Minor Δ33S anomalies coincide with biotic turnover events during the Great Ordovician Biodiversification Event (GOBE) in South China

Global and Planetary Change 184 (2020) 103069

Contents lists available at ScienceDirect

Global and Planetary Change journal homepage: www.elsevier.com/locate/gloplacha

Research article

Minor Δ33S anomalies coincide with biotic turnover events during the Great Ordovician Biodiversification Event (GOBE) in South China Kefan Chen, Dongping Hu, Xiaolin Zhang, Hao Zhu, Lilin Sun, Menghan Li, Yanan Shen

T

⁎

School of Earth and Space Sciences, University of Science and Technology of China, Hefei 230026, China.

A R T I C LE I N FO

A B S T R A C T

Keywords: Multiple sulfur isotopes Anoxic water Faunal turnover Ordovician

In this study, we report multiple S-isotopic data (δ34S and Δ33S) of sedimentary pyrite in Early to Late Ordovician sections from South China. The results reveal two distinct groups of negative Δ33S anomalies during the Dapingian and Sandbian to Early Katian stages, which coincide with two faunal turnover events. The negative Δ33S values reflect the mixing of sulfides with strongly negative δ34S and positive Δ33S, and sulfide with strongly positive δ34S and positive Δ33S. This mixing scenario may have resulted from the impinging of deep anoxic waters onto the continental shelves possibly facilitated by sea-level rise. The temporal co-occurrence of negative Δ33S anomalies with intervals of faunal turnover in brachiopod assemblages of South China suggests that the encroachment of anoxic waters may have driven the diversity crises. Our results provide evidence for a dynamic mechanism linking the recurrent upwelling of deep anoxic waters and faunal turnovers during the Early to Late Ordovician.

1. Introduction The Ordovician (~485–444 Ma) was a critical period in Earth history, characterized by significant changes in the biosphere (Melchin et al., 2013; Servais and Harper, 2018). These changes include a large and sustained diversification of marine organisms, known as the Great Ordovician Biodiversification Event (GOBE), during which the genuslevel diversity quadrupled and the utilization of ecospace increased (Sepkoski, 1995). In addition, the paleoecological context of the biotas changed dramatically with the development of the Paleozoic Evolutionary Fauna which expanded into the new niche space and progressively replaced the Cambrian Evolutionary Fauna in the marine ecosystem (Webby et al., 2004; Harper, 2006), laying the foundation for modern biodiversity levels (Webby et al., 2004; Harper, 2006; Servais et al., 2009, 2010; Servais and Harper, 2018; Edwards, 2019). The GOBE was characterized by the episodic diversification of the benthic community during almost the entire Ordovician (at least 30 Myr), with three major pulses of diversity occurring during the TremadocianFloian, Darriwilian, and Katian stages (Harper, 2006; Zhan and Jin, 2008; Servais et al., 2010; Zhan et al., 2012; Harper et al., 2015). Between the pulses of diversity, the Ordovician radiation was marked by faunal turnover events based on the brachiopod data, within the Middle Darriwilian, the Late Katian, and the Late Hirnantian (Zhan and Jin, 2008; Harper et al., 2015). In South China, the Ordovician evolutionary

⁎

patterns largely tracked the global trend, showing three pules of diversity during the Early Floian, Middle-Late Darriwilian, and the Late Katian, which were interrupted by two faunal turnovers within the Dapingian and Sandbian to Early Katian stages (Zhan and Jin, 2007a, 2008). Several hypotheses have been proposed to explain the GOBE. It has been proposed that the GOBE may have been related to interrelated changes in biotic, climatic, and environmental systems, including widespread sea-level high stands of epicontinental seas (Harper, 2006), continental divergence (Barnes et al., 1996; Servais et al., 2009), a major increase in the global level of orogenic activity (Miller and Mao, 1995), nutrient availability (Cárdenas and Harries, 2010), global cooling (Trotter et al., 2008; Zhang et al., 2010a; Rasmussen et al., 2016), asteroid impacts (Schmitz et al., 2008), and rising atmospheric pO2 (Edwards et al., 2017; Edwards, 2019). Given the importance of reconstructing marine redox conditions which is essential for exploring the relationship between climatic change and biogeochemical cycles, the cause and consequence of biodiversity and mass extinctions, and the evolution of atmospheric compositions, an increasing amount of geochemical data have also been accumulated to constrain the marine redox conditions and their possible link to the biotic events (Zhang et al., 2009, 2011; Thompson and Kah, 2012; Marenco et al., 2013; Melchin et al., 2013; Kah et al., 2016; D'Arcy et al., 2017; Henderson et al., 2019). However, despite these many hypotheses, there is a lack of

Corresponding author. E-mail address: [email protected] (Y. Shen).

https://doi.org/10.1016/j.gloplacha.2019.103069 Received 24 July 2019; Received in revised form 21 October 2019; Accepted 27 October 2019 Available online 31 October 2019 0921-8181/ © 2019 Elsevier B.V. All rights reserved.

Global and Planetary Change 184 (2020) 103069

K. Chen, et al.

succession in the Yichang area is extensively exposed around the Huangling Anticline, characterized by different sedimentary lithofacies (dominantly carbonate and shale) which preserved abundant fossils that can be used for biostratigraphic correlation. We collected samples from three closely-spaced sections, namely the Lianghekou, Dingjiawan, and Puxihe sections, which are all located within the Yichang area of South China (Fig. 1). The composite of these three sections provides a nearly complete Ordovician succession with a continuous sedimentary record (Figs. S1 to S3).

a consensus regarding the viability of any particular candidate among this diverse range of potential drivers of the GOBE. Recent advances in the high-precision measurement of minor Sisotopes of 33S and 36S, and the identification of small but measurable Δ33S variations, have enabled the use of multiple sulfur isotopes to more accurately trace biogeochemical sulfur cycles (Farquhar et al., 2003, 2007; Ono et al., 2006, 2007; Johnston, 2011; Wing and Halevy, 2014; Tostevin et al., 2014). Diagnostic isotopic fractionation of minor isotopes permits the identification of sulfur metabolic processes, including sulfate reduction, sulfur re-oxidation, and disproportionation (Farquhar et al., 2003, 2007; Johnston et al., 2005a, 2005b, 2007, 2008; Zerkle et al., 2010; Sim et al., 2011a, 2011b; Pellerin et al., 2015a, 2015b), even when the 34S fractionations are similar. Therefore, when coupled with δ34S, the minor sulfur isotopes can potentially provide new insights into metabolic pathways and the sulfur cycle, enabling the reconstruction of marine redox variations and the improved discrimination between paleo-environments (Scheiderich et al., 2010; Shen et al., 2011; Sim et al., 2015; Zhang et al., 2015, 2017; Siedenberg et al., 2016; Luo et al., 2018). In this study, we report multiple S-isotopic record (δ34S and Δ33S) of sedimentary pyrite from three composite sections from the Yichang area of South China (Fig. 1), spanning the Early to Late Ordovician. The three study sections provide continuous Early to Late Ordovician sedimentary records with excellent biochronological control (e.g., Zeng et al., 1983; Wang et al., 2005; Zhan and Jin, 2007b; Wu et al., 2010), enabling an examination of the dynamic nature of marine redox changes and their links to faunal turnover events identified within the GOBE in South China.

2.1. Lianghekou section The Lianghekou section (30°51.81′ N; 111°21.682′ E) spans the Early Ordovician and is mainly composed of limestone and shaly limestone (Fig. S1). The section comprises, in ascending order, the Fenhsiang and Hunghuayuan formations. The Fenghsiang Fm. includes two members: the lower member is 10 m thick, mainly composed of thick- to massive-bedded bioclastic to oolitic limestone intercalated with minor yellow-green shale; the 7.5-m-thick upper member consists primarily of yellow-green calcareous shale intercalated with massive cross-bedded bioclastic limestone (Fig. S1). The lower member of the Fenghsiang Fm. yields rare macrofossils with representatives of brachiopods such as Tritoechia, which indicates a lower-intertidal environment (Boucot, 1975). The upper member contains more macrofossils with abundant graptolites, trilobites, and brachiopods, which may indicate a generally high-energy depositional environment (Zeng et al., 1983; Zhan and Jin, 2007b). In addition, a conodont biozone of Paltodus delitifer has been identified throughout the Fenghsiang Fm. (Zeng et al., 1983), which can be correlated with the upper part of the Rossodus manitouensis zone in Argentina, suggesting that the Fenghsiang Fm. is of Tremadocian age (Buggisch et al., 2003). The Hunghuayuan Fm. is typified by dark grey, thick- to massivebedded bioclastic limestone with occasional laminations. Bioclastic grains yield brachiopods, crinoids, and trilobites, and most impressively, cup-shaped, sponge-like organisms (e.g., Archaeocyphia and Calathium), indicating a tropical, shallow-water depositional environment (Zeng et al., 1983; Zhan and Jin, 2007b). Based mainly on the conodont assemblages represented by Oepikodus communis, the Hunghuayuan Fm. is of the latest Tremadocian-earliest Floian age (Zhang et al., 2010b). Unfortunately, the uppermost unit of this formation is located on steep cliffs which were inaccessible, and therefore we only

2. Geological setting and stratigraphy In South China, numerous complete, continuous, and richly fossiliferous Ordovician sequences are preserved (Chen et al., 2004a, 2004b). During the last several decades, stratigraphical and paleontological investigations of the Ordovician sections have been conducted (e.g., Chen et al., 2004a, 2004b; Zhan and Jin, 2007b, 2008; Munnecke et al., 2011). Notably, three Global Stratotype Sections and Points (GSSPs) were established in South China for the bases of the Dapingian, Darriwilian, and Hirnantian stages (Mitchell et al., 1997; Wang et al., 2005; Chen et al., 2006). In particular, an outstanding Ordovician stratigraphic sequence is preserved in the Yichang area. The Ordovician 105 0

110 0

115 0

120 0

N

a hu

nx

Xichang

Yangtze

Yichang 1 2

Sh

3

Changsha

Slo Guiyang

nzh

J

g ian

na

g an

ha

i

Wuhan

Platform Chongqing

ong

Nanjing

i

Chengdu

Dia

100km

30 0

C

30 0 0

25

Han

nan

Nanchang

pe

n

Oldland 25 0

China

Yangtze Platform

Kuming

Jiangnan Slope 105 0

110 0

115 0

120 0

Fig. 1. Location and paleogeography map for the three studied sections: 1-Lianghekou section (30°51.81′ N; 111°21.682′ E), 2-Dingjiawan section (30°52.180′ N; 111°22.624′ E), 3-Puxihe Section (30°55.634′ N; 111°25.712′ E). 2

Global and Planetary Change 184 (2020) 103069

K. Chen, et al.

secondary diagenetic veins. All fresh rock chips were then pulverized into powders less than 200 mesh size using an automated agate mortar device.

sampled the lower unit with a thickness of 11.5 m (Fig. S1). 2.2. Dingjiawan section

3.2. Multiple S-isotopic analyses

The Dingjiawan section (30°52.180′ N; 111°22.624′ E) is well exposed and consists mainly of the Dawan Fm. (Fig. S2). The Dawan Fm. can be divided into three members. The lower member is ~13.5-mthick, consisting of massive-bedded limestone and thin- to mediumbedded nodular limestone interbedded by mudstone (Fig. S2). The middle member contains a 9 m interval, characterized by purple medium- to thick-bedded limestone with minor interbeds of nodular limestone. The 12.5-m-thick upper member is characterized by laminated argillaceous shale, intercalated with lenticular limestone. Biostratigraphically, the Dawan Fm. yields abundant macrofossils, such as brachiopods, graptolites, and trilobites (Zeng et al., 1983; Wang et al., 2005). Based on the brachiopod-dominated association, this formation has been interpreted to experience a transgression event (Zhan et al., 2007). Conodonts are widespread throughout most of the formation and four biozones are well-established in ascending order: the Oepikodus evae biozone, the Baltoniodus triangularis biozone, the Baltoniodus navis biozone, and the Baltoniodus norrlandicus biozone (Fig. S2) (Zeng et al., 1983; Wang et al., 2005).

For pyrite extraction, powdered ~20–40 g samples were treated with a reduced chromium chloride/HCl solution by gently heating at 80 °C for ~2 h. The resulting hydrogen sulfide (H2S) was driven by a flow of nitrogen gas through a water-cooled condenser and then quantitatively trapped as silver sulfide (Ag2S) in 5% silver nitrate (AgNO3) solution (Canfield et al., 1986). The resulting Ag2S was filtered, washed to neutral with Milli-Q water, and oven-dried at 50 °C for ~48 h. The multiple S-isotopic analyses were performed in the Biogeochemistry Laboratory of the University of Science and Technology of China following the same procedure of Zhang et al. (2017) and Lin et al. (2018). Dried ~3 mg Ag2S samples were loaded in a nickel reaction vessel and reacted with ~10× excess fluorine gas (F2) at ~250 °C overnight to produce SF6. The resulting SF6 was first purified using two-stage liquid‑nitrogen-cooled traps at −190 °C and − 110 °C to remove the residual F2 and condensable contaminants, respectively. The SF6 was then transferred to the injection loop of a gas chromatograph (GC) for further purification. S-isotopic measurements of purified SF6 were made using a Thermo Scientific MAT 253 dual-inlet gas source mass spectrometer where the ion beams at m/z = 127, 128, 129, and 131 were detected simultaneously. Multiple S-isotope compositions are reported using the delta notation δ34S = [(34S/32S)sample/ (34S/32S)reference − 1] × 1000 and the capital delta notation Δ33S = δ33S-[(1 + δ34S/1000)0.515–1] × 1000. The analytical reproducibility for δ34S, Δ33S, and Δ36S is better than ± 0.2‰, ± 0.01‰, and ± 0.2‰, respectively, as determined by replicate analyses of IAEA S1.

2.3. Puxihe section The Puxihe section (30°55.634′ N; 111°25.712′ E) spans the Darriwilian to early Katian stages and consists of the Kuniutan, Miaopo, and Pagoda formations in ascending order (Fig. S3). The Kuniutan Fm. is ~3-m-thick in this section and is typified by medium- to thick-bedded argillaceous limestone with minor interbeds of calcareous and nodular mudstone, yielding abundant cephalopods and trilobites (Zeng et al., 1983; Chen et al., 1995). Although a deep water sedimentary environment through this formation is widely assumed, the appearance of more bioturbation and bioclastic limestone indicates a shallowing trend in the upper part (Chen, 1988). Two conodont biozones of Yangtzeplacognatus crassus and Dzikodus tablepointensis have been recognized, indicating a Darriwilian age for the Kuniutan Fm. (Zeng et al., 1983; Wu et al., 2010). The Miaopo Fm. is a ~3-m-thick interval characterized by black shale with limestone intercalations (Fig. S3), mainly yielding graptolites, trilobites, brachiopods, and ostracods (Zeng et al., 1983). The occurrence of the black shale with abundant graptolites likely indicates a deep-water sedimentary environment (Zhan and Jin, 2007b). In addition, based on conodonts, the Pycodus serra biozone has been recognized in the Miaopo Fm., indicating an early Sandbian age (Zeng et al., 1983). The Pagoda Fm. is early Katian in age and is represented here by a ~14.2-m-thick unit composed of medium- to thick-bedded nodular limestone with interbedded calcareous shale. The Pagoda Fm. contains a relatively diverse fauna of brachiopods, trilobites, and other macrofossils, among which cephalopods are the most abundant (Bergström et al., 2009). In particular, the appearance of the small-shelled brachiopods belonging to the deep-water Foliomena fauna may indicate a deep-water depositional environment (Zhan and Jin, 2005). Based on conodonts, two biozones of Hamarodus europaeus and Protopanderodus insculptus have been recognized in ascending order (Zeng et al., 1983).

4. Results The multiple S-isotopic data for the sedimentary pyrite of the Early to Late Ordovician strata from South China are illustrated in Fig. 2 and listed in Table 1. The results exhibit distinctive stratigraphic δ34S-Δ33S patterns through the study successions, indicating changes of the sulfur cycle in the Early to Late Ordovician ocean. During the Early Ordovician (Tremadocian-Floian stage), δ34S ranges from −11.83‰ to +11.63‰, with positive Δ33S values ranging from +0.027‰ and + 0.148‰ (Fig. 2). δ34S then increases markedly from −7.33‰ to prominent positive values with a maximum of +23.21‰ during the Dapingian stage (Fig. 2), coinciding with the first faunal turnover event in South China with brachiopod generic diversity decreased from 46 to 32 (Zhan and Jin, 2008) (Fig. 3). Δ33S in this interval has distinct negative values, ranging from −0.075‰ to −0.017‰ (Fig. 2). Stratigraphically higher within the section, δ34S in the Darriwilian stage ranges from −12.55‰ to +0.93‰, with positive Δ33S values ranging between +0.017‰ and + 0.049‰ (Fig. 2), similar to those of the Tremadocian-Floian stage (Fig. 3). Higher in the section, δ34S in the Sandbian-early Katian stage has pronounced positive values, ranging from +6.87‰ to +22.73‰, with negative Δ33S values ranging from −0.039‰ to −0.015‰ (Fig. 2), similar to those of the Dapingian stage.

3. Materials and methods 5. Discussion 3.1. Sampling and preparation 5.1. Interpretation of δ34S and Δ33S A total of 30 bulk rock samples spanning the Early to Late Ordovician stratigraphic interval were collected from the Puxihe, Dingjiawan, and Lianghekou sections. The rock samples were washed to remove surface contaminants and then cut into small pieces to carefully remove the weathered surface, visually altered materials, and any

In order to explore the implications of multiple S-isotopes for oceanic redox, a well-established sulfur-cycle box model, incorporating microbial sulfate reduction, sulfide oxidation, sulfur disproportionation, and sulfur mixing (Brunner and Bernasconi, 2005; Farquhar et al., 3

Global and Planetary Change 184 (2020) 103069

Lithology

Conodont Zone

Formation

Stage

δ 3 4 S(‰)

Δ 3 3 S(‰)

-15

-5

5

15

25

-0.10

-0.05

0

0.05

0.10

0.15

-15

-5

5

15

25

-0.10

-0.05

0

0.05

0.10

0.15

Pagoda

H.europaeus

P. i. Katian

Late Ordovician

Series

K. Chen, et al.

Miao.

P. s.

4530f07

San. 4584f09

Kuniutan

Darriwilian

D. t. Y. c. L. v. L. a.

Baltoniodus norrlandicus B. navis

Dawan

Dapingian

Middle Ordovician

4673f11

B. t. Oepikodus evae Oepikodus communis

Hunghua -yuan

Floian

Paltodus Delitifer

Fenhsiang

477 7f14

Tremadocian

Early Ordovician

4700f14

Lianghekou section

Dingjiawan section

Puxihe section Pagoda Fm.

Hunghuayuan Fm. Dawan Fm.

Miaopo Fm. Kuniutan Fm.

Fenhsiang Fm.

Fig. 2. Multiple S-isotopic data for the Early to Late Ordovician sediments from South China. Abbreviations: San.-Sandbian; Miao.-Miaopo; P. i.-Protopanderodus insculptus; H. europaeus-Hamarodus europaeus; P. s.-Pycodus serra; D. t.-Dzikodus tablepointensis; Y. c.-Yangtzeplacognatus crassus; L. v.-Lenodus variabilis; L. a.-Lenodus antivariabilis; B. navis-Baltoniodus navis; B. t.-Baltoniodus triangularis.

model can be found in Farquhar et al. (2007) and Zhang et al. (2015, 2017). The diagnostic ranges of multiple S-isotopic compositions of sulfide produced by microbial sulfur metabolism, including sulfate reduction, sulfide oxidation, and sulfur disproportionation, are illustrated in Fig. 4.

2007; Shen et al., 2011; Zhang et al., 2015, 2017), was used to constrain the marine sulfur cycles during the Ordovician. S-isotopic compositions for contemporaneous seawater sulfate with δ34S = 35.9‰ and Δ33S = 0.001‰ (Wu et al., 2014) were used as input to the model, and the output is illustrated in Fig. 4. The details of calculations for the

4

Global and Planetary Change 184 (2020) 103069

K. Chen, et al.

Table 1 Multiple S-isotopic data for the Ordovician sedimentary rocks from South China. Sample

Depth(m)

Stage

Formation

δ33Spy(‰)

δ34Spy(‰)

δ36Spy(‰)

Δ33Spy(‰)

Δ36Spy(‰)

Puxihe section PXH-8 PXH-7 PXH-6 PXH-5 PXH-4 PXH-3 PXH-2 PXH-1

19.4 15.6 13.6 11.6 4 2 1 0

Early katian Early katian Early katian Early katian Sandbian Darriwilian Darriwilian Darriwilian

Pagoda Fm. Pagoda Fm. Pagoda Fm. Pagoda Fm. Miaopo Fm. Kuniutan Fm. Kuniutan Fm. Kuniutan Fm.

9.95 10.07 10.12 11.65 3.51 0.50 −6.43 −2.80

19.49 19.68 19.77 22.73 6.87 0.93 −12.55 −5.48

36.39 37.41 37.77 43.63 13.15 1.43 −23.78 −10.70

−0.039 −0.015 −0.019 0.011 −0.024 0.017 0.049 0.027

−0.962 −0.317 −0.131 0.009 0.053 −0.336 −0.070 −0.319

Dingjiawan section DJW-14 35 DJW-13 32 DJW-12 31 DJW-11 30 DJW-10 27 DJW-9 25.5 DJW-8 24.5 DJW-7 23.5 DJW-6 22.5 DJW-5 21.5 DJW-4 6.5 DJW-3 3.5 1 DJW-2 DJW-1 0

Dapingian Dapingian Dapingian Dapingian Dapingian Dapingian Dapingian Dapingian Dapingian Dapingian Floian Floian Floian Floian

Dawan Dawan Dawan Dawan Dawan Dawan Dawan Dawan Dawan Dawan Dawan Dawan Dawan Dawan

Fm. Fm. Fm. Fm. Fm. Fm. Fm. Fm. Fm. Fm. Fm. Fm. Fm. Fm.

9.62 8.57 5.25 0.15 5.79 6.10 2.28 11.86 11.26 −3.80 −4.15 3.09 2.91 −5.42

18.80 16.80 10.33 0.43 11.41 11.95 4.47 23.21 22.01 −7.33 −8.33 5.89 5.60 −10.60

35.78 31.99 20.11 1.11 21.89 22.73 8.62 44.17 41.91 −13.75 −16.54 10.65 10.23 −20.42

−0.020 −0.052 −0.055 −0.075 −0.071 −0.033 −0.017 −0.031 −0.021 −0.017 0.148 0.061 0.033 0.055

−0.239 −0.180 0.397 0.290 0.106 −0.087 0.112 −0.395 −0.332 0.122 −0.785 −0.580 −0.434 −0.366

Lianghekou section LHK-8 29 LHK-7 23 LHK-6 19 LHK-5 16 LHK-4 14 LHK-3 8 LHK-2 4 LHK-1 0

Floian Floian Floian Tremadocian Tremadocian Tremadocian Tremadocian Tremadocian

Hunghuayuan Fm. Hunghuayuan Fm. Hunghuayuan Fm. Fenhsiang Fm. Fenhsiang Fm. Fenhsiang Fm. Fenhsiang Fm. Fenhsiang Fm.

−2.66 −4.20 −6.06 −3.29 2.12 2.56 3.75 6.01

−5.24 −8.24 −11.83 −6.53 4.04 4.92 7.24 11.63

−10.08 −15.86 −22.55 −12.86 7.31 8.00 13.34 21.96

0.041 0.053 0.045 0.079 0.041 0.029 0.027 0.031

−0.144 −0.275 −0.204 −0.497 −0.383 −1.361 −0.455 −0.257

The field of microbial sulfate reduction is bounded by the solid line where disproportionation could occur but is not required. This model illustrates that the expression of S-isotope fractionation by microbial metabolisms is largely determined by the fraction of sulfate that is reduced during different steps within the cells of bacteria, and the variation in fractionation is a result of different proportions of sulfur intermediates reoxidized to sulfate and the fractionation factors of metabolic pathways (Farquhar et al., 2007). The dotted line represents the limit for 100% of sulfide resulting from sulfate reduction is reoxidized and disproportionated (Fig. 4). Notably, the sulfur-cycle model takes all of the metabolic processes into account which involves the transfer of sulfur between reservoirs, including external and internal sulfate, APS (adenosine-5′-phosphosulfate), sulfite, trithionate, thiosulfate, and internal and external sulfide pools (Farquhar et al., 2007; Zhang et al., 2017). Based on the locations of the multiple S-isotopic values in quadrants I, II, III, and IV in Fig. 4, changes in paleoredox conditions of seawater may be inferred. The multiple S-isotopic signature in quadrant I, with positive δ34S and positive Δ33S, may indicate microbial sulfate reduction in an open system, or the quantitative reduction of sulfate in a nearly closed system in which the supply of sulfate is limited (i.e., sulfate consumption > sulfate supply). As a result of Rayleigh distillation processes, the subsequent quantitative reduction of sulfate would produce sulfide with Sisotopic compositions approaching that of the contemporaneous seawater sulfate (e.g., Shen et al., 2011; Gomes and Hurtgen, 2013; Sim et al., 2015; Zhang et al., 2015). The values plotting within quadrant II, with negative δ34S and positive Δ33S, may be produced by microbial sulfate reduction processes, with or without disproportionation, in an open system relative to the sulfate supply (Farquhar et al., 2007; Shen et al., 2011; Zhang et al., 2015, 2017). The negative Δ33S values in quadrants III and IV, however, cannot be causally ascribed to multiple metabolic processes or to the

quantitative reduction of sulfate alone. Laboratory culture experiments have shown that sulfides produced by microbial sulfate reduction and sulfur disproportionation are characterized by more positive Δ33S values than the reactant sulfate or elemental sulfur, when the supply of the sulfate is unlimited (Johnston et al., 2005a, 2007; Farquhar et al., 2008; Sim et al., 2011a; Leavitt et al., 2014). Under sulfate-limited conditions, sulfide produced by the quantitative reduction of sulfate is characterized by positive Δ33S and positive δ34S, similar to that of the seawater sulfate (Shen et al., 2011; Sim et al., 2015; Zhang et al., 2017). Although it appears that the negative Δ33S values within the area enclosed by the dotted line could be produced when microbial sulfate reduction and sulfur disproportionation both occur, the model outputs may have resulted from specific boundary conditions (Zhang et al., 2017). The dotted boundary assumes that 100% of sulfide produced by sulfate reduction is reoxidized and disproportionated which may be unattainable in the natural environment (Fig. 4). In addition, few laboratory culture studies of sulfate reduction or sulfur disproportionation yield the negative Δ33S output. Rather, both the sulfate reduction and sulfur disproportionation processes in culture studies yield more positive Δ33S values relative to the reactant (Johnston et al., 2005a, 2007; Farquhar et al., 2008; Sim et al., 2011a; Leavitt et al., 2014). Recent studies have shown that sulfide with negative Δ33S values can be produced via the mixing of sulfide characterized by strongly negative δ34S and positive Δ33S, and sulfide with strongly positive δ34S and positive Δ33S (Shen et al., 2011; Sim et al., 2015; Zhang et al., 2015, 2017; Siedenberg et al., 2016; Luo et al., 2018). Accordingly, a two end-member mixing model is here used to explain the occurrence of distinctively negative Δ33S values in the Early to Late Ordovician strata from South China. In this scenario, we take one end-member to be pyrite with a multiple S-isotopic composition (i.e., δ34S = 35.9‰, Δ33S = 0.001‰) equivalent to that of the Early Ordovician seawater sulfate (Wu et al., 2014), and the other is pyrite with the most negative 5

Global and Planetary Change 184 (2020) 103069

K. Chen, et al.

Δ33S(‰)

Formation

Con. Zone

Stage

5

15

25

-0.10 -0.05

0

H.europaeus

Pagoda

Katian

-5

Number of brachiopod genera in South China

0.05 0.10 0.15

0

10

20

30

40

20

30

40

50

60

Sea level Change in South China

High

Low

Brachiopod turnover

D. t.

GOBE

Diversity pluse

Y. c. L. v. L. a. Baltoniodus norrlandicus

Kuniutan

Brachiopod turnover

B. navis

Darriwilian

San. Miao. P. s.

Dapingian

Middle Ordovician

-15

P. i.

Dawan

Late Ordovician

Series

34

δ S(‰)

Oepikodus Oepikodus communis evae Paltodus Delitifer

Floian

Hunghua -yuan Fenhsiang

Tremadocian

Early Ordovician

B. t.

Diversity pluse

-15

-5

5

15

25

-0.10 -0.05

0

0.05 0.10 0.15

0

10

50

60

Fig. 3. Multiple S-isotopic data, brachiopod diversity, and a sea-level curve, across the Early to Late Ordovician in South China (filled red circles refer to negative Δ33S values). The grey-shaded fields represent intervals of major pulses of diversity, while the blue-shaded fields represent intervals of brachiopod diversity turnover. The changes in brachiopod generic diversity are after Zhan and Jin (2008), the sea-level curve is modified from Su (2007). Abbreviation details as in Fig. 2. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) Fig. 4. Cross plot of δ34S and Δ33S for pyrite from the Early to Late Ordovician sedimentary rocks of South China. The solid and dotted black lines illustrate the ranges of S-isotopic compositions of pyrites inferred using a seawater model with sulfate reduction combined with disproportionation. The red nonlinear curve is the mixing line of two pyrite endmembers formed in open and closed systems with negative and positive δ34S values, respectively. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

δ34S values (δ34S = −17‰ with Δ33S = 0.003‰) measured from the study sections (Fig. 4). The resulting mixing line encloses all of the negative Δ33S values in the Early to Late Ordovician strata from South China (Fig. 4). The negative Δ33S values measured from Phanerozoic sedimentary rocks have been attributed to the mixing of two types of sulfide formed in different settings driven by impinging of anoxic waters (Shen et al.,

2011; Zhang et al., 2015, 2017). In this scenario, the rising of deep anoxic waters into shallow oxic environments would increase biological stress, potentially causing the extinction and dramatically reducing or even eliminating bioturbation (Shen et al., 2011; Zhang et al., 2015, 2017). The reduction of bioturbation would result in the inhibition of sulfate exchange with the overlying seawater and the subsequent formation of pyrite with S-isotopic compositions approaching that of the 6

Global and Planetary Change 184 (2020) 103069

K. Chen, et al.

6. Conclusion

contemporaneous seawater sulfate. The mixture of this pyrite and pyrite formed in a previous open system will produce a bulk pyrite composition with negative Δ33S values (Shen et al., 2011; Zhang et al., 2015, 2017). Therefore, the negative Δ33S values of sedimentary pyrite may be a diagnostic signal of dynamic changes in marine redox conditions and sedimentary sulfur cycles, linking the deep anoxic waters to mass extinction events (Shen et al., 2011; Zhang et al., 2015, 2017; Luo et al., 2018).

In this study, we have identified two groups of distinct negative Δ33S anomalies during the Dapingian and Sandbian to Early Katian stages which coincide with two faunal turnover events. Our multiple Sisotopic results provide new insights into the dynamic nature of marine redox variations, linking the recurrent impinging of anoxic waters to the biotic turnover events. The positive Δ33S, with negative or positive δ34S values, during the Tremadocian-Floian and Darriwillian, suggest normal marine conditions which may have provided the new ecospace for the diversification of marine organisms during the GOBE. We propose that further isotopic studies of different sedimentary facies and with well-established biostratigraphy can be carried out in other marine basins worldwide to test our hypothesis, and to improve our understanding of the linkage between marine redox changes and the evolution of early life. Supplementary data to this article can be found online at https:// doi.org/10.1016/j.gloplacha.2019.103069.

5.2. Episodic impinging of anoxic waters and the biotic turnover events Our multiple S-isotopic data exhibit a distinct stratigraphic pattern during the Early to Late Ordovician (Figs. 2 and 3). Specifically, the pyrite from the Tremadocian-Floian and the Darriwilian stages is characterized by positive Δ33S with lower negative δ34S, or slightly positive δ34S values, which coincides with two pulses of brachiopod diversification in South China (Fig. 3). The first pulse of diversity, during the Tremadocian-Floian stage, was dominated by the appearance and diversification of the Sinorthis Fauna in the central part of the Upper Yangtze Platform, during which the number of brachiopod genera increased from 8 to 46 (Zhan and Jin, 2008) (Fig. 3). The second pulse, in the Darriwilian stage, was represented by the development of the Saucrorthis Fauna with an increase in brachiopod generic diversity from 32 to 39 (Zhan and Jin, 2008) (Fig. 3). Correspondingly, our multiple S-isotopic data within these two intervals are located in quadrants II and I (Fig. 4), a field suggesting S-isotopic fractionation associated with typical sulfate reduction, probably with sulfur disproportionation in an open system, implying normal marine conditions which may have paved the way for the biodiversification. By contrast, pyrites from the Dapingian and Sandbian to Early Katian stage exhibit a distinct S-isotopic signature of negative Δ33S values located in quadrants III and IV (Fig. 4). We suggest that the negative Δ33S values may have resulted from the mixing of two distinct generations of pyrite, and may represent a dynamic change in marine redox conditions and sedimentary sulfur cycles driven by the impinging of deep anoxic waters onto shallow shelf settings (Shen et al., 2011; Zhang et al., 2015, 2017). The sedimentary sulfur cycle from an open system to a nearly closed system due to the cessation of bioturbation may have resulted in the positive δ34S values as we observed in the Dapingian and Sandbian to Early Katian stages (Figs. 2 and 3). The two pulses of distinctly negative Δ33S values, with positive δ34S values, in the Dapingian and Sandbian-early Katian stages coincide with the two faunal turnover events in South China during which the number of brachiopod genera decreased from 46 to 32 and 39 to 14, respectively (Zhan and Jin, 2008) (Fig. 3). The temporal relationship between the two suggests a causal link between the impinging of anoxic waters and biodiversity turnover. Our diagnostic multiple S-isotope data, therefore, provide evidence for the dynamic nature of oceanic redox conditions during the Early-middle Late Ordovician, with the episodic incursion of deep anoxic waters onto shallow shelves, and oscillations between anoxic and oxic conditions, which may have played a major role in the biotic turnover events in South China. Our interpretation is broadly consistent with recent geochemical evidence from many other marine basins that suggests that the Ordovician period may have been a time of recurring deep ocean anoxia and euxinia (Thompson and Kah, 2012; Marenco et al., 2013; Kah et al., 2016; D'Arcy et al., 2017; Henderson et al., 2019). More importantly, our multiple S-isotopic data provide new insight into the dynamics of marine redox variations and their causal link to the biotic turnover events during the GOBE. It appears that the impinging of deep anoxic waters is consistent with the sea-level rise during the Dapingian and Sandbian to Early Katian (Su, 2007) (Fig. 3). Thus we suggest that sealevel rise may have facilitated episodic impinging of deep anoxic water onto shelf environments.

Declaration of Competing Interest The authors declare that there is no conflict of interests. Acknowledgments This study was supported by National Natural Science Foundation of China (41520104007, 41721002, 41807314, 41890842, 41877318, 41673003), the 111 project, and the Key Research Program of Frontier Sciences, CAS (QYZDY-SSW-DQC031). We thank Huan Cui and Linda C. Kah for constructive comments that have greatly improved this paper. References Barnes, C.R., Fortey, R.A., Williams, S.H., 1996. The pattern of global bio-events during the Ordovician period. In: Global Events and Event Stratigraphy in the Phanerozoic. Springer, Berlin, pp. 139–172. Bergström, S.M., Chen, X., Schmitz, B., Young, S., Rong, J., Saltzman, M.R., 2009. First documentation of the Ordovician Guttenberg δ13C excursion (GICE) in Asia: chemostratigraphy of the Pagoda and Yanwashan formations in southeastern China. Geol. Mag. 146, 1–11. Boucot, A.J., 1975. Evolution and Extinction Rate Controls. In: Developments in Palaeontology and Stratigraphy. Elsevier, Amsterdam, New York 427 pp. Brunner, B., Bernasconi, S.M., 2005. A revised isotope fractionation model for dissimilatory sulfate reduction in sulfate reducing bacteria. Geochim. Cosmochim. Acta 69, 4759–4771. Buggisch, W., Keller, M., Lehnert, O., 2003. Carbon isotope record of Late Cambrian to Early Ordovician carbonates of the Argentine Precordillera. Palaeogeogr. Palaeoclimatol. Palaeoecol. 195, 357–373. Canfield, D.E., Raiswell, R., Westrich, J.T., Reaves, C.M., Berner, R.A., 1986. The use of chromium reduction in the analysis of reduced inorganic sulfur in sediments and shales. Chem. Geol. 54, 149–155. Cárdenas, A.L., Harries, P.J., 2010. Effect of nutrient availability on marine origination rates throughout the Phanerozoic eon. Nat. Geosci. 3, 430–434. Chen, J., 1988. Ordovician changes of sea level. New Mex. Bur. Min. Mineral Resour. 44, 387–404. Chen, X., Rong, J., Wang, X., Wang, Z., Zhang, Y., Zhan, R., 1995. Correlation of Ordovician Rocks of China: charts and explanatory notes. IUGS Publication 31 104 pp. Chen, X., Zhang, Y., Xu, H., Yu, G., Wang, L., Qi, Y., 2004a. The progressive study to the Ordovician Darriwilian GSSP section (Huangnitang, Changshan, Zhejiang, China). Pap. Collect. Stratigr. Palaeontol. 28, 29–39 (in Chinese with English abstract). Chen, X., Rong, J., Li, Y., Boucot, A.J., 2004b. Facies patterns and geography of the Yangtze region, South China, through the Ordovician and Silurian transition. Palaeogeogr. Palaeoclimatol. Palaeoecol. 204, 353–372. Chen, X., Rong, J., Fan, J., Zhan, R., Mitchell, C.E., Harper, D.A.T., Melchin, M.J., Peng, P., Finney, S.C., Wang, X., 2006. The Global Boundary Stratotype Section and Point (GSSP) for the base of the Hirnantian Stage (the uppermost of the Ordovician System). Episodes 29, 183–196. D'Arcy, J., Gilleaudeau, G.J., Peralta, S., Gaucher, C., Frei, R., 2017. Redox fluctuations in the Early Ordovician oceans: An insight from chromium stable isotopes. Chem. Geol. 448, 1–12. Edwards, C.T., 2019. Links between early Paleozoic oxygenation and the Great Ordovician Biodiversification Event (GOBE): A review. Palaeoworld 28, 37–50. Edwards, C.T., Saltzman, M.R., Royer, D.L., Fike, D.A., 2017. Oxygenation as a driver of the Great Ordovician Biodiversification Event. Nat. Geosci. 10, 925–929. Farquhar, J., Johnston, D.T., Wing, B.A., Habicht, K.S., Canfield, D.E., Airieau, S., Thiemens, M.H., 2003. Multiple sulphur isotopic interpretations of biosynthetic pathways: implications for biological signatures in the sulphur isotope record.

7

Global and Planetary Change 184 (2020) 103069

K. Chen, et al.

definition, concept and duration. Lethaia 51, 151–164. Servais, T., Harper, D.A.T., Munnecke, A., Owen, A.W., Sheehan, P.M., 2009. Understanding the Great Ordovician Biodiversification Event (GOBE): Influences of paleogeography, paleoclimate, or paleoecology? GSA Today 19, 4–10. Servais, T., Owen, A.W., Harper, D.A.T., Kröger, B., Munnecke, A., 2010. The Great Ordovician Biodiversification Event (GOBE): The palaeoecological dimension. Palaeogeogr. Palaeoclimatol. Palaeoecol. 294, 99–119. Shen, Y., Farquhar, J., Zhang, H., Masterson, A., Zhang, T., Wing, B.A., 2011. Multiple Sisotopic evidence for episodic shoaling of anoxic water during Late Permian mass extinction. Nat. Commun. 2, 210. Siedenberg, K., Strauss, H., Littke, R., 2016. Multiple sulfur isotopes (δ34S, Δ33S) and trace elements (Mo, U, V) reveal changing palaeoenvironments in the mid-Carboniferous Chokier Formation, Belgium. Chem. Geol. 441, 47–62. Sim, M.S., Bosak, T., Ono, S., 2011a. Large sulfur isotope fractionation does not require disproportionation. Science 333, 74–77. Sim, M.S., Ono, S., Donovan, K., Templer, S.P., Bosak, T., 2011b. Effect of electron donors on the fractionation of sulfur isotopes by a marine Desulfovibrio sp. Geochim. Cosmochim. Acta 75, 4244–4259. Sim, M.S., Ono, S., Hurtgen, M.T., 2015. Sulfur isotope evidence for low and fluctuating sulfate levels in the Late Devonian ocean and the potential link with the mass extinction event. Earth Planet. Sci. Lett. 419, 52–62. Su, W., 2007. Ordovician sea-level changes: evidence from the Yangtze Platform. Acta Palaeontol. Sin. 46 (Suppl), 471–476. Thompson, C.K., Kah, L.C., 2012. Sulfur isotope evidence for widespread euxinia and a fluctuating oxycline in Early to Middle Ordovician greenhouse oceans. Palaeogeogr. Palaeoclimatol. Palaeoecol. 313–314, 189–214. Tostevin, R., Turchyn, A.V., Farquhar, J., Johnston, D.T., Eldridge, D.L., Bishop, J.K.B., McIlvin, M., 2014. Multiple sulfur isotope constraints on the modern sulfur cycle. Earth Planet. Sci. Lett. 396, 14–21. Trotter, J.A., Williams, I.S., Barnes, C.R., Lécuyer, C., Nicoll, R.S., 2008. Did cooling oceans trigger Ordovician biodiversification? Evidence from conodont thermometry. Science 321, 550–554. Wang, X., Stouge, S., Erdtmann, B.D., Chen, X., Li, Z., Wang, C., Zeng, Q., Zhou, Z., Chen, H., 2005. A proposed GSSP for the base of the Middle Ordovician Series: the Huanghuachang section, Yichang, China. Episodes 28, 105–117. Webby, B.D., Paris, F., Droser, M.L., Percival, I.G. (Eds.), 2004. The Great Ordovician Biodiversification Event. Columbia Univ. Press, New York 484 pp. Wing, B.A., Halevy, I., 2014. Intracellular metabolite levels shape sulfur isotope fractionation during microbial sulfate respiration. Proc. Natl. Acad. Sci. U. S. A. 111, 18116–18125. Wu, R., Stouge, S., Li, Z., Wang, Z., 2010. Lower and Middle Ordovician conodont diversity of the Yichang Region, Hubei Province, Central China. Bull. Geosci. 85 (4), 631–644. Wu, N., Farquhar, J., Strauss, H., 2014. δ34S and Δ33S records of Paleozoic seawater sulfate based on the analysis of carbonate associated sulfate. Earth Planet. Sci. Lett. 399, 44–51. Zeng, Q., Ni, S., Xu, G., Zhou, T., Wang, X., Li, Z., Lai, C., Xiang, L., 1983. Subdivision and correlation on the Ordovician in the eastern Yangtze Gorges, China. Bull. Yichang Inst. Geol. Mineral Resources Chinese. Acad. Geol. Sci. 1–56 (in Chinese and English). Zerkle, A.L., Kamyshny, A., Kump, L.R., Farquhar, J., Oduro, H., Arthur, M.A., 2010. Sulfur cycling in a stratified euxinic lake with moderately high sulfate: Constraints from quadruple S isotopes. Geochim. Cosmochim. Acta 74, 4953–4970. Zhan, R., Jin, J., 2005. New data on the Foliomena Fauna (Brachiopoda) from the upper Ordovician of South China. J. Paleontol. 79 (4), 670–686. Zhan, R., Jin, J., 2007a. Diversity analysis of the Early Ordovician Sinorthis Fauna (Brachiopoda) from the Meitan Formation of Zunyi, northern Guizhou, South China. Earth. Environ. Sci. Trans. R. Soc. Edinb. 98, 239–251. Zhan, R., Jin, J., 2007b. Ordovician-Early Silurian (Llandovery) Stratigraphy and Palaeontology of the Upper Yangtze Platform, South China. Science Press, Beijing 169 pp. Zhan, R., Jin, J., 2008. Aspects of recent advances in the Ordovician stratigraphy and palaeontology of China. Palaeoworld 17, 1–11. Zhan, R., Jin, J., Chen, P., 2007. Brachiopod diversification during the Early–Mid Ordovician: an example from the Dawan formation, Yichang area, central China. Can. J. Earth Sci. 44 (1), 9–24. Zhang, T., Shen, Y., Zhan, R., Shen, S., Chen, X., 2009. Large perturbations of the carbon and sulfur cycle associated with the Late Ordovician mass extinction in South China. Geology 37, 299–302. Zhang, T., Shen, Y., Algeo, T.J., 2010a. High-resolution carbon isotopic records from the Ordovician of South China: Links to climatic cooling and the Great Ordovician Biodiversification Event (GOBE). Palaeogeogr. Palaeoclimatol. Palaeoecol. 289, 102–112. Zhang, Y., Cheng, J., Munnecke, A., Zhou, C., 2010b. Carbon isotope development in the Ordovician of the Yangtze Gorges region (South China) and its implication for stratigraphic correlation and paleoenvironmental change. J. Earth Sci. 21, 70–74. Zhang, T., Trela, W., Jiang, S., Nielsen, J.K., Shen, Y., 2011. Major oceanic redox condition change correlated with the rebound of marine animal diversity during the Late Ordovician. Geology 39, 675–678. Zhan, R., Wang, G., Wu, R., 2012. Late Ordovician Foliomena Fauna (Brachiopoda) of South China. J. Earth Sci. 21, 64–69. Zhang, G., Zhang, X., Li, D., Farquhar, J., Shen, S., Chen, X., Shen, Y., 2015. Widespread shoaling of sulfidic waters linked to the end-Guadalupian (Permian) mass extinction. Geology 43, 1091–1094. Zhang, G., Zhang, X., Hu, D., Li, D., Algeo, T.J., Farquhar, J., Henderson, C.M., Qin, L., Shen, M., Shen, D., Schoepfer, S.D., Chen, K., Shen, Y., 2017. Redox chemistry changes in the Panthalassic Ocean linked to the end-Permian mass extinction and delayed Early Triassic biotic recovery. Proc. Natl. Acad. Sci. U. S. A. 114, 1806–1810.

Geobiology 1, 27–36. Farquhar, J., Johnston, D.T., Wing, B.A., 2007. Implications of conservation of mass effects on mass-dependent isotope fractionations: Influence of network structure on sulfur isotope phase space of dissimilatory sulfate reduction. Geochim. Cosmochim. Acta 71, 5862–5875. Farquhar, J., Canfield, D.E., Masterson, A., Bao, H., Johnston, D., 2008. Sulfur and oxygen isotope study of sulfate reduction in experiments with natural populations from Fællestrand, Denmark. Geochim. Cosmochim. Acta 72, 2805–2821. Gomes, M.L., Hurtgen, M.T., 2013. Sulfur isotope systematics of a euxinic, low-sulfate lake: Evaluating the importance of the reservoir effect in modern and ancient oceans. Geology 41, 663–666. Harper, D.A.T., 2006. The Ordovician biodiversification: Setting an agenda for marine life. Palaeogeogr. Palaeoclimatol. Palaeoecol. 232, 148–166. Harper, D.A.T., Zhan, R., Jin, J., 2015. The Great Ordovician Biodiversification Event: Reviewing two decades of research on diversity's big bang illustrated by mainly brachiopod data. Palaeoworld 24, 75–85. Henderson, M.A., Gomezb, F.J., Szynkiewiczc, A., Feltesb, N.A., Serrab, F., Albanesib, G.L., Kah, L.C., 2019. Sulfur cycling in the Darriwilian (Middle Ordovician) of Argentina: Constraints on a dual-reservoir model for sulfur cycling. Palaeogeogr. Palaeoclimatol. Palaeoecol (in press). Johnston, D.T., 2011. Multiple sulfur isotopes and the evolution of Earth's surface sulfur cycle. Earth-Sci. Rev. 106, 161–183. Johnston, D.T., Farquhar, J., Wing, B.A., Kaufman, A., Canfield, D.E., Habicht, K.S., 2005a. Multiple sulfur isotope fractionations in biological systems: A case study with sulfate reducers and sulfur disproportionators. Am. J. Sci. 305, 645–660. Johnston, D.T., Wing, B.A., Farquhar, J., Kaufman, A.J., Strauss, H., Lyons, T.W., Kah, L.C., Canfield, D.E., 2005b. Active microbial sulfur disproportionation in the Mesoproterozoic. Science 310, 1477–1479. Johnston, D.T., Farquhar, J., Canfield, D.E., 2007. Sulfur isotope insights into microbial sulfate reduction: When microbes meet models. Geochim. Cosmochim. Acta 71, 3929–3947. Johnston, D.T., Farquhar, J., Habicht, K.S., Canfield, D.E., 2008. Sulphur isotopes and the search for life: strategies for identifying sulphur metabolisms in the rock record and beyond. Geobiology 6, 425–435. Kah, L.C., Thompson, C.K., Henderson, M.A., Zhan, R., 2016. Behavior of marine sulfur in the Ordovician. Palaeogeogr. Palaeoclimatol. Palaeoecol. 458, 133–153. Leavitt, W.D., Cummins, R., Schmidt, M.L., Sim, M.S., Ono, S., Bradley, A.S., Johnston, D.T., 2014. Multiple sulfur isotope signatures of sulfite and thiosulfate reduction by the model dissimilatory sulfate-reducer, Desulfovibrio alaskensis str. G20. Front. Microbiol. 5, 591. https://doi.org/10.3389/fmicb.2014.00591. Lin, M., Zhang, X., Li, M., Xu, Y., Zhang, Z., Tao, J., Su, B., Liu, L., Shen, Y., Thiemens, M.H., 2018. Five-S-isotope evidence of two distinct mass-independent sulfur isotope effects and its consequence for the Archean record. Proc. Natl. Acad. Sci. U. S. A. 115, 8541–8546. Luo, G., Richoz, S., Schootbrugge, B.V.D., Algeo, T.J., Xie, S., Ono, S., Summons, R.E., 2018. Multiple sulfur-isotopic evidence for a shallowly stratified ocean following the Triassic-Jurassic boundary mass extinction. Geochim. Cosmochim. Acta 231, 73–87. Marenco, P.J., Marenco, K.N., Lubitz, R.L., Niu, D., 2013. Contrasting long-term global and short-term local redox proxies during the Great Ordovician Biodiversification Event: A case study from Fossil Mountain, Utah, USA. Palaeogeogr. Palaeoclimatol. Palaeoecol. 377, 45–51. Melchin, M.J., Mitchell, C.E., Holmden, C., Storch, P., 2013. Environmental changes in the Late Ordovician-early Silurian: Review and new insights from black shales and nitrogen isotopes. Geol. Soc. Am. Bull. 125, 1635–1670. Miller, A.I., Mao, S., 1995. Association of orogenic activity with the Ordovician radiation of marine life. Geology 23, 305–308. Mitchell, C.E., Chen, X., Bergström, S.M., Zhang, Y., Wang, Z., Webby, B.D., Finney, S.C., 1997. Definition of a global boundary stratotype for the Darriwilian Stage of the Ordovician System. Episodes 20, 158–166. Munnecke, A., Zhang, Y., Liu, X., Cheng, J., 2011. Stable carbon isotope stratigraphy in the Ordovician of South China. Palaeogeogr. Palaeoclimatol. Palaeoecol. 307, 17–43. Ono, S., Wing, B., Johnston, D., Farquhar, J., Rumble, D., 2006. Mass-dependent fractionation of quadruple stable sulfur isotope system as a new tracer of sulfur biogeochemical cycles. Geochim. Cosmochim. Acta 70, 2238–2252. Ono, S., Shanks, W.C., Rouxel, O.J., Rumble, D., 2007. S-33 constraints on the seawater sulfate contribution in modern seafloor hydrothermal vent sulfides. Geochim. Cosmochim. Acta 71, 1170–1182. Pellerin, A., Bui, T.H., Rough, M., Mucci, A., Canfield, D.E., Wing, B.A., 2015a. Massdependent sulfur isotope fractionation during reoxidative sulfur cycling: A case study from Mangrove Lake, Bermuda. Geochim. Cosmochim. Acta 149, 152–164. Pellerin, A., Anderson-Trocme, L., Whyte, L.G., Zane, G.M., Wall, J.D., Wing, B.A., 2015b. Sulfur isotope fractionation during the evolutionary adaptation of a sulfate-reducing bacterium. Appl. Environ. Microbiol. 81, 2676–2689. Rasmussen, C.M., Ullmann, C.V., Jakobsen, K.G., Lindskog, A., Hansen, J., Hansen, T., Eriksson, M.E., Dronov, A., Frei, R., Korte, C., Nielsen, A.T., Harper, D.A., 2016. Onset of main Phanerozoic marine radiation sparked by emerging mid Ordovician icehouse. Sci. Rep. 6, 18884. Scheiderich, K., Zerkle, A.L., Helz, G.R., Farquhar, J., Walker, R.J., 2010. Molybdenum isotope, multiple sulfur isotope, and redox-sensitive element behavior in early Pleistocene Mediterranean sapropels. Chem. Geol. 279, 134–144. Schmitz, B., Harper, D.A.T., Peucker-Ehrenbrink, B., Stouge, S., Alwmark, C., Cronholm, A., Bergström, S.M., Tassinari, M., Wang, X., 2008. Asteroid breakup linked to the Great Ordovician Biodiversification Event. Nat. Geosci. 1, 49–53. Sepkoski, J.J., 1995. The Ordovician radiations: diversification and extinction shown by global genus-level taxonomic data. In: Ordovician Odyssey Short Papers for the Seventh Int. Symp. on the Ordovician System, pp. 393–396. Servais, T., Harper, D.A.T., 2018. The Great Ordovician Biodiversification Event (GOBE):

8