Combining Odontochronology, Tooth Wear Assessment, and Linear Enamel Hypoplasia (LEH) Recording to Assess Pig Domestication in Neolithic Henan, China

Authors


Abstract

Mandibles of Sus scrofa (wild boar/pig) from ritual pits H160 and H208 of Longshangang, a Late Yangshao Neolithic site in Xichuan County, Henan, were analyzed for evidence of domestication. Three methods of dental analysis were applied: odontochronology, tooth wear assessment, and linear enamel hypoplasia (LEH) recording, which provide age at death, season of kill, and season of birth data. We investigate whether: (i) the LEH height frequencies on the second molars of the mandibles correspond with the possibility of double farrowing and (2) double farrowing is supported by the season of and age at slaughter data. If so, these data suggest a substantial degree of human management of suids at the site. Copyright © 2014 John Wiley & Sons, Ltd.

Introduction

The domesticated pig (Sus scrofa) has long been one of the most economically and culturally significant animals in China (e.g. Yuan and Flad, 2002; Yuan et al., 2010). Apart from dogs, pigs were the earliest Chinese domesticated animals. While recent genetic studies of pigs suggest that multiple domestications most likely took place across the Old World (Larson et al., 2005), it is also possible that multiple domestications of pig took place within China (Flad et al., 2006:188). Yuan and colleagues (Yuan, 2001; Yuan et al., 2010) conclude that the earliest evidence for pig domestication comes from the Xinglongwa Site, Chifeng, Inner Mongolia (8200–7000 BP); the Cishan Site, Wu'an, Hebei Province (8000 BP); the Jiahu Site, Wuyang, Henan Province (8500 BP); and Kuahuqiao, Xiaoshan, in Zhejiang Province (8200–7000 BP).

In this study, a continuation of a project begun in summer of 2010 (Pike-Tay and Ma, 2011), we analyzed the dentition of pig mandibles from ritual pits H160 and H208 of Longshangang, a Neolithic site in Xichuan County, Henan Province, for evidence of domestication. The mandibles of wild boar of known age and date of death from Henan and Zhejiang provinces were also examined. Three methods of dental analysis were applied to the Sus mandibles: odontochronology, tooth wear assessment, and linear enamel hypoplasia (LEH) recording. Resultant data regarding the suids' age at death, season of slaughter, and season of birth were evaluated for evidence of human stock management.

Materials

The archaeological site and samples

The Longshangang site from which the pig mandibles were excavated is located in the village of Huanglianshu, Xichuan County, Henan Province, on the tableland east of the Naoyu River (geographic coordinates 111.5°E and 33.1°N) (see Figs. S1a,b; S2). Xichuan County is located in southwestern Henan Province, adjacent to southern Shaanxi and Northwestern Hubei. The northwestern area of the county is mountainous, with hills extending to the southeast and lowland valleys in the central and southernmost parts. The site is still undergoing excavation and analysis. Our study sample is from the 5000-m2 area excavated between May 2008 and October 2009. Longshangang's cultural levels span a time range of several thousand years including the Ming, Qing, Song, Han, and Western Zhou Dynasties, the Wangwan Three Cultures, Shijiahe Culture, Qujialin Culture, and the late Yangshao Culture. The majority of the cultural and faunal remains come from the Neolithic levels, particularly the late Yanghshao (approximately 5500–5000 BP) (Lin, 2011:12–13). Wild sows in Henan normally produce one litter of young per year during the spring, while double farrowing occurs with domestication (Luo, 2010). Evidence has so far provided an unclear story of the origin of pig domestication in this region of China (Ma, 2005).

A total of 15 286 fragments of faunal remains from late Yangshao, Qujialing, and Shijiahe neolithic cultures (ranging chronologically earliest to latest) were excavated from the 5000-m2 area. The late Yangshao stratum yielded a number of identified specimens (NISP) count of 9520, along with 11 house foundations and 36 ash pits. Eleven mammalian species have been identified thus far (Lin, 2011: Tables 1 and 2, pp. 16–17). Six of the ash pits (H121, H160, H165, H205, H206, and H208) in the west of the excavation area stood apart from the other 30: 4434 pig bone fragments (60.9% of all the Sus remains excavated), 89 fragments of middle-sized animal remains, and 60 unidentified fragments were found in these six late Yangshao pits. With the exception of a complete pig skeleton encountered in H206, nearly all the Sus remains in the other five pits were mandibles, with few maxillary fragments (Ibid).

Table 1. Expected age at winter death according to season of farrow with corresponding MWS range
 Farrowing seasonH208 MWS rangeH160 MWS rangeCombined range
First winterspring (10–11 mos)MWS 7–10MWS 8–10MWS 7–10
autumn (5–6 mos)MWS 4–5MWS 4–7MWS 4–7
Second winterspring (22–23 mos)MWS 17–32MWS 22–27MWS 17–32
autumn (17–18 mos)MWS 14–15MWS 15–21MWS 14–21
Third winterspring (34–35 mos)MWS 36–43MWS 35MWS 35–43
autumn (29–30 mos)MWS 35MWS 32MWS 32–35

The sample for the present study consists of the pig mandibles from pits H160 (Sus NISP = 1998) and H208 (Sus NISP = 848). In addition to being the only skeletal element present in these pits, the mandibles were systematically arranged in rows in pit H208, while the more fragmented mandibles of H160 exhibit burning. Lin's actualistic experiments support an interpretation of defleshed mandibles having been deposited in this pit (2011:65–74). Our sample from H160 was comprised of teeth from seven complete mandibles, 94 hemi-mandible fragments (c. 47 left/right pairs), and 82 single-sided fragments. The H208 sample consists of teeth and dental series from 45 complete mandibles, 32 hemi-mandible fragments (16 left/right pairs), and 59 single-sided fragments.

The control samples

The modern reference collection of the complete mandibles of 48 wild boar (15 males, 17 females, and 16 juveniles of unknown sex) of established age and known season of death are from the Wangwushan mountains near the Longshangang site (for sample details, see Pike-Tay and Ma, 2011). The wild boars in this collection were hunted by the Department of Forestry of the Henan Government during a 1-month period from middle December 2005 to middle January 2006. An additional modern sample of 39 wild boar mandibles (16 males, 19 females, and 4 juveniles of unknown sex) from the Quzhou mountain area of Zhejiang Province in southeastern subtropical zone is employed in the current study. The local government's forestry rangers hunted these wild suids from October 16 through November 17, 2008. We identified four age groups within these two regional reference samples on the basis of tooth eruption and wear (following Grant (1982) and Bull and Payne (1982)): ca. 8 months, ca. 20 months, ca. 32 months, and ca. 44 months. We recognize that variability in wild boar size and shape exists across space and through time. Therefore, while we cannot be sure that modern wild boar are the same as those from the Neolithic, for the purposes of odontochronology, the correspondence of LEH with double farrowing, and overall tooth size similarities considered here, we feel justified in referring to these recent wild boar in this exploration of the plausibility of combining the methods and techniques of analysis outlined here.

Methods

As the metric analysis leading to the initial hypothesis that pigs from Longshangang are domesticated is detailed in a Chinese language Masters thesis by one of us (Lin, 2011), we summarize the results below. As tooth wear is ongoing, the width of molar is most unchangeable as opposed to its length, which leads scholars to conclude that molar width is more reliable than length for assessing the difference between wild and domestic pigs (Flannery, 1983; Kusatman, 1991). Furthermore, pig molar width has also been successfully employed in recognizing pig domestication in Chinese Neolithic samples (Ma, 2003; 2007). As the first molar (M1) yields more ambiguous results, researchers tend to apply more the reliable M2 and M3 data. For the present study, Lin compared the length, mesial width, and distal width of the occlusal surfaces of the three mandibular molars (Table S1) from pit H160 to the modern wild boar samples from Wangwushan, where the environment is similar to that of the Longshangang Site (see Figures 1a,b; 2a,b; 3).

Figure 1.

a,b. Comparison of the length, mesial width, and distal width of the occlusal surfaces of the first mandibular molars of Wangwushan wild boar to the pigs of the Neolithic Yangshao Pit H160.

Figure 2.

a,b. Comparison of the length, mesial width, and distal width of the occlusal surfaces of the second mandibular molars of Wangwushan wild boar to the pigs of the Neolithic Yangshao Pit H160.

Figure 3.

Comparison of the length and width of the occlusal surfaces of the third mandibular molars of Wangwushan wild boar to the pigs of the Neolithic Yangshao Pit H160.

As the figures reveal, two different patterns can be seen in the metric comparisons between the Neolithic and modern wild pig samples. The first is shown in Figures 1-a and b, where it is difficult to distinguish Neolithic samples from modern ones. In contrast, relatively distinct differences are shown in the other figures (Figures 2-a, 2-b, and Figure 3). The second pattern shows that the metric data of M2 and M3 from the Yangshao pit H160 are obviously smaller than those from Wangwushan wild boar. Different patterns can also be recognized in the mesial and distal widths of the first molar M1, although this is not as clear as with M2 and M3. Overall, the molar dimension data from Yangshao pit H160 pigs are different from the Wangwushan wild boar. Lin attributes those dimensions that run into the wild boar range to individual body differences, or the fact that a small number of wild boars may indeed have been present in Yangshao pit H160. (If the latter is the case, then some wild boar might still have been hunted and consumed by late Neolithic people). Lin concluded from the statistically significant differences between the M2 and M3 data that the remains from pit H160 were likely those of early domesticates (2011:25–34).

Using Lin's (2011) conclusions as a starting point, three methods are used in the present study to evaluate this possibility of domesticated rather than wild pigs as represented by the mandibles from the H160 and H208 pits at Longshangang: mandibular eruption and wear stage assessment, LEHs, and odontochronology.

Mandibular eruption and wear stage assessment

The first and most basic technique, mandibular eruption and wear stage assessment allowed for the assignment of approximate age based on the presence and stages of eruption and wear of pig and/or wild boar teeth in the mandible (Bull and Payne, 1982; Grant, 1982; Rolett and Chiu, 1994; Ma, 2007). This method entails assigning each molar and P4 per individual a wear stage. Each stage corresponds to a number which when summed together for all the teeth considered equals a mandibular wear stage (MWS). Due to the small number of complete mandibles, the right side of complete mandibles and mandibular fragments with at least two observable molars were examined for pigs from pits H208 and H160.

The sample from H160 furnished 40 hemi-mandibles from a probable 20 individuals as well as a single hemi-mandible each from two different individuals that could be assigned to wear stages (per Grant, 1982). Pit H208 allowed for 52 wear assignments on the basis of seven hemi-mandible fragments and 45 nearly complete mandibles.

LEHs

The second method involved recording the presence of LEH on the teeth, which may indicate a period of nutritional stress in the life of an animal. Pioneering work on suids has been done in this regard by Dobney and colleagues (Dobney and Ervynck, 1998, 2000; Dobney et al., 2004; Dobney et al., 2007). Their work has demonstrated that LEH occurrences on domesticated pigs from archaeological sites are neither rare nor random. Moreover their work provides a chronology of physiological stress events that explain why LEH is always present at same heights of molar crowns:

…birth and weaning are the direct causal agents of two discrete peaks in the height distribution of LEH on the first permanent molar (M1), and a period of under nutrition encountered during the first winter of the animals’ life is thought to be the main causal factor for the occurrence of the single distinct LEH peak noted on the M2. A broad peak on the M3 is similarly interpreted, i.e. as reflecting the animals’ second winter (Dobney et al., 2007: 59).

LEH occurs in wild boar as well, but at a consistently low frequency (Ibid), as is the case with the control sample of wild boar from Henan referred to in this study (Luo, 2010).

To see if the Chinese archaeological sample showed the same patterns, the frequency of LEH within the archaeological populations represented by the suids from pits H160 and H208 was evaluated by height frequency graphs and by the index defined by Dobney et al. as:

display math

where F is the number of LEH lines observed divided by the number of specimens observed calculated per population, for each individual tooth cusp, when the number of specimens is greater than zero (2007: 60–61). The index is a comparison of the relative frequency of LEH (averaged over all the tooth cusps) for all populations together. The standard deviation of the calculated average describes variation between the teeth and cusps within a population (Ibid: 61).

If the LEH frequencies align with the seasonal pattern outlined by Dobney and colleagues, then it may be possible to test for double farrowing as the top of the second molar emerges first. An M2 of a piglet born in spring thus has greater time to develop compared to a piglet born in autumn (Dobney et al., 2004; Vanpoucke et al., 2007). It is expected, therefore, that an LEH observed on the M2 of a spring-farrowed piglet would be lower than an LEH on the M2 of an autumn-farrowed piglet. For this reason, the height frequencies of cusp A of the M2 were analyzed.

The sample for LEH study of Sus from pit H160 consisted of 21 right hemi-mandibles from different individuals. Pit H208's LEH study was based on the whole (conjoined) mandibles of 32 individuals and seven hemi-mandibular fragments. We did not use the entire assemblage of H208's 45 complete mandibles for LEH because 13 of these were too young (not even the first molar had erupted) to do LEH assessment on.

Odontochronology

The third technique, odontochronology, entailed the measuring and recording of incremental growth structures in the root cementum of the suids' thin-sectioned (c.30 microns thick) teeth as viewed under polarized light microscopy at 100× or 250×. This method is based on the fact that a yearly cycle is marked in the mineralized tissues of the teeth of most high-latitude and temperate zone mammals by one wide (growth) zone, temporally corresponding to the warmer seasons; in addition to one narrow annulus (slow growth) and/or a ‘line of arrested growth’, temporally corresponding to ‘winter’, and observable in the dental cementum and/or dentine (cf. Mina and Klevezal, 1970; Castanet, 1981; Francillon-Vieillot et al., 1990; Lieberman, 1993a; 1993b; Pike-Tay, 1995; Klevezal, 1996; Pike-Tay and Ma, 2011). For full accounts of protocol and techniques for specimen preparation, thin sectioning, and data recording for odontochronology, see e.g. Lieberman (1993a,1993b), Pike-Tay (1995), Burke (1995), and Pike-Tay and Ma (2011). The effectiveness of odontochronology for both season of death and independent age at death determinations for Sus from Henan has been demonstrated (Pike-Tay and Ma, 2011).

Results

Odontochronology, season of death

The samples from H160 that underwent odontochronological study included the M1s from 22 different pigs, 19 of which provided results. From H208, the M1s of 19 different individuals were processed and 16 provided results (Table S2). All of the pigs from pit H208 were culled from winter to early spring, with the most kills in early spring (Figure 4a). The mandibles from pit H160 provided indications of late fall/early winter, winter, and early spring with most kills having occurred while the winter annulus was still in formation in the tooth root (Figure 4b).

Figure 4.

a Season of death of Sus from pit H208 as determined by dental cementum analysis. Data in Table S2. b Season of death of Sus from pit H160 as determined by dental cementum analysis. Data in Table S2. This figure is available in colour online at wileyonlinelibrary.com/journal/oa.

Results: MWS assessment

The frequency distributions of the MWSs provide a view of the relative age at death (Table 1; Figure 5 a, b, c). Multiple peak slaughter ages are evident in both samples, which seems to contradict the results from the odontochronology study. One possible explanation for this may have been the occurrence of double farrowing. If there was a spring and an autumn farrow and one season in particular such as late winter/early spring was the preferred season of slaughter (as evidenced by the cementum annuli analysis above), it would be expected that a piglet born in spring and killed in its first winter would be 10–11 months old. Likewise, a piglet born in autumn would be 5–6 months old by late winter. Using this hypothesis, it is possible to determine which mandible wear stages correspond with which season of farrow.

Figure 5.

(a) Frequency distribution of H208. (b) Mandible wear stage frequency distribution H160. c Mandible wear stage frequency distribution, combined samples. This figure is available in colour online at wileyonlinelibrary.com/journal/oa.

Table 1 describes the corresponding mandible wear stages with age, while Figures 5a and b show the frequency distribution with the season of death denoted above, following Vanpoucke et al. (2007). Between mandible wear stages 17 and 30 (coinciding with a spring farrowed group if double farrowing occurred), pit H208 has only three individuals, an interesting absence that would indicate that humans were waiting longer to kill pigs in their second winter. This gap is not evident at H160, and when compared, more pigs were killed in their second winter at H160 than H208. If the age of the pig at slaughter held any meaning for the rituals conducted at these pits, then this may show that the pits were used for different practices.

Results: LEH assessment

Using the method of recording LEH outlined by Dobney and colleagues described above, three populations were examined: the northern wild boar control population from Henan; the southern wild boar control population from Zhejiang province; and the archaeological population taken from pits H208 and H160. The archaeological sample was analyzed by pit and included in the index separately. The index was calculated using the formula from Dobney and Ervynck (1998). Tables 2aa and 2ab show total numbers of cusps examined and LEH recorded for the archaeological and recent Sus teeth. The relative frequency index (Figure 6) revealed that the archaeological population of suids from Longshangang had a higher frequency of LEHs than the modern control population of wild boar (see also Luo, 2010 wild boar results for the Henan control sample), indicating greater reliance on humans. Moreover, the height distribution of LEHs on the M2 from the Longshangang pigs exhibited multiple peaks. In all cases, the sample sizes were small, limiting the extent of any conclusions drawn. Nevertheless, some aspects stand out.

Table 2a. Total cusps examined
CuspNorthern controlSouthern controlH208H160Total
M1a40404119140
M1b40404119140
M2a30401918107
M2b30401918107
M3a91812443
M3b91812443
M3c91812443
Total16721415686623
Table 2b. Total LEH observed
CuspNorthern controlSouthern controlH208H160Total
M1a8213124
M1b327012
M2a1186429
M2b486422
M3a127313
M3b01405
M3c00101
Total27234412106
Figure 6.

Index of LEH frequency. This figure is available in colour online at wileyonlinelibrary.com/journal/oa.

The archaeological population (pits H208 and H160) had a greater frequency of LEH, exhibiting more depressions and pits than lines. Moreover, as many of the first molars from pit H160 were very worn, existing LEH may have disappeared. The number of mandibles from H160 was significantly smaller than H208 and the modern control populations. The H208 population had the highest frequency of overall LEH. Like those on the H160, most of the LEH on teeth from H208 consisted of pits and depressions in the enamel (e.g. Fig. S3).

Only two M1 were found to have more than one LEH (both had two): the first was from the northern wild boar control population and the second from the H208 population. A single M2, from the southern wild boar control population, and one M3, from the H208 population, contained two lines. The H160 population had no molars with multiple LEH. Most LEH were found on the M2 (51 out of 106) followed by the M1 (36 out of 106) and M3 (19 out of 106). This could be an artifact of the heavy wear on an M1 by the time an M3 has fully erupted. In other words, if an LEH was visible on M3, the M1 was usually too worn for LEH to be observed on a macroscopic level. All LEH on the modern control sample observed were slight lines or depressions that were generally very high on the cusp.

The low, overall frequency of LEH in both archaeological and modern samples may explain why the pattern of height frequency does not fit with that observed for the Northern European suids by Dobney and Ervynck (2000). Figure 7a, b, c, d, e, f, g depicts the height frequency for each cusp of the three molars. Moreover, in an LEH study of Sus from 19 Chinese archaeological sites ranging from early Neolithic to late Warring States, Luo (2010) did not find the same seasonal pattern as Dobney and Ervynck.

Figure 7.

(a) Frequency distribution of LEH height on M1, cusp a. (b) Frequency distribution of LEH heights on M1, cusp b. (c) Frequency distribution of LEH height on M2, cusp a. (d) Frequency distribution of LEH height on M2, cusp b. (e) Frequency distribution of LEH heights on M3, cusp a. (f) Frequency distribution of LEH heights on M3, cusp b. (g) Frequency distribution of LEH heights on M3, cusp c. (h) Smoothed frequency distribution of LEH height on M2, cusp a, using moving average (n = 1).

The LEH height frequencies of the M2 were examined here (Figure 7 c,d) for evidence of double farrowing. Multiple peaks on cusp A of M2 observed for H160 archaeological sample are consistent with expectations of double farrowing because peaks are observed above and below the midline of the tooth. Three peaks in H160 were observed, with 52% of LEH observed on M2 of H160 between 2.01 and 2.50 mm, while 25% were at 4.01–4.50 mm and another 25% at 6.01–6.50 mm. The highest peak, at 6.01–6.50 mm, is just above the mid-line of the cusp. For H208, however, the LEH were all generally located on the lower half of the cusp (highest frequencies at 2.01–2.50 mm [33%] and 5.01–5.50 mm [33%], with a small peak at 4.01–4.50 mm [16.67%]), and their nearness may be indicative of the same life event. In addition and contrary to expectations, the both modern, wild groups exhibited multiple peaks but with no discernible pattern. When the frequency distributions are smoothed with a moving average (n = 1), the results are similar (Figure 7h).

While double farrowing may explain the unusual pattern of LEH, the individual variation of tooth development and overall low frequency of LEH may also be the result of greater access to higher nutrient food stuffs during the winter provided by humans at Longshangang. In other words, while the results for LEH show that the archaeological sample was likely domesticated, alone the evidence for double farrowing, although slightly in its favor, is ambiguous.

Discussion and conclusions

As noted above, in his initial study of the Sus mandibles from the late Yangshao stratum of Longshangang, Lin (2011) suggested that the mandibles from the H160 and H208 pits were those of domesticated pigs because the size differences of the M2 and M3 between the samples from H160 and Wangwushan (modern wild boar) are statistically significant. The results of the application of the three methods discussed here lend support to this initial hypothesis.

The season at death study indicates that the pigs from both pits were slaughtered during winter into early spring. Interestingly, the MWS frequency distribution, when analyzed for season of slaughter, corresponds to a preferred winter slaughter if double farrowing was occurring (which happens as a result of domestication). While the appearance of multiple peaks of the M2 LEH height distribution may indicate double farrowing, the overall low frequency of LEH prevents a robust conclusion in this regard. That said, the study of LEH may in and of itself correspond with pig domestication if the animals, which were the primary animal protein source of both economic and social value in Neolithic China, were provisioned during winter. In sum, these multiple lines of evidence suggest a significant degree of human management of the Longshangang pig population.

Acknowledgements

We thank the Henan Provincial Institute of Cultural Relics and Archaeology and Vassar College's Undergraduate Research Summer Institute, Faculty Research Fund, and Environmental Research Institute for generous support of this project. We also gratefully acknowledge the laboratory assistance of Vassar College students Kate Czechowski and Lily Yachen Sun. Finally, we extend thanks to our anonymous reviewers for their helpful and insightful recommendations.

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