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前处理与测试条件差异对化石牙釉质羟磷灰石稳定同位素数据的影响:以步氏巨猿动物群为例

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姜曲怡1,2, 赵凌霞,1,3,*, 胡耀武,4,5,1,2,*1 中国科学院古脊椎动物与古人类研究所,中国科学院脊椎动物演化与人类起源重点实验室 北京 100044
2 中国科学院大学考古学与人类学系 北京 100049
3 中国科学院生物演化与环境卓越创新中心 北京 100044
4 复旦大学文物与博物馆学系 上海 200433
5 复旦大学科技考古研究院 上海 200433

Isotopic (C, O) variations of fossil enamel bioapatite caused by different preparation and measurement protocols: a case study of Gigantopithecus fauna

JIANG Qu-Yi1,2, ZHAO Ling-Xia,1,3,*, HU Yao-Wu,4,5,1,2,*1 Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences Beijing 100044
2 Department of Archaeology and Anthropology, University of Chinese Academy of Sciences Beijing 100049
3 CAS Center for Excellence in Life and Paleoenvironment Beijing 100044
4 Department of Cultural Heritage and Museology, Fudan University Shanghai 200433
5 Institute of Archaeological Science, Fudan University Shanghai 200433

收稿日期:2019-12-3网络出版日期:2020-04-20
基金资助:中国科学院战略性先导科技专项(B类).XDB26000000
国家自然科学基金资助.41773008


Corresponding authors: *zhaolingxia@ivpp.ac.cn;ywhu@fudan.edu.cn
Received:2019-12-3Online:2020-04-20


摘要
牙釉质羟磷灰石的稳定同位素分析被广泛应用于古生物学研究之中,以重建古生态和古环境信息。在对不同研究中的同位素结果进行对比分析时,往往会忽略不同实验室、不同前处理方法可能引发的数据误差。为了探讨这些因素对牙釉质羟磷灰石同位素值的影响,重新测量了湖北省龙骨洞步氏巨猿动物群动物牙釉质样本的碳氧稳定同位素值,该批样本曾使用不同的前处理和实验方法进行过测试(Zhao et al., 2011;Nelson, 2014)。研究结果显示,重测的数据与Zhao et al. (2011)、Nelson (2014)发表的数据结果均存在一定差异。前处理方法与实验室测试差异都会造成牙釉质碳、氧稳定同位素结果的偏差。相较氧同位素而言,碳同位素值会更容易被前处理过程中反应试剂、反应时间等的不同所影响。但上述因素所导致的数据差异较小,不会对后续的分析产生实质性影响。本研究为直接对比不同来源牙釉质同位素值的可行性提供了初步的理论支持。建议为减少由于样品前处理和实验测试方案引发的数据误差,获得更加精确的研究结果,应尽可能采用同样的前处理与测试方案,多进行实验室间数据校正对比分析。
关键词: 牙釉质羟磷灰石;稳定同位素分析;羟磷灰石前处理;同位素数据测量

Abstract
Stable isotopic (C, O) analysis of fossil enamel bioapatite has been widely used in paleontological fields to reconstruct the paleoecology and paleoenvironment. It is common to compare the isotopic data of enamel bioapatite made by different pretreatment and measuring methods in different labs, without considering the isotopic variations possibly caused by different protocols. Here, we chose the same samples from Gigantopithecus fauna in the Longgu Cave (Longgudong), Hubei and remeasured their δ13C and δ18O values, which had been previously reported in Zhao et al. (2011) and Nelson (2014) with different pretreatment and measuring methods, in order to evaluate the effects of the above factors on the isotopic variability. The comparison among three isotopic dataset indicates that there did exist small isotopic variations on the δ 13C and δ 18O values. It seems that the δ 13C values were more influenced, probably due to differential practices to eliminate the diagenetic effects using varied chemicals and retaining reaction time during the process of bioapatite preparation. However, we should emphasize that the small isotopic variations observed here do not have produced substantial isotopic variance among fossil taxa and localities, providing the preliminarily theoretical foundation to make isotopic comparison directly. Even so, we still recommend that it is best to compare the isotopic data according to the same preparing and measuring protocols to remove the systematic errors or to re-measure samples again in different labs to calibrate the data.
Keywords:fossil enamel bioapatite;stable isotope analysis;bioapatite pretreatment;isotopic measurements


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本文引用格式
姜曲怡, 赵凌霞, 胡耀武. 前处理与测试条件差异对化石牙釉质羟磷灰石稳定同位素数据的影响:以步氏巨猿动物群为例. 古脊椎动物学报[J], 2020, 58(2): 159-168 DOI:10.19615/j.cnki.1000-3118.200109
JIANG Qu-Yi, ZHAO Ling-Xia, HU Yao-Wu. Isotopic (C, O) variations of fossil enamel bioapatite caused by different preparation and measurement protocols: a case study of Gigantopithecus fauna. Vertebrata Palasiatica[J], 2020, 58(2): 159-168 DOI:10.19615/j.cnki.1000-3118.200109


1 Introduction

Stable isotope (C, O) analysis of fossil tooth enamel has been widely applied in paleontological research to reconstruct the paleoecology, paleoclimate and paleoenvironment of animals and hominins (Clementz, 2012). Bioapatite, the main inorganic component (97%) in enamel, is the hardest tissue in teeth and resistant to the diagenetic effects during the geological times. Chemically, enamel bioapatite is similar to hydroxyapatite crystal and consists of calcium, phosphate and hydroxyl (Ca10(PO4)6(OH)2) (Metcalfe et al., 2009). The carbonate can substitute for the phosphate and hydroxyl in hydroxyapatite and be called as structural carbonate generally. As there is a strong relationship between the isotope values of animals and their diet (Kohn, 1999), the carbon and oxygen isotope compositions of carbonates in enamel bioapatite are analyzed to reflect the information on diets and habitats of animals during the stage of tooth development (Clementz, 2012; Lee-Thorp and Sponheimer, 2014; Sponheimer and Lee-Thorp, 2014).

The teeth enamel is the hardest tissue with little organic matters (<2%) and high crystallinity in animals (Shin and Hedges, 2012). Therefore, it is always expected to be most resistant to suffering from the diagenetic effects (Clementz, 2012). However, some studies show that it is still possible for enamel to be contaminated during long-term deposits and that the chemical compositions might have been altered to some extents (Zazzo, 2014; Kendall et al., 2018; Price et al., 2019). Thus, various pretreatment methods have been proposed, trying to eliminate the potential contaminants. In general, sodium hypochlorite (NaClO), hydrogen peroxide (H2O2) have been suggested to get rid of the organic matters and acetic acid (CH3COOH) to remove the potentially diagenetic carbonate (Koch et al., 1997; Snoeck and Pellegrini, 2015). But the protocols to utilize the chemicals such as the type, reaction time, concentration etc., are varied and have not reached a consensus yet. Several comparisons have been made to evaluate the chemical effects of the treatment methods on isotopic variations using modern and fossil enamel (Koch et al., 1997; Crowley and Wheatley, 2014; Snoeck and Pellegrini, 2015; Pellegrini and Snoeck, 2016; Skippington et al., 2019). However, it has been routine in paleontological research to directly compare the isotopic data of fossil animals produced in different pretreatment methods and in different labs, without considering the probably isotopic differences (Nelson, 2014; Bocherens et al., 2017; Stacklyn et al., 2017; Suraprasit et al., 2018). To date, the isotopic variations generated by diverse pretreatment methods and labs, using the same samples of vertebrate fossils, have always been neglected and not been investigated systematically yet.

In this paper, we re-measured the stable isotope values of the giant ape (Gigantopithecus blacki) fauna samples in our lab that were reported separately by Zhao et al. (2011) and Nelson (2014) and tried to find out the isotopic variations among them. Our aim was to discuss the factors to influence the isotopic fluctuations among different methods and labs and better understand the feasibility of isotopic comparisons in combination with isotopic data with various sources.

2 Materials and methods

2.1 Materials

The materials used in this study are the same as those in Zhao et al. (2011) and Nelson (2014) and the original numbers are listed in Table 1.


Table 1
Table 1Results of δ13C and δ18O values in Zhao et al. (2011), Nelson (2014) and this study (VPDB, ‰)
NumberNumber (original)Speciesδ13C (our study)δ13C (Nelson, 2014)δ13C (Zhao et al., 2011)δ18O (Nelson, 2014)δ18O (our study)
11Leptobos sp.-15.4-14.4-15.8-9.7-9.9
22Leptobos sp.-15.2-14.5-15.4-9.3-9.6
33Leptobos sp.-16.7-15.8-17.1-9.3-9.6
44Leptobos sp.-15.0-14.3-15.3-7.2-7.2
55Cervus sp.-16.5-15.5-16.8-5.7-5.7
66Cervus sp.-17.4-16.5-17.8-7.6-7.7
77Cervus sp.-14.9-14.1-15.5-6.4-6.2
88Tapirus sinensis-15.9-15.0-16.6-10.4-10.1
99Tapirus sinensis-17.1-16.2-17.7-10.9-10.8
1010Tapirus sinensis-15.6-15.1-16.3-9.2-9.4
1111Tapirus sinensis-15.8-15.7-16.1-12.2-11.3
1212Rhinoceros sinensis-14.0-13.8-14.4-9.7-10.0
1313Rhinoceros sinensis-15.6-15.3-15.8-10.0-10.4
1414Rhinoceros sinensis-14.6-14.1-14.9-6.4-6.1
1515Rhinoceros sinensis-15.5-15.2-15.8-9.4-9.1
1616Pachycrocuta licenti-13.8-13.7-14.1-9.8-9.1
1718Ailuropoda wulingshanensis-17.9-16.7-18.3-7.7-7.2
1823Gigantopithecus blacki-16.7-15.6-17.2-9.4-9.5
1924Gigantopithecus blacki-15.4-15.4-15.9-9.2-9.2
2025Gigantopithecus blacki-17.4-16.6-18.2-8.1-8.7
2126Gigantopithecus blacki-13.7-12.1-14.2-10.5-9.5

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Twenty-one teeth from 7 taxa (Table 1) were sampled from Longgu Cave (Longgudong), Hubei Province for C and O isotope analysis. They included four bovids (Leptobos sp.), three deer (Cervus sp.), four tapirs (Tapirus sinensis), four rhinoceroses (Rhinoceros sinensis), one giant panda (Ailuropoda wulingshanensis), one hyena (Pachycrocuta licenti) and four giant apes (Gigantopithecus blacki). They were used for the following analyses. All the isotopic results listed below are expressed as δ13C and δ18O values relative to V-PDB.

2.2 Methods for enamel preparation and isotopic measurements

2.2.1 Method 1 from Zhao et al. (2011)

Firstly, the surface dirt and remained dentine of enamel samples were cleaned off and then the enamel was powdered. Secondly, the samples were soaked in 5% sodium hypochlorite for 12 h and then were rinsed with distilled water. Thirdly, the samples were soaked in 6% acetic acid for 12 h and then were rinsed with distilled water again to remove diagenetic carbonates. After that they were dried and collected. Finally, the CO2 was extracted by H3PO4 method, reacting with 100% phosphoric acid for 12 h at 25 °C and analyzed by a Finnigan Mat 252 mass spectrometer at the Stable Isotope Laboratory in the State Key Laboratory of Lithospheric Evolution of Institute of Geology and Geophysics, Chinese Academy of Sciences (Zhao et al., 2006). Only the δ13C values of samples were reported and listed here in Table 1. The analytical precision is better than 0.1‰.

2.2.2 Method 2 from Nelson (2014)

Firstly, the enamel was collected by drilling from the surface of same samples. Secondly, the enamel powders were soaked in 3% hydrogen peroxide (H2O2) for 15 min and rinsed by neutral water. After that, the samples were soaked in 0.1 M acetic acid for 15 min and then rinsed again. Finally, the samples reacted with anhydrous phosphoric acid for 17 min at (77±1)°C and were analyzed by a Finnigan MAT Kiel IV device coupled with a Finnigan Mat 253 mass spectrometer at Department of Earth and Environmental Sciences at the University of Michigan. The isotopic results (C, O) were calibrated by international isotopic standards (NBS18 and NBS19) and listed in Table 1. The analytical precisions of both isotopic values are better than 0.1‰.

2.2.3 Method 3 in this study

The samples available for isotopic analysis here were from the enamel powders prepared by Zhao et al. (2011). They were rinsed in distilled water again, freeze-dried, and grinded into powder. The CO2 was prepared by H3PO4 method, reacting with ultrapure phosphoric acid (H3PO4) for 1 h at 80°C, and analyzed by an Isoprime-100 Isotope Ratio Mass Spectrometry (IRMS) coupled with a multi-flow system at the Archaeological Stable Isotope Laboratory in Department of Archaeology and Anthropology, University of Chinese Academy of Sciences. The isotopic results (C, O) were calibrated by international isotopic standards (IAEA CO-8 and IAEA 603) and the measurement stability was monitored by the insertion of another international isotopic standard (NBS 18) into the sample list. The analytical precisions for both isotopic values are better than 0.2‰. The results were listed in Table 1.

3 Results

The isotopic results from published data (Zhao et al., 2011; Nelson, 2014) and our study are presented in the Table 1 and Fig. 1.

Fig. 1

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Fig. 1The comparison of δ13C and δ18O values in Zhao et al. (2011), Nelson (2014) and this study

(Δ1=δ13CNelson-δ13CZhao; Δ2=δ13CNelson-δ13COur Study; Δ3=δ13COur Study -δ13CZhao; Δ4=δ18ONelson-δ18OOur study)


Although the samples for isotopic measurements were selected from the same teeth in three studies, there are still substantial differences among them in Table 1. In our study, the δ13C values are -13.7‰ to -17.9‰, averaged by (-15.7 ±1.2)‰ (n=21), and the δ18O values range from -5.7‰ to -11.3‰, averaged by (-8.9 ±1.6)‰ (n=21). The δ13C values of Zhao et al., (2011) have a range from -14.1‰ to -18.3‰ and the mean value is (-16.2 ±1.3)‰ (n=21). The δ13C values of Nelson (2014) range from -12.1‰ to -16.7‰ with the mean of (-15.0 ±1.1)‰ (n=21) and the δ18O values are from -5.7‰ to -12.2‰ with the mean of (-9.0 ±1.6)‰ (n=21).

We made a histogram plot that described the isotopic differences among three studies. In Fig. 1, largest difference of δ13C values with the mean of (1.1±0.5)‰ (n=21) is observed between Zhao et al. (2011) and Nelson (2014) while there is an intermediate difference of δ13C values with the mean of (0.7±0.4)‰ (n=21) between our study and Nelson (2014). Smallest difference of δ13C values between our study and Zhao et al. (2011), averaged by (0.4±0.2)‰ (n=21), is seen in Fig.1. Generally, there is a small difference of δ18O values between our study and Nelson (2014) with the mean of (0.3±0.3)‰.

Furthermore, the paired samples t-test results show that there are significant differences of the δ13C values (P=0.000, P<0.05) between our study and Nelson (2014), between our study and Zhao et al. (2011) (P=0.000, P<0.05) and between Zhao et al. (2011) and Nelson (2014) (P=0.000, P<0.05). For δ18O values, there is no significant difference (P=0.336, P>0.05) between our study and Nelson (2014).

4 Discussions

Our study in combination with two previous studies presents substantial isotopic variations in the same teeth, which is unexpected. Although Stacklyn et al. (2017) had mentioned that the discrepancy between Nelson (2014) and Zhao et al. (2011) could be caused by the differences in pretreatment. In our opinion, two main factors should be responsible for this phenomenon.

This could have resulted from the different methods to prepare the enamel bioapatite. It should be noted that the type, concentration and reacting time of chemicals used in the preparation procedure are of great difference between Nelson (2014) and Zhao et al. (2011). Nelson (2014) used 3% hydrogen peroxide for 15 min and 0.1 M acetic acid for 15 min while Zhao et al. (2011) used 5% sodium hypochlorite for 12 h and 6% acetic acid for 12 h.

Hydrogen peroxide and sodium hypochlorite are the most common chemicals in bioapatite pretreatment for removing organics in enamel (Snoeck and Pellegrini, 2015). However, both of them are suggestive of some problems. For example, NaOCl can adsorb exogenous carbonates from the external circumstances and change the contents of %CO2 in bioapatite which may not be totally eliminated in the following step of acid treatment and possibly affect the isotopic values measured (Crowley and Wheatley, 2014). In addition, utilization of NaOCl rather than H2O2 might reduce the yields of biogenic carbonate and isotopic results could be less reproducible (Gilg et al., 2004). On the other hand, H2O2, acidic, would cause the carbonate dissolution and change the inner structure of bioapatite possibly, which may trigger the isotopic changes as well (Snoeck and Pellegrini, 2015; Pellegrini and Snoeck, 2016). What’s more, H2O2 is supposed to be insufficient to remove organics even at 80°C (Snoeck and Pellegrini, 2015). In reality, the adoption of NaClO is more than H2O2 as it is suggested that most of the exogenous carbonate produced by NaClO can be removed in the addition of acetic acid afterwards and it is a more efficient chemical to remove organics (Snoeck and Pellegrini, 2015; Pellegrini and Snoeck, 2016).

Acetic acid is widely used to remove exogenous carbonate. If the bioapatite is exposed to more concentrated acids and for longer treatment times, the recrystallization could have occurred, which leads to lower δ13C and higher δ18O values (Kohn et al., 1997; Garvie-Lok et al., 2004). Further, the recent study claims that the long treatment time of acetic acid might affect the isotopic integrity (Skippington et al., 2019). Nevertheless, other study argued that those isotopic differences caused by different treatment times were slight (Yoder and Bartelink, 2010). In general, no consensus on the acid concentration and reacting time has been made yet.

Summarizing the above, the adoption of chemicals and determination of acid concentration and reacting time in different pretreatment approaches can influence the isotopic values somehow. Thus, the significant difference of δ13C values among Zhao et al. (2011), Nelson (2014) and our study could be likely caused by the above factor. The smaller difference of δ13C values is observed between our study and Zhao et al. (2011) than between our study and Nelson (2014), as the samples in our study are just the same as the tooth powder prepared in Zhao et al. (2011). On the other hand, it should be noted that the minor variations of δ18O values between Nelson (2014) and our study suggest that the preparation methods do not have important influence on the δ18O values in enamel bioapatite.

Another important factor, the inter-laboratory differences for isotopic measurements, cannot be ignored. Those can include the measuring conditions, isotopic standards, data calibration method and so on, which also result in considerable variability of isotope data (Roberts et al., 2018; Demény et al., 2019). For example, the δ18O values of enamel can be influenced by reaction conditions of generating CO2 such as temperature and phosphoric acid concentration (Demény et al., 2019). Recent study (Ma et al., 2019) found there existed relatively moderate variations of isotopic data of Asian elephant fauna during the Late Pleistocene between our lab and the lab at the University of Tubingen, Δ=0.42‰ for δ13C and Δ=0.06‰ for δ18O values respectively. Therefore, this possibility cannot be ruled out to interpret the isotopic differences among two previous studies and our study. Small variations of δ18O values in our lab and Tubingen lab (Ma et al. 2019) as well as in Nelson (2014) and our study might imply that oxygen isotope ratios are much less influenced than carbon isotope ratios in different labs. In contrast, recent study (Chesson et al., 2019) alleged that the oxygen isotope ratios changed significantly rather than carbon isotope ratios in a parallel measurement of the same samples in different labs. Obviously, the conditions for isotopic measurements need to be examined in the near future to understand the isotopic variations and calibrate the isotopic data.

All in all, our study finds considerably isotopic variations among two previous studies and our study, targeting the same teeth of Gigantopithecus fauna. This could be derived from two factors, pretreatment methods and labs for isotopic measurements. To be strict, the direct isotopic comparison among studies using different preparation approaches and labs is theoretically impossible, as the substantial fluctuations of isotopic data could have possibly led to mis-explanation. In reality, the reasonable isotopic range, i.e., the minimum meaningful differences (MMD), are supposed to be 1.2‰ and 3.1‰ in bone bioapatite and 0.6‰, 1.6‰ in enamel bioapatite of δ13C and δ18O values respectively (Pestle et al., 2014; Chesson et al., 2019). The isotopic differences observed here are roughly located within the above range, indicating that the isotopic uncertainty caused by the different methods of pretreatment and measurements might have had minor effects on isotopic interpretation.

Given the popularity of direct isotopic comparison and no consensus on pretreatment methods and/or measuring conditions in international fields, we recommend some measures should be taken in the future to avoid the uncertainty of comparing the isotopic data as much as possible. Firstly, more experiments need to be undertaken for better understanding the mechanism on the effects of preparation procedure on isotopic variations. Secondly, repeat measurements of enamel bioapatite in different labs can dramatically eliminate the inner-lab isotopic differences and calibrate the possible systematic errors if it is applicable when comparing the isotopic data previously produced elsewhere.

5 Conclusion

In conclusion, a comparison was conducted to evaluate the differences in the isotopic values of the enamel bioapatite from the same Gigantopithecus fauna pretreated by different pretreatment protocols and labs. The results show there are larger differences in the δ13C values than in the δ18O values among previous studies and our study. The two factors, pretreatment methods and lab measurements, could account for the above phenomenon mainly. However, the direct isotopic comparison among different studies seems still applicable, thanks to the minor isotopic variations observed here. We encourage that more similar studies should be undertaken to better understand the isotopic deviations caused by the above two factors.

Acknowledgement

This work was supported by the Strategic Priority Research Program of Chinese Academy of Sciences (XDB26000000) and National Natural Science Foundation of China (41773008).

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