Early Middle Triassic stromatolites from the Luoping area, Yunnan Province, Southwest China: Geobiologic features and environmental implications

Palaeogeography, Palaeoclimatology, Palaeoecology 412 (2014) 124–140

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Early Middle Triassic stromatolites from the Luoping area, Yunnan Province, Southwest China: Geobiologic features and environmental implications Mao Luo a,c,f, Zhong-Qiang Chen b,⁎, Laishi Zhao c, Steve Kershaw d, Jinyuan Huang e, Liangliang Wu f, Hao Yang b, Yuheng Fang b, Yuangeng Huang b, Qiyue Zhang e, Shixue Hu e, Changyong Zhou e, Wen Wen e, Zhihai Jia g a

School of Earth and Environment, The University of Western Australia, Western Australia 6009, Australia State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan 430074, China c State Key Laboratory of Geological Processes and Mineral Resources, China University of Geosciences, Wuhan 430074, China d Institute for the Environment, Halsbury Building, Brunel University, Uxbridge, United Kingdom e Chengdu Center of China Geological Survey, Chengdu 610081, China f State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 610081, China g School of Resources and Environmental Engineering, Hefei University of Technology, Hefei 230009, China b

a r t i c l e

i n f o

Article history: Received 28 December 2013 Received in revised form 7 July 2014 Accepted 28 July 2014 Available online 12 August 2014 Keywords: Stromatolite Rod aggregate Filamentous structures Early Middle Triassic Luoping SW China

a b s t r a c t An early Middle Triassic stromatolite deposit is documented from the Guanling Formation of the Luoping area, Yunnan, SW China. The Luoping stromatolite shows five types of constructional microbial forms in various magnifications: 1) typical stratified columnar structures, up to 20 cm high, with crinkled laminae. Dark coloured laminae, 1 mm thick, are composed of upright filamentous tubes, averagely 29.4 μm in diameter, showing a vertical growth fabric. 2) Laminoid fenestrae, 0.5–1 mm wide, and 3) prostrate filaments, which are reflected by strong fluorescence in sharp contrast to dolomite cement in fluorescent images. 4) Rod-like aggregates, 4.6–18 μm in diameter, composed of minute dolomite rhombs, are very common in stromatolitic laminae; they resemble present-day cyanobacterial trichome, and thus may represent putative fossilized cyanobacteria. 5) Moreover, small pits, coccoid-like spheroids, calcified biofilms, and fibrous structures are also common in stromatolitic laminae. The last two may represent calcified extracellular polymeric substances (EPS) that contributed to the development and lithification of stromatolites. Authigenic quartz grains are common and may also have involved biological processes in stromatolite formation. Of these microbial functional-groups driving accretion and lithification processes of stromatolite documented in literature, both lithified cyanobacteria/oxygenic phototrophs and possible sulfate-reducing bacteria (SRB), which induced microbial formation of dolomite and contributed to the accretion of the Luoping stromatolite, are suggestive of biogenic origin. The Luoping stromatolite differs from the Permian–Triassic boundary microbialites (PTBMs) in having abundant filamentous structures and growing in an oxic marine environment. Both sedimentary facies analysis and abundant fossilized cyanobacteria may indicate proliferation of oxygenic phototrophs in a normal, oxic habitat during the middle Anisian (early Middle Triassic), a period when hospitable environments, coupled with biotic diversification, prevailed in South China and set an agenda for the full recovery of marine ecosystems in middle–late Anisian. However, the post-extinction stromatolites and other anachronistic facies are not necessarily indicative of anoxic or oxic conditions, and their environmental settings are much more complex than previously thought. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Stromatolites usually occur as the laminated microbial deposits and are the most common life forms in marine ecosystems during the Precambrian (Awramik, 1971; Awramik and Margulis, 1974; Riding and Liang, 2005; Noffke and Awramik, 2013). They have also proliferated in the aftermaths of several major Phanerozoic mass extinctions and ⁎ Corresponding author. Tel.: +86 27 67883068; fax: +86 27 67881234. E-mail address: [email protected] (Z.-Q. Chen).

http://dx.doi.org/10.1016/j.palaeo.2014.07.028 0031-0182/© 2014 Elsevier B.V. All rights reserved.

still occur in present-day oceans and hypersaline lakes (Riding, 2006; Mata and Bottjer, 2011; Reitner et al., 2011). Increasing evidences show that stromatolites provide us a unique window to probe the history of photosynthesis, the evolution of early atmosphere and microbe-environment interactions in the geological past (Awramik, 1992, 2006; Kah and Riding, 2007; Kershaw et al., 2007, 2009, 2012; Mata and Bottjer, 2011, 2012; Noffke and Awramik, 2013). The abundance of stromatolite deposits has undergone conspicuous perturbations since the Proterozoic (Awramik, 1971; Riding and Liang, 2005; Riding, 2006; Mata and Bottjer, 2012; Noffke and Awramik,

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2013). This fluctuation was largely coupled with ecologic turnovers through geological time, characterized by major environmental changes and ecologic crises. For instance, two of the big five Phanerozoic mass extinctions (in Late Devonian and end-Permian, respectively) facilitated the proliferation of microbialites during biotic recovery interval (Mata and Bottjer, 2012). Microbial bloom is suggested to be coupled with extremely low metazoan diversity, which thoroughly decreased the grazing activity and competition and meanwhile decreased bioturbation that facilitated the development of microbialites (Mata and Bottjer, 2012). However, such inference is open to doubt because recent studies on both Permian–Triassic boundary microbialites (PTBMs) and modern stromatolite deposits reveal abundant infaunal metazoans living within microbial niches (Forel et al., 2012; Forel, 2013; Tarhan et al., 2013). Alternatively, the extremely high saturation rate in seawater may also have facilitated the growth of microbialites in Early Triassic (see Kershaw et al., 2012 and references therein). The resurgence of microbial communities represented by microbialites (stromatolites, thrombolites and other forms) occurred through the entire Early Triassic, with peaking in early Griesbachian, late Griesbachian–early Dienerian, Smithian, and late Spathian, respectively (Baud et al., 1997, 2005, 2007; Pruss and Bottjer, 2004; Pruss et al., 2006; Woods and Baud, 2008; Mata and Bottjer, 2012). The environmental range in which stromatolites developed in each stage, and the palaeoenvironmental implications of those biosedimentary structures have been documented in detail (Schubert and Bottjer, 1992; Sano and Nakashima, 1997; Wignall and Twitchett, 2002; Richoz et al., 2005; Hips and Haas, 2006; Pruss et al., 2006; Baud et al., 2007; Farabegoli et al., 2007; Kershaw et al., 2011; Mata and Bottjer, 2011, 2012; Ezaki et al., 2012). The PTBMs were deposited in a wide range of environments from shallow marine shelf to outer ramp settings and locally seamount environment (Sano and Nakashima, 1997; Hips and Haas, 2006; Kershaw et al., 2012). Their formation is often interpreted as the outcome of combined reduction in metazoan diversity and rising seawater saturation state in respect to CaCO3 (Riding and Liang, 2005; Kershaw et al., 2007, 2012; Woods et al., 2007). However, the biogenic mechanisms involved in microbialite formation still remain poorly understood. In particular, the functioning microbial groups and structures that contribute to the accretions of Early Triassic stromatolites have long been disputed. Recent studies show that the Anisian (early Middle Triassic) saw a stable ecosystem indicated by stable carbon isotopic excursion (Payne et al., 2004) and a full recovery of marine ecosystems (Hu et al., 2011; Chen and Benton, 2012). The Anisian stromatolite therefore may provide a comparison with their Early Triassic counterparts in composition and further indicate how the variation of oceanographic conditions influences the microbial development and precipitation of microbial carbonate. A comparative study may also shed light on the formation mechanism of the PTBMs and microbialites from other intervals of the Early Triassic. Here we report a new stromatolite deposit from the early Middle Triassic of the Shangshikan section of Luoping County, Yunnan Province, Southwest China (Fig. 1). This study aims to (1) describe microbial structure and composition of the Luoping stromatolite; (2) elucidate stromatolite's accretion and formation processes; (3) compare the Luoping stromatolite with the Early Triassic and modern counterparts and (4) discuss in a broad context its possible palaeoenvironmental implications. 2. Geological, stratigraphic and palaeoenvironmental settings 2.1. Geological and stratigraphic settings The studied section is located 2 km northeast of the Daaozi Village, 20 km southeast of the Luoping County town, eastern Yunnan Province, Southwest China (Fig. 1). During the early Middle Triassic, the Luoping area, together with border areas between eastern Yunnan and western Guizhou Provinces, was located on the southwestern part of the Yangtze

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Platform and separated from the Nanpanjiang Basin by a shoal complex (Feng et al., 1997; Lehrmann et al., 2005; Enos et al., 2006). Within the vast Yangtze Platform interior region several spatially and temporally separated intraplatform basins or depressions with exceptional fossil preservations, namely the Panxian, Luoping, Xingyi, and Guanling, have been recognized from the late Anisian, late Ladian and Carnian intervals, respectively (Hu et al., 2011; Benton et al., 2013). These basins shared similar features, including a restricted circulation, density stratification of the water column, and dysoxic to anoxic bottom water during the burial of these exceptionally preserved vertebrate faunas in various stages of the Triassic (Benton et al., 2013). In Luoping, abundant marine reptile faunas were preserved in a basinal setting represented by the upper part of Member II of the Guanling Formation (Hu et al., 2011). The highly fossiliferous, dark coloured micritic limestone of the upper part of Member II can be traced over an area of some 200 km2 (Benton et al., 2013). However, Member I and lower and middle parts of Member II of the Guanling Formation record similar successions over the entire Yangtze Platform interior region in the Yunnan–Guizhou bordering areas (Enos et al., 2006). Therein, the stromatolite-bearing unit belongs to the second member of the Middle Triassic Guanling Formation (Zhang et al., 2008). The Guanling Formation is subdivided into two members. Member I is dominated by siliciclastic sediments representing deposition in subtidal to intertidal environment (Hu et al., 1996), while Member II by micritic limestone, bioclastic limestone, oncoidal limestone and dolomite in the lower and middle parts, and by black muddy limestone, cherty limestone, and grey dolomite in the upper part (Fig. 2). Integration of sedimentary facies analysis, palaeoecology and taphonomy indicates that the lower and middle parts of Member II were deposited in the relatively open shallow marine settings, while the upper portion of the member was deposited in a low energy, semi-enclosed intraplatform basin setting with influence of episodic storms (Hu et al., 2011). The Guanling Formation in the Luoping area, overall, records an up-deepening succession (Zhang et al., 2008). Conodont Nicoraella kockeli Zone has been detected from the horizons, about 30 m above the stromatolite-bearing horizon at the upper part of Member II (Fig. 2). This conodont zone includes elements such as Nicoraella germanicus, N. kockeli and Cratognathodus sp., indicative of a Pelsonian age of the middle Anisian (Zhang et al., 2009). The underlying Member I of the Guanling Formation yields bivalves Myophoria (Costatoria) goldfussi mansuyi Hsü, Unionites spicatus Chen, Posidonia cf. pannonica Moj, and Natiria costata (Münster), and contains several clay beds. The bivalve assemblage is of early Anisian age in South China (Zhang et al., 2008), while the clay beds have been regarded as correlation markers of the base of the Anisian in southwest China (Enos et al., 2006; Zhang et al., 2009). Given its higher stratigraphic position and just beneath the Pelsonian conodont zone, the stromatolitic unit is tentatively assigned to the Bithynian of early–middle Anisian in age.

2.2. Palaeoenvironmental analysis At the logged section, Member II of the Guanling Formation comprises Units 1–4 (Fig. 2). Unit 1 (0–38 m) is characterized by thickbedded dolomitic limestone in the lower part and alternating dolomitic limestone and micrite at the middle and upper parts. Dolomitic limestone is partly fossiliferous and has a sutured mosaic fabric (Fig. 3A) or micritic texture, with framboid pyrites being commonly present at some horizons (Fig. 3B), indicating generally dysoxic to anoxic conditions. Dolomitization tends to obliterate the original physical sedimentary structures of the rock, making the very fine-grained sediments representing either deep basinal facies or shallow restricted lowenergy carbonate platform facies. Given that Member I consists mainly of siltstone and sandstone of intertidal to subtidal zones, Unit 1 of the lower Member II was unlikely deposited in a relatively deep basinal

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Fig. 1. A, Middle Triassic palaeogeographic map of South China showing the palaeogeographic setting of the Luoping area during that time [base map was modified from Feng et al. (1997)]. B, Location of the studied Shangshikan section in the Luoping County, eastern Yunnan Province, SW China.

setting, but instead may represent a low-energy, shallow carbonate platform facies. Unit 2 (38–68 m) is composed of bioclastic limestone, thick-bedded muddy limestone, and medium-bedded oncoidal packstone at the lower part (Fig. 3C–F), and dark grey to yellowish-grey, medium- to thick-bedded, laminated micritic limestones, bearing cherty nodules and submarine erosional surfaces at its upper part. The basal bioclastic limestone usually possesses a packstone texture, while the muddy limestone has stromatolitic texture and yields stromatolite deposit that is

the focus of this study. The former indicates a normal, open platform environment, while the latter lithology may represent sedimentation in a relatively low energy, subtidal zone below storm wave base zone. The packstone–wackestone of the lower part of Unit 2 is composed of fragmented fossil skeletons that underwent recrystallization (Fig. 3C, F). Coarsely grained texture of oncolites may indicate a relatively high energy shoreface facies. The medium-bedded micritic limestone of the upper part of Unit 2 usually possesses a wackestone texture, while thick-bedded limestone

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Fig. 2. Lithology and palaeoenvironmental analysis of Member II of the Guanling Formation at the logged section. Note the described stromatolite occurs at the upper part of Unit 2 (black arrow), and the exceptionally preserved Luoping biota in Unit 3.

has a packstone texture, and contains abundant conodonts of Nicoraella kockeli Zone (Zhang et al., 2009), which usually live in a normal shallow sea habitat. Moreover, thick-bedded limestones are normally graded,

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and with pronounced submarine erosional surface that shows evidence of storm activity and indicates a very shallow platform environment with oxic bottom water. Thus, both lithofacies and palaeoecology suggest that Unit 2 overall represents an open, shallow platform to proximal ramp environment (Bai et al., 2009). Unit 3 (68–78 m) is composed of dark grey, thin-bedded, laminated dolomitic mudstone and micritic limestone at the lower part (Fig. 3G), light grey thick-bedded muddy limestone at the middle part, and dark grey, thin-bedded, laminated muddy limestone at the upper part (Zhang et al., 2009). Both the lower and upper thinbedded, laminated limestones are enriched in fossil fishes, reptiles, arthropods, mullascans, and plants, and have been referred to as the lower and upper Luoping biota horizons, respectively (Zhang et al., 2008; Hu et al., 2011). The dolomitic mudstone of the basal Unit 3 is characterized by millimetre-scale laminations and submarine erosional surfaces (Fig. 3H) and yields some fossil fishes, molluscs, and distinctive reticulated ridge structures, sharing the same genesis as microbial mats (Luo et al., 2013). The lower thin-bedded, laminated limestones are characterized by fine laminations, cherty nodules, and slump structures, and also contain horizontal burrows and abundant exceptionally marine vertebrate fossils (Hu et al., 2011). They usually possess a wackestone to micritic texture, which, together with small, horizontal burrow-dominated ichnoassemblage, indicates a low energy, semiclosed setting with dysoxic to anoxic bottom water, as suggested by similar ichnoassemblage in Early Triassic (Chen et al., 2011). Moreover, slump structures may indicate the existence of a gentle slope at the distal ramp (Benton et al., 2013). The middle muddy limestone bear cherty nodules and slump structures, and yield few body fossils of fishes, reptiles and invertebrates, but are highly bioturbated and contain abundant complex and vertical burrows, namely Diplocraterion, Thalassinoides and Rhizocorallium, indicative of an oxygen-enriched ichnofacies in late Early Triassic (Chen et al., 2011). The upper laminated micritic limestones are similar to the lower laminated limestones in lithology and fossil assemblages, although lacking slump structures and cherty nodules. They are also finely laminated and possess a wackestone to micritic texture. Both lithofacies and fossil assemblages indicate a low energy, semi-enclosed intraplatform basin environment (Benton et al., 2013). The overlying Unit 4 (78–90 m) is dominated by light grey, massive limestone, which usually has packstone texture and yields abundant normal shallow marine faunas, indicative of a normal platform setting (Bai et al., 2009). Integration of sedimentary facies analysis, palaeoecology and taphonomy indicates that Unit 1 was deposited in a low energy, semienclosed platform, indicated by the prevailing micritc texure in the rocks and episodic presence of framboid pyrites. Unit 2 represents an open platform to proximal ramp environment with oxic conditions in which bioclastic packstone, stromatolites, and oncoids were deposited. The Luoping area became a low energy, semi-enclosed distal ramp to intraplatform basin setting with influence of episodic storms during the deposition of Unit 3 (Hu et al., 2011). It should also be noted that conodonts are common in the upper part of Unit 2, but very few have been found from Unit 3. Since conodonts are typical elements of open marine environment, it is reasonable to assume that the Luoping basin became semi-restricted and stagnant, changing from a semi-enclosed basin at the time of the lower part of Unit 3, after a short time of reoxygenation indicated by the bioturbated limestone of middle Unit 3, to a deep, relatively stagnant basin at the time of the upper part of Unit 3. The occurrence of conifer debris and terrestrial animals (e. g. millipedes) indicates a location close to land (Benton et al., 2013). The overlying massive limestone of Unit 4 indicates a normal platform environment and the end of the restricted basin (Bai et al., 2009). To sum up, Member II of the Guanling Formation of the Luoping area represents depositional environments varying from a semi-restricted platform (Unit 1) to an open platform to proximal ramp (Unit 2), and

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Fig. 3. Photomicrographs and field photos showing selected rock types of Member II of the Guanling Formation. A–B, Photomicrographs showing dolomitic limestone with sutured mosaic fabric (A) or micritic texture, with framboid pyrites being commonly present at some horizons (B); both from Unit 1. C, Photomicrograph of dolomitic wackestone beneath columnar stromatolite (Unit 2). Note bioclasts were usually recrystallized and altered to coarse dolomite. D–E, Inter-stromatolite oncoidal wackestone–packstone with distinct oncoids, bivalve shell fragments and foraminiferal tests from Unit 2. F, Bioclastic packstone–wackestone capping the columnar stromatolite from Unit 2. G, Field photos showing the thin-bedded dolomitic mudstone yielding fine, horizontal stratification (black arrows) at the basal Unit 3. H, Photomicrograph showing the millimetre-scale laminations with pronounced submarine erosional surfaces (black arrows) within dolomitic mudstone from Unit 3.

to a semi-enclosed distal ramp to shelf basin (Unit 3), and then became a normal, open platform (Unit 4) again. Of these, the Luoping stromatolite grew in an open platform environment. 3. Methods Both polished slabs and petrographic thin sections were made to examine internal fabrics and diagenetic features of the stromatolite. Freshly broken and polished chips were prepared for a micro-analysis under scanning electron microscope (SEM). Samples were cleaned first by deionized water and then etched with 0.5% hydrochloric acid

for 3–5 s, followed by a second rinse by deionized water and ethyl alcohol. Some samples for SEM analysis were polished with 200 mesh diamond dust before chemical etching and cleaning. Samples were all coated with gold for a surface texture analysis and Energy Dispersive X-ray Spectrometry (EDS) analysis using Zeiss VP FESEM 1555 in the Centre of Microscopy, Characterization and Analysis (CMCA) at the University of Western Australia. Fluorescent imaging analysis is undertaken to check for the distribution of residual organic matter in stromatolite using a fluorescent microscopy equipped at the China University of Geosciences (Wuhan), China. Aromatic and certain conjugated organic molecules can cause

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organically activated luminescence, making residual organic matter the most important activators of fluorescence in calcite and dolomite (Cuif et al., 1990; Reitner and Neuweiler, 1995; Russo et al., 1997, 2000; Mastandrea et al., 2006). Fluorescence was induced by a Hg vapour lamp linked to an imaging microscope equipped with bandpass filter with wavelength from 450 to 490 nm. When containing abundant organic matter, the rock appears strong fluorescent light in both green and purple exciting lights. In contrast, when containing few or lacking organic matter, the rock appears very weak or does not appear any fluorescent lights (Cuif et al., 1990; Reitner and Neuweiler, 1995; Russo et al., 1997, 2000; Mastandrea et al., 2006). Terminology and methods documenting stromatolite microfabrics follow Shapiro (2000) who observed microbial fabrics at three different scales. 4. Results 4.1. Non-stromatolite facies associations The substrate of stromatolite is 15 cm thick and comprises dolomitic bioclastic limestone, which has wackestone texture (Fig. 3C). Fossil fragments are mostly recrystallized. The matrix is dominated by microbial limestone. Inter-stromatolite facies is dominated by oncoidal packstone–wackestone, yielding fragmented stromatolites and various shell fragments of bivalves, foraminifers and crinoids, which are mostly coated with microbial micrite and microbes to form various oncoids (Fig. 3D–E). Bioclasts and peloids are commonly present in this facies. Capping facies of the stromatolite is composed of bioclastic packstone–wackestone and oncoidal packstone. The former is dominated by microbial filaments and microbial micrite with few recrystallized fossil fragments (Fig. 3F), while the latter is characterized by abundant irregularly shaped oncoids. Capping facies rock has a thickness of no more than 20 cm.

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filamentous structures interweave to form consortia, which are filled with micrites and microsparites (Fig. 6C). Individual filamentous tubes are circular in plan view (Fig. 5C, black arrows) and mostly straight, but slightly curved occasionally in side view. Diameters of upright filamentous tubes range from 20 to 30 μm, with an average value at 29.4 μm based on measurements of 37 individuals. Filamentous fabrics are composed of microsparite in the core, and their walls are defined by micrites (Fig. 6B–C). The prostrate filamentous tubes are usually strongly curved, crinkled and wavy, but, overall, distributed nearly parallel to laminae (Fig. 6D–F). Individual filamentous structures have similar sizes to the upright tubes and are also characterized by the microsparitic cores and micritic walls (Fig. 6F). They also interweave to form consortia (Fig. 6D–F). Light grey laminae are 2–5 mm thick and contain laminoid fenestrae (Figs. 5A, 6A). The irregularly shaped fenestrae, around 0.5–1 mm wide, are commonly present in some interlayed areas and parallel to laminae (Figs. 5A, 6D–F). These fabrics exhibit micritic texture (Fig. 6D–F). Under fluorescent microscope, areas composed of prostrate filamentous structures showed a strong fluorescence under blue exciting light. This is contrasted with none or very weak fluorescence of coarsely grained dolomite cement (Fig. 7A–B). Moreover, the micritized areas within dark laminae, although lacking the well-preserved filaments, also showed a strong fluorescence under blue exciting light (Fig. 7C–D). Strong fluorescence indicates the existence of abundant organic matter in those microfabrics (Cuif et al., 1990; Reitner and Neuweiler, 1995; Russo et al., 1997, 2000; Mastandrea et al., 2006).

4.3. Microstructures

4.3.1. Rod aggregates Under SEM, well-preserved, rod-like aggregates are commonly present in the dark laminated layers of stromatolite (Fig. 8B–F). This is in sharp contrast with the micro-textures in the substrate of stromatolite, which only showed floating dolomite rhombs in carbonate matrix (Fig. 8A). Individual rods are straight to slightly curved in outline (Fig. 8B, D). They are mostly scattered within laminae, but aggregate locally to form rod colonies (Fig. 8C–F). When clustering together, these trichome-like rods interwove to form 3-dimensional consortia, in which subrounded pores interwoven by filamentous rods are conspicuous (Fig. 8F). Diameters of rod-like filamentous structures range from 4.6 to 18 μm, with an average value at 8.5 μm based on measurements of 26 individuals. In plan view, each rod usually shows a center filled with minute dolomite rhombs (Fig. 8D). Vertical cross sections show that dolomite grains are all euhedral rhombs that are no more than 5 μm long (Fig. 8B–D, F). They form a mosaic fabric or are intensively stacked, with rhombs interpenetrating one another to form rods (Fig. 8B–C). Dolomitic rods are usually well-orientated, which are in sharp contrast to the surrounding dolomite grains that are irregularly arranged. The contact between the two is rather distinct (Fig. 8B–C). When rod-like filamentous structures are well-preserved, the sheathed mould is pronounced (Fig. 9), although the center was usually filled with coarse dolomite grains. The center is surrounded by a sheathed rim layer, which is 2 μm thick (Fig. 9). In particular, nanosized dolomite grains are in proximity with those dolomite rhombs comprising rods.

Under polarizing microscope, planar and columnar stromatolites are characterized by undulating laminations with a few skeletal grains (Fig. 5A). The overlying oncoidal packstone caps the laminated stromatolites (Fig. 5D–E), with a distinct contact between the two. Stromatolitic laminae comprise alternations of dark-grey, laminated micritic dolomite and light-grey microsparitic dolomite. Dark-grey laminated layers, about 1 mm thick, are characterized by copious filamentous structures, which include upright and prostrate types. The upright filamentous tubes usually originate from narrow light-grey layers, which are filled with microsparite, and penetrate the entire dark laminated layers. They are usually perpendicular to laminae and show an up-straight growth fabric (Figs. 5B–C, 6A–C). These upright

4.3.2. Rounded pits Small, rounded pits are also commonly present in the dark laminated layers of stromatolite (Fig. 10A). They are circular in outline and 20–45 μm in diameter with a mean value of diameters at 28.5 μm based on measurement of 16 individuals. These rounded pits are usually 3–4 μm deep with slightly flat floor. They were filled with micritized dolomites. Given the large size and slightly flat floor, these pits could not be impressions of either filamentous rods, as described above, or small spheroid balls (see below). Instead, the similar size and flat floor suggest that those pits could be impressions of ends of either upright filamentous tubes or prostrate filamentous structures observed under petrographic microscope.

4.2. Mega-, macro- and mesostructures of Luoping stromatolite Stromatolite horizon from outcrop exhibits typically stratified columnar structures, contrasting with surrounding rocks (Fig. 4A– B). Stromatolite columns are up to 30 cm high and can be traced laterally around 12 m in distance. In cross section, stromatolitic laminae are crinkled and laterally linked. These initial, space-linked hemispheroids at the base pass into discrete, vertically-stacked hemispheroids upwards to form columnar forms (Fig. 4A-B). Discrete, vertically stacked hemispheroids are composed of closelylinked hemispheroidal laminae that are 2–4 mm thick (Fig. 4B). Stromatolite columns are usually 3–5 cm in diameter and grow to a maximum height of 20 cm. In polished slabs, the crinkled to columnar laminae are characterized by vertically-stacked hemispheroids passing into close-linked hemispheroids by upward growth (Fig. 4C). In plan view, discrete spheroids show a structure that consists of concentrically-stacked hemispheroids, 1–3 cm in diameter (Fig. 4D–E).

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Fig. 4. Field photos showing macro-structures of the stromatolite. A, Field view showing domal structures and laminae in stromatolite; hammer is 35 cm long. B, Upright, branching stromatolite columns with well defined laminae (outlined by white lines). C, Polished slab showing columnar stromatolite structures and pronounced alternations of dark and light coloured laminae. Note boxed area A was sampled for SEM microanalysis, while boxed area b was sampled for thin section observation. D, Plan view of stromatolite columns. Note columns preserved as rounded reliefs (white arrows). E, Close-up of column top in view D on a polished slab showing spheroidal structures.

4.3.3. Spheroid balls Small spheroid balls are commonly present in rod aggregates in the stromatolitic laminae (Fig. 10B, D). They were usually found in association with rods and biofilms (see below). These round spheroids were clustered by many minute rhombic dolomite crystals. These spheroids are 10–12 μm in diameter.

4.3.4. Calcified biofilms and fibrous structures Another feature typifying the dolomitic rod aggregates is the common presence of calcified biofilms (Fig. 10C, E–G). These biofilms form fibrous structures and thin films, which cover or coalesce minute

dolomitic rhombs. Biofilms are commonly present and usually preserved in association with rod aggregates (Fig. 10C–E). 4.3.5. Authigenic quartz Quartz crystals are also pronounced in stromatolite microstructures. They coexist with minute dolomite rhombs within stromatolitic laminae. Quartz crystals are characterized by euhedral outlines and pronounced crystal structures on both ends (Fig. 10H). Quartz crystals vary from silt to fine sand in size and occur over stromatolite laminae. They also cluster occasionally or touch other fossil skeletons (Fig. 10H) with the undulated contact between quartz and fossil skeletons. Euhedral quartz crystals show no signs of abrasion, scatter

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Fig. 5. Photomicrographs of the Luoping stromatolite. A, Thin section of boxed area b in Fig. 4C showing domal structures defined by well-preserved laminations, with dark coloured laminae alternating with light coloured laminae. The orange line represents the boundary between domal stromatolitic bindstone and the overlying oncoidal packstone. B, Close-up of boxed area in view A showing the upright, thin filaments and fenestrae represented by small, rounded holes in dark laminae of stromatolite. C, Close-up of boxed area in view B showing both upright filaments in life position (white arrows). Circular structures (black arrows) represent filamentous structures in plan view. D, Close-up of boxed area in view A showing oncoidal packstone of stromatolite-capping facies. Note irregular bioclasts were coated with micrite. E, Bioclastic packstone–wackestone of stromatolite-capping facies showing irregularly shaped clotted structures and bioclasts. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 6. Photomicrographs of the Luoping stromatolite. A, Close-up of boxed area in Fig. 5A showing the well-preserved filamentous tube colony comprising individual upright filaments in life position (white arrows) and fenestrae (black arrows) in dark laminae. B–C, Close-ups of individual upright filaments and filament sheath indicated by white arrows in view A in various scales showing upright filaments in growing position; view C shows individual filamentous tube possesses a microsparite core surrounded by dark micrite walls (black arrows). D, Closeup of boxed area in Fig. 5A showing that the clotted fabrics formed erratic filamentous consortia, in which filaments were arranged prostrate. E–F, Close-ups of central area in view D in various scales showing prostrate filament sheath and clotted structures exhibiting micritic textures.

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Fig. 7. Filament-rich and clotted fabric areas in dark laminated layers of stromatolite in transmitted light and fluorescent light. A, Filament-rich and irregularly clotted fabrics are composed of filaments in laminae of the stromatolite. B, The same area as that in view A but captured by fluorescent microscope. Note the strong fluorescent lights in green colour showing clearly filamentous structures. C–D, Another view of clotted fabrics in dark laminae of stromatolite in both transmitted and fluorescent lights. Although filaments were weakly defined in transmitted light image (C), strong fluorescence was also observed in proximity with micrites. Coarsely grained dolomite cement (defined by green line area in C) was poorly responded to fluorescent light (D). Note views B and D were captured under blue exciting light (wavelength 450–490 nm). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

in stromatolite laminae and do not concentrate to form layers or horizons, which are typical of detrital quartz grains. These crystals therefore are likely authigenic in origin, showing no sign of transportation. 5. Discussion 5.1. Biogenetic origin and geobiologic process associated with accretion of the Luoping stromatolite Increasing evidences show that various microbial colonies coexisted in different layers within stromatolite laminae. They initiated various metabolic processes coupling with one another (Dupraz et al., 2004). These bio-reactions control bio-carbonate precipitation and dissolution and subsequently drove accretion and lithification of stromatolite. Six typical functional-groups have been found to be key components driving those processes (Dupraz and Visscher, 2005; Visscher and Stolz, 2005, Dupraz et al., 2009). They are (i) oxygenic phototrophs (cyanobacteria) that use light energy to generate adenosine triphosphate (ATP) and fix carbon; (ii) anoxygenic phototrophs that use reduced sulfur to generate ATP; (iii) aerobic heterotrophic bacteria that consume organic carbon and O2 for a respiration and living, while producing CO2 needed in photosynthesis at the same time; (iv) fermenters that use organic carbon or sulfur compounds for a metabolism; (v) anaerobic heterotrophs (predominantly SRB) that consume organic carbon to carry out sulfate reduction process; (vi) sulfide oxidizing bacteria that oxidize reduced sulfur by consuming O2 while fixing CO2. All bio-reactions together contribute to the establishment of a semi-closed system in stromatolite that enables to maintain efficient element cycling and highest metabolic rates (Visscher et al., 1998; Dupraz et al., 2004). These bio-reaction processes were summarized based on modern stromatolite studies because prolific living bacteria consortia and biosignatures can be directly detected and observed in situ. However, it is not always the case that all of these six bio-

reactions are universally present in extant microbial mat system because microbial metabolism within microbial mat varies strongly under different sedimentary systems and environments (Reid et al., 2000; Baumgartner et al., 2006; Dupraz et al., 2009; Heindel et al., 2012; Voorhies et al., 2012). Biosignatures from ancient lithified examples are crucial in understanding genesis and accretion process of stromatolites in the geological past (Noffke and Awramik, 2013). For example, Heindel et al. (2012) studied a Holocene microbialite and detected the existence of sulfate reducing bacteria (SRB) and their involvements in carbonate precipitation. Herein, the Luoping stromatolite provides evidence for at least two key functioning groups involved in stromatolite accretion processes. 5.1.1. Lithified cyanobacteria and oxygenic phototrophs in stromatolite Although upright and prostrate filamentous tubes and rod aggregates are rather common in undulating laminae of the Luoping stromatolite, they differ clearly from one another in sizes. The former tubes have an average diameter of 28.4 μm, whereas the diameter of rods has a mean value of 8.5 μm. Although these filament sizes were measured under petrographic optical microscope and SEM, respectively, those large filamentous structures possess similar sizes to the rounded pits, ranging from 21 to 42 μm in diameter under SEM (Fig. 10A). Morphologically, these rounded pits are very similar to modern examples of mineralized capsules from the Lake Vai Si'I, Tonga (Kaźmierczak and Altermann, 2002, Fig. 1B, D), whose diameters range from 15 to 35 μm. The pits in Luoping stromatolite often form small groups, which are also typical for mineralized capsules from modern microbial mats (Kaźmierczak and Altermann, 2002). Accordingly, two types of filamentous structures co-existed in the dark laminae of Luoping stromatolite. Regardless of classification of these different filaments, these filament-rich layers usually show strong fluorescence under fluorescent microscope (Fig. 7A–D), indicating the existence of rich organic matter, as detected in other stromatolitic dolomites (Cuif et al., 1990; Reitner

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Fig. 8. SEM images of micro-fabric and filamentous structures detected in dark laminae of the Luoping stromatolites. A, Floating dolomite rhombs on carbonate matrix. B–D, Individual filamentous rods (B) and rod aggregates (C–D). Note the rod aggregates in D (white arrows) preserved in various orientations. Dashed circle in D denoted the plan view of rod, which is filled by micron-sized dolomite crystals. E, Filamentous rod consortia from dark laminated area in stromatolite in which filaments wove to form subrounded pores. F, Close-up of boxed area in view E showing subrounded pores woven by filamentous rods. Samples for SEM imaging were etched with HCl. A–D were secondary electron images. E–F were backscattered electron images.

and Neuweiler, 1995; Russo et al., 1997, 2000; Mastandrea et al., 2006). Petrographic analysis shows that those organic matter likely concentrate in the dark micrites of tube walls (Fig. 7B, D). These filamentous structures therefore may possess organic matter-rich tube walls. SEM imaging also shows that rods, pits and spheroid balls were stuck with nano-sized dolomite grains, which further recrystallized to form micron-sized rhombs. When clustering together, these dolomitic rhombs constructed mineralized rod-like structures that interwove to form the 3-dimensional consortia. The latter structures resemble remarkably the cyanobacterial trichome from presentday microbial mats (Brigmon et al., 2008, Fig. 5, 14A). Such well-arranged, rod-like aggregates of minute rhombic dolomite crystals have also been observed from the Pliocene lacustrine dolomite of La Roda, Spain (García Del Cura et al., 2001) and Miocene carbonate stromatolite in the Caltanissetta Basin of Sicily, Italy (Oliveri et al., 2010). The Spanish dolomite aggregates have been interpreted as biogenic structures (García Del Cura et al., 2001), while the Italian example of elongate filaments were explained as the fossilized Beggiatoa-like sulfur bacteria (Oliveri et al., 2010). The Luoping rod aggregates are likely the fossilized forms of cyanobacteria. This inference is derived from similarity in size and interweaving pattern between the Luoping rods

and fossilized cyanobacteria in literature (Golubic et al., 2000; Seong-Joo et al., 2000) and modern stromatolites from hypersaline lakes (Kaźmierczak et al., 2011). If so, these putative fossilized cyanobacteria may represent primary producers that constructed the Luoping stromatolites. Therein oxygenic phototrophs may have contributed to carbon fixation and oxygen production and facilitated other microbial-functioning groups to conduct their metabolism. It has been suggested recently that certain filamentous cyanobacteria species (e.g. Phormidium) in microbial mats can thrive in low-O 2 environment and perform primary production through anoxygenic photosynthesis other than oxygenic photosynthesis (Voorhies et al., 2012). Precautions, however, need to be taken when inferring metabolic functions of filamentous cyanobacteria in the fossil record (Voorhies et al., 2012). Nevertheless, these cyanobacteria mat communities studied by Voorhies et al. (2012) were not lithified, and thus there are also uncertainties on the lithification potential of anoxygenic photosynthetic cyanobacteria (Phormidium). Thus, it is more likely that the fossilized filamentous cyanobacteria represent oxygenic phototroph rather than anoxygenic phototroph. This inference is also strengthened by the vast evidence that revealed prolific examples of lithified filamentous cyanobacteria mostly from photosynthetic microbial

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Fig. 9. Close-up of an individual rod in the pore under SEM. The rod in the centre area has a sheathed outer layer, which is 2 μm thick (rim boundary is defined by dashed white lines). The centre of the rod was filled with coarse dolomite crystals (dashed white arrow). Note that the nano-sized dolomite rhombs (white arrows) were stuck on rod during the preliminary phase of the growth.

mats (Merz-Preiβ, 2000; Brigmon et al., 2008; Planavsky et al., 2009). 5.1.2. Role of EPS and sulfate-reduced bacteria (SRB) on dolomite formation in Luoping stromatolite Although both bacteria sulfate reduction and a microbial process mediating dolomite precipitation in subsurface environment (sensu Wright and Wacey, 2005) have not been directly observed, several lines of evidence indicate the existence of the SRB-induced microbial formation of dolomite in the Luoping stromatolite. As stated above, the Luoping stromatolite has abundant nano-sized rhombic dolomites that formed rod aggregates. Comparable structures have been interpreted as a result of microbial metabolism caused by bacteria sulfate reduction elsewhere (García Del Cura et al., 2001; Oliveri et al., 2010). Moreover, authigenic quartz grains in conjunction with minute rhombic moulds are also rather abundant in stromatolitic laminae. The formation of euhedral quartz crystals has been interpreted as a result of lowered pH by sulfide oxidizing, in which sulfide was produced by sulfate reduction (Chafetz and Zhang, 1998). As a result, the growth of euhedral authigenic quartz may indicate the bacteria sulfate reduction and sulfide oxidation processes (Friedman and Shukla, 1980), which facilitated adjacent minute dolomite rhombs to form rod aggregates. It should also be noted that the possibility that those euhedral quartz originated from volcanism cannot be ruled out because volcanic eruptions have also produced many morphologically same authigenic quartz recorded in the Permian–Triassic rocks in South China (Yin et al., 1992). Volcanism has been very active through the Early–Middle Triassic in South China (Chen and Benton, 2012). Minute dolomite rhombs were associated closely with fibrous materials and biofilms. Mucilaginous materials or biofilms covered minute rhombic dolomite grains and coalesced different rod individuals (Fig. 10C, E, G). They may represent the calcified extracellular polymeric substances (EPS) produced by microbial communities that contribute to the development and lithification of stromatolites (Dupraz et al., 2004, 2009). Fibrous fabrics have also been usually interpreted as the residues

of deflated EPS, which boosted the formation of unstructured fibrils and deflated films on dolomite grain surfaces (Renaut et al., 1998). In fact, EPS have played a crucial role not only in calcium carbonate precipitation (Riding, 2000; Dupraz et al., 2004, Dupraz and Visscher, 2005; Braissant et al., 2007; Bontognali et al., 2010), but also in dolomite precipitation process in subsurface condition (Bontognali et al., 2010; Krause et al., 2012). This is because EPS might have served as a template to induce the dolomite formation directly from solutions, and extracellular polymeric substances were visualized as an alveolar organic network, within which the precipitation of dolomite was initiated (Bontognali et al., 2010). The ability of EPS to preferentially bind Mg and Si over Ca may play a crucial role in overcoming the kinetic barriers that prevent nucleation of dolomite at subsurface environment (Bontognali et al., 2010). Krause et al. (2012) further emphasized that precipitation of a high Mg/Ca molar ration carbonate crystal that associated with EPS excreted of SRB provides templates for nucleation of stoichiometric dolomite. SRB therefore played an important role in this process (Baumgartner et al., 2006; Heindel et al., 2012). In the Luoping stromatolite, EDS analysis of two different dolomite components (Fig. 11A–B) suggests that the growth of dolomite rod aggregates might have followed the EPS template mechanism mentioned above. Mineralogical compositions of minute dolomite rhombs are rich in Mg and Ca, with small percentage of Si (Fig. 11b). This is probably due to the subsequent Ca incorporation within the previously formed Si–Mg phase that was encapsulated by EPS matrix. In addition, the intimate relationship between biofilms, representing EPS residues, and rod aggregates of dolomite also supports the view that EPS may have played a crucial role in the formation of primary dolomite. It is also true that minute dolomite rhombs, forming the filamentous rods in Luoping stromatolite show neither ‘bacterial shapes’ nor dumbbell forms, both of which are usually considered direct evidences indicating a microbial origin of dolomite (Vasconcelos et al., 1995; Vasconcelos and Mckenzie, 1997; García Del Cura et al., 2001). This is probably, in part, due to progressive dolomitization and subsequent recrystallization during shallow and deep burial

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Fig. 10. SEM images showing spheroids, thin biofilms and fibrous slimes in contact with minute dolomite and rod aggregates. A, Spherical pits that coexisted with rods in dark laminae. B, Coccoid-like spherical structure composed of micron-sized dolomite rhombs. C, Mucilaginous fibres coalescing rod aggregates. D, Close-up of upper rectangular area in view C showing minute dolomite grains forming a spheroid. E, Close-up of lower rectangular area in view C showing filamentous biofilms (white arrows) that contacted minute dolomite rhombs. F, Thin slime of biofilms (white arrows) covered minute rhombic dolomite crystal. G, Mucilaginous fibres (white arrow) contacting various dolomite grains. H, Euhedral quartz grains with double terminations in contact with minute dolomite grains (white arrow). Note that the rills (black arrow) are pronounced on surface of quartz crystals.

that commonly obliterated the primary dolomite microfacies (Mastandrea et al., 2006) or an alteration from diagenetic selforganization (Wright, 1999). This neomorphic process of crystal growth is not uncommon; as such alterations have been documented from Holocene marine dolomites (Gregg et al., 1992) and even in microbial mats of the coastal Sabkha of Abu Dhabi (Bontognali et al., 2010). Accordingly, abundant rod aggregates might indicate active metabolism of putative SRB in stromatolite. Through excreting EPS in great

abundance, SRB might have induced the formation of dolomitized rod aggregates and entailed the fossilization of putative filamentous cyanobacteria (Bontognali et al., 2010). To sum up, two main microbial functioning groups, fossilized filamentous cyanobacteria sheath and SRB represented by copious rod aggregates composed of minute dolomite grains, are distinct in dark laminae of the Luoping stromatolite. They both might represent the most active microbial communities in stromatolite ecosystem. Other important microbial components include aerobic heterotrophs,

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Fig. 11. EDS analytical results of three different components of dolomite grains in the Luoping stromatolites. White cross corresponds to analysing point. Element Au indicates goad coating of samples. A, Floating dolomite grains that showed a composition of Ca dolomite (indicated by EDS spectrum in a), with low percentage of element Si. B, Rod covered with minute dolomite rhomb, which showed low percentage of element Si in composition (indicated by EDS spectrum in b).

anoxygenic phototrophs and sulfide oxidizing bacteria, which may have also contributed to the accretion of stromatolite, but were not observed in the case of the Luoping stromatolite. 5.1.3. Origin of the fenestrae facies Laminoid fenestrae are also rich in the Luoping stromatolite (Figs. 5A–C, 6A). Reid et al. (2003) treated the comparable fenestrae as the space that was initially occupied by the organic framework of accreting mat. Small spheroid balls are also analogous to those seen in other ancient stromatolites (Mastandrea et al., 2006; Perri and Tucker, 2007) and modern-day stromatolites (Kaźmierczak and Altermann, 2002). Subrounded pores are also pronounced within the complex rod consortia (Fig. 8F). They resemble the rounded pores within cyanobacterial filaments from the Yellowstone National Park hot spring, US (Mata et al., 2012). The latter was interpreted as representing stabilization of gas bubbles produced on the surface of cyanobacterial mats (Mata et al., 2012). Other microbial processes such as aerobic respiration, aerobic sulfide oxidation, and fermentation would also result in the dissolution of CaCO3 and degradation of organic matter in framework and might have induced the subsequent formation of those laminoid fenestrae (Ezaki et al., 2012). 5.2. Comparisons with Early Triassic stromatolites and other forms of microbialites Microbialites including stromatolites, thrombolites and other unknown forms characterize the P–Tr boundary (PTB) successions in many shallow marine facies sections (Kershaw et al., 2012). They are interpreted as a sedimentation phenomenon related to the severe end-Permian mass extinction. However, stromatolites are not common among the PTBMs. Of these, one PTB stromatolite deposit from the Bükk Mountains in Hungary yields abundant microstructures such as sphere clusters, aggregates of micrite clots and bundles of prostrate micrite threads (Hips and Haas, 2006). These authors interpreted the spheres as calcified coccoid cyanobacteria, and inferred that bundles of prostrate threads may represent calcified

filamentous cyanobacteria in stromatolite (Hips and Haas, 2006) without documenting convincing evidence indicating the presence of fossilized filamentous cyanobacteria. Yang et al. (2011) described a stromatolite deposit from the Chongyang PTB section of southern Hubei Province, South China. In addition to Renalcis-like structures found in stromatolitic laminae, the Chongyang stromatolite is dominated by coccoid bacteria (Yang et al., 2011). Other PTB stromatolites have also been reported from the Cürük Dag of Turkey and Hambast of Iran (Kershaw et al., 2011, 2012). However, their microbial compositions remain unclear because no geomicrobiological studies have been undertaken yet. Other forms of PTBMs (e.g. thrombolites, dentrolites) have also been investigated from around the world (Lehrmann, 1999; Ezaki et al., 2003, 2008; Wang et al., 2005; Kershaw et al., 2011; Wu et al., 2014). Of these, abundant coccoid-like small balls were found in the PTB thrombolites from Sichuan and Guizhou Provinces, South China (Ezaki et al., 2003, 2008). These coccoid-like objects are characterized by drusy microspar at central area surrounded by micrite walls and were usually interpreted as coccidal bacteria (Ezaki et al., 2008), which resemble those microfossils in morphology and size range from the PTB stromatolites in the Chongyang County of South China and Bükk Mountains of Hungary (Hips and Haas, 2006; Yang et al., 2011). The similarity in microbial compositions suggests a similar forming mechanism of these PTBMs in terms of microbial metabolism. Interestingly, Wu et al. (2014) interpreted the microbial structures of thrombolites and dentrolites in the PTBMs from South China as planktic cyanobacterium Microcystis rather than Renalcis. These authors also considered that the bloom of such planktic Microcystis cyanobacteria may have resulted in toxin to other metazoans, which is accountable for the presence of anoxia in shallow marine settings (Wu et al., 2014). This viewpoint opens a brand new window insight into the possible forming mechanism of microbialite deposits during the Early Triassic recovery interval. Except for coccoidal objects stated above, the Luoping stromatolite also yields abundant putative filamentous cyanobacterial microfossils (Figs. 6 and 8). In contrast, most PTBMs (including stromatolites and thrombolites) were characterized by predominantly coccoidal cyanobacteria (including Renalcis), with rare occurrence of fossilized filamentous microfossils (Lehrmann, 1999; Ezaki et al., 2003, 2008; Hips and Haas, 2006; Kershaw et al., 2011, 2012; Yang et al., 2011). After observing modern open marine Bahamian stromatolites, Reid et al. (2000) suggested that two different forms of cyanobacteria performed together to account for the growth and preservation of Bahamian stromatolite. During periods of rapid sedimentation, filamentous cyanobacteria dominate the stromatolite surface, whereas climax communities of endolithic coccoidal bacteria develop during prolonged hiatal periods (Reid et al., 2000). Such difference in microbial composition between Luoping stromatolite and PTBMs might result from either the differential carbonate sedimentation dynamics or evolution of microbial communities within microbial mat system. The latter may be a response to the return of normal oceanic conditions in the early Middle Triassic. Such ameliorated oceanic condition in the early Middle Triassic is also supported by a return of stable carbon cycle and complex marine ecosystem with equivalent diversity to pre-extinction interval (Payne et al., 2004; Chen and Benton, 2012). However, there is also a possibility that the scarcity of filamentous cyanobacteria microfossils within PTBMs could be a result of preservation potential, which exerts a strong control on the calcification of cyanobacteria (Planavsky et al., 2009). Regarding the abundant preservation of coccoid cyanobacterial microfossils in PTBMs, it is more likely that the scarcity of filamentous cyanobacteria in PTBMs is a reflection of different microbial compositions rather than preservation bias. The younger Early Triassic stromatolites have also been reported from the late Griesbachian to Dienerian, Smithian and Spathian, respectively (Pruss et al., 2006; Baud et al., 2007; Mata and Bottjer, 2012). These younger microbialite deposits occurred worldwide, including

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Japan, Germany, eastern Greenland, southern Turkey, central Iran, western United States, and South China (Schubert and Bottjer, 1992; Sano and Nakashima, 1997; Paul and Peryt, 2000; Wignall and Twitchett, 2002; Pruss and Bottjer, 2004; Baud et al., 2007; Mata and Bottjer, 2011; Paul et al., 2011; Ezaki et al., 2012). However, detailed studies on geomicrobiology of these deposits lagged behind their ecologic studies. Chen et al. (2012) and Luo and Chen (2014) reported briefly a Smithian (Early Triassic) stromatolite from the Kockatea Shale Formation, northern Perth Basin of Western Australia. Recent geobiologic study revealed that both filamentous structures and spheroids are characteristics of microbial assemblage of the Perth Basin stromatolite (Chen et al., 2014), which therefore is comparable with the early Middle Triassic stromatolite described herein. However, the Perth Basin stromatolite differs clearly from the latter in the lack of rod aggregate and EPS indicated by calcified biofilms and fibrous structures. Ezaki et al. (2012) detected that the late Early Triassic stromatolite from Guizhou of South China was constructed by the activity of sulfate-reducing or anoxygenic phototrophic bacteria. Its microbial composition is related to the inhospitable anoxic/sulfidic marine conditions that prevailed in Early Triassic. The deleterious environment might have prevented the growth of oxygenic phototrophs such as cyanobacteria but enhanced the accretion of anoxygenic phototroph that utilized copious HS− in stressed habitats for a metabolism (Ezaki et al., 2012). The early Middle Triassic Luoping stromatolite therefore might be different from the late Early Triassic counterparts in terms of the functioning microbial groups. Other Early Triassic stromatolites have also been reported worldwide (see reviews by Pruss et al., 2006; Baud et al., 2007; Kershaw et al., 2012). Nevertheless, their microbial compositions and genesis remain unclear, although it is believed to be that those stromatolites are all biogenic in origin. The late Early Triassic microbialite deposits have also been found in association with sponge and encrusted metazoans to form ecologically complex reefs (Szulc, 2007; Brayard et al., 2011; Marenco et al., 2012; Oliveri et al., 2014). Metazoan buildups of comparative ecologic complexity have also been reported from the Spathian Virgin Limestone Member of Nevada, western US (Pruss et al., 2007). Those primitive metazoan reefs suggest that ameliorated environmental conditions might have returned to certain shallow marine regions during the late Early Triassic. However, no detailed geobiologic studies of these microbialites have been undertaken, and thus prevent a detailed comparison with the Luoping stromatolite. 5.3. Palaeoenvironmental implications Early Triassic stromatolites have been reported from around the world (Schubert and Bottjer, 1992; Sano and Nakashima, 1997; Richoz et al., 2005; Hips and Haas, 2006; Pruss et al., 2006; Farabegoli et al., 2007; Kershaw et al., 2011; Chen et al., 2012, 2014; Mata and Bottjer, 2012). They are major components of the post-extinction microbialites. Although the debate on genesis of the P–Tr microbialites still continues (Kershaw et al., 2007, 2012; Mata and Bottjer, 2012), biogeochemical signals show that microbes were extremely abundant immediately after the end-Permian extinction even in the microbialite-free areas such as Meishan (Xie et al., 2005). Some biogeochemical signals mirroring various microbial communities associated with benthic microbial mats have been detected from diagenetic carbonate crystal fan deposits of Dienerian–Smithian age (Heindel et al., 2014). Thus, microbes existed widely in various niches of the post-extinction oceans. Moreover, Kershaw et al. (2007) and Woods et al. (2007) also emphasized that the elevated carbonate supersaturation caused by the upwelled CaCO3-rich anoxic waters mixed with aerated surface waters may be the key driver for the precipitation of PTBMs. As such, the highly saturated carbonate conditions in the post-extinction oceans (Grotzinger and Knoll, 1995; Woods et al., 1999; Riding and Liang,

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2005; Pruss et al., 2006; Riding, 2006; Baud et al., 2007) combined with factors unfavourable to most normal skeletal organisms may also have facilitated the formation of the PTBMs. However, recent elemental and pyrite framboid analyses reveal that some PTBMs may also be deposited in oxic conditions (Liao et al., 2010; Loope et al., 2013). Similarly, abundant and diverse ostracods faunas derived from the PTBMs also indicate that the PTBM was neither anoxic nor inhospitable to shelly organisms (Forel et al., 2012; Forel, 2013). The late Early Triassic stromatolites have different microbial compositions, which indicate different redox conditions. Ezaki et al. (2012) documented an Olenekian stromatolite from South China and considered that it grew in the inhospitable anoxic/sulfidic marine conditions. In contrast, the Smithian stromatolite from the Perth Basin, Western Australia grew in an oxic condition (Chen et al., 2014). Similarly, the close association of the stromatolites with various metazoans from the late Early Triassic of western US indicates an oxic shallow marine environment (Brayard et al., 2011; Marenco et al., 2012). As stated above, the Luoping stromatolite ecosystem is characterized by a great amount of biomass in putative filamentous cyanobacteria and SRB. It is superficially similar to those of the Type II stromatolite described from the Highborne Cay, Bahamas (Decho et al., 2005). The latter is characterized by the higher biomass within layer 1 and layer 3 in stromatolites, corresponding to the content peaks of cyanobacteria and SRB, respectively (Reid et al., 2000; Decho et al., 2005). Abundant filamentous cyanobacteria may indicate the proliferation of oxygenic phototrophs in a normal, oxic habitat. Another important microbial component, SRB, has been traditionally considered not only as anaerobic heterotrophs, but also organisms that are incapable of tolerating oxygen and thus exist only in anoxic environments. This is because (1) isotopic studies revealed that SRB evolved well before the advent of atmospheric oxygen (Shen and Buick, 2004), and (2) inaccurate visual observations of microbial mats and logic inference suggested that anaerobic SRB usually inhabit the black anoxic zone within a microbial mat profile (Visscher et al., 2000). However, recent experimental studies and field observations revealed that SRB can tolerate and even respire oxygen, and are abundant and very active in the oxic zones of microbial mat (Baumgartner et al., 2006). These sulfate-reducing bacteria are also actively involved in the lithification of microbial mat and closely associated with cyanobacteria in the oxic zone of the mat (Ito et al., 2002; Baumgartner et al., 2006). Consequently, the Luoping stromatolites may have grown in an oxic habitat during the mid-Anisian time, just before the full recovery of marine ecosystems in middle–late Anisian in the same area (Hu et al., 2011; Chen and Benton, 2012). This inference is strengthened by the open platform setting indicated by the stromatolitebearing strata in Unit 2, as stated in the above palaeoenvironmental analysis. The contemporaneous oxic oceanic condition in southwestern Chinese basins is also reinforced by the presence of metazoan reefs (Payne et al., 2006) and benthic diversification in the Qingyan area of the same oceanic basin (Chen et al., 2010). Accordingly, the Luoping stromatolite grew in a period when oxic conditions prevailed in the early Middle Triassic oceans in South China, which seem to set an agenda for full recovery of marine ecosystems in middle–late Anisian (early Middle Triassic). To sum up, the Anisian stromatolite differs clearly from the PTBMs in microbial composition and growth oceanographic conditions. It, however, may be similar to some counterparts from the Olenekian, but is very different from others of the same stage in terms of microbial composition and environmental settings. As a result, the post-extinction stromatolites and other types of anachronistic facies are not necessarily indicative of anoxic or oxic conditions (Woods, 2014). Their microbial compositions and environmental settings are much more complex than previously thought. Whether microbialite deposits indicate an environmental stress can be determined only when biological, sedimentologic and geochemical data are available (Woods, 2014).

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6. Conclusions The Luoping stromatolite shows the typically stratified columnar structures with crinkled laminae. Dark coloured laminae are composed of prostrate and upright filamentous structures; the latter show an up-straight growth fabric. Laminoid fenestrae are also commonly present. Dark coloured laminae show strong fluorescence in sharp contrast to dolomite cement on fluorescent images, indicating high contents of organic matter. The rod-like aggregates, filled with minute dolomite rhombs, are also very common in laminae. They resemble present-day cyanobacterial trichomes, and thus may represent fossilized cyanobacteria. Moreover, small pits, coccoid-like spheroids, calcified biofilms, and fibrous structures are also commonly present in stromatolite laminae. The last two may represent the calcified extracellular polymeric substances (EPS) that contributed to the development and lithification of Luoping stromatolite. Authigenic quartz grains are also abundant and probably indicate biologic involvement in stromatolite formation process. Putative lithified cyanobacteria/oxygenic phototrophs and probable SRBinduced microbial formation of dolomite are distinct during the growth of stromatolite, strengthening the view that the Middle Triassic stromatolite is biogenic in origin. The Luoping stromatolite differs clearly from the PTBMs in having abundant putative filamentous cyanobacteria and growing in an oxic condition. It, however, resembles some late Early Triassic stromatolites, but is very different from others of the same stage in terms of microbial composition and environmental settings. As a result, the post-extinction stromatolites and other types of anachronistic facies are not necessarily indicative of anoxic or oxic conditions, and their environmental settings are much more complex than previously thought. Acknowledgments The authors wish to thank Peter Duncan and Lyn Kirilak from CMCA, the University of Western Australia for their guidance and helpful suggestions in sample preparation and SEM imaging. Two anonymous reviewers are thanked for their critical comments and constructive suggestions, which have improved greatly the quality of the paper. This study is supported by the 973 Program of China (2011CB808800) and the 111 Program of China (Biogeology and Environmental Geology), two research grants from the State Key Laboratory of Biogeology and Environmental Geology, and the State Key Laboratory of Geological Processes and Mineral Resources, China University of Geosciences (GBL11206 and GPMR201302 to ZQC), and an NSFC grant (No. 41272023 to ZQC). Moreover, the senior author's study was also financially supported by a grant (No. OGL-201102) from the State key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry and a geological survey project (No. 1212011120621) of Chengdu Centre of China Geological Survey. It is a contribution to the IGCP 572 “Permian–Triassic ecosystems”. References Awramik, S.M., 1971. Precambrian columnar stromatolite diversity: reflection of metazoan appearance. Science 174, 825–827. Awramik, S.M., 1992. The oldest records of photosynthesis. Photosynth. Res. 33, 75–89. Awramik, S.M., 2006. Respect for stromatolites. Nature 441, 700–701. Awramik, S.M.,Margulis, L., 1974. Definition of stromatolite. In: Walter, E. (Ed.), Stromatolite Newsletter. 2, p. 5. Bai, J.K., Zhang, Q.Y., Yin, F.G., Zhou, C.Y., Lu, T., Feng, J., 2009. Carbonate microfacies in the second member of the Middle Triassic Formation in Luoping, Yunnan. Sediment. Geol. Tethyan Geol. 29, 15–21 (in Chinese). Baud, A., Cirilli, S., Marcoux, J., 1997. Biotic response to mass extinction: the Lowermost Triassic microbialites. Facies 36, 238–242. Baud, A., Richoz, S., Marcoux, J., 2005. Calcimicrobial cap rocks from the basal Triassic units: western Taurus occurrences (SW Turkey). C.R. Palevol 4, 501–514. Baud, A., Richoz, S., Pruss, S., 2007. The Lower Triassic anachronistic carbonate facies in space and time. Glob. Planet. Chang. 55, 81–89.

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