Journal of Asian Earth Sciences 135 (2017) 70–79

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Journal of Asian Earth Sciences

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Multiple sulfur isotope records at the end- (Permian) at Chaotian, China: Implications for a role of bioturbation in the Phanerozoic sulfur cycle ⇑ Masafumi Saitoh a, , Yuichiro Ueno b,c, Fumihiro Matsu’ura b, Tetsuya Kawamura b, Yukio Isozaki d, Jianxin Yao e, Zhansheng Ji e, Naohiro Yoshida c,f a Research and Development (R&D) Center for Submarine Resources, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Natsushima-cho, Yokosuka 237-0061, Japan b Department of Earth and Planetary Sciences, Tokyo Institute of Technology, Meguro-ku, Tokyo 152-8551, Japan c Earth-Life Science Institute, Tokyo Institute of Technology, Meguro-ku, Tokyo 152-8551, Japan d Department of Earth Science and Astronomy, The University of Tokyo, Meguro-ku, Tokyo 153-8902, Japan e Geology Institute, Chinese Academy of Geological Science, Beijing 100037, China f Department of Chemical Science and Engineering, Tokyo Institute of Technology, Midori-ku, Yokohama 226-8503, Japan article info abstract

Article history: A recent study on quadruple sulfur isotopes (32S, 33S, 34S, and 36S) of sedimentary pyrite suggested that Received 28 May 2016 the end-Guadalupian extinction was caused by shoaling of the sulfidic deep-water. This scenario is based Received in revised form 9 December 2016 on the assumption that sulfur isotopic compositions of pyrite from hosting sediments were controlled by Accepted 9 December 2016 benthos activities, thus by the redox conditions of the sedimentary environments. Nonetheless, the rela- Available online 18 December 2016 tionship between the sulfur isotope records and redox conditions, reconstructed from litho- and bio- facies, are poorly known. In order to examine the effect of bioturbation in sediments, quadruple sulfur Keywords: isotopic compositions of sedimentary pyrite from the end-Guadalupian succession in Chaotian, South Guadalupian China, were analyzed. Black mudstones of deep-water facies immediately below the extinction horizon Extinction D33 ‰ Quadruple sulfur isotope records have consistently high S values of ca. +0.079 , clearly suggesting a sulfate reduction in the anoxic Bioturbation water column. Our new data are consistent with the emergence of a sulfidic deep-water mass prior to Sulfate supply into sediments the end-Guadalupian extinction; the upwelling of the toxic deep-water may have contributed to the Sulfide burial extinction. In contrast, shallow-marine bioclastic limestones with burrows deposited under oxic condi- tions have negative D33S values. This anomalous isotopic signal indicates the mixing of two distinct types of pyrite; one generated during the sulfate reduction in an open system and the other in a closed system. We interpret that bioturbation supplied sulfate in the sediments and promoted sulfate reduction and in- situ sulfide precipitation within the sediments. The negative D33S values of oxic sediments in Chaotian are inconsistent with the previous model and demonstrate that the sedimentary sulfur cycle associated with bioturbation was more complicated than previously thought. Our study also implies that, more gen- erally, the role of bioturbation in increasing seawater sulfate concentration in the Phanerozoic may have been overestimated in the previous studies, because bioturbation may have enhanced sulfide burial or sulfur output from the oceans. Ó 2016 Elsevier Ltd. All rights reserved.

1. Introduction Around the Guadalupian- (Late Permian) boundary (G- LB), several global-scale geologic phenomena occurred, such as The end-Paleozoic mass extinction was one of the largest biodi- the eruption of the Emeishan flood basalts in South China (Chung versity crises in the Phanerozoic (e.g., Erwin, 2006; Alroy, 2010) and Jahn, 1995; Zhou et al., 2002), the onset of prolonged deep- and had two phases: the biodiversity decline at the end- sea anoxia (Isozaki, 1997), a substantial global sea-level fall (Jin Guadalupian (ca. 260 Ma) and the abrupt extinction at the latest et al., 1994; Haq and Schutter, 2008; Kofukuda et al., 2014), the Permian (ca. 252 Ma) (Jin et al., 1994; Stanley and Yang, 1994). ‘Kamura’ cooling event (Isozaki et al., 2007, 2011), and authigenic carbonate precipitation (Grotzinger and Knoll, 1995; Saitoh et al., 2015). Many researchers have considered the Emeishan volcanism ⇑ Corresponding author at: 2-15 Natsushima-cho, Yokosuka 237-0061, Japan. as the leading candidate for the cause of the end-Guadalupian E-mail address: [email protected] (M. Saitoh). http://dx.doi.org/10.1016/j.jseaes.2016.12.009 1367-9120/Ó 2016 Elsevier Ltd. All rights reserved. M. Saitoh et al. / Journal of Asian Earth Sciences 135 (2017) 70–79 71 extinction (e.g., Wignall et al., 2009). However, the causal link cycle in the end-Guadalupian oceans at Chaotian, focusing on the between the global environmental changes and the extinction at redox conditions of the sedimentary environments and benthos the end-Guadalupian remains a topic of discussion (e.g., Clapham activity, and examines the main role of bioturbation in the oceanic et al., 2009; Bond et al., 2010; Jost et al., 2014). Recently, several sulfur cycle in the Phanerozoic. studies reported anoxic/sulfidic conditions in the oceans along the continental margins on a global scale at the end-Guadalupian (Schoepfer et al., 2012, 2013; Saitoh et al., 2013a, 2013b; Yan 2. Geological setting and stratigraphy et al., 2013; Zhang et al., 2015; Shi et al., 2016). The upwelling of the anoxic/sulfidic deep-waters may have contributed to the South China was located on the eastern side of Pangea at low end-Guadalupian biodiversity decline (Saitoh et al., 2014a). latitudes during the Permian (Fig. 1c; Scotese and Langford, Measurements of all four stable sulfur isotopes (32S, 33S, 34S, and 1995). On its extensive platform, shallow-marine carbonates and 36S) in geologic records are useful for understanding the evolution- terrigenous clastics with abundant fossils were thickly accumu- ary history of the ocean/atmosphere system (e.g., Farquhar et al., lated (Fig. 1d; Zhao et al., 1981; Jin et al., 1998). On a slope/basin 2000; Johnston, 2011). Coupled with photochemical experiments, setting in northern Sichuan along the northwestern edge of South this method has shed light on the characteristic sulfur cycle in China, carbonates and mudstones of relatively deep-water facies the Archean atmosphere (e.g., Ono et al., 2003; Ueno et al., 2008, were accumulated (Fig. 1d; Wang and Jin, 2000). The Chaotian sec- 2009, 2015). Moreover, the quadruple sulfur isotopic analysis of tion in northern Sichuan is located nearly 20 km north of the city of geologic records and products of microbial incubation experiments Guangyuan (32°370N, 105°510E; Fig. 1a; Isozaki et al., 2004, 2008; is useful for detecting the biogeochemical processes in the oceans Saitoh et al., 2013a, 2013b). At Chaotian, we mapped the eastern from the Proterozoic to the present (e.g., Farquhar et al., 2003; bank of the Jialingjiang River at a narrow gorge called Mingyuexia, Johnston et al., 2005; Aoyama et al., 2014). Shen et al. (2011) first where Middle Permian to lowermost Triassic carbonates are con- applied the analysis of quadruple sulfur isotopes to the end- tinuously exposed (Fig. 1b). Paleozoic mass extinction event. They analyzed carbonate rocks The Permo-Triassic rocks at Chaotian (>300 m thick in total) are across the Permian-Triassic boundary (P-TB) at the Meishan sec- composed of the Guadalupian Maokou Formation, Lopingian Wuji- tion, the Global Stratotype Section and Point (GSSP) for the P-TB, aping and Dalong formations, and lowermost Triassic Feixianguan in South China and suggested that the episodic shoaling of anoxic Formation, in ascending order (Fig. 3; Isozaki et al., 2008; Saitoh deep-water caused the latest Permian extinction. Recently, Zhang et al., 2013a, 2013b, 2014b). The Maokou Formation (>150 m thick) et al. (2015) analyzed the quadruple sulfur isotopic compositions consists mainly of massive dark gray bioclastic limestone with of carbonates across the G-LB at two sections in South China, diverse shallow-marine fossils such as calcareous algae, bra- including the Penglaitan section in Guangxi, the GSSP for the G- chiopods, crinoids, rugosa corals, and fusulines. The uppermost LB, and the EF section in west Texas, USA. Based on the results, part (11 m thick) of the formation is composed of thinly bedded Zhang et al. (2015) used the upwelling scenario proposed by black mudstone and chert with radiolarians and ammonoids. The Shen et al. (2011) to the end-Guadalupian case and suggested that Wujiaping Formation (70 m thick) is composed of massive dark the shoaling of sulfidic deep-waters contributed to the end- gray bioclastic limestone containing shallow-marine fossils such Guadalupian extinction. as fusulines, rugosa corals, and algae. The Dalong Formation The common and critical isotopic signal in Shen et al. (2011) (25 m thick) is dominated by bedded black siliceous mudstone 33 33 32 and Zhang et al. (2015) are negative D S (={( S/ S)sample/ with radiolarians and bedded limestone with ammonoids. The 33 32 34 32 34 32 0.515 ( S/ S)reference [( S/ S)sample/( S/ S)reference] }) values of Feixianguan Formation (>30 m thick) is composed mainly of thinly pyrites in the analyzed rocks. This anomalous evidence indicates bedded light gray micritic limestone, which contains few con- the mixing of 34S-enriched and 34S-depleted sulfur (Ono et al., odonts and ammonoids. 2006). Both Shen et al. (2011) and Zhang et al. (2015) interpreted In the present study, we focus particularly on the 60 m thick that the negative D33S values of pyrites, and thus the mixing of sul- Middle–Upper Permian rocks, which are composed of the three fur from two different sources, recorded the shutdown of bioturba- stratigraphic units in the following ascending order: (1) the early tion in the sediments caused by shoaling of toxic (anoxic/sulfidic) Capitanian (Late Guadalupian) Limestone Unit of the Maokou For- deep-waters. According to their model, negative D33S values would mation, (2) the middle(?)-late Capitanian Mudstone Unit of the only be recognized in anoxic sediments with no bioturbation. Maokou Formation, and (3) the lower part of the early Wuchiapin- However, they did not examine the correlation between the gian (Early Lopingian) Wujiaping Formation (Fig. 3; Isozaki et al., quadruple sulfur isotope records and the redox conditions of the 2008; Lai et al., 2008; Saitoh et al., 2013a, 2015). The Limestone sedimentary environments, which were reconstructed by litho- Unit of the Maokou Formation is composed of massive bioclastic and bio-facies characteristics, including ichnofabrics, of the ana- limestone with diverse shallow-marine fossils, such as algae, fusu- lyzed rocks. Thus, the shoaling scenario at the end-Guadalupian lines, and corals, deposited on a shallow euphotic shelf. The Lime- by Zhang et al. (2015) has not been fully validated. stone Unit was deposited under oxic conditions as evidenced by The roles of bioturbation in the oceanic geochemical cycles in the frequent bioturbation (Fig. 2). Burrows of 1–3 mm in diameter the Phanerozoic were recently emphasized (e.g., Boyle et al., are commonly observed in the limestones although no particular 2014; Tarhan et al., 2015). In particular, Canfield and Farquhar alignment of burrows is recognized. The burrows are mostly filled (2009) pointed out a role of bioturbation in the oceanic sulfur cycle with lime mud and finer bioclasts. Meniscate backfill structure is in the past. According to their model, bioturbation promotes sulfur observed in some burrows. Linings by lime mud are recognized recycling from the sediments to the oceans because the benthic in some burrows; in such cases, the central part of the burrow is fauna ‘‘dig out” sediments and supply oxygen deep into the sedi- filled with sparite cement (Fig. 2b). ments to promote the oxidation of once buried sulfide. Hence, bio- The overlying Mudstone Unit (11 m thick) of the Maokou For- turbation likely contributed to the increase in seawater sulfate mation is composed of thinly bedded black calcareous mudstone concentration throughout the Phanerozoic, but its role in the ocea- and black chert/siliceous mudstone with abundant radiolarians, nic sulfur cycle has not been evaluated in detail. conodonts, and ammonoids, and unique authigenic carbonate pre- The present study analyzed quadruple sulfur isotope records of cipitate beds (Saitoh et al., 2015). No trace fossil is observed in the marine carbonates of shelf/slope facies across the G-LB at Chaotian Mudstone Unit, and lamination parallel to the bedding is consis- in northern Sichuan, South China. This article discusses the sulfur tently developed in the black calcareous mudstone throughout 72 M. Saitoh et al. / Journal of Asian Earth Sciences 135 (2017) 70–79

Fig. 1. Locality and paleogeographic maps of the Chaotian section. (a) Locality map of Chaotian, (b) a distant view of the outcrop at Chaotian, (c) global paleogeographic map at the end-Guadalupian (modified from Scotese and Langford, 1995), (d) sedimentary facies distribution of South China in the Capitanian (Late Guadalupian) (modified from Wang and Jin, 2000). A star represents the location of Chaotian.

the unit (Fig. 2d). In addition to the absence of bioturbation, sub- mental sulfur, rinsed with distilled water and centrifuged. The stantially high total organic carbon (TOC) contents (up to 16%), residue was dried for >24 h at room temperature. The sulfide was abundant occurrence of small-sized pyrite framboids, and high extracted using a modified method from Hsieh and Shieh (1997). proportions of pyrite Fe to highly reactive Fe in the rocks indicate Less than 5 g of the dried residue and an alkaline Zn trap were that the Mudstone Unit was deposited on a relatively deep dispho- placed in a 500 ml glass bottle with two stopcocks. The bottle tic slope/basin, particularly under sulfidic conditions (Saitoh et al., was purged with nitrogen; then, the sample was reacted with 2013a, 2013b, 2014a). 20 ml of 5 M HCl and subsequently with a 20 ml chromium (II) The lower Wujiaping Formation (11.5 m thick) is composed solution for >48 h at room temperature (Canfield et al., 1986). mainly of shallow-marine bioclastic limestone with abundant Chromium (II)-reducible sulfur (CRS) was reduced to H2S and pre- algae deposited on a euphotic shelf. The lower Wujiaping Forma- cipitated as ZnS in a 20 ml alkaline Zn trap. In this extraction pro- tion was deposited under oxic conditions, as indicated by some cedure, acid volatile sulfur (AVS) was also reduced to H2S and bioturbation. Burrows of 1–2 mm in diameter, filled with fine bio- precipitated as ZnS, but our preliminary analysis showed that only clasts, are observed in the shallow-marine bioclastic limestones in a small amount of AVS was contained in the rock samples (data not the lower Wujiaping Formation. A 2 m thick Wangpo bed (tuffa- shown). Then, ZnS was converted to Ag2S by reaction with 0.1 M ceous mudstone; Deconinck et al., 2014) occurs at the base of the AgNO3. The resulting Ag2S was cleaned by repeated centrifugation Wujiaping limestone. On the basis of fossil ages (conodonts, fusu- using distilled water and dried at 70 °C for >12 h. Ag2S was reacted lines, radiolarians, and ammonoids), the end-Guadalupian extinc- with excess F2 at 300 °C in a nickel reaction tube overnight to pro- tion horizon at Chaotian is assigned to the top of the Mudstone duce SF6, which was purified using cryogenic techniques and gas Unit, whereas the biostratigraphically defined G-LB is placed at chromatography. The isotopic composition of SF6 was determined the base of the lower Wujiaping limestones (Isozaki et al., 2008; using a ThermoFinnigan MAT253 mass spectrometer with a dual Saitoh et al., 2013a). inlet system at the Tokyo Institute of Technology. The sulfur isotopic compositions are presented using delta 34 34 32 34 32 3. Analytical methods notation d S=(( S/ S)sample/( S/ S)standard 1) and capital x x 32 x 32 34 32 delta notation D S=[( S/ S)sample/( S/ S)standard (( S/ S)sample/ 34 32 0.515 34 33 36 Fresh rock samples were collected by field mapping and deep ( S/ S)reference) ] (x = 33, 36). The d S, D S, and D S values drilling to a depth of >150 m at Chaotian. For the sulfur isotope are reported in ‰ relative to the Vienna Canion Diabro Troilite analysis, powdered sample (0.5–30.0 g) was ultrasonically washed (V-CDT) standard. The analytical reproducibility of the d34S, D33S, and soaked in a 10% NaCl solution for 24 h, rinsed with distilled and D36S values, as determined by replicate analyses of the inter- water and centrifuged to remove the soluble sulfate. Then, the resi- national reference material IAEA-S1, is ±0.4‰, ±0.01‰, and due was washed and soaked in acetone for 24 h to dissolve the ele- ±0.1‰ (1r), respectively. M. Saitoh et al. / Journal of Asian Earth Sciences 135 (2017) 70–79 73

Fig. 2. Trace fossils at Chaotian. (a–c) Burrows in the Limestone Unit of the Maokou Formation, (d) well-laminated black calcareous mudstone in the Mudstone Unit. c was also shown in Saitoh et al. (2013a). Note a lime mud lining in a burrow in the lower part of b. (e–g) SEM images of pyrite framboids (e, g: backscattered electron image; (f) secondary electron image).

4. Results ues in the dark gray carbonate range from 41.0‰ to 25.0‰, with an average value of 35.6‰. The D33S values in the dark gray Table 1 lists all of the d34S, D33S, and D36S values of pyrites of carbonate range from +0.034‰ to +0.103‰, with an average value the analyzed rocks at Chaotian. The d34S values were reported by of +0.068‰. The D36S values in the dark gray carbonate range from Saitoh et al. (2014a). Fig. 3 shows the chemostratigraphic profiles 0.39‰ to +0.05‰, with an average value of 0.22‰. The overly- of the d34S, D33S, and D36S values across the G-LB. Fig. 4 shows a ing bioclastic limestones in the lower Wujiaping Formation are cross-plot of the d34S and D33S values. also characterized by scattered d34S values, relatively low D33S val- The d34S, D33S, and D36S values are systematically different ues, and relatively high D36S values. The d34S values in the lower according to the rock types. The shallow-marine bioclastic lime- Wujiaping Formation range from 38.9‰ to +7.3‰, with an aver- stones in the Limestone Unit of the Maokou Formation are charac- age value of 11.3‰. The D33S values in the lower Wujiaping For- terized by scattered d34S values, relatively low D33S values, and mation range from 0.105‰ to +0.056‰, with an average value of relatively high D36S values. The d34S values in the Limestone Unit 0.022‰. The D36S values in the lower Wujiaping Formation range range from 29.5‰ to +10.0‰, with an average value of from 0.46‰ to +0.72‰, with an average value of +0.14‰. 12.8‰. The D33S values in the Limestone Unit range from 0.055‰ to +0.026‰, with an average value of 0.017‰. The D36S values in the Limestone Unit range from 0.20‰ to 5. Discussion +0.64‰, with an average value of +0.16‰. In marked contrast, the black calcareous mudstone and dark gray carbonate in the 5.1. Sulfur mixing by bioturbation Mudstone Unit of the Maokou Formation (particularly the black mudstone) are characterized by consistently low d34S, high D33S, The present quadruple sulfur isotope records correlate remark- and low D36S values. The d34S values in the black calcareous mud- ably with the tripartite subdivision of lithostratigraphic units stone range from 41.5‰ to 34.0‰, with an average value of across the G-LB at Chaotian, and thus with the redox changes in 38.1‰. The D33S values in the black calcareous mudstone range the sedimentary environments (Figs. 3 and 4). One of the distinct from +0.057‰ to +0.100‰, with an average value of +0.079‰. characteristics in the present results are the consistently high The D36S values in the black calcareous mudstone range from D33S values in the Mudstone Unit of the Maokou Formation with 0.49‰ to 0.07‰, with an average value of 0.28‰. The d34S val- respect to the other units. In this Mudstone Unit, the black calcare- 74 M. Saitoh et al. / Journal of Asian Earth Sciences 135 (2017) 70–79

Table 1 Quadruple sulfur isotopic compositions of the analyzed rocks at Chaotian. d34S values were reported in Saitoh et al. (2014a).

Formation/unit Sample ID Lithology Thickness (m) d34S(‰) D33S(‰) D36S(‰) Lower Wujiaping Fm 99W017 Bioclastic limestone 55.6 7.2 0.010 0.06 Lower Wujiaping Fm 11W 8 Bioclastic limestone 54.1 7.3 0.011 0.46 Lower Wujiaping Fm 11W 7 Bioclastic limestone 52.7 8.7 0.017 0.11 Lower Wujiaping Fm 11W 6.5 Bioclastic limestone 50.6 20.3 0.018 0.29 Lower Wujiaping Fm 11W 6 Bioclastic limestone 49.5 10.0 0.038 0.62 Lower Wujiaping Fm 11W 5 Bioclastic limestone 48.4 1.9 0.019 0.18 Lower Wujiaping Fm 11W 4 Bioclastic limestone 47.1 5.9 0.042 0.34 Lower Wujiaping Fm 11W 3 Bioclastic limestone 46.5 5.0 0.022 0.04 Lower Wujiaping Fm 11W 2 Bioclastic limestone 45.1 1.0 0.013 0.19 Lower Wujiaping Fm 11W1.5 Bioclastic limestone 43.7 14.8 0.074 0.44 Lower Wujiaping Fm 11W 1 Bioclastic limestone 43.7 5.9 0.097 0.46 Lower Wujiaping Fm 99W 13 Bioclastic limestone 42.3 36.5 0.052 0.27 Lower Wujiaping Fm 99W6 Bioclastic limestone 41.4 20.8 0.037 0.18 Lower Wujiaping Fm 99W5 Bioclastic limestone 41.2 29.4 0.014 0.09 Lower Wujiaping Fm 99W 3 Bioclastic limestone 40.8 38.9 0.056 0.04 Lower Wujiaping Fm 99W2 Bioclastic limestone 40.7 14.4 0.105 0.72 Mudstone Unit of the Maokou Fm E 72 Black calcareous mudstone 35.7 34.0 0.082 0.33 Mudstone Unit of the Maokou Fm E 54 Dark gray carbonate 35.2 25.0 0.034 0.09 Mudstone Unit of the Maokou Fm E 48 Black calcareous mudstone 34.9 35.8 0.099 0.17 Mudstone Unit of the Maokou Fm E 31 Dark gray carbonate 34.4 33.4 0.060 0.27 Mudstone Unit of the Maokou Fm E 26 Black calcareous mudstone 34.3 41.5 0.100 0.49 Mudstone Unit of the Maokou Fm E 21 Black calcareous mudstone 34.1 40.3 0.088 0.32 Mudstone Unit of the Maokou Fm E 13 Black calcareous mudstone 34.0 36.6 0.086 0.47 Mudstone Unit of the Maokou Fm E 1 Dark gray carbonate 33.8 40.9 0.086 0.29 Mudstone Unit of the Maokou Fm D 106 Dark gray carbonate 33.1 35.6 0.063 0.26 Mudstone Unit of the Maokou Fm D 98 Dark gray carbonate 32.9 40.0 0.079 0.26 Mudstone Unit of the Maokou Fm D 85 Black calcareous mudstone 32.4 37.6 0.081 0.26 Mudstone Unit of the Maokou Fm D 71 Black calcareous mudstone 31.9 38.2 0.075 0.34 Mudstone Unit of the Maokou Fm D 60 Dark gray carbonate 31.6 36.3 0.067 0.05 Mudstone Unit of the Maokou Fm D 59 Black calcareous mudstone 31.5 41.0 0.072 0.33 Mudstone Unit of the Maokou Fm D 53 Dark gray carbonate 31.4 30.6 0.068 0.39 Mudstone Unit of the Maokou Fm D12 Black calcareous mudstone 29.8 39.7 0.065 0.32 Mudstone Unit of the Maokou Fm C 62 Black calcareous mudstone 28.8 38.2 0.060 0.09 Mudstone Unit of the Maokou Fm C 55 Black calcareous mudstone 28.4 36.3 0.057 0.21 Mudstone Unit of the Maokou Fm C 54 Dark gray carbonate 28.4 39.3 0.070 0.27 Mudstone Unit of the Maokou Fm C 43 Dark gray carbonate 28.1 38.8 0.059 0.05 Mudstone Unit of the Maokou Fm C 28 Dark gray carbonate 27.6 34.7 0.054 0.30 Mudstone Unit of the Maokou Fm C 10 Black calcareous mudstone 27.1 38.4 0.079 0.07 Mudstone Unit of the Maokou Fm B 16 Dark gray carbonate 26.5 36.9 0.103 0.33 Limestone Unit of the Maokou Fm 07MU 31 Bioclastic limestone 25.4 29.5 0.004 0.16 Limestone Unit of the Maokou Fm 07MU 29 Bioclastic limestone 24.9 4.4 0.018 0.20 Limestone Unit of the Maokou Fm 07MU 25 Bioclastic limestone 24.3 6.2 0.028 0.03 Limestone Unit of the Maokou Fm 07MU 22 Bioclastic limestone 23.4 4.3 0.055 0.31 Limestone Unit of the Maokou Fm 07MU 16 Bioclastic limestone 21.3 22.1 0.001 0.02 Limestone Unit of the Maokou Fm 07MU 12 Bioclastic limestone 20.1 8.2 0.035 0.28 Limestone Unit of the Maokou Fm 07MU 8 Bioclastic limestone 18.9 19.6 0.017 0.18 Limestone Unit of the Maokou Fm 07MU 4 Bioclastic limestone 17.6 21.3 0.006 0.42 Limestone Unit of the Maokou Fm 07MU2 Bioclastic limestone 16.2 4.0 0.031 0.13 Limestone Unit of the Maokou Fm 07MU1 Bioclastic limestone 15.8 20.0 0.005 0.04 Limestone Unit of the Maokou Fm 03Mao 17 Bioclastic limestone 13.9 24.6 0.026 0.15 Limestone Unit of the Maokou Fm 03Mao16 Bioclastic limestone 12.5 25.5 0.013 0.02 Limestone Unit of the Maokou Fm 03Mao 15 Bioclastic limestone 11.0 23.2 0.002 0.00 Limestone Unit of the Maokou Fm 03Mao14 Bioclastic limestone 9.9 15.0 0.009 0.03 Limestone Unit of the Maokou Fm 03Mao13 Bioclastic limestone 8.4 2.3 0.041 0.44 Limestone Unit of the Maokou Fm 03Mao12 Bioclastic limestone 7.2 10.0 0.017 0.64 Limestone Unit of the Maokou Fm 03Mao11 Bioclastic limestone 4.8 8.4 0.043 0.18 Limestone Unit of the Maokou Fm 03Mao9 Bioclastic limestone 0.0 10.4 0.052 0.59

ous mudstones exhibit slightly higher D33S values than dark gray reduction in an open system with respect to sulfate, probably in muddy carbonates. The average D33S value of black calcareous the water column, which was enriched in sulfate (Figs. 3 and 4; mudstones in the unit (+0.079‰) is substantially higher than that Saitoh et al., 2014a). The Mudstone Unit was deposited on the rel- of seawater sulfate at the end-Guadalupian (+0.020‰), which Wu atively deep slope/basin under sulfidic conditions (Saitoh et al., et al. (2010) estimated from model calculations. Similarly, the 2013a, 2013b, 2014a). Most sulfides in the unit are pyrite fram- average d34S value of black calcareous mudstones in the Mudstone boids that were produced in the anoxic water column by water- Unit (38.1‰) is substantially lower than the estimated value of mass sulfate reduction and subsequently buried in the sediments. seawater sulfate (+16.2‰). Several incubation experiments (e.g., Hence, the high D33S values of pyrites in the Mudstone Unit pro- Johnston et al., 2007; Sim et al., 2011a, 2011b) have demonstrated vide additional evidence for the emergence of a sulfidic deep- that the D33S value of hydrogen sulfide produced by microbial sul- water mass immediately before the end-Guadalupian extinction. fate reduction under sulfate-enriched conditions is higher than the This evidence supports the idea that the upwelling of the toxic value of substrate sulfate. The consistently high D33S and low d34S deep-water may have contributed to the extinction (Saitoh et al., values relative to those of seawater sulfate indicate the sulfate 2013a, 2013b, 2014a). High D33S and low d34S values of dissolved M. Saitoh et al. / Journal of Asian Earth Sciences 135 (2017) 70–79 75

Fig. 3. Stratigraphy across the Guadalupian-Lopingian (Middle-Upper Permian) boundary at Chaotian. The sedimentary environments and d34S values were reported in Saitoh et al. (2013a) and Saitoh et al. (2014a), respectively. carb.: carbonate; ms.: mudstone; calc.: calcareous; sil.: siliceous; c.n.: chert nodule; M.: Mudstone; Word.: Wordian; Wuchiap.: Wuchiapingian; Ch.: Changhsingian; Dal.: Dalong; Tr.: Triassic; In.: Induan; Gr.: Griesbachian; Fei.: Feixianguan; P-TB: Permian-Triassic boundary.

Fig. 4. Plot of d34S and D33S values at Chaotian. Open and filled stars represent the average black mudstone and the Permian seawater sulfate estimated by model calculations (Wu et al., 2010), respectively; a dashed red curve represents the mixing line of these two endmembers. A solid black curve shows isotopic values of accumulative sulfide produced during sulfate reduction in a closed system, assuming that the initial sulfate with isotopic compositions is comparable to the estimated Permian seawater sulfate, and the 34e and 33k values in sulfate reduction are 53.5‰ and 0.514 (red arrow), respectively. The number on the curve is a fraction of sulfate converted to sulfide. A black arrow represents the evolution of instantaneously produced hydrogen sulfide in the closed system. Black dashed curves show the mixing lines of accumulative sulfides produced in the closed sediments and sulfides produced in an open system with respect to sulfate. Fields where disproportionation is required and not required and open circles, triangles, and squares are from Zhang et al. (2015). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) hydrogen sulfide relative to those of sulfate are often observed in 34e and 33k values in the water-column sulfate reduction in the modern euxinic environments (e.g., Li et al., 2010; Zerkle et al., Mudstone Unit are 53.5‰ and 0.514 (Fig. 5), respectively, based 2010). Generally, sulfur isotope fractionations during microbial on the sulfur isotopic compositions of the average black mudstone 34 34 32 sulfate reduction can be described by e (=1000 [1 ( S/ S)sul- in the unit and seawater sulfate at the end-Guadalupian in Wu 34 32 33 33 32 33 32 fide/( S/ S)sulfate]) and k (=ln[( S/ S)sulfide/( S/ S)sulfate]/ln et al. (2010) (Figs. 4 and 5). 34 32 34 32 x 32 33 [( S/ S)sulfide/( S/ S)sulfate]) values, where ( S/ S)sulfide and In marked contrast, the D S values in the bioclastic limestones x 32 ( S/ S)sulfate are the sulfur isotope ratios of sulfide and sulfate, in the Limestone Unit of the Maokou Formation and the lower respectively (x = 33, 34) (e.g., Sim et al., 2011b). The estimated Wujiaping Formation are relatively scattered and largely less than 76 M. Saitoh et al. / Journal of Asian Earth Sciences 135 (2017) 70–79

record the above-mentioned mixing between the two distinct pyr- ites. The observed variation in d34S and D33S values probably reflects the degree of mixing rate of the two types of pyrites. Bio- turbation may also have supplied oxygen deep into the sediments and stimulated sulfide oxidation (e.g., Canfield and Farquhar, 2009), although sulfur isotope fractionation during sulfide oxida- tion was not significant (e.g., Zerkle et al., 2009, 2016; Johnston, 2011). In general, secular changes in sulfur isotopic composition of hydrogen sulfide produced via sulfate reduction and of the residual sulfate in a closed system follow the Rayleigh distillation model. When sulfate was partially reduced in the closed sediments, the isotopic compositions of accumulative sulfide would be on the upward-convex curve (black solid curve in Fig. 4), if we assume that the d34S and D33S values of the initial sulfate are 16.2‰ and 0.020‰ (filled star), respectively, and the 34e and 33k values in sul- Fig. 5. Plot of 34e and 33k values estimated at Chaotian (star) and previously fate reduction are 53.5‰ and 0.514 (red arrow), respectively. The reported in microbial incubation studies (Sim et al., 2011a, 2011b; Leavitt et al., 2013; Bradley et al., 2016). Uncertainties of the estimated values at Chaotian were present isotopic data at Chaotian are clearly off this curve. The pre- calculated by propagating errors, but they are smaller than the symbol. sent data also demonstrate no mixing between the partially accu- mulative sulfides in the closed system and the sulfides produced in an open system with respect to sulfate (Fig. 4). In the sediments at ‰ D33 0 (Figs. 3 and 4). These negative S values cannot be explained Chaotian, sulfate has been quickly and quantitatively reduced and solely by microbial sulfate reduction or sulfur disproportionation generally depleted, as discussed above. (Shen et al., 2011; Sim et al., 2015; Zhang et al., 2015). Instead, these anomalous isotopic signals suggest the mixing of sulfur with d34 substantially high and low S values (Ono et al., 2006). In Fig. 4, 5.2. Bioturbation and the sedimentary sulfur cycle in the Phanerozoic open and filled stars represent the averaged black mudstone at Chaotian and the estimated seawater sulfate at the end- The present pyrite-mixing model is inconsistent with the previ- Guadalupian, respectively. The dashed red curve represents the ously proposed models for the sedimentary sulfur cycle associated mixing line of sulfur pools comparable with isotopic composition with bioturbation at the end-Paleozoic. For example, Shen et al. to the compositions of the two endmembers. The present sulfur (2011) analyzed the sulfur isotopic compositions of carbonates isotopic data are largely aligned on the red mixing line, which sug- across the P-TB at Meishan in South China and found negative D33 gests that the negative S values of the bioclastic limestones can D33S values of pyrites at the time of the major extinction. They be explained by the mixing of two distinct pyrites with isotopic interpreted that the negative D33S values recorded the mixing of compositions of the endmembers. As discussed above, when two types of pyrite: one with substantially low d34S values pro- microbial sulfate reduction occurs in an open system with respect duced via sulfate reduction in an open system and the other with d34 D33 to sulfate, sulfides with substantially low S and high S values substantially high d34S values produced via quantitative sulfate are generated. In contrast, when sulfate reduction occurs in a reduction in a closed system. Shen et al. (2011) further interpreted closed system, such as in the sediments, and the sulfates are fully that the pyrite mixing likely recorded the shutdown of bioturba- d34 D33 reduced, the S and S values of the produced pyrites become tion because of the shoaling of anoxic deep-water that led the identical to those of the sulfate (Shen et al., 2011; Sim et al., 2015; extinction. According to their model, the within-sediment setting D33 Zhang et al., 2015). Thus, the negative S values of the bioclastic under oxic conditions was a fully open system because of the limestones at Chaotian can be attributed to the mixing of two pyr- enhanced bioturbation, where the pyrites with substantially low ites; one produced during sulfate reduction in an open system and d34S values generated. When the anoxic water shoaled along the the other produced during the quantitative sulfate reduction in a continental margin, bioturbation was shut down and the sulfate closed system. supply into the sediments was suppressed. As a result, the sedi- These bioclastic limestones were deposited on the shallow ments changed from an open system to a closed system, and pyr- euphotic shelf under oxic conditions with frequent burrows ites with high d34S values were produced during quantitative (Saitoh et al., 2013a, 2014a). We infer that the bioturbation sup- sulfate reduction. The negative D33S values were a result of the plied sulfate into the limestones and promoted the above- mixing of the pyrites generated in the former open system and mentioned pyrite mixing. Within-sediment setting usually formed the latter closed system in the sediments. The identical scenario d34 D33 a closed system, where pyrites with identical S and S values with a slight modification was shared by Zhang et al. (2015), to the seawater sulfate were produced via quantitative sulfate who reported the negative D33S values of pyrites around the G- reduction. The bioclastic limestones at Chaotian are mainly com- LB in several sections in China and the USA (Fig. 6). They inter- posed of dark gray to black limestone with TOC of largely 0.1– preted that pyrites with substantially low d34S values may also 0.4% (Saitoh et al., 2013a, 2014a). A sulfate reduction rate in the have been produced in the sulfidic water column and suggested sediments may have been higher than the rate of diffusive sulfate that the shoaling of sulfidic deep-waters contributed to the end- supply into the sediments because of the ample amount of organic Guadalupian extinction. matter in the sediments (Ohmoto, 1992; Ohmoto and Goldhaber, In contrast to the previous models, the present data at Chaotian 1997). However, bioturbation may have supplied sulfate into the indicate that the within-sediment settings under oxic conditions sediments and generated a local open system with respect to sul- are not always an open system with respect to sulfate, even if bio- fate in the sediments that was connected to the sulfate-enriched turbation is associated. The negative D33S values in the bioclastic water column through the burrows. We interpret that the sulfate limestones with common burrows at Chaotian are clearly inconsis- reduction in the local open system in the bioclastic limestones tent with the scenarios of Shen et al. (2011) and Zhang et al. (2015), d34 D33 has produced pyrites with substantially low S and high S because their model requires the shutdown of bioturbation to D33 values, and the negative S values of the bioclastic limestones make negative D33Svalues(Fig. 6). The present results demonstrate M. Saitoh et al. / Journal of Asian Earth Sciences 135 (2017) 70–79 77

Fig. 6. Schematic diagram of the shoaling of deep-water associated with the sedimentary sulfur cycle at the end-Guadalupian, proposed in Zhang et al. (2015) (a, c) and this study (b, d). In a and c, the star represents the estimated depositional site (shallow shelf) of sedimentary rocks at the sections in Zhang et al. (2015). Similarly, in b and d, a star represents the depositional site of the Limestone Unit and Mudstone Unit of the Maokou Formation (shallow shelf and deep slope/basin, respectively) at Chaotian. The direct shallow-marine records immediately before the extinction are lacking at Chaotian due to a local deepening of the sedimentary environment (d; Saitoh et al., 2013a).

Fig. 7. Schematic diagram of a role of bioturbation in the sedimentary sulfur cycle in Earth’s history.

that the sedimentary sulfur cycle associated with bioturbation is oceans, and decreases the seawater sulfate concentration. The bi- more complicated than previously suggested. lateral ‘‘dual” roles of bioturbation in the sedimentary sulfur cycle Canfield and Farquhar (2009) emphasized a significant role of suggest that the contribution of bioturbation to the increase in sea- bioturbation in the sulfur cycle in the Phanerozoic (Fig. 7). Accord- water sulfate concentration in the Phanerozoic may have been ing to their model, bioturbation supplies oxygen deep into the sed- overestimated. The correlation between the secular trends in the iments to promote the re-oxidation of buried sulfide, or the sulfur global patterns of bioturbation and in the seawater sulfate concen- recycling from the sediments to the oceans. Hence, bioturbation tration will reveal the role of bioturbation on the sulfate concentra- may have played an important role in increasing the seawater sul- tion in the Phanerozoic oceans. fate concentration in the Phanerozoic. On the contrary, the present results suggest a completely opposite role of bioturbation in the 6. Conclusions sedimentary sulfur cycle (Fig. 7). Bioturbation supplies sulfate, as well as oxygen, into the sediments and stimulates the sulfate In order to examine the sedimentary sulfur cycle associated reduction and in-situ sulfide precipitation in the sediments. This with bioturbation at the end-Guadalupian, quadruple sulfur iso- process enhances the sulfide burial, or sulfur output from the topic compositions of pyrites in the Guadalupian-Lopingian rocks 78 M. Saitoh et al. / Journal of Asian Earth Sciences 135 (2017) 70–79 were analyzed at Chaotian, Sichuan, China. The following new Erwin, D.H., 2006. 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