, and seeds, have clinical warmer and wet conditions of the Terminal Pleistocene, the applications. Bamboo leaves and shoots have been an es- geographic range of wild rice would have expanded north- sential ingredient of traditional Asian medicines in general, ward (Fuller et al., 2010). as well as Chinese and Indian (Ayurveda) medicines in To date, the earliest evidence for wild rice gathering has particular (Chongtham et al., 2011; Nirmala et al., 2014, been identified in Fahien rock shelter in dated to 2018). ~45000 B.P. (Premathilake and Hunt, 2018), but evidence Proportions of bamboo and palm phytoliths appear to from South China has been dated much later. To date, the mirror each other throughout the sequence. In the oldest units oldest phytolith remains of Oryza sp. in China have been dating to MIS 3, there is no palm and only bamboo. By the found in sites dating to the end of the Pleistocene and early Holocene, the palm is a majority of identified phytoliths, and Holocene at 12000–9000 cal yr BP. from Xianrendong, bamboo is much rarer. A detailed understanding of this Diaotonghuan, Shangshan and Hehuashan sites (Qiu et al., phenomenon is difficult in the absence of a better phytolith 2019; Wu et al., 2014; Zhao, 2010; Zuo et al., 2017). taxonomy, which would allow us to identify the precise However, the question if these are wild or domesticates re- species of bamboo and palm. Both bamboo and palm are mains unresolved. Evidence for wild rice remains in ar- used for similar products, so it does not appear to be related chaeological sites is scant. in a shift in function or human preferences, and indicates A single report of Pleistocene rice has been reported in strong adaptability to different raw material sources. Southeast Asia from Xom Trai, , dated to ~16000 B. P. O. nivara phytoliths have been recovered from the 4.1.2 Wild rice Yangtze River basin dating to ~17000 B.P. Also, rice finds The question of the origin, timing, and location of rice dating to the Late Pleistocene have been recorded off the (Oryza sativa) utilization by humans is one of the main Shanghai coast and in the Sorori peat deposits in Korea questions in East Asian archaeology. The question of the (Fuller et al., 2010). These dates are roughly consistent with domestication in southern China has been widely debated. the genetic analysis of domesticated rice and wild progeni- Collection and management of wild rice have long been an tors and which suggests that the first domesticated rice po- essential focus of archaeological research in China (Qiu et pulation split off from the wild O. sativa ssp. japonica al., 2019; Wang et al., 2010; Wu et al., 2014; Zhao, 2010; between 24.1–13.1 ka (Choi et al., 2017). However, these http://engine.scichina.com/doi/10.1007/s11430-020-9640-3 10 Wu Y, et al. Sci China Earth Sci finds were not associated with anthropogenic involvement in China, only a few sites of the flake-tool industry were dis- their accumulation. covered in southwest China and mainland Southeast Asia. The wild Oryza phytoliths found in Yahuai dated to These include, beside Yahuai, phases 1 and 2 of Bailiandong 15850–16366 cal yr B.P. represent the earliest known evi- Cave, Guangxi, that date between 36 and 18 ka, Lang Ron- dence for human gathering of wild rice in South China. Wild grien rock shelter in Krabi Province, southern rice present in Guangxi region during H1 event was gathered (Anderson, 1990, 1997, 2005; Mudar and Anderson, 2007), and utilized by humans prior to domestication. The presence as well as Nguom rock shelter, Mieng Ho Cave and Na Khu of wild rice in Yahuai provides supporting evidence that the Cave in Vietnam (Hoang and Nguyen, 1998; Nguyen, 2007, origin of Chinese domesticated rice was in this region, as 2008; Van Cay, 1995; Van Tan, 1985). suggested by genetic data (Huang et al., 2012). Among them, the Nguom Rockshelter site is the most important for understanding the dispersal of northern popu- 4.1.3 Urticineae (cf. Ulmus sp.) lations into the south during MIS 3 and the LGM. The site is Urticineae species of all families have been used in tradi- located in the Than Sa Valley, Thai Nguyen Province, tional Chinese medicine (Hu, 2000). In particular, elm leaves Northern Vietnam. Cultural remains from this site can be are used in many regions as famine food with the young divided into three stages. Stage 1 includes the stone artifacts fruits used as a green vegetable in China (Hu, 2000). Based from layers 4 and 5 attributed to a new industry termed the on phytolith analysis, Morris et al. (2009) suggested that “Nguom Culture” dated between 40 and 23 ka that has many paleolithic people may have consumed elm as food in the parallels with Yahuai units 4 and 3. The Nguom Culture is American southwest. In addition, elm leaves and bark are very similar to the flake-tool industries in South China, also an established traditional Chinese and Korean herbal especially the Yahuai cave assemblage. Nguom Culture and remedy for diuresis, edema, and soothing of the nerves, plus Yahuai cave assemblage share many common character- have the effect of pain-killing and arresting the blood (Choi istics: direct stone hammer percussion is the primary method et al., 2010; Kim et al., 2016; Lee et al., 2007). Indeed, for flake detachment and tool making; most of the tools were archaic humans have been noted to have utilized plants for made on flakes, simply and unifacially retouched; they are medical purposes (Hardy et al., 2012). The presence of Ur- small in size, and lack of uniformity; types of the tool include ticineae and more so the possible presence of elm suggests choppers, scrapers, and points with scrapers predominant. dietary or medicinal usage. Future studies may allow us to Utilization of elm in the Late Pleistocene reflects more distinguish between these possibilities. than just a biogeographic dispersal from north to south. The One of the main issues raised by the presence of cf. Ulmus sudden emergence and continued spread of lithic assem- sp. is understanding the biogeography of the species is re- blages similar to those in North China cannot be adequately lated to the movement of humans during MIS 3 and LGM. In explained by parallel and convergent development. How- the Late Pleistocene, two cultural traditions were common in ever, instead, these assemblages should be considered in the China, a northern small flake tool tradition and a southern context of human dispersal between northern and southern pebble tool tradition. One might assume that with the cooling parts of East Asia during the Late Pleistocene. Thus, South of the climate, southern populations would have adapted to China may have served as a refuge for human populations consume and use species such as elm utilizing their cultural escaping the cold, harsh climate in the north with more tradition. However, a closer inspection of the lithic traditions ameliorate conditions. indicates that this is not the case. The stone tool assemblages in units 2 and 3 cannot be attributed to the pebble/cobble industry as expected from the geographic location of Yahuai 5. Conclusion in Guangxi. The lithic assemblages are more similar to technologies that were common in North China. This study presents human-plant utilization over the past We propose that prehistoric populations from northern 30000 years in Yahuai cave, Guangxi, China. Economically regions migrated into southern China, bringing their tool kit essential species identified from phytoliths include putative with them. Sites of small flake-tool assemblages were also elm, bamboo, and palm and wild rice. found in the middle and lower reaches of the Changjiang Some species from North China such as cf. Ulmus, ex- (Yangtze) River, which is situated north of the Five Ridges panded their range due to cooler temperatures of the end of (Wang, 2016; Yuan, 1996; Yuan et al., 1994). Thus, the new MIS 3 and the LGM. The possibility that humans, seeking forager populations which arrived in South China and refuge from the colder north, brought their tool kit with them mainland Southeast Asia would have continued to use their (and utilized familiar northern taxa such as elm) is evinced technology to make small flake tools and were familiar with by the unique stone tool assemblages which resemble those the northern plants such as elm. in North China. Compared to the pebble tool industry known from South With the end of the deglaciation ~16000 cal yr B.P., hu- http://engine.scichina.com/doi/10.1007/s11430-020-9640-3 Wu Y, et al. Sci China Earth Sci 11 mans began to gather wild rice. Such behavior has been japonica. J Medicinal Food, 13: 1019–1023 known to be the prerequisite for rice domestication. While Chongtham N, Bisht M S, Haorongbam S. 2011. Nutritional properties of bamboo shoots: Potential and prospects for utilization as a health food. additional studies are warranted to constrain the taxonomic Comprehensive Rev Food Sci Food Saf, 10: 153–168 identification, current evidence from Yahuai cave provides Fangwu Z, Weisan L. 1997. The dental caries of the Neolithic Population critical information about the adaptability of modern humans From Zengpiyan Cave of Guilin, China. Acta Anthropol Sin, 16: 271– 273 in the Late Pleistocene in South China. Fenwick R S H, Lentfer C J, Weisler M I. 2011. Palm reading: A pilot study to discriminate phytoliths of four Arecaceae (Palmae) taxa. J Archaeol Sci, 38: 2190–2199 Acknowledgements We would like to thank Ofer Bar-Yosef, Tuo Fredlund G G, Tieszen L T. 1994. Modern phytolith assemblages from the Yang, and Xinying Zhou for their assistance. 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