Biosedimentological features of major microbe-metazoan transitions (MMTs) from Precambrian to Cenozoic

Earth-Science Reviews 189 (2019) 21–50

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Biosedimentological features of major microbe-metazoan transitions (MMTs) from Precambrian to Cenozoic

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Zhong-Qiang Chena, , Chenyi Tua, Yu Peia, James Ogga,b,c, Yuheng Fanga, Siqu Wua, Xueqian Fenga, Yuangeng Huanga, Zhen Guoa, Hao Yanga a

State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences (Wuhan), Wuhan, 430074, China State Key Laboratory of Oil and Gas Reservoir Geology and Exploitation, Chengdu University of Technology, Chengdu, Sichuan 610059, China c Department of Earth, Atmospheric and Planetary Sciences, Purdue University, West Lafayette, IN 47907, USA b

A B S T R A C T

Biotic activities are involved in almost all sedimentation processes throughout the evolutionary history of life on our planet. However, deep-time organism-induced sedimentation and biosedimentary records remain unclear in terms of lithologic types, strata stacking patterns and possible controlling factors. We document biosedimentary features of major transitions from microbe-dominated switching to metazoan-dominated biosedimentary systems based on the global distributions of both microbial and metazoan carbonates through Precambrian to Phanerozoic times, with emphasis on sedimentary records from China. The compilation of 150 and 180 well-documented metazoan and microbial reefs, respectively, from China, reveals that metazoan reefs proliferated during the Middle Ordovician, Middle Devonian and Middle Permian, whereas microbial reefs were well developed during the Cambrian, Late Devonian and Early–Middle Triassic, plus a moderate development during the early Silurian. These stratigraphic abundances of metazoan and microbial carbonates of China generally match the global patterns. The updated variation trends of microbial and metazoan carbonates throughout the late Precambrian and Phanerozoic reveal that there were five major microbemetazoan transitions (MMTs): the late Ediacaran, the Cambrian, and the aftermaths of the mass extinctions of the end-Ordovician, Late Devonian, and end-Permian. The late Ediacaran MMT began with microbe-dominated oceans with occasional occurrences of metazoans. The presence of Cloudina-dominated reefs in the latest Ediacaran marks the completion of the switching of this microbe-dominated depositional system into a metazoan-dominated system. The Cambrian saw the expansion of skeletal microbes (i.e., Epiphyton, Renalcis) in the oceans; and the stratigraphic successions yield the most diverse biosedimentary deposits and/or structures of the entire Phanerozoic. The Cambrian MMT was the longest microbial-metazoan alternation period and is marked by two metazoan occurrence peaks marked by dominance of abundant archaeocyath buildups during its Epoch 2 and by maceriate and lithistid sponge reefs during the late Furongian Epoch. The early Silurian in China saw the deposition of a thick suite of organic-rich black shales followed by alternations of microbe-rich sediments (oil shales) and metazoan-bearing deposits, which are replaced by microbial and metazoan reefs during the late early Silurian. The Late Devonian MMT started during the late Frasnian and persisted into the early Mississippian, and thus extended slightly longer than the aftermath of the Frasnian–Famennian extinction interval. Alternating occurrences of microbial and metazoan reefs characterize this Late Devonian MMT. Almost all microbe-mediated sediments/structures observed in the Cambrian MMT reoccurred in the aftermath of the end-Permian mass extinction during the Early–Middle Triassic MMT, suggesting high similarities between those two MMTs. Cambrian and Early–Middle Triassic MMTs also share comparable carbon and sulfur isotopic perturbations, warming regimes, and generally oxygen-deficient seawaters. Some of these environmental and climatic extremes may also occur during other MMTs, but they usually did not occur synchronously. Most MMTs seem to have undergone four developmental stages. They initiated as microbe-dominated successions (Stage A), and then were characterized by alternations of microbe-dominated and of metazoan-bearing or bioturbated successions (Stage B). Both microbial and metazoan reefs co-occurred during Stage C; and a dominance of metazoan reefs marks the development of Stage D. Ediacaran and Cambrian MMTs seem to have undergone the first three development stages, whereas the three post-extinction MMTs experienced the full set of Stages A−D, corresponding to metazoan survival, initial recovery and full recovery. The majority of volatile-rich Large Igneous Provinces (LIPs), coupled with intensive acidification events, anoxia and global warming regimes, took place during the Mesozoic–Cenozoic. However, microbe-dominated sediments were only widely deposited during the Early Triassic, and greatly declined after that time. Therefore, it seems that microbial abundance in MMTs may not be directly related to these extreme LIP events. This is probably because a primary source of food for the metazoans might have shifted to phytoplankton (e.g., coccoliths, dinoflagellates, and radiolarians) in the marine waters since the Triassic. Certainly, the preMesozoic oceans were not dominated by phytoplankton. Perturbations in the carbon isotope record characterize all MMTs, and thus may be reliable proxies indicating MMT biosedimentary systems.

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Corresponding author. E-mail address: [email protected] (Z.-Q. Chen).

https://doi.org/10.1016/j.earscirev.2019.01.015 Received 6 June 2018; Received in revised form 20 January 2019; Accepted 21 January 2019 Available online 24 January 2019 0012-8252/ © 2019 Elsevier B.V. All rights reserved.

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1. Introduction

Microbial mats include various types of the microbially induced sedimentary structures (MISSs), e.g., wrinkle structures, pictograph-like sand crack-fills, fusiform sand crack-fills, polygonal sand crack-fills, sinuous crack-fills, and levelled ripple marks (Noffke et al., 2001, 2003; Noffke, 2010; Davies et al., 2016; Xu et al., 2017).

There is growing evidence that biotic activities are involved in most, if not all, sedimentation processes from the ancient geological past through the present day (Zadoroshnaya et al., 1982; Fagerstrom, 1987; Zeng et al., 1988, 1992; Geldsetzer et al., 1989; Grotzinger and Knoll, 1995, 1999; Fan, 1996; Yu and Shen, 1998; Wood, 1999; Stanley Jr., 2001; Stanley, 2003; Stanley, 2011; Kiessling et al., 2002; Riding, 2002, 2006, 2011; Riding and Liang, 2005; Knoll, 2012, 2015; Knoll et al., 2012, 2016; Chen et al., 2017a; Lee and Riding, 2018). The study focusing on organism-induced sedimentation, also termed biosedimentology, has attracted increasing interest from global paleontologists and sedimentologists. Of the deep-time biosedimentary records, both metazoan-induced and microbe-mediated carbonates often form spectacular mountains in the field and are commonly present worldwide within upper Precambrian to Phanerozoic successions. Flügel and Kiessling (2002) and Kiessling et al. (2002) compiled a global dataset of metazoan reefs through the Phanerozoic; and they found that reef abundance peaked during the Middle Ordovician, the Middle Devonian, the Middle and Late Permian, and the Jurassic, but was reduced after mass extinctions (i.e., end-Ordovician, Late Devonian, end-Permian, and end-Triassic) (Kiessling et al., 2002). Riding (2002, 2006) confirmed that microbial carbonates exhibit an opposite pattern to metazoan-induced sediments in their abundance. In particular, the switching between metazoan carbonate and microbial carbonate depositional systems typically corresponds to major environmental, climatic and biotic changes linked with mass extinctions. Many Chinese occurrences of both metazoan and microbial buildups were not included in those databases. In China, marine Paleozoic and Triassic strata are widely distributed and are continuously exposed in many areas. Both metazoan reefs and microbial carbonates are also well developed. Accordingly, our study critically reviews these Chinese occurrences to update the global databases of metazoan reefs and microbial carbonates, and then compares the abundance distributions of both types of bio-carbonates during the late Neoproterozoic through Phanerozoic. The associated extinctions and recoveries, large volcanic episodes, oceanic anoxia, oceanic acidifications, sea-surface temperature variations, glaciations, and geochemical proxies, such as carbon and sulfur isotopes, are also summarized to probe into the physical and chemical mechanisms affecting the abundance of both types of carbonates during critical periods in the evolution of life. Depositional features of several microbe-metazoan evolutionary intervals are detailed to reveal biosedimentations during these critical intervals. Metazoan-induced and microbe-mediated carbonates are here viewed as proxies revealing oceanic geochemical conditions. These two types of carbonates are among the most common sedimentary rocks in the geological record and alternately dominate sedimentary successions. We focus on two major questions about the relationships among organisms and their environmental and climate regimes: (1) What are the common sedimentary patterns of critical microbe-metazoan transitions (MMTs) within stratigraphic sections during late Neoproterozoic through Cenozoic? (2) What were the responses of carbonate production to environmental, climatic and biotic crises during the geological past? The overall goal of this paper is to provide an overview of biological processes from the Ediacaran to the Cenozoic as recorded in China, together with their possible consequences and controls. We emphasize three aspects: (1) the types of microbial-mediated sediments (i.e., microbialites, oolites, oncolites) and various microbial mats, (2) the forms of metazoan buildups (i.e., bioherms, biostromes, and reefs), and (3) the (bio)geochemical signals of environmental and climatic change during their critical transitions. It should be noted that metazoan buildups include bioherm, biostrome, and reef in term of geometry, while microbialites include stromatolite, thrombolite, and dendrolite, and they are also referred as microbial reefs or buildups (Burne and Moore, 1987; Kershaw, 1994; Riding, 1999, 2002; Flügel, 2004).

2. Chinese records vs. global data of both metazoan and microbial buildups 2.1. Overview of late Neoproterozoic to Phanerozoic metazoan and microbial reefs in China A total of 191 metazoan reefs and 206 microbial buildups have been reported in China from the Ediacaran through to the Quaternary (Holocene) (Zeng et al., 1988, 1992; Fan, 1996; Yu and Shen, 1998; Gong et al., 2013). Of these, 150 metazoan and 180 microbial reefs are well documented. We have tabulated their occurrences, stratigraphic settings and localities in the online supplementary data (Table S1). Of these, the Precambrian reefs are mostly microbial in origin and occur primarily within Mesoproterozoic and Neoproterozoic successions, with only a few Paleoproterozoic microbial carbonates reported from the Beijing area of North China. Mesoproterozoic microbial reefs (microbialite, Burne and Moore, 1987) have been reported mainly from the entire North China craton (Liaoning, Tianjin, Beijing, Hebei, Shandong, northern Jiangsu, Henan, Shanxi and Inner Mongolia) and northwestern China (Gansu and Xinjiang areas), and to a lesser extent from South China (northwestern Hubei and central Yunnan areas). Neoproterozoic microbial carbonates generally have similar distributions to the Mesoproterozoic examples, although they have a more extensive distribution within South China (i.e., Jiangxi and Guizhou areas) (Fig. 1A). Paleozoic metazoan and microbial reefs are abundant in both North China and South China. Cambrian metazoan reefs are mainly distributed in the southern Shanxi, northern Jiangsu, Shandong and southern Liaoning areas of the North China craton, and in the Guizhou, Hunan and western Hubei areas of South China. Coeval microbial reefs occur mainly in the Henan, Shandong, Hebei and Beijing areas of North China, the Xinjiang areas of northwestern China, and the western Hubei area of South China (Fig. 1B). Ordovician metazoan reefs are widely distributed throughout North China and South China as well as the southern Xinjiang of northwestern China, whereas microbial carbonates of the same age have been reported mainly from the Jiangsu and Jiangxi areas of South China (Fig. 1B). Silurian metazoan and microbial reefs are confined to the Guizhou and Sichuan areas of South China, but with a few examples documented from Inner Mongolia. Upper Paleozoic metazoan reefs are well developed and widely distributed in South China and in the southern part of North China. A few metazoan reefs of Carboniferous-Permian age have also been reported from the Xinjiang area of northwestern China and from Inner Mongolia, northern China. Microbial carbonates of Carboniferous-Permian age are not commonly present and are confined to Guangxi and western Hubei areas of South China (Fig. 1C). In China, carbonates and reefs are abundant in the Triassic, but they are limited to South China (Fig. 1C). The Jurassic-Cretaceous marine deposits are mainly distributed in Tibet, western China, with a few metazoan reefs reported from that region. Cenozoic marine deposits of both microbial and metazoan carbonates are exposed along the eastern Chinese coastal areas and occur within the South China Sea (Fig. 1D). 2.2. Chinese occurrences vs. global patterns of both metazoan and microbial buildups Metazoan reefs within China exhibit three major peaks during the Ordovician, Devonian and Permian in their number and accumulative thicknesses of the buildups (Fig. 2A−B). The numbers of Cambrian and Triassic reefs are also relatively high (> 10), and the accumulative 22

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Fig. 1. Temporal distributions of metazoan and microbial reefs (outcrop examples only) of (A) Precambrian, (B) Early Paleozoic, (C) Late Paleozoic, and (D) Mesozoic-Cenozoic within China. (Details for the stratigraphic and geographical distributions of these reefs are in online supplementary Table S1).

only three reef constructors (rugose corals, stromatoporoids, and macroalgae) underwent significant proliferation. Sponges and bryozoans remained at similar levels as in the Silurian. Metazoan reef-builders became depauperate beginning in the Famennian and throughout the Carboniferous, and were dominated by rugose corals and macroalgae with minor constituents of sponges and bryozoans. Reef-building organisms diversified again during the Permian as the number and accumulative thickness of reefs dominated by rugose corals, sponges, bryozoans, Tubiphytes, and macroalgae significantly increased. Metazoan reef-builders proliferated during Middle and Late Permian times (Guadalupian and Lopingian epochs) (Gong et al., 2013). Triassic and younger reefs are rather rare, probably due to rarity of marine deposition within China. In China there are four important evolutionary turnovers. (1) Archaeocyathids were the major reef-builders during early Cambrian (Zhuravlev et al., 2015; Yang et al., 2016a,b), but maceriate sponges were the key constructors of the middle-late Cambrian metazoan reefs (Lee et al., 2015). During most of the Cambrian, lithistid sponges, demosponges, and coralmorphs, together with microbes, occasionally built microbe-metazoan reefs (Riding and Zhuravlev, 1995; Adachi et al., 2015; Lee et al., 2015; Yan et al., 2017; Ezaki et al., 2017). (2) Ordovician reefs expanded, including during the Great Ordovician Biodiversification Event, with the newcoming of four major reef-

thickness of the Triassic metazoan reefs is also prominent (Fig. 2A−B). The pre-Jurassic records of metazoan reefs from China show patterns that are comparable to the global record of metazoan reef abundances in both relative numbers and accumulative thicknesses (Kiessling, 2002; Flügel and Kiessling, 2002), which also have these three major peaks during the Ordovician, Devonian and Permian (Fig. 3). In China, major reef-building organisms of Phanerozoic metazoan reefs include archaeocyathids, maceriate (maze-like) sponges, bivalves, bryozoans, calathiids, lithistid sponges, rugose corals, stromatoporoids, Tubiphytes, and macroalgae (referred herein to red and green skeletal algae). Both archaeocyathids and calathids are taxonomically assigned to sponges by some authors (Lee and Riding, 2018), but some regard calathiids as algae; therefore, they are treated herein as reef builders independent from sponges. Metazoan reefs became common during the middle-late Cambrian in the regions of China when archaeocyathids, maceriate sponges and macroalgae were major reef builders (see below). Archaeocyaths, the major reef-builder of early Cambrian time, disappeared in the midCambrian. The Ordovician had six major builders, of which five were newcomers. Calathiids became abundant, but are confined to the Ordovician (Fig. 4). The Silurian marked a decline in China for metazoan reefs and saw dramatic depletions of five of the reef-building groups. Although metazoan reefs flourished again during the Devonian, 23

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Fig. 2. (A) Numbers and (B) accumulative thicknesses (in m) of metazoan reefs through the Phanerozoic in China. Peaks in abundance of metazoan reefs occur during the Ordovician, Devonian and Permian.

(Flügel and Kiessling, 2002; Riding, 2005). Metazoan reefs peaked during the Middle Ordovician, Middle Devonian, Middle Permian and latest Permian, whereas microbial reefs were locally abundant during the Cambrian, Late Devonian−Carboniferous and Early Triassic times.

builders (corals, bryozoans, stromatoporoids, and calathiids), but suffered a loss of calathiids and a dramatic depletion of five previous major reef-constructors (i.e., corals, macroalgae, sponges, bryozoans, and stromatoporoids) at the end of this period (Fig. 4). (3) Another major loss of reef-builders occurred at the Frasnian−Famennian (F−F) boundary, with distinct depletions of five reef-builders (corals, macroalgae, sponges, bryozoans, and stromatoporoids); and this depauperate state of metazoan reefs persisted into the Late Carboniferous. (4) The most important losses of reef constructors were coupled with the greatest biotic mass extinction at the end of the Permian (Fig. 4), with all major reef-building organisms of the Permian having vanished in the Early Triassic (Flügel and Kiessling, 2002; Knoll et al., 2007a; Chen and Benton, 2012; Stanley et al., 2018; Fig. 4). Chinese records show the co-existence of both microbial and metazoan reefs during the Cambrian. Microbial reefs dominated the Cambrian and Early Ordovician carbonate buildups, but the dominance switched across the Early-Middle Ordovician boundary to metazoan reefs (Lee and Riding, 2018), although corals did not become diversified until the Sandbian-Katian (Middle-Late Ordovician). This mirrors the global pattern of microbial carbonate abundances from a Cambrian peak to a late Ordovician valley identified by Riding (2002, 2005) (Fig. 5). The Ordovician to Triassic development of reefs seems to have been strongly affected by the mass extinctions. Metazoan reefs usually expanded prior to each of the five major mass extinctions, whereas microbial reefs proliferated after these events. Microbes underwent a bloom in the aftermaths of F−F and Permian−Triassic (P−Tr) mass extinctions, but did not bloom in the aftermath of the Ordovician−Silurian (O−S) extinction, although some microbialites occurred at that time (Li et al., 2017b). In summary, Chinese records are similar to the global pictures

2.3. Evolutionary traits of metazoan and microbial carbonates: microbemetazoan transitions (MMTs) We updated the average thickness of global metazoan reefs (Flügel and Kiessling, 2002) and the estimated microbial carbonate abundance (Riding, 2005) by adding Chinese records (Appendix 1: Online supplementary data; Table S1). The updated global picture shows that major accumulative thickness peaks of metazoan reef development occurred during the early Late Devonian (Frasnian) and Middle Permian. The former is characterized by abundant coral and stromatoporoid reefs (Copper, 2001, 2002), whereas the Middle Permian reef peak is mainly attributed to the thriving of sponge buildups worldwide (Flügel and Kiessling, 2002). Several secondary peaks occur during the Middle Ordovician, Middle Triassic and Late Jurassic to Early Cretaceous (Fig. 6). Major Phanerozoic microbial carbonate abundance peaks occur during the Cambrian and Late Devonian (Famennian), with two lesser peaks in the early Silurian and Early−Middle Triassic (Riding and Liang, 2005). Overall through the Phanerozoic, the peaks in the accumulative thickness of metazoan reefs correspond to lower percentages of microbial carbonate abundance, and the lower values occur during abundance peaks of microbial carbonates (Fig. 6). There are several critical microbe-metazoan transitions (MMTs) in terms of ecosystem evolution. The sedimentary features of a MMT are represented by the switch of a microbe-dominated depositional system into a metazoan-dominated system, which is reflected by an upward change from 24

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Fig. 3. Chinese records vs. global data of Phanerozoic metazoan reefs. (A) Number of reefs in China; (B) Accumulative thicknesses (in m) of metazoan reefs in China; (C) Numbers of global reefs; (D) mean thickness of global reefs. The statistics are tabulated per million years. Global values according to Flügel and Kiessling (2002).

3. Biosedimentary features and depositional patterns during major microbe-metazoan transitions from the Ediacaran to Cenozoic

a succession of microbe-mediated sediments into overlying metazoandominated buildups. We identified five major microbe-metazoan transitions (MMTs) from the late Precambrian to the Holocene (Fig. 6). The first MMT witnessed the rise of complex multicellular organisms that terminated the dominance of microbial mat-dominated ecosystems of the late Ediacaran, although marine algae (or microbes) may have acted as ecologically important food sources for early animals during the Cryogenian (Brocks et al., 2017; Knoll, 2017). Microbial participation has been crucial in the establishment of the new metazoan-dominated ecosystems, even though the emergence of new efficient browsinggrazing habits (i.e., by worms, arthropods and mollusks) disturbed or consumed the microbial mats that had formerly dominanted the seafloor. Thus, it was the evolution of the food chain that changed the seafloor, and some of the new skeletal animals constructed reefs. Due to the early Cambrian rise of marine animal life (Erwin et al., 2011), the shallow sea floors changed from microbial mat soft grounds into bioturbated substrates (Bottjer et al., 2000). Microbial-cemented and skeletal metazoan reefs characterize the early Cambrian MMT, but these retreated during the middle and late Cambrian. The next three MMTs are linked to environmental stress in the aftermaths of the Ordovician−Silurian (O−S), Frasnian−Famennian (F−F) and Permian−Triassic (P−Tr) mass extinctions. These extinction-recovery events, which occurred during the MMTs, seem to have been more profound than those of the end-Triassic and end-Cretaceous mass extinctions (Fig. 6).

Five major MMTs occurred during the Ediacaran, Cambrian, early Silurian, Late Devonian, and Early−Middle Triassic (Fig. 6). We summarize the major biosedimentary features of these five MMTs to identify biotic evolution and depositional patterns recorded in the changing sedimentary systems. 3.1. Ediacaran Prior to the Snowball Earth interval, microbial communities had dominated marine Earth’s ecosystems for more than 2.5 billion years. Stromatolite reefs first appeared during the Archean (Grotzinger, 1989; Hofmann et al., 1999; Allwood et al., 2006), proliferated during the Paleoproterozoic−Mesoproterozoic, and declined in the late Neoproterozoic (Grotzinger and Knoll, 1999; Riding, 2006; Knoll, 2011, 2012, 2015). The Snowball Earth crisis of the middle Neoproterozoic is believed to have been the key factor causing the decrease in stromatolite reefs (Riding, 2011), partly because the combination of low temperatures and rising dissolved pCO2 levels would have decreased the seawater saturation state of carbonate, thereby inhibiting microbial calcification. However, the apparent decline of stromatolites in abundance and diversity of morphologies may also be due to preservational biases. Stromatolites had partly recovered and became common within the Ediacaran cap carbonates of the Moonlight Valley Formation and of the Boonall Formation that overly the Marinoan glacial and the later Gaskiers glacial strata, respectively, in the Kimberley region of northwestern Australia (Fig. 7). Coeval microbialites are also conspicuous 25

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Fig. 4. Major reef-builder groups and their occurrence abundances throughout the Phanerozoic in China. Note that sponges in this diagram exclude both archaeocyathids and calathiids. Macroalgae include both red and green skeletal algae. FFB = Frasnian-Famennian boundary, Archaeo. = Archaeocyathids, Stromatop. = Stromatoporoids. Horizontal scale bar represents 20 reefs.

of South Australia and at Mistaken Point of Newfoundland (Gehling, 1999; Liu et al., 2015). One of the most remarkable discoveries of early life in China are exceptionally preserved animal embryos from the late Ediacaran Doushantuo Formation in the Guizhou Province (Zhang, 1988, 1989; Xiao et al., 1998). These tiny eggs demonstrate reproductive patterns and processes of animal cells, and are considered to mark the emergence of the earliest animals. Microbes were intimately involved in the preservation of these animal embryos (Xiao et al., 1998). Another important find bearing on the origin of early metazoan life is the early Ediacaran Lantian biota from Anhui Province, which probably represents the earliest known assemblage of macroscopic and morphologically differentiated eukaryotes, including diverse algal (including microbes) and putative animal fossils (Yuan et al., 2011; Guan et al., 2017). Cloudina, a small tube-like metazoan, is present in skeletal reef buildups, often in association with thrombolites and stromatolites, in the Nama Group of Namibia during late Ediacaran (Penny et al., 2014;

within the cap carbonates that overly the Marinoan of northwestern Namibia and the western US (Hoffman and Schrag, 2002; Corsetti and Grotzinger, 2005). Stromatolites have been widely reported from the postglacial carbonate successions in the Jiangsu, Zhejiang, Jiangxi, western Hubei, northwestern Hunan, Guizhou and Sichuan areas of South China, in the Liaoning, Hebei and Shanxi areas of the North China craton, and in the eastern and northern margins of the Tarim Basin, Xinjiang, northwestern China (Cao, 1997, 1999; Cao et al., 2001; Cao and Yuan, 2003, 2009; Xiao et al., 2014; Fig. 1A; Table S1). Stromatolites are also commonly present within the Ediacaran carbonate platform of Oman (Grotzinger and Al-Rawahi, 2014). Therefore, it appears that stromatolites were common within the Ediacaran carbonate successions worldwide. Their absence from some Ediacaran siliciclastic or deeper-water carbonate settings is likely due to inhospitable habitats for stromatolite formation. In siliciclastic shallow-marine settings, many Ediacaran-type multicellular animals co-occur with microbial mats in the Flinders Ranges

Fig. 5. Numbers of microbial carbonates (in red color) and metazoan reefs (in blue color) throughout the Precambrian to Phanerozoic in China with comparisons to global microbial carbonate abundance (modified from Riding, 2005). Pre. = Precambrian, Cam. = Cambrian, Ord. = Ordovician, Sil. = Silurian, Dev. = Devonian, Car. = Carboniferous, Per. = Permian, Tri. = Triassic, Jur. = Jurassic, Cre. = Cretaceous, Pal. = Paleogene, Neo. = Neogene, Qu. = Quaternary. Ec. = Ectasian, Fo. = Fortunian, Wu = Wuliuan, Ji. = Jiangshanian, Hi. = Hirnantian, Te. = Telychian, Fr. = Frasnian, Ch. = Changhsingian, An. = Anisian, Rh. = Rhaetian, Be. = Berriasian, Ma. = Maastrichtian, Ru. = Rupelian.

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Fig. 6. Variations of mean thickness of metazoan reefs, relative abundances of global metazoan and microbial reefs, and major biotic events (mass extinction and recovery) throughout the Phanerozoic. Five major microbe-metazoan transitions (MMTs) are during the late Ediacaran, Cambrian, early Silurian, Late Devonian, and Early−Middle Triassic. Abbreviations: Divers./Recov. = Diversification/Recovery, Pt3 = Neoproterozoic, Pre-C = Precambrian. The geologic timescale ages follow Ogg et al. (2016). Data for biotic diversification, recovery and mass extinctions are after Chen et al. (2014a). Data for accumulative thickness of metazoan reef and for microbial carbonate abundances are updated from Flügel and Kiessling (2002) and Riding and Liang (2005), respectively, by adding the biosedimentary records from China (see Table S1).

Fig. 7. Stromatolites within Ediacaran cap carbonates of the Moonlight Valley Formation that overly glacial deposits of the Marinoan (A) and of the Boonall Formation that overly the Gaskiers glacial deposits (B), Kimberley, northwestern Australia. The harmer is 25 cm long, while the coin is 2 cm in diameter. 27

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Voronova, 1984; Kruse et al., 1996). One ‘worm reef’ formed by operculate tubular “Ladatheca” occurs in the late Fortunian (Landing, 1993) and was considered as reminiscent of Ediacaran Cloudina reefs (Lee and Riding, 2018). Therefore, the Fortunian to mid-Age 2 reefs were assigned to a microbial-‘Ladatheca’ development interval by Lee and Riding (2018). Archaeocyath sponges (Debrenne et al., 2015) originated in the Tommotian of the Siberian Platform and formed the earliest diverse skeletal metazoan-dominated reefs of the Phanerozoic (Riding and Zhuravlev, 1995; Zhuravlev et al., 2015). They appeared slightly later in China in the Nangaoan(= Atdabanian of the Siberian Platform and Stage 3 in Fig. 9) (Yang et al., 2016a,b). Archaeocyath reefs are particularly abundant on the northern margins of the Yangtze Platform during the Nangaoan−Duyunian interval (= Stage 3−Stage 4 in Fig. 9), and eight growth phases of Archaeocyath reefs are well recorded in the lower Xiannudong Formation of the southern Shanxi Province of North China (Yang et al., 2016b). The highest archaeocyathid reef is 1−2 m in thickness and contains abundant metazoans and microbes, but these reefs suddenly disappear in the upper Xiannudong Formation with a fall in sea level (Yang et al., 2016b). Globally, archaeocyaths and their reefs lasted over ca. 23 million years (535−512 Ma) (Zhuravlev et al., 2015), and then vanished worldwide during the mid-Toyonian (Zhuravlev et al., 2015) or at the mid-Duyunian of China (= mid-Stage 4 in Fig. 9) (Yang et al., 2016a). Thus, midAge 2 to late Age 4 was the microbial-archaeocyathid reef interval (Lee and Riding, 2018). Microbe-mediated deposits, including stromatolites, thrombolites, dendrolites, giant ooids, oncoids, and flat pebble conglomerates (Fig. 10), are present throughout the Cambrian in China (Chen et al., 2009b; Lee et al., 2015, 2016; Adachi et al., 2015; Lee et al., 2015; Yan et al., 2017; Ezaki et al., 2017). Thrombolites, stromatolites, and other microbial reefs are extremely abundant within the Miaolingian strata (Fig. 10), and their renewed abundance has been interpreted as the consequence of the extinction of archaeocyaths (Fig. 9; Woo and Chough, 2010; Lee et al., 2014, 2015, 2016; Adachi et al., 2015; Qi et al., 2016, 2017; Yan et al., 2017; Ezaki et al., 2017). These microbemediated deposits display an overall decrease in abundance towards the end of Cambrian (Fig. 9). The number of calcified microbe genera surged during Cambrian Epoch 2, and then underwent a stepwise decline toward the end of Furongian (Fig. 9). Maceriate sponges constructed other metazoan-dominated reefs. They rose during the Drumian of Miaolingian and flourished during the late Cambrian (Furongian Epoch) (Fig. 9; Lee et al., 2015), which matches microbial-lithistid sponge reef development (Lee and Riding, 2018). The rapid increase of abundance in maceriate reefs, coupled with a decrease in microbialites (mainly thrombolites), occurred during the mid-Paibian (Fig. 9). This critical interval is also characterized by a gradual global increase in carbonate δ13C carbon isotopes (Steptoean Positive Isotopic Carbon Excursion; or SPICE), which lasted ca. 2−4 Myr (Saltzman et al., 2000, 2004; Lee et al., 2015). This SPICE is interpreted as increased burial of organic carbon, thereby implying high phytoplankton production and a cooling regime consistent with a sea-level fall. However, the cooling climatic conditions may have inhibited benthic microbe proliferation and been beneficial to the growth of metazoan and maceriate sponge reefs (Lee et al., 2015). Lithistid sponge-microbe reefs occurred in the Tommotian (late Terreneuvian) on the Siberian Platform and were constructed by lithistid sponges and Renalcis, as well as other bafflers (archaeocyaths, spiculate sponges, and hyoliths) (Riding and Zhuravlev, 1995). Similar lithistid sponge-microbe reefs are also commonly present in Cambrian Series 2 through Furongian strata (Adachi et al., 2015; Lee et al., 2014, 2015; Yan et al., 2017; Ezaki et al., 2017), and their occurrence only slightly fluctuates during the middle and late Cambrian (Fig. 9). Demosponges and coralmorphs joined microbes to form hybrid metazoanmicrobe reefs, but these are confined to Series 3 in the aftermath of archaeocyathid extinction (Ezaki et al., 2017).

Fig. 8. Cartoons showing comparable living states of Cloudina inhabiting microbe-metazoan reefs of the late Ediacaran in Namibia (left; modified from Penny et al., 2014) with those of tube-like microconchids within PTB thrombolites (right; modified from Yang et al., 2015a,b). Both Cloudina and microconchids seem to have shared similar morphology and lifestyles.

Wood and Curtis, 2014; Wood et al., 2017). The earliest bioturbation is also recorded in this Nama Group (Muscente et al., 2018). In China, except for within the widespread microbial reefs, Ediacaran metazoans (i.e., Cloudina and other metazoans) are commonly associated with thrombolites above glacial deposits in the Hubei-Shaanxi border areas (Hua et al., 2005). The coexistence of both microbes and metazoans seems to have set the agenda for minimal metazoan biodiversification during the late Ediacaran. Ediacaran reefs changed during this MMT from mainly microbial into mainly skeletal structures, and are characterized by microbial-Cloudina reefs in the late Ediacaran (Lee and Riding, 2018). In addition, Cloudina is morphologically comparable with microconchids that commonly dwelled in thrombolites near the Permian−Triassic boundary (PTB) (Yang et al., 2015a, b) (Fig. 8). Accordingly, to some extent, the late Ediacaran Cloudina-microbe reefs resemble the microconchid-rich microbialites that occur immediately after the PTB mass extinction, which suggests a scenario that the PTB post-extinction ecosystem, somehow, had been degraded to a return to Precambrian microbe-metazoan relationships (Knoll et al., 1996).

3.2. Cambrian The Phanerozoic begins with the well-known Cambrian explosion or Cambrian radiation (Zhuravlev and Riding, 2001), marked by emergence of new metazoan groups. As these evolved, shallow-marine substrates were fundamentally altered from Neoproterozoic microbially-cemented seafloors (hardgrounds) to bioturbated niches during the ‘Cambrian substrate revolution’ (Bottjer et al., 2000). Some Ediacaran-type microbial matground ecosystems persisted into the earliest Cambrian (Frustian) (Buatois et al., 2014). Tarhan et al. (2015) and Tarhan (2018) suggested that substratum bioturbation did not significantly change immediately after the Precambrian−Cambrian boundary. Global ichnodiversity, ichnodisparity (= architectural designs) and bioturbation data show that the main change in substratum bioturbation occurred during the late Fortunian (Mangano and Buatois, 2014; Buatois et al., 2016; Fig. 9). Modern-style intensities of sediment reworking on seafloors did not occur until at least the late Silurian due to the delayed appearance of sea-floor bulldozers (mobile infaunal deposit-feeders, such as bivalves, gastropods, trilobites, annelids), which are the most efficient bioturbators in modern marine settings (Tarhan, 2018). The Furongian through Early−Middle Ordovician was named as the Cambro-Ordovician bioturbation interval, preceded by the early−middle Cambrian bioturbation interval (Fig. 9; Tarhan, 2018). Tarhan et al. (2015) derived their data from siliciclastic successions. Cambrian carbonate successions in China have abundant vertical burrows of Skolithos (see interpretation of Knaust et al., 2018) and other trace fossils, which may require revision of this current bioturbation model if applied to all marine settings (Tarhan et al., 2015; Tarhan, 2018). The earliest Cambrian (Terreneuvian) reefs were dominated by stromatolitic and calcimicrobial buildups (Drosdova, 1980; Riding and 28

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Fig. 9. Estimated relative abundances of microbial and metazoan carbonates throughout the Cambrian, coupled with numbers of calcified microbe genera and with the extent of substrate bioturbations as indicated by ichnodiversity, ichnodisparity, bioturbation index and borrowing depth (Mángano and Buatois, 2014; Buatois et al., 2016). Note that sponge-microbe reefs are mainly lithistid sponge-microbe skeletal structures. Abbreviations: SPICE = Steptoean Positive Isotopic Carbon Excursion, Drum = Drumian, Guz = Guzhangian, Pai = Paibian, Jiang = Jiangshanian, BI = bioturbation interval.

3.3. Ordovician-Silurian

Alternations of metazoan and microbe reefs are rare; and such a metazoan-microbe reef-stacking pattern is present in Cambrian Series 2 and in the Furongian. Alternations of archaeocyath-dominated reefs and Renalcis thrombolites are present within the Xiannudong Formation of southern Shanxi (Yang et al., 2016b). Epiphyton- or Renalcis-dominated thrombolites are interbedded with maceriate reefs in the Zhangxia and Chaomidian formations of North China (Chen et al., 2009b; Woo and Chough, 2010; Lee et al., 2016; Yan et al., 2017; Fig. 6). Thrombolites/microbialites are interbedded with highly bioturbated carbonates or metazoan carbonates within Cambrian Series 2 through Furongian strata of North China (Fig. 11; Qi et al., 2014, 2017). Alternations of digitate stromatolites and Skolithos-bearing bioturbated limestone layers are conspicuous within the Zhangxia Formation of the Lushan-Dengfeng areas, Henan Province, North China (Fig. 11). Accordingly, the Cambrian MMT may be characterized by the change from the frequent occurrence of alternating microbialite layers and metazoan-bearing or bioturbated carbonate layers to these microbe-metazoan reef alternations.

The Early Ordovician saw the common occurrence of lithistid sponge-bryozoan and bryozoan-pelmatozoan reefs, and the decline in sponge-microbial reefs, marking the distinct shifts of reef constructions from microbial to metazoan reefs (Adachi et al., 2011). The Great Ordovician Biodiversification Event (GOBE, Harper, 2006; Servais et al., 2008, 2010; Servais and Harper, 2018) marks the first proliferation of metazoan reefs following the Cambrian MMT. Calathium reefs proliferated globally during the Early Ordovician, and Calathium-microbial reefs are common in China (Li et al., 2017d; Wang et al., 2017). In China metazoan-dominated reefs declined towards the Late Ordovician, and microbe-dominated build-ups again proliferated locally in carbonate settings (Fig. 6; Gong et al., 2013). Microbes increased again after the end-Ordovician mass extinction in China with local stromatolite resurgences during early Silurian (Sheehan and Harris, 2004, but see Stanley, 2011). However, in South China, there are no microbialites immediately after the end-Ordovician crisis because black shales of the Wufeng and Longmaxi formations overlie the O-S extinction horizon. These black shales are organic-rich

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Fig. 10. Typical microbe-mediated biosedimentary deposits within Miaolingian: (A) stromatolites, (B) thrombolites, (C) digitate stromatolite and flat pebble conglomerate, (D) oncoids, and (E−G) giant ooids from the Dengfeng area of Henan Province, North China (this study). A−B, D, E−F are from the Zhangxia Formation; C, G are in the Mantou Formation. The coin is 2 cm in diameter.

3.4. Late Paleozoic

and provide source rocks for shale gas (Zou et al., 2015; and Zou et al., 2019 in this volume). They are overlain by alternating fine-grained clastics and muddy limestone of the Shiniulan Formation in GuizhouChongqing, southwest China, which yield brachiopods, corals, crinoids, and rare stromatolites (Fig. 12; Li et al., 2017b). Not until the late Aeronian (Llandovery) are microbial and metazoan reefs present in China. Stromatolite buildups formed in the nearshore zone, whereas coral reefs grew on the outer-shelf ramp (Li et al., 2017b). Co-existence of microbial and metazoan reefs during the late Aeronian characterizes the early Silurian MMT in China (Fig. 6). The lower Silurian succession of South China is characterized by microbe-rich organic-rich shale in its basal part, rare benthic faunas with microbialite layers in the lowermiddle part, and alternations of abundant metazoan faunas, metazoan reefs and microbial reefs in the upper portion (Aeronian). Therefore, the early Rhuddanian (earliest Silurian) metazoan communities represent the initial recovery following the O−S crisis, and the Aeronian metazoan reefs in its upper part mark a full recovery of the marine ecosystem (Fig. 12).

The Late Devonian of China exhibits another surge in microbialdominated sedimentation following the Frasnian–Famennian (F–F) mass extinction. These microbialite deposits are not confined to the aftermath of the F–F extinction but had already become common during the Frasnian (Shen et al., 2010). In China, lower Frasnian reefs are typically built by stromatoporoids and corals (Fan, 1996; Chen et al., 2001, 2002; Gong et al., 2013; Fig. 13). Upper Frasnian reefs reflect the Late Devonian proliferation of coral-stromatoporoid reefs overlain by rare Famennian patch reefs (Copper, 2002). The overlying Famennian limestones contain stromatolites and thrombolites (Chen and Tucker, 2003). These are well-represented by the microbial reefs that developed in Guangxi and Hunan (Fig. 13; Shen et al., 1997, 2017; Yu and Shen, 1998; Chen et al., 2001, 2002), and represent a microbial ‘bloom’ following the F–F mass extinction (Yao et al., 2016b). This progression indicates that the Late Devonian MMT is much more extensive than those of other ages. As consequences of the F−F mass extinction and the subsequent 30

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Fig. 11. (A) Schematic composite stratigraphic columnar of Cambrian Series 2 to Furongian carbonate successions in the Lushan and Dengfeng areas, Henan Province, North China with MMT stacking patterns of microbe-dominated, metazoan-dominated and microbe-metazoan mixed units, and with stratigraphic distributions of trilobites, sponge spicules, echinoderms, and ichnofossils (Qi et al., 2014, 2016, 2017). (B) Alternations of stromatolites and highly bioturbated (Sk: Skolithos sp.) limestone (or carbonate piperock) in the Mantou Formation of Miaolingian age, Lushan (this study). (C) Close-up of digitate stromatolite (st) and limestone layers (this study).

diversified, and coral, bryozoans and macroalgae buildups had a resurgence (Yao and Wang, 2016; Yao et al., 2016a). After the mid-Carboniferous extinction interval (Chen et al., 2014d), a diversity of buildups, including those constructed by Palaeoaplysina, phylloid algae, and other macroalgae and with aragonitic radial-fibrous cements, developed in the Pennsylvanian strata of South China and northwestern China (Chen, 2012; Gong et al., 2013; Yao and Wang, 2016a). During the Permian, metazoan reefs underwent three major phases of flourishing. The first of these reefal proliferations occurred during the Early Permian in the moderate-latitude regions of the Urals and North America (Wahlman, 2002; Flügel and Kiessling, 2002) and also the Xinjiang areas of northwestern China (Chen et al., 2003). In contrast, metazoan reefs are very rare in the low-latitude South China region during this phase. Instead, oncoids of the Chuanshan Formation

Devonian−Carboniferous Hangenberg extinction event (Caplan and Bustin, 1999; Kaiser et al., 2016), metazoan buildups were very rare worldwide during the early Mississippian (earliest Carboniferous) (Webb, 1998, 2002). Instead, microbial buildups are often present during this time (Webb, 2002, 2005; Shen and Webb, 2004a, b) and probably were due to the demise of skeletal bioconstructors (Yao et al., 2016b). In South China, both stromatolitic and thrombolitic carbonate buildups dominate the reef and mound settings of the Tournaisian–Viséan (Chen et al., 2014d). These are characterized by microbial textures and the lack of any skeletal frameworks, like the typical Waulsortiantype reef/mound that was typically generated in relatively quiet, deepwater basin or slope settings (Lees et al., 1985; Aretz and Chevalier, 2007; Rodríguez-Martínez et al., 2010). With the metazoan radiation and recovery during the Viséan, most reef-forming organisms 31

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Fig. 12. Early Silurian MMT from Guizhou-Chongqing area, southwestern China. The composite lower Silurian stratigraphic column shows microbial units interbedded with metazoan units in the lower portion, and alternating microbial and metazoan reefs in the upper part (Aeronian). The columnar section and fossil distributions of the Shiniulan and Hanchiatien Formations are modified from Li et al. (2017b), while the succession of the Wufeng and Longmaxi Formations follows Gong et al. (2017). Hir. = Hirnantian, Ord. = Ordovician. WF = Wufeng Formation, Fm. = Formation, Dist. = distributions.

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Fig. 13. Depositional sequences of late Middle to Late Devonian carbonate successions from Guilin area, Guangxi Province, South China (Shen and Zhang, 1997; Shen et al., 2017). Alternations of metazoan and microbial buildups on the platform margin setting characterize this Late Devonian MMT.

Metazoan reefs had their third phase of resurgence during the Changhsingian until the eve of the P−Tr mass extinction (Shen and Xu, 2005; Gong et al., 2013). This succession of Wuchiapingian−Changhsingian development of metazoan and microbial reefs constitutes the Late Permian (Lopingian) MMT.

(also termed "Chuanshan balls" by locals) are widely distributed over an estimated area of some 500,000 km2 across the entire South China (Shi and Chen, 2006). These oncoids are unusually large (3−20 mm in diameter), microbial-mediated carbonate grains. A single oncoid bed within the Chuanshan Formation may be 2.5 m thick, and the whole oncoid-bearing succession may attain up to 12 m. These exceptional thicknesses of the Chuanshan oncoid-bearing interval have no parallels in modern oncoid deposits. The Chuanshan Formation yields fusulinids of the Triticites Zone, Sphaeroschwagerina moelleri Zone and Schwagerina tschernyschewi Zone, and therefore ranges from Gzhelian to Sakmarian, which spans the main episode of the Late Paleozoic Ice Age (Shi and Chen, 2006). Metazoan reefs had their second phase of global proliferation during the Middle Permian, when they were dominated by sponges and corals (Flügel and Kiessling, 2002), including those in the Maokou Formation of South China (Shen and Xu, 2005; Gong et al., 2013). However, these buildups collapsed near the end of the Capitanian (late Guadalupian) as part of the Guadalupian−Lopingian extinction wave (Chen et al., 2009a; Huang et al., 2019a). Therefore, the succeeding Wuchiapingian (early Late Permian) records only a few metazoan reefs worldwide, with only one sponge reef reported from South China (Huang et al., 2019c). Instead, microbial reefs are common, although coral biostromes are also occasionally present in the Wuchiapingian (Shen and Xu, 2005; Huang et al., 2019c). Coeval biosedimentary buildups reported from the Germanic Basin are mainly bryozoan-microbe reefs (Peryt et al., 2012, 2016; Raczynski et al., 2017).

3.5. Paleozoic–Mesozoic (Permian–Triassic) transition The Paleozoic–Mesozoic (also Permian–Triassic: P–Tr) transition witnessed the greatest crisis for life on Earth during the Phanerozoic. Marine ecosystems were severely devastated, but this was followed by the most profound recovery (Chen and Benton, 2012). One of the most distinct features of the P−Tr mass extinction (PTME) event in sedimentary systems is the extensive presence of microbialites within the overlying Lower Triassic succession. Chen and Benton (2012) had initially argued that microbes dominated the post-extinction oceans after PTME extinguished the majority of metazoans. However, microbialites do not occur throughout the entire Lower Triassic strata; but instead their occurrence seems to peak at four to six different time intervals during the Early Triassic (Baud et al., 1997; Pruss et al., 2006). However, few studies have examined the microbial development and preservational forms between those apparent microbialite peak intervals of the Early−Middle Triassic. We don't know whether microbes were also abundant in the intervals between the microbialite-buildup intervals, and what forms of microbes, if they occur, are preserved in those intervals. 33

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(caption on next page)

Chatalov, 2017). They are vaguely grouped into a broad "anachronistic facies" (e.g., Baud et al., 2007) or "microbially induced sedimentary structures" (MISS; Noffke et al., 2003). These include oncoids, giant ooids, microbial mats, sand veins, wrinkle structures, vermicular

In fact, in addition to these distinctive microbialites, other unusual biosedimentary facies are preserved worldwide within Lower Triassic successions (Pruss et al., 2006; Baud et al., 1997, 2005, 2007; Mata and Bottjer, 2012; Woods, 2014; Abdolmaleki and Tavakoli, 2016; 34

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Fig. 14. A dozen types of common unusual biosedimentary buildups and structures of ‘anachronistic facies’ or MISS from China that occurred in the aftermath of the end-Permian mass extinction. (A−D) Stromatolites from the Lower Triassic of South China; A, C, from the Daye Formation, Lichuan (Fang et al., 2017b); B, from the PTB beds, Lichuan (Pei et al., 2019); D, the Lower Triassic Nanlinhu Formation, Susong (Luo et al., 2016). (E−F) Thrombolites from the PTB beds, Guangan (this study). (G) Dendrolites from the PTB beds, Xiushui (Wu et al., 2017). (H, K) Wrinkle structures; H, from the Lower Triassic Xiahuangcang Formation, Qinghai (Feng et al., 2019); K, from the Lower Triassic Liujiagou Formation, Yiyang (Tu et al., 2016). (I) Microbial mats from the lower Middle Triassic Guanling Formation, Luoping (Luo et al., 2013). (J, L) pictograph-like and polygonal sand crack-fills; J, from the Lower Triassic Xiahuangcang Formation, Qinghai (Xu et al., 2017); L, from the Lower Triassic Liujiagou Formation, Yiyang (Tu et al., 2016). (M) Giant ooids from the Lower Triassic Daye Formation, Lichuan (this study). (N) Oncoids from the Lower Triassic Daye Formation, Lichuan (this study). (O) Vermicular limestone from the Lower Triassic Daye Formation, Daxiakou (this study). (P) Flatpebble conglomerate from the Lower Triassic Daye Formation, Daxiakou (this study). (Q) Carbonate cement fans from the Anisian (early Middle Triassic) Qingyan Formation, Guiyang (this study). (R) Calcareous nodules within claystone from the Lower Triassic Xiaqinglong Formation, Jurong, southern Jiangsu Province (this study).

limestones, flat-pebble conglomerates, cement fans, and limestone nodules in claystone (Fig. 14). Interestingly, most of these sedimentary features also occur within the Cambrian carbonate successions, and their resurgences within the Lower Triassic hints at a temporary return to a more primitive ocean ecosystem (Baud et al., 2007). These "anachronistic facies" are widely distributed in the Lower Triassic of China (Zhao et al., 2008). We will briefly examine some of the sedimentary characteristics of these various microbially induced deposits or structures.

microbialites through the Early–Middle Triassic may have peaked at six separate intervals: earliest Griesbachian, late Griesbachian–early Dienerian, early Smithian, late Smithian, late Spathian, and early Anisian (Pruss et al., 2006; Baud et al., 2005, 2007; Mata and Bottjer, 2012; Chen et al., 2014b; Luo et al., 2014, 2016; Fang et al., 2017a,b). These six occurrence peaks of Early−Middle Triassic microbialites are recorded in China (Fig. 15). Their distributions, however, are strongly uneven, with the greatest number (up to 34) of published sites being the microbialites near the PTB (or earliest Griesbachian), followed by the late Spathian microbialites reported from five sites; but the other microbialite peak periods are indicated by the presence of numerous microbialite-type or MISS features (mainly stromatolites) (Fig. 15). In summary, the PTB-microbialites are dominated by thrombolites and dendrolites with a few cases of stromatolites; whereas the microbialites of other ages are dominated by stromatolites, with few thrombolites occurring within the upper Spathian microbialites. The PTB-microbialite not only straddles the PTB, but also is immediately above the P−Tr mass extinction and therefore has attracted considerable interest from geologists (Chen and Benton, 2012). The

3.5.1. Microbialites (stromatolite, thrombolite, dendrolite) Microbialites are widely recognized from P–Tr boundary beds throughout the tropical Paleo-Tethyan region (Kershaw et al., 2012). They are also commonly present in the Lower Triassic and locally within the lower Anisian (early Middle Triassic) (Baud et al., 2007; Luo et al., 2014). It thus appears that microbes proliferated rapidly immediately after the mass extinction, and continued in importance throughout the Early Triassic and into the early Anisian (Luo et al., 2014). Our updated database suggests that the resurgence of

Fig. 15. Spatial distributions of Early-Middle Triassic microbialites in South China. The six peak episodes of microbialite occurrences are represented by various symbols. Localities 1−34 represent PTB microbialites (PTBMs); 35 has Dienerian stromatolites; 36 has early Smithian stromatolites; 38 has late Smithian stromatolites; 39−43 represent late Spathian stromatolites; and 44−46 are early Anisian stromatolites. Section number codes: 1-Yudongzi, 2-Panlongdong, 3-Xiejiacao1, 4Jianshuigou, 5-Baizhuyuan, 6-Dongwan, 7-Tudiya, 8-Laolongdong, 9-Wenxinchang, 10-Xiejiacao, 11-Ruiping, 12-Cili, 13-Chongyang, 14-Xiushui, 15-Xishan, 16Ziyun, 17-Rongbao, 18-Laibin, 19-Dajiang, 20-Heping, 21-Dongjiawan, 22-Xinbaihou, 23-Hochang, 24-Jinya, 25-Tianwan, 26-Zuodeng, 27-Longling, 28-Leye, 29Lingyun, 30-Taiping, 31-Fengshan, 32-Donglan, 33-Pingguo, 34-Tieshikou, 35-Xingyi, 36-Lichuan, 37-Zigui, 38-Wuxi, 39-Xiejiacao2, 40-Susong, 41-Chaohu, 42Fanchang, 43-Liyang-1, 44-Luoping, 45-Shizong, 46-Liyang-2. Detailed information for these microbialites is in Table S1. 35

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may have enhanced the rapid formation of these intriguing carbonates (Luo et al., 2016). However, their volumetric contribution to the formation of microbialites might be limited due to their tiny size and relatively low abundance. In addition to various forms of putative cyanobacteria, a variety of metazoans, such as foraminifers, microgastropods, microconchids, ostracods and bivalves, are also abundant within the PTB-microbialites (Yang et al., 2015a,b). This implies that metazoans were not as rare in this type of post-extinction microbialite ecosystem as previously thought; and their presence signifies a pioneering recovery of shelly faunas in niches within the microbialite after the first phase of the P−Tr mass extinction. The cyanobacteria and other microbes were primary producers that essentially provided the necessary nutrition for the revival of shelly faunas. Therefore, the post-extinction microbialite ecosystems may not have been hostile for some metazoans, but instead provided special habitats to re-diversify the fauna in the aftermath of the major biocrisis. In contrast to the PTB-microbialites with their dominance by thrombolites, the microbialites at the higher horizons of the Lower and Middle Triassic are dominated by stromatolites. In particular, the Smithian stromatolites not only yield the best-preserved microorganism assemblages (Fig. 17A−C, E), but also formed the largest (thickest) microbial reefs (up to 16 m in thickness; Fang et al., 2017b) among all Lower−Middle Triassic microbialites in the world. The filament sheathes are well preserved and are comparable with the modern-day cyanobacteria sheaths from the stromatolites of Shark Bay, Western Australia (Fig. 17D). Both pyrite framboid analysis and geobiologic features indicate that these stromatolites likely grew in a well-oxygenated environment (Chen et al., 2014b; Fang et al., 2017b). However, even though the oxygen conditions should have been favorable, no metazoans have been detected in these younger microbialite systems, in sharp contrast to the abundant and diverse metazoans that inhabited the PTB-microbialite ecosystem (Yang et al., 2011, 2015a,b; Forel et al., 2013; Forel, 2015; Foster et al., 2017, 2018). This implies that oxygen levels were not the primary factor controlling the distributions of microbes and metazoans in microbialite ecosystems.

underlying uppermost Permian bioclastic limestone usually has an irregular top surface, which has been interpreted as a submarine dissolution surface due to oceanic acidification, or as a subaerial exposure surface owing to a sea-level fall prior to the establishment of the overlying microbialite (Payne et al, 2007, 2009; Collin et al., 2009; Yin et al., 2014; Lehrmann et al., 2015). A complete PTB-microbialite unit spans the stratal interval ranging from the equivalents of the latest Permian conodonts Clarkina meishanensis Zone, C. changxingensis Zone, C. taylorae Zone, and basal Triassic Hindeodus parvus and Isarcella staeschei Zones of the Meishan GSSP biozonation (Chen et al., 2015). However, of these, the first three conodont zones of latest Permian are usually missing at the base of the PTB microbialite unit due to the hiatus represented by the irregular surface capping the uppermost Permian bioclastic limestone (Yin et al., 2014). The basal parts of most PTB-microbialites possess stromatolites or oolites, the latter indicating a high-energy condition near the fairweather wave base (Fang et al., 2017a; Wu et al., 2017; Tang et al., 2017; Pei et al., 2019). However, most thrombolites, which are common in the main body of PTB-microbialites, are interpreted to grow in relatively low energy conditions between the fair-weather wave base and the storm wave base (Fang et al., 2017a); and in a few cases, microbialites are interpreted to have grown in a low-energy offshore setting below the storm wave base (Kershaw et al., 2012). Such a quiet environment should have been favorable for the deposition of volcanic products (e.g., glass, high-temperature quartz). However, the PTB microbialite contains much less volcanic grains in comparison with the relatively high contents of volcanic products within the underlying Permian bioclastic limestone (Pei et al., 2019). Thus, returning to the dating controversy, it is difficult to envision how the volcanic ashes that cap the PTB-microbialite could be reworked products derived from nearby ashes that are below the PTB-microbialite without also resulting in deposition of volcanic grains during the formation of the intervening PTB-microbialite. The rarity of volcanic products within the PTB-microbialite also indicates that volcanism was apparently not active during the growth of the PTB microbialite, implying that it was not directly related to volcanism (Pei et al., 2019), in contrast to earlier suggestions (Xie et al., 2010). Even if the radiometric age estimate is not presently reliable (Bagherpour et al., 2017), correlation of the conodont biostratigraphy within the microbialite with their counterparts at the Meishan GSSP suggests that the PTB-microbialite spanning the H. parvus and I. staeschei Zones may have formed in only ~30 kyr based on radiometric dating by Burgess et al. (2014). Several other aspects of the PTB-microbialites remain enigmatic despite extensive studies. The most debated issues include 1) what were the geobiologic accretion process and the biologic ecosystem, 2) what was the redox condition, 3) was the environment hostile for metazoan inhabitation, 4) how do the various PTB-microbialites vary in their ecosystem composition, and 5) did subaerial exposure or submarine acidification contribute to the genesis of the irregular surfaces beneath these PTB-microbialites? Except for the last question, a series of studies on the microbialites, such as those at Xiushui, provides some insights. Recent geobiologic studies revealed that Gakhumella-like columns are very common in the PTB-microbialites (Fig. 16F–J); therefore, Gakhumella-like microorganisms likely have played an important role in constructing these microbial reefs (Fang et al., 2017a; Fig. 16). Spheroid microfossils are also frequently reported from the PTB-microbialites (Wang et al., 2005; Mastandrea et al., 2006; Perri and Tucker, 2007; Yang et al., 2008, 2011; Ezaki et al., 2008, 2012; Chen et al., 2014b; Luo et al., 2014, 2016; Adachi et al., 2017; Fang et al., 2017a). These calcispheres are often interpreted as algal cysts (Luo et al., 2016; Fig. 16A–B). Some relatively large, coccoid-like spheroids (60–150 μm in diameter) and clump-like spheroids of presumed bacterial origin are also commonly present in the PTB-microbialites and within microbialites of other ages (Luo et al., 2016; Fang et al., 2017a; Fig. 16C–D). These larger spheroids are related to microorganisms that

3.5.2. Microbially induced sedimentary structures (MISSs) Post-extinction proliferation of microbes in siliciclastic shallowmarine and terrestrial settings is also indicated by widespread microbially induced sedimentary structures (MISSs) (Chu et al., 2015; Tu et al., 2016; Xu et al., 2017; Feng et al., 2019). Of these, matground (microbial mats) (Fig. 14I), pictograph-like and polygonal sand crackfills (Fig. 14J, L) and wrinkle structures (Fig. 14H, K) are most common forms of MISSs recorded in Lower–Middle Triassic strata (Pruss et al., 2004; Mata and Bottjer, 2009; Luo et al., 2013; Chu et al., 2015; Tu et al., 2016; Xu et al., 2017; Feng et al., 2019). Proliferation of Early Triassic MISS-related microbial mats implies that the P–Tr mass extinction provided favorable habitats for MISS development in both marine and terrestrial ecosystems. For example, increases in MISSs appear to coincide with die-back of terrestrial vegetation, disappearance of coal beds, extinction of pareiasaur tetrapods, and decreased bioturbation of lacustrine sediments (Chu et al., 2015). However, MISSs may occasionally form as unusual biofacies that juxtapose both intense infaunal and epifaunal bioturbation, and thus may have also provided an oasis for post-extinction fauna to flourish in shallowmarine environments in aftermath of the PTB-microbialite (Feng et al., 2019). 3.5.3. Giant ooids/oolitic limestone Like microbialites, oolites are also widely distributed worldwide within Lower Triassic carbonates (Li et al., 2015, 2017c, 2019). In particular, some giant ooids (> 100 μm in diameter) are conspicuous in PTB intervals worldwide, where they often are associated with microbialites or are within other carbonates. For example, the well-known Tesero Oolite Bed in the Southern Alps of Italy that immediately 36

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Fig. 16. Common microfossils in the PTB-microbialites in South China. (A−B) Microphotograph showing coccoid-like micritic spheroids that possess sparitic nuclei surrounded by micrite envelopes. (C−D) Microphotographs showing clumped bacteria-like spheroids that embrace micritic nuclei surrounded by thin sparry rays. (E) Microphotograph showing Renalcis-like calcimicrobes. (F−G) Gakhumella-like column aggregates and single column, suggestive of putative cyanobacteria. (H−J) SEM images showing Gakhumella-like columnar structures. Images A, C−D are from the Susong section, Anhui Province, South China (Luo et al., 2016), while images B, E−J are from Zuodeng section, Guangxi Province, South China (Fang et al., 2017a).

mediated carbonate precipitates, and represent one of the most common anachronistic facies widespread in the Early Triassic oceans. In South China, in addition to the PTB oolite units, giant ooid banks developed four times throughout the Early Triassic: earliest Griesbachian, late Griesbachian, early Dienerian, and early Smithian (Mei and Gao, 2012). These four regional expansions of giant ooids appear to be coupled with microbial blooms. Those four occurrence peaks of Early Triassic ooids have been interpreted to be related with coeval large transgressions (Mei and Gao, 2012). Such massive ooid banks are particularly well developed in the Upper Yangtze region of the South China block. For example, a 30-m-thick ooid bank (Fig. 19A), together with a large stromatolite (16 m high), was built during the early Smithian in the Lichuan area, western Hubei Province, South China (Fang et al., 2017b). The ooid shapes are circular, compound, superficial and irregular (Fig. 19B−C). Some interior layers within the ooids exhibit intense fluorescence (Fig. 19D−K), indicative of microbial organo-mineralization, which may have contributed to the formation of these ooids. Oncoids (Fig. 14N) are also commonly present in shallow-shoal facies of Lower Triassic successions worldwide, and they are often associated with ooid banks (Li et al., 2015). Some algae, i.e. Girvanella, are

overlies the end-Permian mass extinction horizon yields abundant normal-sized and giant ooids (i.e., Bulla section; Gorjan et al., 2007) (Fig. 18). These Tesero ooids are therefore stratigraphically equivalent to the PTB-microbialites in South China. PTB ooid banks have been recorded from at least 38 sections around the world, of which more than half are associated with the PTB-microbialites (Li et al., 2013, 2015). Ooids were previously considered as one of the common abiotic carbonate grains that mostly form in local environments characterized by relatively high-energy, agitated hydrodynamic conditions (Flügel, 2004). However, ancient ooids record imprints of primitive nano-scale extracellular polymeric substances (EPS) and have similar rare earth element (REE) compositions and distributions to that of modern-day seawaters (Li et al., 2017c). These characteristics suggests that microbes may have been involved in the formation of the ooids, particularly of the giant ooids (Li et al., 2017c). After examining the possible influence of microbial organo-mineralization in the formation of modern-day ooids, Batchelor et al. (2018) developed a mathematical model for ooid growth. The model concludes that the biofilms and growth rings of ancient ooids are comparable with those observed in experimentally grown ooids in a microbe-rich environment. Accordingly, ooids and giant ooids are likely microbe37

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Fig. 17. (A−C, E) SEM images showing well-preserved filament sheaths from the dark laminae of stromatolites of Smithian age preserved in the Kockatea Shale Formation of northern Perth Basin, Western Australia (Chen et al., 2014b). (D) Living filaments under the microscope from modern stromatolites in the Shark Bay, Western Australia (this study).

like structures on the surface and within the rock. The worm-like structures vary in shapes, and they are usually densely packed within the rock. Their origin still remains enigmatic despite intensive study (Zhang and Tong, 2010). Although some authors proposed that strong bioturbation might have resulted in the formation of vermicular limestone (Woods, 2014), this scenario of metazoan biotic origin needs to be further confirmed. Limestone nodules within claystone facies are another possible sediment facies with microbe-mediated carbonate cementation (Figs. 14R, 20). Recently, Yang et al. (2019) found in-situ stromatolitelike structures and cement fans within limestone nodules in claystone strata from the lowest Triassic succession of the Tieshikou section on the southern margin of the eastern Yangtze Platform, South China. The columnar structures resemble mini-stromatolites in profile, while most branches are patchy or stripe-shaped, with clotted structures in plan view, resembling those of a thrombolite. Fan-shaped cement precipitates consist of multiple crystal fans that have a radiating texture and show distinct growth laminae. The radiating fabrics contain rodshaped filaments indicative of a microbial origin. Abundant nano-scaled organic grains (intraparticle micropores, fibrous biofilms, and filamentous sheaths) and EPS are detected in those stromatolite-like structures (Fig. 20), demonstrating that microbes may have participated in the formation of these limestone nodules interbedded in claystone strata. The finding of stromatolitic nodules implies that the widely distributed nodular claystone or argillaceous limestones of Early Triassic successions in South China may have been deposited in microbe-rich environments in which terrigenous supply was abundant. Cement fans formed on sea-floor are also very common in Lower Triassic successions outside South China (Woods et al., 2007; Kershaw et al., 2011; Woods, 2014; Friesenbichler et al., 2018). They are certainly related to the enhanced precipitation of calcium carbonate

observed within the oncoids, which suggests that microbes were involved in the formation of these biosedimentary grains (Flügel, 2004; Shi and Chen, 2006). 3.5.4. Other anachronistic facies Other common anachronistic facies of Lower Triassic in China also include vermicular limestone (Fig. 14O), flat-pebble conglomerate (Fig. 14P), carbonate cement fans (cement precipitates), and limestone nodules within claystone (Figs. 14R, 20). Of these, flat-pebble conglomerates had been common within Cambrian to Lower Ordovician carbonate successions, but then became very rare after that time. Recurrent flat-pebble conglomerates in the Lower Triassic suggest a temporary return to a similar environment as in Cambrian times. In South China, flat-pebble conglomerates are encountered in settings ranging from storm-dominated platform carbonates to the deep basin. Their origin is still problematic (Wignall and Twitchett, 1999), although storm currents are believed to have been involved. However, most fragmented sediments caused by rolling during storm currents are usually irregular in shapes and are usually randomly orientated. Thus, the thin clasts in the flat-pebble conglomerate imply that they likely underwent an early lithification prior to their fragmentation. Wignall and Twitchett (1999) interpreted this process as twofold: an initial suppression of bioturbation that allowed the preservation of thin beds, which was then followed by rapid submarine lithification. In fact, microbial sealing could directly prevent the fragmentation of thin beds when being rolled by storm currents. Therefore, microbes likely may have been involved in the formation of flat-pebble conglomerates during the Early Triassic. Vermicular limestone is another problematic type of carbonate sediments that is commonly present in the Lower Triassic successions in South China (Fig. 14O). They are characterized by dark-colored worm38

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metazoan reefs co-occurred during the early Middle Triassic, prior to the full recovery of marine ecosystems in the late Pelsonian or middlelate Anisian (i.e., the Luoping biota and Qingyan faunas; Chen and Benton, 2012). Accordingly, the Early through Middle Triassic MMT (Fig. 6) represents a characteristic post-extinction ecosystem trend that lasted for ~7–8 Myr following the P–Tr mass extinction (Chen and Benton, 2012). 3.6. Triassic−Jurassic and Cretaceous−Paleogene transitions Mass extinctions at the Triassic−Jurassic and the Cretaceous−Paleogene boundaries severely impacted biodiversity and ecosystems. But, in contrast to the Paleozoic and PTB cases, metazoans recovered relatively quickly from those biotic crises and no microbial communities and sediments are known to widely represent post-extinction ecosystems at those episodes, although some microbially induced sediments are locally present (e.g., in the lowest Jurassic of England; Ibarra et al., 2014, 2016; Kershaw and Guo, 2016; Peterffy et al., 2016). The sediment successions following the Triassic−Jurassic extinction are, in most cases, characterized by bioclastic limestone, thereby indicating metazoan involvement in Early Jurassic biosedimentation. Although there is a secondary peak of microbial carbonate abundance in the Middle Jurassic, this is probably due to the early Toarcian Oceanic Anoxic Event (T-OAE) (see below), and contemporaneous metazoan buildups are quite abundant (Figs. 5−6). Hence, no MMT trend can be recognized in this Early Jurassic time interval. Similarly, no widespread microbial sediments have been seen in the aftermath of the Cretaceous−Paleogene extinction. 3.7. General development stages of MMT The Ediacaran MMT initiated with matground-dominated ecosystems, followed by alternating successions of microbial mats and multicellular organisms of Ediacara-type or trace-making animals. The establishment of this MMT was marked by the co-existence of both Cloudina-dominated reefs and microbialites during the late Ediacaran (Penny et al., 2014). Similarly, the Cambrian MMT also started with microbe-dominated successions in its initial stage, and then is characterized by alternating successions of matground substrate and bioturbated substrate. Two peaks in metazoan occurrence, with the dominance by abundant Archaeocyathid reefs during the Miaolingian and the dominance by maceriate sponge reefs during the late Furongian (Chen et al., 2014c; Lee and Riding, 2018; Fig. 9), mark the establishment of the Cambrian MMT. Metazoan reefs (i.e., stromatoporoids, bryozoan-tabulates, and receptaculitids) were not present until the Middle Ordovician (Lee and Riding, 2018). Moreover, both microbe-dominated buildups and the microbe-lithistid sponge associations occurred throughout all development stages of Cambrian MMT. The early Silurian MMT is dominated by a thick accumulation of organic-rich black shales during its initial stage, followed by alternating microbe-rich sediments and metazoan-bearing deposits. These were eventually replaced by coeval microbial and metazoan reefs and then by metazoan reef-dominated ecosystems in the late early Silurian (Li et al., 2017a). The Late Devonian MMT was initiated in the prelude to the Frasnian–Famennian crisis, is characterized by alternating occurrences of abundant microbial and metazoan reefs, and persisted into the early Mississippian. Widespread metazoan reefs did not return until the late Mississippian (Yao and Wang, 2016). The Early−Middle Triassic MMT began immediately after the P–Tr mass extinction. Its initial phase is characterized by microbe-mediated sediments and has an anomalous global abundance of microbialites and oolites, plus an assortment of anachronistic facies, such as oncolites, vermicular limestone, flat-pebble conglomerates, and wrinkle structures (Fig. 14). Alternations of microbe-mediated deposits and metazoan-bearing or bioturbated successions are also commonly present

Fig. 18. Polished surface showing ooids from lower Tesero Oolite Unit (Bed 8 of Gorjan et al., 2007) of the Werfen Formation, Bulla section, Southern Alps, northern Italy (this study).

(Woods, 2014), but some microbial signals have been detected from similar cement carbonates, i.e., calyx-shaped carbonate crystal fans of the Lower Triassic in Oman (Heindel et al., 2015). Although cement fans have not been reported from the Lower Triassic, they occur occasionally in the lowest Middle Triassic in Qingyan area of Guiyang City, Guizhou Province (Fig. 14Q), just before the full recovery of metazoans in the mid-late Anisian (Chen and Benton, 2012). 3.5.5. MMT stacking patterns in the Lower and Middle Triassic Microbial reefs dominate the Lower Triassic carbonate buildups in most regions of the world. This means that, although a few metazoanmicrobe associations locally proliferated in open carbonate ramp settings, the microbe-dominated communities prevailed in the oceans in the aftermath of the PTME. Microbes may have been active in forming sediments other than microbialites, as in the anachronistic facies types discussed above, but were not continuously dominant. For example, there are highly bioturbated limestone layers interbedded with vermicular limestone and flat-pebble conglomerates, indicating an alternation of microbe-dominated and metazoan-dominated units within some Smithian−Spathian (Olenekian) successions (Fig. 21). There are a few massive sponge-microbial buildups known from Griesbachian−Dienerian strata in Armenia (Friesenbichler et al., 2018) and some small sponge-microbial patch reefs occur locally within Smithian strata in the western US (Brayard et al., 2011), but these seem to be rare situations during the Early Triassic. In contrast, metazoandominated reefs (i.e., Tubiphytes, sponges) started to proliferate during the early Middle Triassic (Payne et al., 2006), although individual Tubiphytes have been reported in the Lower Triassic (Song et al., 2011). At the same time, stromatolites were also common during the Early Triassic and early Anisian (Luo et al., 2014, 2016). Both microbial and 39

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Fig. 19. Giant ooid bank from the upper Daye Formation (early Smithian) in the Lichuan area, western Hubei Province, South China (after Fang et al., 2017b). (A) Surfaces of one sample from the basal part of Bed 7 showing ooids are arranged along the laminated layers to form distinct ‘ooid laminations’ (white arrows) or 'oolitic lenses' (black arrows). Giant ooids form laminae (arrows) in the outcrop. (B) Two different sizes of ooids in an oolitic grainstone composed of giant ooids (orange arrows) with local oolite intraclasts (red arrow). The sample was etched by diluted hydrochloric acid. (C) Weathered surface of oolitic grainstone from Bed 2 showing aggregation of giant ooids. (D−K) Photomicrographs of ooids in plane-polarized transmitted light (D, H) and different wavelengths of fluorescent light under various exciting light wavelengths (E–G, I–K). Note that dark laminae in ooid samples are all actively responding to exciting light wavelengths, reflecting a high content of organic matter. In contrast, the coarse-grained dolomite or calcite cement responds poorly to fluorescent light, pointing to a lesser content of organic matter.

Chen and Benton (2012). Microbe-sponge associations occur throughout all stages of MMT, and thus seem not to indicate a recovery of the ecosystem.

during the late Early Triassic (Fig. 21). Microbe-sponge buildups or patch reefs occurred throughout the Early Triassic, but typical metazoan reefs did not appear until the early Middle Triassic, and they dominated marine ecosystems of the late Middle Triassic (Payne et al., 2006). Accordingly, the deep-time MMTs seem to have undergone four development stages (A–D; Fig. 22). They initiated with microbe-dominated successions (Stage A), and then are characterized by alternations of microbe-dominated and metazoan-bearing or bioturbated successions (Stage B). Both microbial and metazoan reefs co-occurred during Stage C, then a dominance of metazoan reefs marks development Stage D (Fig. 22). Both Ediacaran and Cambrian MMTs experienced the first three development stages (Stages A–C), but lacked Stage D. In contrast, the full set of Stages A–D of MMT development are fully recorded in the post-extinction successions of three major Phanerozoic mass extinctions. Stage A of MMT is coupled with rather low levels of metazoan biodiversity and bioturbation due to the dominance of microbes in the ecosystem. Stage B saw frequent variations of biodiversity and bioturbation levels due to alternating occurrences of microbes and metazoans in the stratigraphic successions. MMT Stage C is characterized by varied biodiversity and relatively high bioturbation levels, and Stage D witnessed high and stable biodiversity and bioturbation levels (Fig. 22). Thus, MMT Stage A reflects the survival stage immediately after a major mass extinction, Stages B and C characterize the initial recovery stages, and Stage D attains the full recovery of biotas, following the stepwise recovery model of marine ecosystems proposed by

4. Climatic and environmental perturbations during major MMTs 4.1. Ediacaran and Paleozoic MMTs After the Snowball Earth event, a set of major negative and positive shifts of carbon isotopes recorded in the Ediacaran sequences indicate a succession of perturbed ecosystems (e.g., Zhu et al., 2007), of which the extended Shuram-Wonaka event is the largest known negative carbonisotope excursion in the geologic record and has been recognized worldwide (Grotzinger et al., 2011). Several anoxic-oxic redox switches are also recognized from the Doushantuo Formation of South China (Li et al., 2010, 2019). Various geochemical proxies show that shallow parts of the ocean became largely oxic (Sperling et al., 2015), although oceans could be redox-stratified with significant euxinic wedges (Li et al., 2019) after the Shuram-Wonaka excursion. The oceans became completely oxic during the last 10 Myr of the Ediacaran. The frequent anoxic conditions facilitated microbial proliferation during the earlymiddle Ediacaran, whereas the oxygenated oceans of the late Ediacaran were beneficial to the rise of multicellular animals (McFadden et al., 2008). Thus, the late Ediacaran MMT trend was coupled with environmental perturbations and variations of oxygen contents in the ocean. 40

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Fig. 20. Limestone nodule embedded within claystone near the P–Tr boundary and its microstructures from South China (Yang et al., 2019). (A) Limestone nodules embedded within claystones slightly above the P–Tr boundary in the Tieshikou section, Xinfeng County, southern Jiangxi Province. Inset cartoon diagram showing in-situ preservation of a limestone nodule embedded in claystone. (B) Single nodule showing bowl-shaped outline. (C–F) Stromatolite-like and carbonate cement structures within a limestone nodule. Note that the brown-colored columns are photographed under plane polarized light, while the green-colored columns are Photoshop-enhanced.

Late Ordovician (Jin et al., 2018); therefore, the active cool-water upwellings may have prevented the proliferation of metazoan reefs. During the Phanerozoic, life on Earth experienced the “Big Five” mass extinctions of the end-Ordovician, end-Frasnian, end-Permian, end-Triassic and end-Cretaceous (Sepkoski et al., 1981), plus up to 15 additional lesser extinction events (Chen et al., 2014a). Geochemical proxies reflect several of these major biotic extinction and environmental events. Distinct geochemical signatures, which are well recorded in China, characterize depositional systems during several of these and other major life and environmental turning points, such as the extinctions at the O−S boundary, F−F boundary, Guadalupian−Lopingian (G−L, Middle−Late Permian) boundary, and during oceanic anoxic events (OAEs) of the mid-Jurassic and mid-Cretaceous (Fig. 23). The end-Ordovician (Hirnantian) biocrisis was the first of the five severe extinctions, and has been ranked as the second largest Phanerozoic biocrisis by many authors (Rong and Huang, 2014). Marine life suffered two discrete pulses of mass extinction associated with the coupled climatic and oceanographic effects of the extraordinary ice sheet advance and demise at Gondwana's South Pole during the latest Ordovician (Harper et al., 2014). The first extinction pulse is the largest loss of nektonic and planktonic species, as well as those living in shallow shelf and deeper water environments, followed by the appearance of the presumably cool-adapted Hirnantia fauna (Sheehan, 2001). Several effects, such as glacial-induced cooling, falling sea level and chemical recycling in the oceans, have been proposed as killing mechanisms for this first extinction phase (Zou et al., 2018). The second pulse is less well defined, but is associated with the end of a positive δ13C excursion and includes the demise of the Hirnantia fauna. This second phase during a distinct transgression through the late Hirnantian and beginning of the Silurian is also clearly linked with a near-global anoxia (Rong and Huang, 2014). Widespread euxinia

Immediately after the early Cambrian explosion of metazoan life, marine substrates did not change too much; instead, the earliest Cambrian seafloors share many similarities to the Ediacaran according to various ichnoecologic measures (Buatois et al., 2017). However, carbon isotopes underwent dramatic variations during the early Cambrian, with a negative excursion to -8‰, followed by a positive surge up to +5−6‰, for a total variation amplitude of 13−14‰. The late Cambrian has only slightly lesser amplitudes in the carbon-isotope excursions of ~8−10‰; meanwhile, sulfur isotopes had a major variation amplitude of 25‰. These major and frequent excursions in both carbon and sulfur isotopes indicate that the Cambrian MMT trend was also coupled with environmental perturbations and oxygen-deficient conditions (Saltzman et al., 2000, 2011, 2015; Lee and Riding, 2018). At the same time, global sea surface temperatures were usually hot (> 30°C), and did not cool significantly until the mid-Ordovician (Trotter et al., 2008). This global regime of elevated seawater temperatures may have stimulated the calcification of microbes (Riding, 2005), and thus expedited microbial carbonate buildups. The resulting biosedimentary responses are the widely distributed microbe-mediated buildups and structures within the Cambrian successions. However, the environmental perturbation responses that favored alternating microbe-dominated and metazoan-dominated layers versus an abundance of metazoan reefs still remain unclear. Chinese records show a clear decline in abundance of metazoan reefs coupled with resurgence of microbe-dominated build-ups towards the Late Ordovician (Fig. 5; Gong et al., 2013). This pattern contrasts with the Ordovician in Laurentia in which tabulate and rugose corals and stromatoporoids formed reefs almost everywhere during the Middle and Late Ordovician (Geldsetzer et al., 1989). This could be because the Chinese plates were situated at the equatorial ‘cool-water tongue’ impacting this part of the peri-Gondwana region during the 41

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concluded that the combination of these simultaneous effects resulted in the end-Ordovician catastrophe. Perturbed environments persisted into much of the early Silurian. However, a relatively fast recovery (< 1 Myr) of benthos occurred during the earliest Silurian; and both microbial and metazoan reefs did not re-appaer until the late early Silurian (Li et al., 2017b; Fig. 23). The first part of the early Silurian MMT is characterized by alternations of microbe-mediated siliciclastic sediments and benthic fauna-rich layers; and carbonate deposits of MMT occurred during the late early Silurian (Fig. 23) in China. In contrast, no microbialites occurred in the lower Silurian on the Baltic and Laurentian plates, although the Late Ordovician is marked by a pair of coralstromatoporoid reef extinctions – one at the end of the Katian and a second at the end of the Hirnantian. After the O−S extinction, the early Rhuddanian coral patch reefs are indicative of the initial recovery, and Aeronian coral-stromatoporoid reefs reflect a full recovery in the Laurentia region. The Chinese record of microbial bloom and prevailing anoxia in the aftermath of the O−S extinction could be due to cold upwelling affecting South China, which might have been still impacted by the equatorial cold-water tongue during the earliest Silurian (Jin et al., 2018). The latest Frasnian has two widespread anoxic events, the lower Kellwasser and upper Kellwasser, and these are well defined by two distinctive positive carbon isotope excursions in carbonates. Of these, the upper Kellwasser event, just below the Frasnian−Famennian (F−F) boundary and considered to be coincident with the F−F mass extinction, displays a positive shift followed by a pronounced negative shift of carbonate carbon isotopes (Fig. 23). The same pattern is also reflected in organic carbon and sulfur isotopic excursions (Xu et al., 2012). The major kill-factor of the upper Kellwasser event and F−F extinction is widely considered to have been oceanic anoxia, which may have resulted from increases in sea level, in seawater temperature, and in physical and chemical weathering (Bond and Grasby, 2017). The ultimate trigger could have been the eruption of a large igneous province (LIP) in the Siberian region (Bond and Grasby, 2017). The Famennian ecosystem was subsequently stressed further by the Hangenberg anoxic event at the Devonian−Carboniferous boundary. The Hangenberg event is marked by a distinct negative carbon isotope excursion in carbonates in Europe and South China (Bond and Grasby, 2017). The expansion of oncoids within the Chuanshan Formation of South China during the earliest Permian has been linked with the Late Paleozoic Ice Age (Shi and Chen, 2006). It appears that when a continental ice sheet developed on southern Gondwana during this icehouse regime, metazoan reefs grew in abundance in northern mid-latitudes, whereas microbes bloomed over vast regions of the low latitudes. Their linkage mechanisms to the climate changes still remain unclear. Two lesser extinctions occurred during the mid-Capitanian and endCapitanian (latest Middle Permian) (Bond and Grasby, 2017). Both of these extinction events are marked by pronounced negative shifts in carbon isotope values. A distinctive negative shift in sulfur isotopes has also been recognized from the end-Capitanian extinction horizon, suggesting an upwelling incursion of deep euxinic seawater into shallow habitats. The Emeishan LIP volcanism is considered as a trigger for the end-Capitanian extinction.

Fig. 21. Alternations of highly bioturbated limestone and anachronistic facies in the Helongshan and Nanlinghu formations (Olenekian age) from the Yashan section, Anhui Province, eastern China (modified from Chen et al., 2011). Green bars represent weakly bioturbated microbe-dominated carbonate (including vermicular limestone, flat-pebble conglomerates) layers, while blue bars represent highly bioturbated layers yielding abundant high-tier traces of Rhizocorallium (Feng et al., 2018). Column ii = ichnofabric index for which 1 to 5 indicates lowest to highest level of bioturbations. Trace fossil symbols indicate highly bioturbated horizons. CZ = conodont zone, AZ = Assemblage zone, St. = Substage.

4.2. Early–Middle Triassic MMT In contrast to the extreme cold followed by deglaciation across the Ordovician−Silurian transition, the P−Tr interval represents a sudden transition from a warm into an overheated Earth. A rapid 8 oC increase in seawater temperature was associated with the P−Tr boundary biocrisis (Joachimski et al., 2012; Sun et al., 2012). Several factors with potential triggering by the massive Siberian LIP eruptions that include increased carbon dioxide concentrations, rapid global warming, oceanic anoxia and hypercapnia (CO2 poisoning) have been proposed as contributing to the P−Tr biotic extinction (Knoll et al., 2007a; Chen and

and intensive volcanisms (Gong et al., 2017), together with habitat destruction due to global tectonic activity, may also have contributed to the biocrisis at the end of the Ordovician. Harper et al. (2014) 42

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Fig. 22. Diagram showing generalized biosedimentary features of a typical MMT. Development stages A to D include biotic survival to initial recovery, and then full recovery after a major mass extinction.

minimum zone (OMZ) (Algeo et al., 2011; Winguth and Winguth, 2012) as a long-term reservoir that fed episodic incursions of H2S-bearing waters into shallow-marine habitats, thereby delaying biotic recovery throughout the Early Triassic (Bottjer et al., 2008). The P−Tr global warming also severely impacted continental habitats and terrestrial life. The terrestrial effects could have been substantial, with elevated chemical weathering following stripping of vegetation, long-term aridification and episodes of lethal heating and acid

Benton, 2012; Chen et al., 2017b, 2018, 2019). There is increasing evidence that incursions of euxinic waters onto shallow shelves may have been another important contributing killing agent. These incursions are interpreted as a combination of upward and oceanward expansion of photic-zone euxinia, possibly fuelled by elevated riverine nutrient fluxes from land due to climatic warming, terrestrial ecosystem destruction and enhanced erosion (Algeo et al., 2011). Euxinic water masses at intermediate depths could have formed an expanded oxygen

Fig. 23. Environmental, climatic and biotic extremes, and biosedimentary processes of the late Neoproterozoic and Phanerozoic. Abbreviations: PETM = Paleocene−Eocene Thermal Maximum, OAE 1a = Early Aptian Oceanic Anoxic Event, OAE 2 = Cenomanian−Turonian Oceanic Anoxic Event, TOAE = Early Toarcian Oceanic Anoxic Event, LIP = Large Igneous Province, MMT = microbe-metazoan transition. Dates on the geologic timescale follow Ogg et al. (2016). Data for biotic diversification, recovery and mass extinctions are after Chen et al. (2014a); data for LIP, anoxia, acidification, glaciation and sulfur isotopes follow Bond and Grasby (2017); carbon isotope data follow Rong and Huang (2014); data on accumulative thickness of metazoan carbonate and microbial carbonate abundance are from Fig. 6. 43

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Oxic (Wu et al., 2017)

Dysoxic to oxic (Wu et al., 2017)

Oxic (Liu et al., 2010)

Dysoxic to oxic (Pei et al., 2019)

Low (oxic?) (Shen et al., 2015)

Dysoxic (Fang et al., 2017a)

Oxic (Forel et al., 2009) Dysoxic (Crasquin-Soleau and Kershaw, 2005) TSC

TOC

Low (oxic?) (Tang et al., 2017) Low (oxic?) (Tang et al., 2017)

Oxic (Collin et al., 2015) REE (Cerium anomaly)

Dysoxic (Ezaki et al., 2008; Liao et al., 2017) Oxic (Collin et al., 2015) Dysoxic (Wang et al., 2016) Oxic (Loope et al., 2013) Dysoxic (Liao et al., 2010) Pyrite framboids

Ostracods

Xiushui XJC CY Zuodeng Dajiang Cili

The Triassic−Jurassic (T−J) mass extinction is also marked by a pronounced negative carbon isotope excursion, probably linked to the LIP volcanism on the margins of the future Central Atlantic. Similar to the association of LIPs with the P−Tr, F−F and G−L mass extinctions, this T−J LIP may also have caused global warming, elevated chemical and physical weathering on land, and widespread oceanic anoxia (Ruhl

LLD

4.3. End-Triassic through Cenozoic

Yudongzi

rain. Apart from the loss of an estimated > 70% of life on land, the P−Tr crisis also resulted in the removal and prolonged absence of forests from the Earth surface for up to 10 Myr, thereby creating a pronounced coal gap and major changes in terrestrial ecosystems through the Early Triassic (Benton and Newell, 2014; Lucas, 2018). In turn, these physical crises on land also negatively impinged on the oceans, leading to a tight interlocking feedback of the terrestrial and the marine crises (Algeo et al., 2011). Carbon isotopes underwent at least four dramatic negative-positive shifting cycles before finally stabilizing in early Middle Triassic (Payne et al., 2004; Tong et al., 2007) when metazoan and microbial reefs co-existed. Sulfur isotopes also have frequent excursions during this interval (Song et al., 2014), and the oceanic redox history indicates four major anoxic episodes through the Early−Middle Triassic (Huang et al., 2017, 2019b). The Early Triassic oceans generally remained at elevated temperatures, although they also cooled twice during this epoch (Sun et al., 2012). We don’t know if these high-temperature conditions were beneficial to microbial proliferation and had facilitated the precipitation of microbial carbonates. However, it is clear that alternations of microbial and metazoan deposits correspond to environmental and climatic perturbations through the Early Triassic, but metazoan reefs did not become widespread in the ocean until conditions became relatively stable and seawater significantly cooled during the early Middle Triassic (Anisian). In addition, an episode of extended widespread anoxia is indicated by multidisciplinary evidence from P−Tr boundary beds around the world (Wignall and Twitchett, 2002; Bond and Wignall, 2010; Huang et al., 2017, 2019b; Elrick et al., 2017; Zhang et al., 2018). However, a detailed pyrite framboid analysis of the Meishan section in South China reveals that those PTB beds record two distinct anoxic phases. An intervening dysoxic to oxic phase during the formation of Meishan Bed 27 of the H. parvus Zone separates anoxic conditions during the depositions of Meishan Beds 25–26 and of Beds 28–34 (Chen et al., 2015; Li et al., 2016; Huang et al., 2017, 2019b). Interestingly, the PTB-microbialites are coeval with Meishan Bed 27 (Yang et al., 2011; Kershaw et al., 2012). Despite extensive studies, various proxies for redox conditions (e.g., ostracod paleoecology, pyrite framboid size and morphology, or cerium anomaly) have yielded conflicting interpretations for the PTBmicrobialites (Table 1). For instance, the abundance and diversity of their metazoans would suggest an oxygenated or dysoxic setting for the microbialite ecosystem (Crasquin-Soleau and Kershaw, 2005; Liu et al., 2010; Forel et al., 2009; Yang et al., 2015a,b). Cerium anomalies of REEs from microbialites are also indicative of oxic conditions. In contrast, the associated pyrite framboid sizes and morphologies usually indicate an anoxic to dysoxic environment for the PTB-microbialites (Wu et al., 2007, 2017; Liao et al., 2010; Yang et al., 2011; Wang et al., 2016). One option is that there was a wide range of redox conditions. One model is that the PTB-microbialites had a very high precipitation rate, indicative of calcium carbonate supersaturation within shallow water masses, which may have resulted from the upwelling of alkaline anoxic deep water, followed by high rates of evaporation at the surface due to the elevated temperatures during the PTBM (Woods, 2014). Accordingly, we infer that the growth of PTB-microbialites seems not to have been restricted by oxygen levels, but rather was affected by other conditions of seawater chemistry and depositional setting. Additional PTB-microbialites need be studied by multiple independent techniques to confirm such an inference and to compare the consistency of proxies for bottom-water oxygen conditions.

PTBM sections

Table 1 Redox condition interpretations of the PTB-microbialites based on various proxies from South China. PTBM = PTB-microbialite, LLD = Laolongdong, CY = Chongyang, XJC = Xiejiacao; REE = Rare Earth Element, TOC = Total Organic Contents, TSC = Total Sulfur Content

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from the updated global variations of both microbial and metazoan carbonates. The onset of each major MMT is characterized by an increasing abundance in microbial carbonate coupled with a decrease in metazoan reefs. These five MMTs share similar patterns with four development stages in their biosedimentary records. They are initiated with microbe-dominated successions (Stage A), followed by alternations of microbe-dominated and metazoan-bearing or bioturbated successions (Stage B). Both microbial and metazoan reefs co-occur during Stage C, and then a dominance of metazoan reefs marks development Stage D. Both the Ediacaran and the Cambrian MMTs have undergone only the first three development stages, while the post-extinction MMTs experienced the full set of development Stages A−D that correspond to metazoan biotic survival, initial recovery and full recovery. The late Ediacaran MMT is characterized by the co-existence of both sponge-dominated reefs and microbialites. The Cambrian MMT is the longest and saw a great microbial proliferation throughout the entire period. The Cambrian MMT is characterized by two peaks in metazoan occurrence with dominance by abundant Archaeocyathid reefs during Cambrian Epoch 3 (Miaolingian) and dominance by maceriate sponge reefs during the late Furongian. The early Silurian MMT in China is dominated by a thick accumulation of organic-rich black shales during its initial stage, followed by alternating microbe-rich sediments and metazoan-bearing deposits, which eventually are replaced by microbial and metazoan reefs in the late early Silurian. The Late Devonian MMT was initiated in the prelude to the Frasnian-Famennian crisis, is characterized by alternating occurrences of abundant microbial and metazoan reefs, and persisted into the early Mississippian. The Early−Middle Triassic MMT began in the aftermath of the greatest mass extinction of life on Earth. The initial phase of microbemediated sediments has an anomalously high global abundance of microbialites and oolites, plus an assortment of anachronistic facies, such as giant ooids, wrinkle structures, and flat-pebble conglomerates. Moreover, almost all of the types of microbial sediments and buildups prevailing in the Cambrian oceans re-occurred in the post-extinction ocean of the Early Triassic, suggesting high similarities between these two MMTs. Biosedimentary similarities between Cambrian and Early−Middle Triassic MMTs are also reflected in comparable carbon and sulfur isotopic perturbations, warming regimes, and generally oxygen-deficient seawaters (Fig. 23). Some of these environmental and climatic extremes may also occur in other MMTs, but they usually did not occur synchronously. The end-Permian mass extinction associated with the eruption of the enormous Siberian Traps is the first of a series of volatile-releasing LIPs during the Mesozoic−Cenozoic (Fig. 23). The resulting global warming, acidification and anoxia regimes apparently became much more pronounced during the Mesozoic−Cenozoic events than those during the Paleozoic LIP episodes. However, only the Early Triassic MMT has widely deposited microbe-dominated sediments, and the importance of MMTs was greatly subdued or even non-existent in the aftermaths of the end-Triassic through Cenozoic environmental stresses (Fig. 23) probably owing to a primary food source for the metazoans shifting to phytoplankton (e.g., coccolith, dinoflagellate, and radiolarian) since the Late Triassic. This implies that microbial proliferations in the early phases of MMTs may not be directly related to these volatile volcanisms and extreme climatic events. Nevertheless, carbon isotopic excursions indicating significant perturbations of the carbon cycle characterizes all MMTs, and thus are a reliable proxy indicating MMT biosedimentary systems changing initially into a microbe-dominance, then trending back to a metazoan-dominated system. The exceptional records of the Ediacaran–Devonian metazoan and microbial carbonates in China, as well as excellent and complete Permian–Triassic microbe-metazoan successions, provide unique opportunities to study the patterns and formation mechanisms of MMTs and their responses to major global events. In addition, excellent modern-day analogs to metazoan reefs and microbial carbonates are currently found in the South China Sea and in the abundant salt lakes

et al., 2011; Greene et al., 2012; Richoz et al., 2012; Lucas and Tanner, 2015; Stanley et al., 2018) (Fig. 23).Three oceanic anoxic events (OAEs) caused Mesozoic ecologic crises during the Early Jurassic and the middle−late Cretaceous. The latest Pliensbachian−earliest Toarcian (Early Jurassic) extinction (Harries and Little, 1999) is associated with an OAE, a major negative carbon isotope excursion, a marine transgression and global warming, all of which may have been triggered by flood basalt magmatism (McElwain et al., 2005). However, the chronology of these physical events and associated biocrisis require greater precision to clarify their possible linkage and mechanisms. The OAEs in the early Aptian (middle Cretaceous) and at the Cenomanian−Turonian (C−T) transition (early Late Cretaceous) (Fig. 23) are marked by carbon isotope excursions and are associated with lesser biotic marine extinctions (Bambach, 2006). Various geochemical proxies (i.e., biomarkers) reveal repeated anoxic/euxinic events that coincided with climatic warming and biotic extinctions within intermediate to surface waters during these critical periods (Kaiho et al., 2014). Cenozoic climatic extremes have been relatively well studied, and the Paleocene−Eocene Thermal Maximum (PETM) at ~55 Ma is believed to potentially mirror greenhouse gas-induced global warming trends that might again occur in the near future. This abrupt global warming has been variously linked to LIP volcanism that caused major disruption of the carbon cycle and to large and rapid releases of fossil carbon (Gutjahr et al., 2017). Global warming was accompanied by extreme changes in hydroclimate and accelerated weathering, deepocean acidification, and possible widespread oceanic anoxia (Barnosky et al., 2004; Cui et al., 2011). Even though many of the characteristics of the suite of end-Triassic through PETM environmental crises seem similar to the episodes associated with the Paleozoic and Early−Middle Triassic MMTs, none of these later situations resulted in widespread abundance of microbial carbonates, therefore there were no significant microbe-metazoan transitions (Fig. 6). MMTs were restricted to the Ediacaran through Middle Triassic. This implies that microbial proliferations in the early phases of MMTs may not be directly related to volatile volcanisms and extreme climatic events. The low abundance of microbe-related sediments in the aftermaths of major extinction and other extreme events after the Triassic could have resulted from two possible causes. Firstly, metazoan biodiversity and abundance rapidly increased in the post-Triassic Mesozoic (Sepkoski et al., 1981) when marine predation became more intensified than before, as a consequence of the Mesozoic Marine Revolution (Vermeij, 1977), facicliating feeding on primary producers (i.e, microbes) by low-tier animals, and thus suppressing microbial blooms (Chen and Benton, 2012). Secondly, the base of the trophic web of marine ecosystems has changed during the Late Triassic, which witnessed the increasing abundance of phytoplankton (e.g., coccolith, dinoflagellate, and radiolarian) (Knoll et al., 2007b; Knoll and Follows, 2016). Thus, the shift of a primary food source for the metazoans from microbes to phytoplankton in the Late Triassic may likely account for the depauperate nature of microboes following major biotic and environmental crises during the Meosozic-Cenozoic. 5. Conclusions This study compiled well-documented occurrences in China of 150 metazoan reefs and 180 microbial reefs from Precambrian to Cenozoic strata. The pre-Jurassic records of China share high similarities with the global database in that metazoan reefs proliferated during Middle Ordovician, Middle Devonian and Middle Permian times, whereas microbial reefs are well-developed during the Cambrian, Late Devonian and Early−Middle Triassic, with a moderate development in the early Silurian. Five major microbe-metazoan transitions (MMTs) – the late Ediacaran, the Cambrian, and the aftermaths of the end-Ordovician, Late Devonian, and end-Permian mass extinctions – are recognized 45

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and hot springs in western China. These provide natural laboratories for biosedimentologic studies under contrasting environmental settings. These deep-time and modern natural records guarantee future major advances in biosedimentology research in China, including understanding why past global warming episodes led to these anomalous microbe-dominated ecosystems.

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Acknowledgments This report is derived from multiple discussions at the Xiangshan Sedimentology Workshop held in Beijing in September of 2016. We are grateful to Judith Mckenzie, Hongfu Yin, Robert Riding, Chengshan Wang, Chuanming Zhou, Shucheng Xie, Chao Li and Ping Luo for the input of their ideas and constructive suggestions at the Xiangshan Workshop. Editor in Chief Andre Strasser and three anonymous reviewers are thanked for their critical comments and constructive suggestions, which have improved greatly the quality of the paper. This study was supported by four National Natural Science Foundation of China research grants (41821001, 41572091, 41772007, 41661134047), a Hubei Provincial Natural Science Foundation grant (2017CFA019), and a National Key R & D Program of China grant (2017YFC0603103). It is a contribution to the International Geosciences Program (IGCP) project 630: Permian–Triassic climatic and environmental extremes and biotic response. Appendix A. Supplementary data The detailed database of deep-time reef occurrences, stratigraphic settings, and localities from China. References Abdolmaleki, J., Tavakoli, V., 2016. Anachronistic facies in the Early Triassic successions of the Persian Gulf and its palaeoenvironmental reconstruction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 446, 213–224. Adachi, N., Ezaki, Y., Liu, J.B., 2011. Early Ordovician shift in reef construction from microbial to metazoan reefs. PALAIOS 26, 106–114. Adachi, N., Kotani, A., Ezaki, Y., Liu, J.B., 2015. Cambrian Series 3 lithistid sponge-microbial reefs in Shandong Province, North China: reef development after the disappearance of archaeocyaths. Lethaia 48, 405–416. Adachi, N., Asada, Y., Ezaki, Y., Liu, J.B., 2017. Stromatolites near the Permian-Triassic boundary in Chongyang, Hubei Province, South China: a geobiological window into palaeo-oceanic fluctuations following the end-Permian extinction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 475, 55–69. 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. Palaeogeogr. Palaeoclimatol. Palaeoecol. 308, 1–11. Allwood, A.C., Walter, M.R., Kamber, B.S., 2006. Stromatolite reef from the early Archaean era of Australia. Nature 441, 714–718. Aretz, M., Chevalier, E., 2007. After the collapse of stromatoporid sponge coral reefs—the Famennian and Dinantian reefs of Belgium: much more than Waulsortian Mounds. In: Alvaro, J.-J., Aretz, M., Boulvain, F., Munnecke, A., Vachard, D., Vennin, E. (Eds.), Palaeozoic Reefs and Bioaccumulations: Climatic and Evolutionary Control. 275. Geological Society Special Publications, London, pp. 163–188. Bagherpour, B., Bucher, H., Baud, A., Brosse, M., Vennemann, T., Martini, R., Kuang, G.D., 2017. Onset, development, and cessation of basal Early Triassic microbialites (BETM) in the Nanpanjiang pull-apart Basin, South China Block. Gondwana Res. 44, 178–204. Bambach, R.K., 2006. Phanerozoic biodiversity mass extinctions. Annu. Rev. Earth Planet. Sci. 34, 127–155. Barnosky, A.D., Koch, P.L., Feranec, R.S., Wing, S.L., Shabel, A.B., 2004. Assessing the causes of Late Pleistocene extinctions on the continents. Science 306, 70–75. Batchelor, M.T., Burne, R.V., Hery, B.L., Li, F., Paul, J., 2018. A biofilm and organomineralisation model for the growth and limiting size of ooid. Sci. Rep. 8, 559e. Baud, A., Cirilli, S., Marcoux, J., 1997. Biotic response to mass extinction: the lowermost Triassic microbialites. Facies 36, 238–242. Baud, A., Richoz, S., Pruss, S., 2005. The lower Triassic anachronistic carbonate facies in space and time. International symposium on Triassic Chronostratigraphy and Biotic Recovery, Chaohu, Anhui, China. Albertiana 33, 17–19. Baud, A., Richoz, S., Pruss, S., 2007. The lower Triassic anachronistic carbonate facies in space and time. Glob. Planet. Chang. 55, 81–89. Benton, M.J., Newell, A.J., 2014. Impacts of global warming on Permo−Triassic terrestrial ecosystems. Gondwana Res. 25, 1308–1337. Bond, D.P., Grasby, S.E., 2017. On the causes of mass extinctions. Palaeogeogr. Palaeoclimatol. Palaeoecol. 478, 3–29. Bond, D.P.G., Wignall, P.B., 2010. Pyrite framboid study of marine Permian–Triassic

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