Two Episodes of Environmental Change at the Permian–Triassic Boundary of the GSSP Section Meishan

Earth-Science Reviews 115 (2012) 163–172

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Earth-Science Reviews

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Two episodes of environmental change at the Permian–Triassic boundary of the GSSP section Meishan

Hongfu Yin a,⁎, Shucheng Xie a, Genming Luo a, Thomas J. Algeo b, Kexin Zhang a a State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan 430074, China b Department of Geology, University of Cincinnati, Cincinnati, OH 45221, USA article info abstract

Article history: High-resolution stratigraphic records through the Permian–Triassic boundary (PTB) interval of the global Received 4 May 2012 stratotype section and point (GSSP) at Meishan, Zhejiang Province, China reveal that the PTB crisis was not a sin- Accepted 10 August 2012 gle, abrupt catastrophe. A bed-by-bed analysis of environmental and biotic changes makes clear that the crisis Available online 29 August 2012 can be resolved into two discrete episodes, each consisting of three stages: A) unstably oscillating conditions, B) peak crisis conditions, and C) ameliorating conditions. The ﬁrst crisis episode commenced in Bed 23, peaked Keywords: in Beds 24e–26, and ameliorated in Beds 27 and 28, while the second crisis episode commenced in Bed 29, Mass extinction – Conodont biostratigraphy peaked in Beds 34 38, and ameliorated in Beds 39 and higher. The macroscopic mass extinctions happened Carbon isotopes not at the beginning, nor the end of each cycle, but at times when the crisis or perturbation of environments Volcanic event beds began. These extinction events do not show detectable feedbacks to concurrent environmental changes. In Biomarkers each episode, cyanobacteria proliferation postdated the macroscopic extinction while proliferation of green sul- Geomicrobial functional groups fur bacteria predated the environmental crisis. Causational analysis between environmental and microbial changes show that geomicrobial functional groups exercised pronounced effects on the marine C–N–Scycles and ocean redox conditions during the PTB crisis. It is possible thus that the microbial crises played an important role in strengthening or evening triggering the environmental crisis. © 2012 Elsevier B.V. All rights reserved.

Contents

1. Introduction ...... 164 2. Methods ...... 164 3. Event sequence at Meishan ...... 165 3.1. Pre-crisis: relatively normal conditions (Beds 22 and lower) ...... 165 3.2. Episode 1, Stage A: oscillating conditions (Beds 23 and 24d) ...... 166 3.3. Episode 1, Stage B: crisis peak (Beds 24e–26)...... 166 3.3.1. Bed 24e ...... 166 3.3.2. Bed 25 ...... 166 3.3.3. Bed 26 ...... 167 3.3.4. Environments of Beds 24e–26...... 167 3.4. Episode 1, Stage C: ameliorating conditions (Beds 27 and 28) ...... 168 3.5. Episode 2, Stage A: oscillating conditions (Beds 29–33)...... 168 3.6. Episode 2, Stage B: crisis peak (Beds 34–38)...... 169 3.7. Episode 2, Stage C: ameliorating conditions (Beds 39 and higher) ...... 169 4. Discussion and conclusion ...... 169 Acknowledgments ...... 170

⁎ Corresponding author at: Ofﬁce of President, China University of Geosciences, Wuhan, Hubei, 430074, China. Tel.: +86 27 67884812(h.), +86 27 87481030(secr.); fax: +86 27 87481392. E-mail addresses: [email protected], [email protected] (H. Yin), [email protected] (S. Xie), [email protected] (G. Luo), [email protected] (T.J. Algeo), [email protected] (K. Zhang). URL: http://www.cug.edu.cn (H. Yin).

Appendix A. Supplementary data ...... 170 References ...... 170

1. Introduction the lower part of the Isarcicella isarcica Zone (the full range of which is Beds 29b–51). The duration of the I. isarcica Zone (~390 Kyr) was The mass extinction at the Permian–Triassic boundary (PTB) has been constrained by cyclostratigraphic analyses of PTB sections at Chaohu recognized as the largest mass extinction in geological history (Erwin, (Anhui Province) and Daxiakou (Hubei Province), on the basis of 1993). Biotic, climatic, and environmental events accompanying this which we estimated the duration of Beds 29b–38 as ~100 ka. The extinction have been extensively investigated at Meishan, the GSSP of Bed 29b–38 interval consists of ca. 20 high-frequency sedimentary the PTB, based on many types of paleobiologic and chemostratigraphic cycles (Zhang et al., 1997, 2009; Wu et al., 2012), which thus repre- records (Yin et al., 2001). To date, these events have been reported in sent a sub-Milankovitch periodicity (~5 Kyr) (Guo et al., 2008; Wu et separate publications, and many of them are regarded as isolated (i.e., al., 2012). These considerations yield an estimated age of 252.00 Ma mono-episodic) phenomena. Recent advances in isotopic dating (S.Z. for Bed 38, and the total duration of the interval from Bed 24e to Bed Shen et al., 2011) and biostratigraphic zonation (Zhang et al., 2009)of 38 (the focus of this study) is thus about 0.3 Ma. The nearest overlying the PTB interval have laid the groundwork for our development of a eventwithaδ13C excursion, interpreted as coincident with a microbial high-resolution temporal framework for the Meishan succession. This boost, is located at the Griesbachian–Dienerian transition, within the framework includes 8 conodont zones, yielding a temporal resolution Neospathodus kummeri Zone, a few hundred of thousand years younger of ~0.01 Myr, thus making feasible a detailed synthesis of the event than the interval considered here (Payne et al., 2004; Zuo et al., 2006). sequence at Meishan. In this paper, we compile the various events that This makes the Beds 23–39 interval a critical PTB interval of ancient have been documented in the Meishan GSSP into a single record, in global change readily separated from under- and overlying strata. order to understand better the patterns and processes of global change The stratigraphic framework of the Meishan succession is based on during the PTB crisis. the following references: system boundary and formation names (Yin et al., 2001), bed numbers and their descriptions (Yin et al., 1996), age 2. Methods (Shen et al., 2011a, plus a 252.00 age of Bed 38); conodont zonation (Zhang et al., 2009, which is a synthesis of most published conodont stud- According to earlier publications, the PTB extinction at Meishan began ies of the Meishan GSSP, see Supporting material). Changes of the proxy inBed24eandendedinBed28(Xie et al., 2007; Yin et al., 2007a; S.Z. datasets in the columns of Figs. 1 and 2 are interpreted within narrowly Shen et al., 2011). As documented herein, however, the environmental deﬁned stratigraphic intervals and subdivided into peaks, ebbs, and crisis actually continued to Bed 38 (Figs. 1 and 2). Beds 29b–38 cover other relevant trends as shown in Fig. 3. Abscissa values of the proxies

Fig. 1. The PTB event sequence at Meishan. Beds within the mass extinction interval (Beds 24–28; 27a/b and 27c/d each regarded as a single bed) are given larger and roughly averaged thicknesses than the other beds; all data are re-dotted to the rescaled columns. The original references are as follows: system boundary and formation names (Yin et al., 2001), bed numbers and their descriptions (Yin et al., 1996), age (Shen et al., 2011a,b,c, and others, see text); conodont zonation: Zhang et al. (2009); diversity (species): Jin 13 13 et al. (2000, SOM); cyanobacteria (C31 2MHP index): Xie et al. (2005); δ Ccarb: Cao et al. (2002); Xie et al. (2007); δ Corg: Cao et al. (2009); redox (isorenieratane, black; aryl isoprenoids, lg (C14–C27), (ppm/TOC) light blue): Grice et al. (2005), (pyrite framboids, red): Shen et al. (2007);δ15N: Cao et al. (2009). H. Yin et al. / Earth-Science Reviews 115 (2012) 163–172 165

Fig. 2. The PTB event sequence at Meishan (continued). All data are re-dotted to the rescaled columns. The original references are as follows: terrestrial input (C29-M/C30-HP, red; C30-M/C30-HP, black): Xie et al. (2007); (light blue square): Wang (2007); DBF: Xie et al. (2007, 2009); volcanic ash: Yin et al. (1996); wildfire (black carbon, red): Xie et al. (2007), W.J. Shen et al. (2011); (PAHs, black): W.J. Shen et al. (2011); TOC: Cao et al. (2002) (light blue); Grice et al. (2005) (red); W.J. Shen et al. (2011) (black); δ18O: Joachimski et al. (2012); sea level: Cao and Zheng (2009) (red); Zhang et al. (1997) (black). are arranged such that correlation of their fluctuations can be visually but, rather, consisted of multiple fluctuations defining two main perceived, so the values may either increase or decrease toward the episodes. right side. Generally but not always, excursions toward the left would imply deterioration of the environment, and excursions toward the 3. Event sequence at Meishan right, amelioration of the environment. Temporal correlation of these events clearly shows that the PTB event sequence of Meishan was episod- 3.1. Pre-crisis: relatively normal conditions (Beds 22 and lower) ic. Abnormal and relatively normal intervals alternate in most event sequences. The environmental crisis and accompanying extinction were The Changhsingian strata up to Bed 22 at Meishan belong to a stage not a unidirectional process of environmental and biotic deterioration with relatively normal environment. It is relative because there were

Fig. 3. Episodes and stages of the PTB event sequence at Meishan. Bed thicknesses as in Fig. 1; Mbl. = microbialite. 166 H. Yin et al. / Earth-Science Reviews 115 (2012) 163–172 still anoxic phases in the succession (Wignall and Hallam, 1993). A for soil erosion discussed above. Decimation of the tropical forest highstand systems track prevailed, characterized by carbonate deposi- Gigantopteris flora and strengthened terrestrial erosion in South tion in an inter-platform depression and a diversified biota within a China during the latest Permian (Yin et al., 2007b) suggests that the stable marine ecosystem. The biota consisted of warm-water benthic for- climate may have turned from humid to arid. Increased soil erosion aminifers, corals, brachiopods, and nektonic ammonoids and conodonts and chemical weathering was not confined to Meishan but was a assigned to the Collaniella–Palaeofusulina foraminifer fauna (Yin et al., global event at the PTB as shown by greater pedogenic production 1996; Zhang et al., 1997; Cao and Zheng, 2009). Carbon isotopes were of clay minerals and increased fluxes of siliciclastics to marine shelves 13 13 stable (δ Ccarb ≈+3‰, δ Corg ≈−29‰), and terrestrial detrital, volca- in many regions (Algeo and Twitchett, 2010; Algeo et al., 2011). nic, and wildfire proxies exhibit low values, although with sporadic irregularities. However, redox conditions and microbial indices began 3.3. Episode 1, Stage B: crisis peak (Beds 24e–26) to oscillate above Bed 22. 3.3.1. Bed 24e 3.2. Episode 1, Stage A: oscillating conditions (Beds 23 and 24d) Bed 24e is a 20-cm-thick micritic limestone containing warm- water fauna. Its base is a slightly uneven hard ground, in which depres- Beds 23 and 24d are bioclastic to micritic limestones (1.9 m thick), sions were filled with thin calcareous limonitic mudrock and abraded somewhat siliceous, containing the same fauna as the underlying bioclastics. The microfacies across the basal surface are discontinuous. beds. Unstably oscillating environmental conditions began in Bed Strata below this surface show coarsening-upward character, forming 23, as shown by coordinated shifts toward lower or higher values a progradational parasequence set, whereas the overlying beds are for many proxies in Figs. 1 and 2, including carbon and oxygen iso- retrogradational. These features document a short hiatus and a Type 2 topes, C29,30-M/C30-HP, DBF, and black carbon. Aryl isoprenoids and sequence boundary (SB2) at the base of Bed 24e (Zhang et al., 1997). isorenieratanes reach peak concentrations in Bed 24. They are The overlying beds (24e–26) constitute a shelf margin systems tract regarded as molecular proxies of green sulfur bacteria, an anoxygenic (SMST) that is widely present across the northern and southern rims photosynthetic organism that thrived only in the lower, H2S-rich part of the Yangtze Platform (Xia et al., 2004; Tong and Zhao, 2005; Feng of a stratified photic zone, so that their abundance usually denotes et al., 2007; Jiang et al., 2011). Marine regression, commencing from photic-zone euxinia (Grice et al., 2005; Cao et al., 2009). Negative Bed 24e, exposed the main part of the Yangtze Platform as well as iso- δ34S with negative Δ33S of pyrite analysis indicates a near shutdown lated carbonate islands of the Guizhou–Guangxi region. As a conse- of bioturbation during episodic shoaling of anoxic water in the inter- quence, the Clarkina meishanensis and H. changxingensis zones are val of Beds 22–24 (Y. Shen et al., 2011; cf. Algeo et al., 2007). The AIR widely missing, replaced by a hiatus between the C. latidentatus Zone index (the ratio of the peak area in m/z 133 mass chromatogram for of the Changxing Limestone and the Hindeodus parvus Zone of the over- the short-chain C13–C17 aryl isoprenoids to the intermediate chain lying microbialite (Kershaw et al., 1999; Lehrmann et al., 2003; Payne et C18–C22 homologues) of green sulfur bacteria (Schwark and al., 2007). This regression was widespread across the Tethyan region Frimmel, 2004) and the Pr/Ph (pristane/phytane) ratio (Ten Haven and on the northern rim of Gondwana, where a Type 2 sequence bound- et al., 1987) are usually regarded as indicative of redox conditions ary has been observed in most well-studied sections (Shen et al., 2006; in a sedimentary environment. Huang et al. (2007) have shown fre- Yin et al., 2007a). quent and coordinated oscillations of the AIR index and Pr/Ph ratio Bed 24e witnessed the extinction of rugose and tabulate corals, in Bed 24. The Pr/Ph peaks of reducing environments are usually of fusulinids, pseudotirolitid ammonoids, and many Permian-type short duration, implying that the photic water body was not always brachiopods, bryozoans, and gastropods. Measurements of Clarkina

H2S-rich but frequently interrupted by oxic conditions. TOC values, P1 elements show that their average size decreased from 0.63 to which record the combined influences of primary productivity and 0.69 mm in Bed 24a–d to 0.54 mm in Bed 24e (Luo et al., 2008). organic matter preservation under reducing conditions, also show Approximately synchronous extinctions also happened in other large variations. Because these beds contain a diversified biota, ben- sections in South China and the western Tethys, usually several cen- thic anoxia is unlikely to have existed over long intervals but, more timeters to a few meters below the main extinction level. This event likely, waxed and waned frequently. is regarded variously as the beginning of the PTB mass extinction The negative shift of carbonate δ13C reached 2–3‰ in Bed 24d (S.Z. Shen et al., 2011) or its prelude phase (Yin et al., 2007a). (Cao et al., 2002; Xie et al., 2007). Simultaneously, the δ18O value Kaiho et al. (2006) claimed that the mass extinction began 3 cm measured on phosphate-bound oxygen in conodont apatite (Clarkina below the top of Bed 24e, where the above-mentioned taxa and Hindeodus) decreased by 1(+)‰ in the latest Permian, translat- disappeared concurrently with an abrupt shift toward lower δ34S ing into low-latitude (i.e., peri-South China) surface-water warming (22.9‰→8.9‰)andanomaliesof87Sr/86Sr, Ni, and P. At about the of 5 °C (Joachimski et al., 2012). Although not discovered in Meishan, same level, Cao and Zheng (2009) also noted wavy bedding and older volcanic ash beds in other PTB sections document that volca- evidence of a depositional hiatus associated with black, tuffaceous nism was already extensive in South China during the latest Permian volcaniclastics. (Yin et al., 1992; Xie et al., 2010). This together with simultaneous Trends in geochemical proxies began in Bed 24a–d and generally 13 volcanic activities may have added isotopically light carbon to the continued into Bed 24e (Fig. 1). However, δ Corg exhibits a shift ocean–atmosphere system, increased greenhouse gas levels, and toward more positive values in Bed 24e after a long negative shift also released SO2 and H2S that enhanced marine euxinia. through Beds 23 and 24d, a feature that was also recorded in many 13 The moretane/hopane ratios (C29-M/C30-HP, C30-M/C30-HP) are δ Cprofiles globally (Korte and Kozur, 2010). Proxies of both indicative of terrestrial input and the diagenetic maturity of organic terrestrial input and wildfire show a weak climax in Bed 24e matter, whereas the DBF index (DBF/(DBF+DBT+F)) denotes land (Wang, 2007; Xie et al., 2007, 2009; Shen et al., 2011b), which soil material transported and deposited in the marine environment. suggests that climatic conditions may have become more arid than Both show increasing tendencies from Bed 23 to Bed 24, implying a it was previously. strengthening of terrestrial erosion and detrital fluxes to the ocean. Black carbon and PAHs (polycyclic aromatic hydrocarbons) in ancient 3.3.2. Bed 25 sediments mainly originate from forest wildfires (Schmidt and Noack, Bed 25 is a 4-cm-thick, whitish illite-montmorillonite claystone of 2000; Menzie et al., 1992). An increase of black carbon particles at hydrolyzed volcanic ash origin. The volcanic material was acidic to in- this stage is indicative of damage to land vegetation (Xie et al., termediate in composition, minerals, and structures, and came from 2007; W.J. Shen et al., 2011), which is consistent with the evidence the southwest (i.e., southern paleomargin of South China) rather H. Yin et al. / Earth-Science Reviews 115 (2012) 163–172 167 than from the north (i.e., the Siberian Traps; Yin et al., 1992; Xie et al., used to be called a “transitional fauna” (Yin, 1985), characterized 2010). It is informally termed the “White Clay” and represents the by a mixture of ‘Permian type’ survivors of the extinction event and base of the Yinkeng (or Qinglong) Formation. Bed 25 is the horizon ‘Triassic type’ newcomers. The ‘Permian type’ relicts include calcare- coinciding with the main phase of the PTB mass extinction. An analy- ous foraminifers (Bradyina, Glomospira, Globivalvulina, Hemigordius, sis of 333 species of the Meishan composite standard section showed Nodosaria and Textularia), and brachiopods (Cathaysia, Crurithyris, a sudden decrease of diversity at this level, the rate of extinction Neochonetes, Paryphella, Ucinunellina, Prelissorhynchia, Araxathyris, being 48% and 52% at the base of Bed 25 and within Bed 25, respec- Paracrurithyris and Tethyochonetes). Otoceras? is the last representa- tively. The number of identified species in each bed is shown in the tive of the Permian Otoceratacea, but other ammonoids (Hypohiceras, diversity column of Fig. 1 (Jin et al., 2000, SOM). Actual extinction Metophiceras, Tompophiceras, Glyptophiceras) belong to the dominant- rates may have been even larger than reported owing to the Si- ly Early Triassic Ophiceratidae, although most of these taxa did not gnor–Lipps effect (Signor and Lipps, 1982). The extinction shows survive beyond the Griesbachian. Peribositra is an ancestral genus of that high selectivity against stenotopic organisms adapted to oxic the Early Triassic claraiid bivalves, while other bivalve genera (Pteria conditions (corals, demosponges, calcareous foraminifers) and was and Towapteria) are Permian relicts that did not survive beyond the due to anoxia–euxinia (Wignall and Hallam, 1993; Grice et al., transitional beds (Yin et al., 1996). Benthic macrofossils are miniatur-

2005) or, possibly, hypercapnia caused by elevated ρCO2 (Knoll et ized, having thin and small shells (He et al., 2007). The lithology and al., 2007). Ce/Ce* ratios of conodonts provide new evidence of a taphonomy suggest a stagnant and slow depositional environment. shift from oxic or dysoxic to markedly anoxic conditions in Bed 25 Correlative horizons have been discovered only on the northern and (Zhao et al., 2009). It is to be noted that this main extinction event southern rims and on the slopes of the Yangtze Platform (i.e., at the took place sometime later than the onset of environmental deteriora- Daxiakou, Shangsi, Huangsi, Bianyang and other deep-water sections). tion (Bed 24e) and does not seem to have had any identifiable feed- In sequence stratigraphic terms, Bed 26 represents the upper part of back to the environment. the SMST or the onset of a transgression (Zhang et al., 1997). The base of Bed 25 is uneven and represented by a very thin In contrast to the impoverished macro-biota, microbes of Beds 25 and (b1mm)“ferruginous crust”, an oxidized lamina of pyrite (Wignall 26 experienced considerable development. The 2-MHP (methylhopane) and Twitchett, 2002) within which have been discovered a δ34S index is a ratio of the abundance of cyanobacterial biomarkers to more anomaly, a large quantity of sulfur, fullerenes (C60/C70), and abundant general bacterial biomarkers. Usually C32-2-MHP is regarded as a more Fe–Ni–Si particles. These features were once considered as evidence of dependable index of cyanobacteria, because 2-MHP index with carbon an extraterrestrial impact (Becker et al., 2001; Kaiho et al., 2001; Basu numbers less than C32 may have other origins. However, the sample con- et al., 2003), but this hypothesis was not supported by later tent of C32 is very small and its extractability is much lower than re-investigations (Farley et al., 2005). However, this special micro-bed C31-2-MHP, so the latter is commonly used to reflect the abundance of does represent a short depositional hiatus. The White Clay is wide- cyanobacteria (Summons et al., 1999; Farrimond et al., 2004). As shown spread in relatively deep-water localities of South China, but it may in Fig. 1,theC31-2-MHP index exhibits a secondary peak in Bed 26 (Xie have been eroded away and replaced by the hiatus at the base of Bed et al., 2005), and aryl isoprenoids, a proxy for green sulfur bacteria, dis- 25 during a regression that affected shallow-water platforms and play a pronounced increase (Grice et al., 2005). In addition, abundant islands. prasinophyte algae have been found in this bed (Yin et al., 1992). Togeth- The main phase of the marine PTB mass extinction happened er with high TOC (Cao et al., 2002, 2009; Grice et al., 2005; W.J. Shen et al., synchronously with the sedimentary-ecosystem transition from 2011), these proxies demonstrate that marine microbes were not deci- skeletal carbonates containing a humid tropical biota to oolites and mated after the macroscopic extinction but, rather, maintained consider- calcimicrobialites deposited under arid climatic conditions. At the able abundance. Bulla section in the Italian Alps (Farabegoli et al., 2007) and the Çürük Dagh section of southwestern Turkey (Baud et al., 2005), this transition 3.3.4. Environments of Beds 24e–26 took place in two steps. The first step is a sudden change from the latest The quantity and mean diameters of pyrite framboids can be used Changhsingian skeletal wackestone-packstone (i.e., upper Bellerophon to infer redox conditions in marine paleoenvironments (Wignall and and Pamuçak formations) to oolitic packstone-grainstone (i.e., Tesero Newton, 1998). Changes in pyrite framboid character at Meishan in- Oolite Member of Werfen Formation and uppermost Pamuçak Forma- dicate redox fluctuations between weakly dysoxic (Bed 24e) and tion), representing the beginning of arid climate conditions. The second strongly dysoxic conditions (pyrite laminae, Beds 25 and 26) (Shen step is a transition from oolitic limestone to calcimicrobialite of the ear- et al., 2007). The laminated, Corg-rich lithology and high content of liest Triassic age (i.e., lower Mazzin Member of Werfen Formation and aryl isoprenoids provide evidence of a highly dysoxic-anoxic, and lower Kokarkuyu Formation). In the Italian Alps, the main extinction usually euxinic, environment at this time (Grice et al., 2005; Cao et and negative carbon-isotope shift occurred in a ~25-cm-thick interval al., 2009). However, frequent oscillations of the AIR index and Pr/Ph that includes the uppermost regressive Bulla Member and the basal ratio (Huang et al., 2007) denote unstable redox conditions rather 34 oolitic part of the Tesero member. The skeletal carbonates and than prolonged euxinia. Moreover, detailed records of δ SCAS show parvus-bearing microbialites can be correlated readily between the large fluctuations (−7to+24‰ VCDT) across Beds 24e–26, indicat- Italian Alps and South China, demonstrating that the stratigraphically ing a shallow unstable chemocline overlying euxinic deep waters that intermediate oolitic units must correspond to Beds 25 and 26 of the periodically upwelled into the photic zone (Riccardi et al., 2006). Meishan. In terms of paleoclimate, these correlations suggest a nearly Y. Shen et al. (2011) observed a sulfur isotope signal (negative δ34S synchronous transition from humid to arid climate conditions through- with negative Δ33S) that may have resulted from limitation of sulfate out the Tethyan region coincident with the main extinction phase. supply in the ocean. This condition was recognized earlier in the Cili section (Hunan Province), where large-amplitude variations in 34 3.3.3. Bed 26 δ SCAS suggest a small oceanic sulfate reservoir size, and the co-variation 13 34 Bed 26 is a 6-cm-thick, dark gray claystone that is, in part, calcar- between δ Ccarb and δ SCAS implies a marine-driven C cycle in an 15 eous and silty. It is informally termed the “Black Clay”, in contrast anoxic ocean (Luo et al., 2010). δ Norg declined gradually from to the underlying “White Clay”. This bed contains finely laminated ~+3‰ in the Wujiapingian to ~+1–2‰ in the late Changhsingian. 15 illite‐montmorillonite (possibly hydrolyzed volcanic ash) and has Above Bed 25, δ Norg declined further to ~0‰, remaining in that yielded microspherules, hexagonal bipyramidal β quartz pseudo- range through Bed 34 (Cao et al., 2009). In Meishan as in other sec- morphs, and other volcanic materials similar to those from Bed 25 tions of South China, concurrent abrupt negative shifts of δ15Nand 13 15 (Yin et al., 1992; Zhang et al., 2005). Macrofossils of Beds 25–27 δ Corg at the main extinction horizon and persistently low δ N 168 H. Yin et al. / Earth-Science Reviews 115 (2012) 163–172 values thereafter suggest that microbial nitrogen fixation became Yangtze carbonate platform, Bed 27 is replaced by parvus-bearing the main source of biologically available nitrogen. Enhanced N fixa- calcimicrobialites composed of cyanobacterial masses from 2 to 10 m tion is probably indicative of the prevalence of stratified anoxic in thickness. The calcimicrobialites are discontinuous laterally, being re- water masses characterized by intense denitrification and/or anaer- placed by ordinary limestone due to an uneven platform surface. These obic ammonium oxidation (Luo et al., 2011). calcimicrobialites are suggested to have formed under warm and arid cli- The carbonate δ13Cprofile reached its lowest values in Beds 25 and mate conditions and, possibly, elevated salinities (Wang et al., 2005). The 26. The magnitude of the negative shift from the top of the Changxing percentage of filter-feeders (FF%) in the calcimicrobialite facies varied Formation (Bed 24e) through Bed 25 is 5.7‰ (Cao et al., 2002; Xie et with benthic redox conditions, with high FF% associated with more al., 2007). The moretane/hopane ratio and the DBF index yield high reducing conditions (Lethiers and Whatley, 1994). The FF% of ostracods values in Beds 24 and 26, indicating relatively strong soil erosion and ranges from 7% at Jinya (Guangxi Province) to 60% at Laohudong terrestrial fluxes to the ocean at this time. Also, the wildfire proxies (Chongqing Municipality) (Crasquin-Soleau and Kershaw, 2005). To (i.e., black carbon and PAHs) reached an acme in Bed 26 (Wang and sum it up, Bed 27 belongs to an interval of ameliorating environmental Visscher, 2007; Xie et al., 2007; W.J. Shen et al., 2011), reflecting arid cli- conditions, characterized by a transgression, warm and arid climate, mate conditions and forest decimation. All these events happened dur- reduced stresses in land areas, and oxic to somewhat dysoxic marine ing a peak interval of volcanic activity, and many or all of them can be redox conditions. It should be emphasized that at many shallow- attributed to that process. To sum up, Beds 24e–26 belong to peak crisis water PTB sections within the Tethyan region, from the Yangtze episode characterized by rapid regression, arid climate, extensive volca- Platform through Iran to the Southern Alps, the oolitic limestones, nism, wildfire-vegetation-soil crisis on land, and frequently euxinic seas calcimicrobialites, and parvus-bearing limestone that are equivalent to having a very small sulfate reservoir, all of which together triggered the Meishan Bed 27 are not highly dysoxic, as suggested by general ocean PTB mass extinction. redox models (Isozaki, 1997). Rather, these beds are frequently fossilif- erous and sometimes contain reef-forming elements, indicating well- 3.4. Episode 1, Stage C: ameliorating conditions (Beds 27 and 28) oxygenated shallow-marine environments. Bed 28 is a 4-cm-thick illite-montmorillonite claystone of volcanic Bed 27 is a 16-cm-thick, light gray micrite subdivided into four origin showing characteristics similar to Bed 25. Previous literature sub-beds (a–d), each ~4 cm thick. The GSSP of the PTB was set at denotes this bed either as a second (epilogue) mass extinction (Xie the base of Bed 27c, where the index taxon Hindeodus parvus first ap- et al., 2005; Yin et al., 2007a) or the end of the main extinction pears (Yin et al., 2001). The base of Bed 27 is the transgressive surface event (S.Z. Shen et al., 2011). Our new statistics of 550 species in (TS) of a new sequence, followed by a transgressive systems tract 260 genera of 18 marine fossil groups from seven Chinese sections in- (TST) that extends to at least Bed 40 (Zhang et al., 1997). The lateral cluding Meishan reveal, however, that the epilogue phase actually equivalent of Bed 27 is present widely across South China, corre- happened by the end of Bed 28, or the 29/28 boundary(Song et al., sponding to parvus-bearing microbialites of the Yangtze Platform submitted for publication). If the extinction at the 25/24 boundary and the Guizhou–Guangxi islands. In proximity to the Cathaysia and is taken as extinction at Bed 25, the second extinction should be at- Yunnan–Xikang Oldlands, this bed undergoes a facies change to calcar- tributed to Bed 29. eous claystone and siltstone, and in deep-water regions such as the Nanpanjiang Basin the equivalents consist of marl and carbonaceous calcareous claystone (Yin et al., 2007b; Chen et al., 2008). Three hard 3.5. Episode 2, Stage A: oscillating conditions (Beds 29–33) ground horizons, characterized by bioclastic micro-laminae and burrowed fabrics, have been discovered in Bed 27: within Sub-bed According to Jin et al. (2000, Fig. 1; SOM),extinction rates at the 27b, near the 27b/c contact, and within Sub-bed 27d (Cao and Zheng, species level are 52% for Bed 28 and 42% for the base of Bed 29, second 2009). This widespread transgressive horizon, accompanied by the cos- only to the extinction rates for Beds 25 and 26. Species diversity de- mopolitan distribution of Hindeodus parvus, indicates that this trans- creased to 12 (Bed 29) and remained at that level up to Bed 40. Bed gression was rapid and covered not only South China, but the whole 29/28 boundary witnessed the extinction of Permian relicts including world. most small brachiopods, bivalves and the Hypophiceras ammonoid Macrofossils still show the mixed character of the “transitional fauna. Brachiopods experienced 3 episodes of extinction: in Bed 25 fauna”, but diversity decreased to 30–37 species (Fig. 1). Hindeodus (extinction rate 91.2%), Bed 27 (57.7%), and Bed 28 (80.5%) (Chen replaced Clarkina as the dominant conodont. With regard to microbial et al., 2005). Foraminifer species diversity suffered a severe decrease: abundance, the cyanobacterial (MHP) index exhibits relatively low values Permian type from 15 to 2 and transitional type (newcomers after (Fig. 1), which may be partly due to greater water depths at Meishan Bed 25) from 19 to 2 (Song et al., 2009). Dominance among following a transgression, because parvus-bearing calcimicrobialites, usu- conodonts shifted from Hindeodus to Isarcicella. To sum it up, Bed ally regarded as largely due to cyanobacterial activities, were extensively 29/28 boundary records an ‘epilog extinction’ during which Permian deposited on shallow-water platforms elsewhere across South China. relicts that had survived the main extinction phase (Bed 25) Beds 27 and 28 are characterized by large shifts in environmental succumbed, and the extinction rate was high due to the low species proxies. Analysis of pyrite framboids, aryl isoprenoids and isorenieratane diversity prevailing at that time. Because Beds 28 and 29 are of show relatively oxic conditions, which is reflectedalsoinlowTOCcon- Early Triassic age, we prefer the designation ‘PTB extinction’ rather centrations (~0.1%) and intense bioturbation of these pale limestone than ‘end-Permian or latest Permian extinction’. beds, denoting unfavorable conditions for organic matter burial. After Beds 29–33 are clayey dolomitic micrites containing two illite- reaching a minimum in Beds 25 and 26, carbonate δ13Cvaluesagain montmorillonite claystones of volcanic origin: Bed 31 (9 cm) and shifted in a positive direction in Beds 27 and 28, a trend possibly related Bed 33 (5 cm). This is the survival stage of the PTB biotic crisis. to the contemporaneous transgression and oxic environmental condi- Macro-organisms maintained a low diversity (12 species) and a low 13 tions. Higher δ Ccarb values are found in correlative strata in PTB sections extinction rate (17%). Disaster species such as the paper pectinids globally (Korte and Kozur, 2010). Proxies for wildfire and terrestrial (claraiids) were abundant and occasionally covered whole bedding input show low values at this time, suggesting ameliorated conditions planes. Their stratigraphic ranges are usually rather narrow, as for in land areas. Oxygen isotope ratios measured on phosphate-bound Pseudoclaraia wangi (Yin, 1990). Although it is a volcanic ash layer, oxygen in conodont apatite decreased by ~2‰ relative to Beds 22 and Bed 33 yields less β quartz and zircons than Beds 25 and 28 (Yang 23, translating into a low-latitude ocean-surface warming of ~8 °C et al., 1991, ZCB4) and had less apparent influence on environmental (Joachimski et al., 2012). At many localities on the shallow-water and biotic change. H. Yin et al. / Earth-Science Reviews 115 (2012) 163–172 169

This interval is characterized by generally unstable, oscillating en- TOC. Data of many proxies are lacking hereafter, however macro- 13 13 vironmental conditions. Most proxy values (δ C, TOC and proxies of organism diversity remained low beyond Bed 39 and δ Ccarb kept redox condition, terrestrial input, and wildfire) shift toward deterio- stable until the Griesbachian–Dienerian boundary (Payne et al., rated environment, i.e., shift leftward in the columns of Figs. 1 2004). These features suggest that the second environmental crisis and 2. Moreover, the shifts of these indices are not smooth, but fluc- was restricted to Beds 34–38 and relatively ameliorating conditions tuate like those of Beds 23 and 24d. The 2-MHP index (cyanobacteria) were re-established relatively quickly thereafter. 13 exhibits small oscillating peaks; negative shifts of both δ Ccarb and 13 δ Corg reached 2–4%; analyses of pyrite framboids and aryl 4. Discussion and conclusion isoprenoids suggest at least periodically dysoxic to anoxic marine condition; TOC oscillated at a higher level than in Beds 27 and 28 i) The PTB environmental crisis waxed and waned through Beds 23 δ18 and O of conodonts yields the lowest value in Bed29. Ce/Ce* ratios to 40 of the Meishan GSSP. Changes in environmental conditions exhibit a second shift toward higher values (following one in Bed 25) can be summarized as follows: indicative of more reducing conditions (Zhao et al., 2009). These phenomena demonstrate a water body with high temperature and salin- ity, intermittently dysoxic, anoxic or even euxinic, with extremely Pre-crisis Beds 22 and lower: normal 8 low macrofossil diversity but relatively high microbial abundance. Crisis Episode 1 < Stage AðÞ Beds 23–24d : oscillating ðÞ– On the land, proxies of wildfire and terrestrial input into the ocean : Stage B Beds 24e 26 : crisis peak Crisis Episode 2 Stage Cð Beds 27–28Þ: ameliorating fluctuated, meanwhile it rapidly increased during this interval, pre- 8 < Stage AðÞ Beds 29–33 : oscillating saging a second crisis peak for land vegetation and soil erosion. It is ðÞ– : Stage B Beds 34 38 : crisis peak to be noted that beginning from this horizon, the lithology becomes Stage Cð Beds 39 and higherÞ: ameliorating dark colored and consists of 2 to 3 orders of Milankovitch cyclothems formed by rock types from argillaceous limestone to mudstone. This event sequence clearly shows a two-episode pattern of environmental changes through the PTB interval at Meishan, as previously 3.6. Episode 2, Stage B: crisis peak (Beds 34–38) reported by Xie et al. (2005, 2007). However, our data add more signifi- cant details to the patterns of environmental change during each episode, These beds constitute cyclothems of marls, calcareous mudstone, and namely: normal→oscillating→crisis peak→ameliorating, spanning ca. black mudstone (>8 m), becoming less calcareous and more muddy up- 0.2 Myr per episode of environmental change. ward. Macrofossils remain at the survival stage with very low total diversity. The disaster species of paper pectinids Claraia aurita-C. stachei ii) This two-fold pattern of environmental-biotic changes is not assemblage replaced Ps. wangi. Besides, there are many bedding planes restricted to Meishan but has been reported from other PTB fully covered by juvenile bivalves of unknown taxa, customarily named sections, including marine sections at Gartnerkofel, Austria as “Posidonia”. This interval is characterized by leftward shifting of most (Schönlaub, 1991) and Shahreza, Iran (Korte et al., 2004;as 13 15 environmental proxies in Figs. 1 and 2. Cyanobacteria, δ Ccarb, δ Norg, interpreted by Xie et al., 2007). Double negative excursions of aryl isoprenoids (green sulfur bacteria), terrestrial input, and wildfire all δ13C across the PTB, approximately at the meishanensis and reached maxima or minima for the PTB interval, recording a second envi- isarcica zones, respectively, have been reported in relatively ronmental crisis peak following the first one in Beds 24e–26. According to deep-water sections of South China, including Huangsi 13 13 the meanings of the proxies explained in previous text, it is likely that the (δ Corg, Xia et al., 2004), Daxiakou (δ Ccarb, Tong et al., 13 marine environment was hot and hypersaline, dysoxic-anoxic or euxinic, 2007), Shangsi (δ Corg, Riccardi et al., 2006), and Dongpan 13 probably due to intermittent anoxic water upwelling as shown in the (δ Corg, Zhang et al., 2006). In summarizing carbon isotopic highly oscillating pattern of aryl isoprenoids in Fig. 1.Further,land variation across the PTB worldwide, Korte and Kozur (2010) areas were arid and hot, with strong soil erosion and severe deforestation. claimed that the general trend consists of two minima, at Such conditions are in accord with the high temperatures inferred from about the PTB and the lower isarcica Zone, respectively, sepa- stomatal indices of seed ferns (Retallack, 2002), and with changes in rated by a slight positive shift. Although their first minimum river morphology (Ward et al., 2000) during the earliest Triassic. TOC (≈Bed 27 of Meishan) is a little higher than the observed min- also fluctuated during this interval, possibly reflecting a collapse of ma- imum at Meishan (Beds 25 and 26), it is worth noting that rine primary productivity across South China after the mass extinction multi-episodic environmental changes during the PTB interval and continuing for an extended interval into the Early Triassic (Algeo et may be a worldwide phenomenon. al., in press). Although causes of the second crisis are far from clear, two iii) The results of the present study demonstrate that the PTB crisis possibilities may be worth further investigation. First, it may be that was not a single, abrupt catastrophe. Rather, it represented a this second crisis rather the first one in Beds 24e–26 was triggered by sustained environmental crisis that waxed and waned in inten- eruption of the Siberian Traps, because unlike the first crisis which was sity, with intervals of relatively normal conditions separating closely related with acidic-intermediate volcanism directed from beyond intervals of environmentally harsh conditions. Furthermore, southwestern China, this crisis does not show an intimate relationship ocean redox conditions at a given time are not spatially uniform. with regional volcanism. The Siberian Traps may have its eruption age Euxinia rarely pervades the entire deep ocean (“superanoxia”; (U/Pb) dated to earliest Triassic rather than end-Permian (Kamo et al., Isozaki, 1997) but, rather, more frequently develops within 2003),andhavethestrengthtoproduceevenmoredeteriorationthan an unconfined oxygen-minimum zone at mid-water depths, the first crisis induced by regional volcanism. Second, it may be that the allowing the redox chemocline to migrate freely within the terrestrial environmental and biotic crisis extended later than the marine water column (e.g., Li et al., 2010). For this reason, the same crisis (De Kock and Kirschvink, 2004), which caused a second and even pattern of environmental-biotic changes may not be encoun- stronger peak of wildfire, terrestrial input, and accompanying marine en- tered in all PTB sections. Also, due to rapid and widespread re- vironmental changes. gression around the PTB, some sections may appear to record an abrupt and mono-episodic crisis as a consequence of erosion 3.7. Episode 2, Stage C: ameliorating conditions (Beds 39 and higher) or non-deposition of some strata. This situation exists on isolated platforms of the Guizhou–Guangxi region, which record a After Bed 38 the majority of recorded proxies returned to the right single negative δ13C excursion but are generally lacking the 13 side of Fig. 1, including cyanobacteria, δ Ccarb, terrestrial input and C. meishanensis and H. changxingensis zones. 170 H. Yin et al. / Earth-Science Reviews 115 (2012) 163–172

iv) The main phase of the PTB macrofaunal mass extinction (Bed Professors Tong Jinnan, Feng Qinglai, and Wang Yongbiao. Professor 25) happened somewhat after the beginning of environmental C. Henderson gave valuable advice on conodont names. We also 13 crisis (Bed 24e), at a point that δ Corg (and maybe also thank Shen Jun and Zhou Wenfeng who helped with logging in the 13 δ Ccarb) rebounds toward slightly more positive values. The lab and drawing the figures of the manuscript. This paper is a contri- end or epilogue of the PTB mass extinction (Bed 29) coincided bution to IGCP Project 572, Recovery of Early Triassic Ecosystems. with the beginning of an unstably oscillating environment. v) There is evidence for causal relationships among marine mi- Appendix A. Supplementary data crobes, oceanic environmental conditions, and land vegetation during the PTB crisis. Lipid biomarker records show that Supplementary data to this article can be found online at http:// geomicrobial functional groups (GFGs) at the PTB are composed dx.doi.org/10.1016/j.earscirev.2012.08.006. of cyanobacteria, anaerobic prokaryotes, and other autotrophic microbes. Nitrogen and sulfur isotope data indicate that aerobic References N2-fixing cyanobacteria, anaerobic ammonium-oxidizing bacte- fi ria, and anaerobic sul de-oxidizing bacteria are the main auto- Algeo, T.J., Twitchett, R.J., 2010. Anomalous Early Triassic sediment fluxes due to elevat- trophic GFGs during the PTB interval, while denitrifying ed weathering rates and their biological consequences. Geology 38, 1023–1026. bacteria, sulfate-reducing bacteria and methanogenic archaea Algeo, T.J., Ellwood, B.B., Nguyen, T.K.T., Rowe, H., Maynard, J.B., 2007. The Permian– Triassic boundary at Nhi Tao, Vietnam: evidence for recurrent influx of sulfidic are the main anaerobic heterotrophic GFGs. water masses to a shallow-marine carbonate platform. Palaeogeography, Palaeoclimatology, Palaeoecology 252, 304–327. GFGs exercised pronounced effects on the marine C–N cycles dur- Algeo, T.J., Chen, Z.Q., Fraiser, M.L., Twitchett, R.J., 2011. Terrestrial-marine teleconnections in the collapse and rebuilding of Early Triassic marine ecosystems. ing the PTB crisis. Higher proxy values for cyanobacteria and green Palaeogeography Palaeoclimatology Palaeoecology 308, 1–11. http://dx.doi.org/ sulfur bacteria (redox column; Fig. 1), accompanied by higher TOC 10.1016/j.palaeo.2011.01.011. concentrations (associated with reducing conditions), demonstrate Algeo, T.J., Henderson, C.M., Tong, J., Feng, Q., Yin, H., Tyson, R., in press. 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